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Nothing in Evolution Makes Sense Except in the Light of Genomics: Read–Write Genome Evolution as an Active Biological Process

Department of Biochemistry and Molecular Biology, University of Chicago, GCIS W123B, 979 E. 57th Street, Chicago, IL 60637, USA
Biology 2016, 5(2), 27;
Submission received: 12 February 2016 / Revised: 20 May 2016 / Accepted: 2 June 2016 / Published: 8 June 2016
(This article belongs to the Special Issue Beyond the Modern Evolutionary Synthesis- what have we missed?)


The 21st century genomics-based analysis of evolutionary variation reveals a number of novel features impossible to predict when Dobzhansky and other evolutionary biologists formulated the neo-Darwinian Modern Synthesis in the middle of the last century. These include three distinct realms of cell evolution; symbiogenetic fusions forming eukaryotic cells with multiple genome compartments; horizontal organelle, virus and DNA transfers; functional organization of proteins as systems of interacting domains subject to rapid evolution by exon shuffling and exonization; distributed genome networks integrated by mobile repetitive regulatory signals; and regulation of multicellular development by non-coding lncRNAs containing repetitive sequence components. Rather than single gene traits, all phenotypes involve coordinated activity by multiple interacting cell molecules. Genomes contain abundant and functional repetitive components in addition to the unique coding sequences envisaged in the early days of molecular biology. Combinatorial coding, plus the biochemical abilities cells possess to rearrange DNA molecules, constitute a powerful toolbox for adaptive genome rewriting. That is, cells possess “Read–Write Genomes” they alter by numerous biochemical processes capable of rapidly restructuring cellular DNA molecules. Rather than viewing genome evolution as a series of accidental modifications, we can now study it as a complex biological process of active self-modification.

1. Introduction

The title of this mini-review is a paraphrase of Dobzhansky’s famous dictum, “Nothing in biology makes sense except in the light of evolution” [1,2]. The reason for this paraphrase is to emphasize how, since Dobzhansky’s day, genetics and evolution science have moved into the era of a revolutionary new technology, DNA sequencing. Whenever such a technological revolution occurs, science must always ask itself what impact data from the new methods has on the validity of prevailing concepts.
Our current ideas of heredity center on DNA replication and transmission [3]. Although cell and organismal heredity involves transmission of all cellular molecules, we conventionally view RNAs, proteins, lipids, polysaccharides and other biomolecules as derivative products resulting from biochemical activities determined by genomic DNA sequences [4]. According to this DNA-centered perspective, stable inherited changes in organismal properties result primarily from alterations in the genome. New DNA sequences can encode new biochemical capabilities that lead to novel traits. If evolution is the acquisition of new characters over time [5], the most basic causal events should emerge from the processes that generate new DNA sequences. Those events are traceable in genome sequences, which today serve as the ultimate empirical data to test evolutionary hypotheses.
In this brief review, we will examine some of the evolutionary lessons from genome sequence data. Given the broad extent of the subject matter, only a select range of examples will receive attention. The investigation shows that many evolutionary changes result from cellular processes that produce abrupt changes in genome structure and organismal characters. These processes include symbiogenesis, horizontal DNA transfer, hybrid speciation and natural genetic engineering, especially the action of mobile DNA elements [6,7]. At the molecular level, evolution is often saltational rather than gradual [8], and punctuated equilibrium [9] is the default pattern to expect in the history of phenotypic properties. As we shall see, this view is quite different from Dobzhansky’s thinking. In particular, molecular sequence analysis documents many genomic elements and novel forms of hereditary variation that were hardly conceivable in Dobzhansky’s lifetime.

2. The Genome as a Highly Formatted Sequence Database

Genomes serve as controlled read-write databases for the reliable transmission and regulated expression of DNA sequence information [7,8,10]. Because controls over expression, replication and transmission are essential to survival and reproduction, genomes contain abundant cis-acting DNA formatting elements in addition to coding sequences determining RNA and protein primary structures [11].
Many of the formatting DNA elements are generic and present at multiple genome locations. Consequently, repetitive DNA is a major component of all genomes, and repeats frequently represent the majority of an organism’s DNA [12]. In the human genome, the repetitive content is about two-thirds of the total DNA, compared to well under 5% for protein-coding sequences [13].
For evolution, the significance of genome formatting by repeat DNA elements is that important phenotypic alterations can occur as a result of changes to so-called “non-coding” sequences. Recent discoveries about the functions of “non-coding” ncRNA molecules illustrate this point [14,15,16,17,18,19], as do Evo-Devo findings that many developmental alterations distinguishing related organisms occur in regulatory DNA elements rather than coding sequences [20,21].

3. Molecular Phylogenies Based on Core Information-Processing Systems

The most basic impact of genomics on evolution science has been the use of sequence data to establish relationships among different organisms. In the 1970s, Carl Woese pioneered molecular phylogenetic methodologies [22]. Woese chose to base his initial phylogenies on the sequence of small subunit ribosomal RNA for two reasons: (i) ssrRNA was abundant and amenable to 1970s sequence analysis methods; and (ii) the ribosome is a highly conserved central component of information transfer from the genome to the proteome. Because all cells have similar but still distinctive ribosomes, this organelle provided phylogenetic data to establish connections between very diverse organisms.
Using ssrRNA sequence analysis, Woese and his colleagues unexpectedly discovered that there are in fact two separate kingdoms of prokaryotic organisms (those lacking separate cell nuclei), not one bacterial kingdom as previously believed [23]. The two groups of prokaryotic organisms turned out to exhibit ssrRNA sequence clusters as phylogenetically distant from each other as both clusters were from the ssrRNA sequences of eukaryotic (nucleated) organisms. The evolutionary distance between the two prokaryotic groups was further confirmed by major differences in their cell membranes as well as by differences in the basic processes of genome replication and expression. The newly discovered prokaryotic cell kingdom was labeled Archaea because the first members to be studied were organisms isolated from extreme environments thought to resemble the early Earth [24]. Today, however, there is no reason to assume that Archaea are any more ancient than Bacteria.
The most basic tenet of evolution science—the genetic relatedness of all living organisms—is abundantly supported by molecular biology, in particular the universal features of the triplet code for amino acids and the similarities of core cell structures, like the ribosome, associated translation factors [25], and DNA and RNA polymerases. Nonetheless, the first phylogenetic application of genomics revealed a previously unknown complexity in the biosphere and, as we shall see in the next section, provided compelling evidence for a large number of evolutionary processes excluded by conventional evolutionary thinking based on population genetics and the Modern Synthesis [26,27]. As highlighted below, the phylogenies of Bacteria, Archea, eukaryotes and giant viruses continue to pose intriguing challenges in understanding the networked evolutionary connections between all domains of life [28].

4. Eukaryotic Origins and Major Eukaryotic Taxonomic Originations through Symbiogenesis

The identification of an unsuspected bifurcation among prokaryotes, the most abundant living organisms [29], immediately raised questions about the historical relationships between Archaea and Bacteria without nuclei, on the one hand, and Eukarya, the organisms with nucleated cells, on the other. Eukaryotes formed a coherent separate group based on ribosomal RNA sequences, and molecular phylogenies of different eukaryotic groups confirmed well-established taxonomic classifications, such as fungi, plants and animals. But the generic eukaryotic cell was closer to Bacteria in some features—membrane composition, metabolic pathways—and closer to Archaea in other features—replication, transcription and translation [30,31]. This phenotypic dichotomy gave support for longstanding but hotly disputed arguments championed by Lynn Margulis and others that symbiogenetic cell fusions served to create complex eukaryotic cells from simpler prokaryotic progenitors [29,32,33,34,35,36].

4.1. Endosymbiotic Bacterial Origins of Eukaryotic Organelles

Molecular phylogenetics unequivocally documented the role of symbiogenesis in Eukarya evolution by analysis of the two cell organelles that have their own genomes: (1) the mitochondrion, carrying out oxidative metabolism; and (2) the chloroplast, carrying out oxidative photosynthesis. All eukaryotic cells contain a functional mitochondrion or a non-oxidative derivative organelle [37,38,39]. Thus, the ancestral eukaryote must have acquired an endosymbiotic mitochondrial precursor, and molecular phylogenetics unambiguously identified the mitochondrion as belonging to the Alpha-proteobacteria group [40,41,42]. Similarly, photosynthetic eukaryotes, including red and green algae and plants, have chloroplasts, and molecular phylogenetics identified the chloroplast as a member of the cyanobacteria [43,44,45]. The chloroplast, and derivative plastid organelles in phylogenetically related non-photosynthetic eukaryotes, therefore must have descended from one or more endosymbiotic cyanobacteria [46,47].

4.2. DNA Transfer between Endosymbiotic Organelle and Nuclear Genomes

The genomes of mitochondria and chloroplasts do not encode all the proteins inherited from their bacterial ancestors. Many organelle proteins are encoded in the nuclear genome as a result of DNA transfers into the nuclear genome from mitochondria [48,49,50,51] and from chloroplasts [52,53,54,55]. These intracellular DNA transfers from one genomic compartment to another continue and have been analyzed in real time [56,57,58,59,60]. Interestingly, mitochondrial DNA transfer to the nucleus affects life-span in yeast cells [61], increases with age in rat cells [62], generates inherited disease loci in humans [56,63], occurs frequently in cancer cells [64], and participates in nuclear double-strand DNA break repair in organisms as distant as yeast and humans [56,65]. Chloroplast to nucleus DNA transfer is stimulated by stress conditions [59]. There is further evidence of organelle genomes acquiring nuclear and other external DNA [66,67,68]. Active import of DNA into plant mitochondria has been documented in real time [69].
Since the genetic content of mitochondria, chloroplasts and plastids differs significantly among taxonomic groups, important factors in eukaryotic taxonomic divergence are organelle to nucleus DNA transfer [49,50,70] and organelle genome restructuring: in mitochondria [51,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87], by loss of mitochondrial oxidative capacity [38,88,89,90], in chloroplasts [45,47,54,91,92,93,94,95,96], and by loss of chloroplast photosynthetic capacity [47,54,97,98,99,100].

4.3. Origins of Photosynthetic Eukaryotic Taxa by Secondary Endosymbiogenesis

A large number of photosynthetic eukaryotes did not evolve directly from algae or plants and are most closely related taxonomically to non-photosynthetic organisms [37]. These organisms originated from “secondary” eukaryote to eukaryote symbiogenetic events where a red or green alga has become an endosymbiont in the initially non-photosynthetic lineage [101,102,103,104,105,106]. The resulting photosynthetic cells have four different genome compartments that exchange DNA segments: nucleus, mitochondrion, plastid and nucleomorph (descended from the algal nucleus) [107,108,109,110,111,112,113]. As with mitochondria and chloroplasts, the major intracellular DNA transfers occur from the organelles, including the nucleomorph, into the nuclear genome. The photosynthetic taxa arising from secondary endosymbiosis include euglenids and chlorachniophytes from green algal endosymbiosis and the chromalveolates from red algal endosymbiosis [37]. The large chromalveolate phylum includes major photosynthetic organisms responsible for a large fraction of atmospheric oxygen, such as brown algae, dinoflagellates and diatoms.
Photosynthetic endosymbiosis is not restricted to unicellular eukaryotes. There are cases where animals have acquired photosynthetic capabilities by symbiogenetic events [114,115,116]. The photosynthetic animals include sea slugs [117,118,119] and molluscs [120,121].

4.4. Formation of a Primitive Eye-Like Organ in a Unicellular Eukaryote by Serial Endosymbioses

Among the photosynthetic dinoflagellates resulting from algal ensymbiosis, there is a group labeled “ocelloids,” which possess a remarkable light-harvesting organ (the ocelloid) that resembles a complex camera-like animal eye [122,123]. The ocelloid has analogues to the cornea, lens, iris and retina. A noteworthy recent paper reports that genomic analysis reveals that each of these structures resulted from a distinct endosymbiogenetic event [124]:
“Here we show, using a combination of electron microscopy, tomography, isolated-organelle genomics, and single-cell genomics, that ocelloids are built from pre-existing organelles, including a cornea-like layer made of mitochondria and a retinal body made of anastomosing plastids. We find that the retinal body forms the central core of a network of peridinin-type plastids, which in dinoflagellates and their relatives originated through an ancient endosymbiosis with a red alga. As such, the ocelloid is a chimaeric structure, incorporating organelles with different endosymbiotic histories.”
The genomics-verified example of ocelloid formation by serial endosymbiogenesis has to be considered in light of Darwin’s famous statement: “If it could be demonstrated that any complex organ existed, which could not possibly have been formed by numerous, successive, slight modifications, my theory would absolutely break down.” [5] (p. 189). While the endosymbiogenetic origin of the ocelloid does not demonstrate the impossibility of camera eyes evolving by Darwinian gradualism, this striking case of adaptive evolution by repeated cell fusion events clearly lies outside the parameters of evolutionary processes envisioned by the author of Origin of Species as well as by the Modern Synthesis.

5. Eukaryotic Speciation by Inter-Specific Hybridization, Whole Genome Duplications and Genome Restructuring

When we ask how novel species arise from human intervention, it is significant that there are no cases where selection has led to species formation. Selection only modifies existing characteristics by reducing or amplifying them. Artificial species arise through hybridization, as in the case of the wheat-rye hybrid Triticale [125,126], and involve genome mergers and whole genome duplication (WGD) events [127,128]. A similar “cataclysmic evolution” process involving hybridization of wild grasses was at the origin of flour wheat (Triticum) several thousand years ago and can be reproduced in real time [129,130]. Ongoing abrupt hybrid speciation has been observed to occur in wild sunflowers [131]. A recent paper reports laboratory formation of a novel tobacco species with a double genome by fusion of tissue culture cells from two different natural Nicotiana species [132].
Many genomes contain duplicate copies of extended chromosome regions holding homologous genetic loci in a conserved (“syntenic”) order [133,134,135]. By documenting the prevalence of numerous syntenic duplications, genomic analysis provides compelling evidence that hybrid speciation and WGD have been common events in the history of evolution in all eukaryotic groups, including yeasts and other fungi [136,137,138,139], ciliated protists [140], plants [141,142] and animals, including two successive WGD events at the origins of vertebrates [143,144,145,146,147], followed by further WGD events in bony fishes [148,149].
In addition to WGD, interspecific hybridization leads to episodes of genome instability and restructuring [150,151,152]. Chromosome rearrangements have long been recognized as major features of speciation and taxonomic divergence [153,154,155]. Repetitive and mobile DNA elements play special roles in chromosome restructuring [156,157,158,159], as exemplified in primate evolution by the recently published gibbon genome [160].

6. Adaptations Acquired and Comingled by Horizontal Transfers

The conventional view of evolution maintained by Dobzhansky and his colleagues is that traits are transmitted vertically from progenitors to offspring, with evolutionarily important hereditary changes occurring within each particular line of descent. That is the pattern of “descent with modification” illustrated at the end of Origin of Species [5]. According to this perspective, each new adaptation has to evolve within a distinct lineage. In contrast to this conventional view, genomic analysis revealed that the molecular phylogenies of genetic loci encoding certain adaptive functions do not always match the taxonomic histories of the basal host genomes [30]. The genomic evidence indicated that organisms could acquire independently evolved DNA providing adaptive benefits from unrelated organisms by “horizontal” DNA transfer [161,162]. Genomic evidence shows that it often proves more efficient to adapt to a new ecological niche by borrowing functions from distant taxa rather than evolving them internally from the pre-existing genome.

6.1. Horizontal Transfer among Prokaryotes

The ability of prokaryotic organisms to exchange advantageous DNA segments is evident from studies of antibiotic resistance starting in the early years of molecular genetics ( [163,164,165,166]. Horizontal DNA transfer can occur between prokaryotic cells by uptake of DNA released by cells to the environment (transformation), direct cell-to-cell contact (conjugation), or viral infection (transduction) [167]. Sometimes the horizontally acquired DNA constituted an independently replicating molecule in the prokaryotic cell [168], and sometimes the horizontally acquired DNA was integrated into the existing genome, often as extended “genomic islands” encoding many different proteins for complex traits like metabolism, defense and pathogenicity [169,170,171,172]. Special site-specific recombination structures called “integrons” exist in the genomes of some bacteria for the serial integration of antibiotic resistance cassettes [173,174] and, in particular species, “super-integrons” have accumulated cassettes encoding up to hundreds of diverse adaptive functions [175,176,177,178]. Horizontal transfer occurs across the Bacteria-Archaea divide and can even lead to the formation of novel taxa [179,180,181,182,183].
The prevalence of prokaryotic horizontal DNA exchange gave rise to the idea of a vast super-cellular pan-genome that prokaryotes can sample facultatively by transformation, conjugation and transduction to assemble novel genomes for cell adaptation to particular ecological niches [184,185,186]. This controversial notion has gained wider credibility in recent years as a result of metagenomic analysis, which has revealed unexpectedly large numbers of known and unknown coding functions present in environmental DNA samples, particularly those encapsidated in virus particles [187,188,189,190,191,192,193]. There has even been the suggestion that environmental metagenome data indicate the possible existence of major new cell types [194].

6.2. Horizontal DNA Transfer from Prokaryotes and Fungi to Multicellular Eukaryotes

Horizontal DNA transfer is not limited to prokaryotes. Genomic analysis provides abundant examples of eukaryotic adaptations with prokaryotic (and fungal) origins. These include:
  • Biochemical pathways [195,196,197,198,199];
  • Phytopathogenicity in Botrytis fungi [200];
  • Ability to live in extreme environments [201];
  • Capacity of plant parasitic nematodes to digest cellulose and other phytopolymers [202,203,204,205,206,207,208]. We know that this horizontal DNA transfer strategy was used repeatedly because each lineage of plant parasitic nematodes acquired their digestive enzymes from different fungi or bacteria;
  • Energy metabolism and defense functions subject to purifying selection in a marine shrimp [209];
  • Sequences of unknown but selectively conserved function transferred from marine bacteria to fish after the divergence of teleosts from other vertebrates [210].
Many bacteria live as endosymbionts in animals, and there is abundant evidence that parts or all of endosymbiont genomes have be incorporated into host genomes [211,212,213,214,215]. In Drosophila ananassae, for example, more than 2% of the genome comes from Wolbachia endosymbionts [216].

6.3. Horizontal Transfer from Eukaryotes to Bacteria

Although less widely documented than prokaryote to eukaryote horizontal transfer, the analysis of endosymbiotic and pathogenic bacteria infecting eukaryotic cells has turned up examples where these prokaryotes appear to have integrated eukaryotic host cell sequences into their genomes [217,218,219,220,221]. The restricted taxonomic distribution of the eukaryotic domains among the infectious bacteria indicates recent horizontal acquisition rather than shared vertical ancestry with eukaryotes [217].
Bacteria use the proteins containing typically eukaryotic domains encoded by horizontally acquired DNA sequences as injected “effector” molecules to modulate host cell metabolism and defenses in order to facilitate the infection process [222,223,224,225,226,227,228,229]. The ability of many infectious bacteria to grow in diverse eukaryotic hosts, such as amoebae and mammals [230], apparently plays an important role in the acquisition of eukaryotic domains from one kind of host (e.g., amoebae) and their utilization as invasion functions in another kind of host (e.g., mammals).

6.4. Horizontal DNA Transfer among Eukaryotes

In addition to fungi, other eukaryotes can transfer DNA horizontally across taxonomic boundaries [162,231]. This phenomenon is prevalent among unicellular protists [232,233,234], but various classes of DNA transfer have been documented between multicellular lineages:
  • Mitochondrial genomes in flowering plants [235,236,237];
  • Chloroplast genomes in plants [238];
  • Mobile DNA elements [239,240,241,242,243,244,245];
  • Sequences encoding diverse adaptive functions, including glyoxylate cycle enzymes in metazoa [246], photosynthetic carbon cycles in plants [247,248], anti-freeze proteins in fish [249], and mimicry pattern determinants in butterflies [250];
  • Miscellaneous expressed functions acquired by a parasitic plant from its host [251].
Infectious bacterial endosymbionts and pathogens are widely considered as potential vectors for horizontal transfer between multicellular organisms [252,253,254,255,256]. Investigators have documented endosymbiont transfers between different multicellular host species [257,258,259], and many bacteria known as vertebrate pathogens also infect lower eukaryotes, especially amoebae [260,261,262,263,264,265,266]. Among these multivalent infectious bacteria, a number are capable of taking up DNA from their immediate environment [267,268,269,270].

6.5. Viral Integrations into Host Genomes

Viruses of all kinds (including RNA viruses) insert their genomes into eukaryotic host genomes with surprisingly high frequency [271,272,273,274,275,276,277,278,279,280,281,282,283,284,285,286,287,288]. Integration can occur by retroviral integrase functions, sometimes followed by recombination with other viral sequences [289], or by non-homologous end-joining (NHEJ) at DNA breaks [290,291]. Integration events at DNA breaks have the potential to generate novel sequence configurations.

6.6. The Amoeba-Megavirus “Melting Pot” of Sequences from All Three Cell Kingdoms

Viruses have long been considered both as substrates for evolutionary innovation [292,293] and as vectors for horizontal DNA transfer. Particular attention has recently focused on a group of Nucleocytoplasmic Large DNA Viruses (NCLDVs) with genomes comprising hundreds of thousands or millions of base-pairs [294,295,296]. Most significantly, NCLDVs acquire cellular genome fragments and have been found to carry a mixture of DNA sequences from all three major domains of life ( [297,298,299,300]. NCLDVs can infect both protists and multicellular hosts and thus transfer the incorporated cellular sequences. Amoebae are common hosts for many of these large DNA viruses, and amoeba have consequently been designated to constitute an evolutionary “melting pot” ( [301]. The designation is especially appropriate for two reasons: (1) amoebae are phagocytic and can acquire DNA sequences from engulfed cells [302] and (2) amoebae are hosts to bacteria that both exchange DNA [303] and infect more complex eukaryotes, including both plants and animals [260,261,262,263,264,265,266].
Combining the phenomenology of viral infection, amoebael phagocytosis, multivalent bacterial infectivity and endosymbioses with the documentation of viral and prokaryote to eukaryote DNA transfers, it is more than clear that multiple pathways exist by which cells can acquire and transmit DNA segments from one eukaryotic host to another. Specific biochemical activities are distributed among distantly related domains of life [304,305], and we can expect further genomically-documented examples of horizontally acquired adaptations to multiply with continued genome sequencing.

7. Protein Evolution by Exon Shuffling and Exonization from “Non-Coding” DNA

Among the most striking results of genomics was the realization that many proteins and the DNA that encodes them are not continuous unitary structures. Many proteins consist of strings of functionally different but interacting “domains,” each one of which may be found iterated in distinct proteins [306,307,308]. Correspondingly, the cognate protein-coding regions are often discontinuous and composed of expressed coding segments (“exons”) separated by intervening segments (“introns”) [309,310]. While not always the case, DNA exons tended to encode functional protein domains or subdomains [311].
The segmented nature of proteins and protein-coding DNA has major implications for genome functionality and protein evolution:
  • A given genetic locus can encode multiple protein products by joining different combinations of exons into the final mRNA by alternative splicing [312,313,314,315,316,317,318,319];
  • New protein functionalities can arise rapidly by Lego-like assembly of exons from different sources, known as exon or domain shuffling [320,321,322,323];
  • Totally new protein domains can originate rapidly by conversion of non-coding DNA segments into exons (“exonization”) and contribute to novel biochemical functions by subsequent duplication and exon shuffling [308,324,325,326].
Both the rapid evolution of new functionalities by exon shuffling and the origination of sequences encoding extended domains by exonization have potential for protein innovation beyond what is possible through codon-by-codon changes to existing proteins. Exon shuffling has an inherently high probability of producing adaptive novelties because it rearranges previously evolved sequences that encode established protein functionalities. This potential has been exploited in biotechnology where domain shuffling has proved an efficient method of protein engineering [327,328,329].
Mobile DNA elements play major roles in both exon shuffling and exonization. The genomic record indicates transposons and retrotransposons can incorporate and relocate exons [330,331,332,333,334,335,336,337], and mobile DNA-mediated exon shuffling has been studied in real time [338,339,340]. Genomics reveals numerous instances of exonization from mobile element insertions in humans and other mammals [308,326,341,342,343,344,345,346] as well as in plants [325].

8. Regulatory Signal Evolution Involving Mobile DNA Elements

The involvement of mobile DNA in genome change marks one of the most basic divergences between Dobzhansky’s Modern Synthesis perspective and a genomics-based view of the evolutionary process. The Modern Synthesis focused on isolated allelic changes at individual loci [347]. Mobile elements, on the other hand, are distributed at many sites throughout the genome and have the potential to generate coordinated changes rewiring distributed regulatory networks involving many loci ( [8,348,349,350,351,352,353,354,355,356].
Genomics documents at least three episodes of regulatory innovation involving mobile elements in the course of vertebrate evolution [357,358], and mobile DNA has been a major source of regulatory motifs in human genome evolution [359,360]. Moreover, the fact that mobile elements are often the most taxonomically specific genome components potentially confers distinctive evolutionary trajectories on different lineages [361,362,363].

9. Adaptations and Innovations in Mammalian Reproduction Arising by Natural Genetic Engineering Processes Involving Mobile DNA and “Non-Coding” ncRNA Molecules

Because of their medical relevance, reproductive biology, embryonic development and stem cell biology in mammals have received particular attention from genomicists. The analysis has uncovered major roles for mobile DNA elements and ncRNAs derived from them. Rather than serving as “fossils that litter our genomes” [364], as conventional evolutionary thinking would assert, these elements are both essential evolutionary tools and active participants in contemporary genome function.

9.1. Retroviral Involvement in Placenta Evolution

Mammalian reproduction depends upon development of a syncytial placenta from the zygote to nourish the fetus during pregnancy. At repeated stages in mammalian evolution, distinct endogenous retroviral “envelope” (Env) proteins have been exapted as fusionogenic “syncytins” involved in forming placental tissue in different mammalian lineages ( [365,366,367,368,369,370]. Moreover, endogenous retroviruses (ERVs) provide transcriptional regulatory signals to direct imprinted expression of other proteins, such as insulin-like growth factor, required for placental function [371,372,373].

9.2. Mobile DNA Recruitment of Maternal Functions

The endometrium is the maternal tissue that nourishes the placenta in mammalian pregnancy. Endometrial development in the uterus involves the hormone-regulated expression of over 1,500 different proteins. The transcriptional regulatory signals coordinating biogenesis of this pregnancy-specific cohort evolved mainly from mobile DNA elements, both transposons and retrotransposons [374,375,376,377]. Convergent patterns of regulatory rewiring can be traced in the endometria of distinct mammalian lineages with well-sequenced genomes [378]. Thus, evolutionary innovations for both fetal and maternal sides of viviparous reproduction arose, to a large degree, through the ability of mammalian cells to mobilize repetitive components of their genomes to adaptive locations.

9.3. Mobile DNA and lncRNAs in Stem Cell Programming and Early Embryogenesis

Transcripts from human endogenous retroviruses (HERVs) have been found to be the most stage-specific RNAs expressed during early human embryonic development [379], and there is intrinsic retroviral reactivation in human pre-implantation embryos and pluripotent stem cells [19,380]. Although functional studies are not possible in human embryos, direct functionality has been established for a retroviral RNA in mouse, where MuERV-L transcripts expressed just 8–10 h after fertilization at the 2-cell stage are necessary for developmental competence at the 4-cell stage but not afterwards [381].
HERVs and other mobile DNA elements are the major components of long non-coding lncRNAs, which play important roles in (re)programming embryonic and stem cell genomes (“83% of lncRNAs contain at least one TE (transposable element), while of the total number of base pairs that comprise lncRNA sequences, 42% is derived from TEs” [382]). These include the lincRNA ROR (“regulator of reprogramming”) beginning with a HERV-H transcript needed for formation of human induced pluripotent stem cells (HiPSCs) [383,384], plus LINC01108 (Linc-ES3) and human L1TD1 lncRNAs required to maintain stem cell pluripotency [385,386]. A recent genomic census of over 4000 human-specific binding sites for the transcription factors which reprogram HiPSCs remarkably found between 99.8% and 100% of the sites to be located in mobile DNA repeats [387].
There is a burgeoning literature relating mobile DNA to the evolution of ncRNA-based circuitry essential for mammalian (and, more specifically, human) stem cell and embryonic development [351,375,384,385,388,389,390,391,392,393,394]. The lncRNAs bind to and tether a variety of epigenetic modification complexes that execute genome reprogramming [18,395], and the mobile DNA element sequences in each molecule have been proposed to constitute a combinatorial code of RNA domains that link together different genome modification processes (Called the “RIDL hypothesis” for Repeat Insertion Domains of LncRNAs) [394]. In addition to lncRNAs, mobile DNA elements have also been documented to be sources for cell regulatory miRNAs [396,397,398,399].

10. A 21st Century Evolutionary Principle: Cell-Mediated Variation of Read–Write (RW) Genomes

To recapitulate, a genomics-based view of evolutionary variation introduces novel features to hereditary control of cell biology impossible to predict when Dobzhansky and other evolutionary biologists formulated the neo-Darwinian Modern Synthesis in the middle of the last century:
  • The existence of three distinct realms of cell evolution, Bacteria, Archaea and Eukarya;
  • Symbiogenetic fusions involving these different realms leading to the formation of eukaryotic cells bearing organelles with multiple genome compartments;
  • Horizontal organelle, virus and DNA transfers affecting adaptive traits across all cell types;
  • The functional organization of proteins as systems of distinct interacting domains encoded by exons and subject to rapid evolution by exon shuffling and exon origination from non-coding DNA (exonization);
  • Establishment of adaptive, distributed genome networks integrated by mobile DNA elements dispersing repetitive regulatory signals to multiple loci;
  • Regulation of cell differentiation in multicellular development by non-coding lncRNA molecules composed largely of mobile repetitive DNA elements that serve as scaffolds for epigenetic modifying activities.
Altogether, the combinatorial coding and regulatory aspects of cell heredity, plus the biochemical abilities cells possess to rearrange DNA molecules, constitute a powerful toolbox for adaptive genome rewriting. Revelations from genomic analysis oblige us to reconsider the simplifying assumptions made in the past two centuries about the nature of evolutionary variation. Rather than single gene traits, we recognize that all phenotypes involve coordinated activity by multiple interacting cell molecules. As summarized above, we have evidence that genomes contain abundant and functional repetitive components in addition to the unique coding sequences envisaged in the early days of molecular biology [12]. Instead of the “Constant Genome,” subject to accidental modification, we know today that cells possess “Read–Write Genomes” they can alter by numerous biochemical processes capable of rapidly restructuring cellular DNA molecules [6,8]. Genomics has modernized our understanding of the evolutionary process. Rather than viewing genome evolution as a happenstance series of copying errors, we are now in a position to study it as a complex biological process of active self-modification.


The author is grateful for the invitation to contribute this review and the opportunity it presented to formulate basic ideas about the status of evolution science.

Conflicts of Interest

The author declares no conflict of interest.


  1. Ayala, F.J. Nothing in biology makes sense except in the light of evolution: Theodosius Dobzhansky: 1900–1975. J. Hered. 1977, 68, 3–10. [Google Scholar] [PubMed]
  2. Dobzhansky, T. Nothing in biology makes sense except in the light of evolution. Am. Biol. Teach. 1973, 35, 125–129. [Google Scholar] [CrossRef]
  3. Watson, J.D.; Crick, F.H. Genetical implications of the structure of deoxyribonucleic acid. Nature 1953, 171, 964–967. [Google Scholar] [CrossRef] [PubMed]
  4. Alberts, B.; Johnson, A.; Lewis, J.; Raff, M.; Roberts, K.; Walter, P. Molecular Biology of the Cell; Garland Science: New York, NY, USA, 2002. [Google Scholar]
  5. Darwin, C. Origin of Species; John Russel: London, UK, 1859. [Google Scholar]
  6. Shapiro, J.A. Evolution: A View from the 21st Century; FT Press Science: Upper Saddle River, NJ, USA, 2011. [Google Scholar]
  7. Shapiro, J.A. Constraint and opportunity in genome innovation. RNA Biol. 2014, 11, 186–196. [Google Scholar] [CrossRef] [PubMed]
  8. Shapiro, J.A. How life changes itself: The Read-Write (RW) genome. Phys. Life Rev. 2013, 10, 287–323. [Google Scholar] [CrossRef] [PubMed]
  9. Gould, S.J. Punctuated equilibrium and the fossil record. Science 1983, 219, 439–440. [Google Scholar] [CrossRef] [PubMed]
  10. Shapiro, J.A. The basic concept of the read-write genome: Mini-review on cell-mediated DNA modification. Biosystems 2016, 140, 35–37. [Google Scholar] [CrossRef] [PubMed]
  11. Myers, R.M.; Stamatoyannopoulos, J.; Snyder, M.; Dunham, I.; Hardison, R.C.; Bernstein, B.E.; Gingeras, T.R.; Kent, W.J.; Birney, E.; Wold, B.; et al. A user’s guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 2011, 9, e1001046. [Google Scholar]
  12. Shapiro, J.A.; Sternberg, R.V. Why repetitive DNA is essential to genome function. Biol. Rev. Camb. Philos. Soc. 2005, 80, 227–250. [Google Scholar] [CrossRef]
  13. De Koning, A.P.; Gu, W.; Castoe, T.A.; Batzer, M.A.; Pollock, D.D. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet. 2011, 7, e1002384. [Google Scholar] [CrossRef] [PubMed]
  14. Wang, S.; Tran, E.J. Unexpected functions of lncRNAs in gene regulation. Commun. Integr. Biol. 2013, 6, e27610. [Google Scholar] [CrossRef] [PubMed]
  15. Huarte, M. LncRNAs have a say in protein translation. Cell Res. 2013, 23, 449–451. [Google Scholar] [CrossRef] [PubMed]
  16. Necsulea, A.; Soumillon, M.; Warnefors, M.; Liechti, A.; Daish, T.; Zeller, U.; Baker, J.C.; Grützner, F.; Kaessmann, H. The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 2014, 505, 635–640. [Google Scholar] [CrossRef] [PubMed]
  17. Guan, D.; Zhang, W.; Zhang, W.; Liu, G.H.; Belmonte, J.C. Switching cell fate, ncRNAs coming to play. Cell Death Dis. 2013, 4. [Google Scholar] [CrossRef] [PubMed]
  18. Guttman, M.; Donaghey, J.; Carey, B.W.; Garber, M.; Grenier, J.K.; Munson, G.; Young, G.; Lucas, A.B.; Ach, R.; Bruhn, L.; et al. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011, 477, 295–300. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  19. St Laurent, G.; Shtokalo, D.; Dong, B.; Tackett, M.R.; Fan, X.; Lazorthes, S.; Nicolas, E.; Sang, N.; Triche, T.J.; McCaffrey, T.A.; et al. VlincRNAs controlled by retroviral elements are a hallmark of pluripotency and cancer. Genome Biol. 2013, 14. [Google Scholar] [CrossRef] [PubMed]
  20. Carroll, S.B. Evo-devo and an expanding evolutionary synthesis: A genetic theory of morphological evolution. Cell 2008, 134, 25–36. [Google Scholar] [CrossRef] [PubMed]
  21. Prud’homme, B.; Gompel, N.; Carroll, S.B. Emerging principles of regulatory evolution. Proc. Natl. Acad. Sci. USA 2007, 104, 8605–8612. [Google Scholar] [CrossRef] [PubMed]
  22. Sogin, S.J.; Sogin, M.L.; Woese, C.R. Phylogenetic measurement in procaryotes by primary structural characterization. J. Mol. Evol. 1971, 1, 173–184. [Google Scholar] [CrossRef] [PubMed]
  23. Woese, C.R.; Fox, G.E. Phylogenetic structure of the prokaryotic domain: The primary kingdoms. Proc. Natl. Acad. Sci. USA 1977, 74, 5088–5090. [Google Scholar] [CrossRef] [PubMed]
  24. Woese, C.R.; Magrum, L.J.; Fox, G.E. Archaebacteria. J. Mol. Evol. 1978, 11, 245–251. [Google Scholar] [CrossRef] [PubMed]
  25. Kyrpides, N.C.; Woese, C.R. Universally conserved translation initiation factors. Proc. Natl. Acad. Sci. USA 1998, 95, 224–228. [Google Scholar] [CrossRef] [PubMed]
  26. Huxley, J. Evolution: The Modern Synthesis; Allen & Unwin: London, UK, 1942. [Google Scholar]
  27. Mayr, E. The Growth of Biological Thought: Diversity, Evolution, and Inheritance; Belknap Press: Cambridge, MA, USA, 1982. [Google Scholar]
  28. Albers, S.V.; Forterre, P.; Prangishvili, D.; Schleper, C. The legacy of Carl Woese and Wolfram Zillig: From phylogeny to landmark discoveries. Nat. Rev. Microbiol. 2013, 11, 713–719. [Google Scholar] [CrossRef] [PubMed]
  29. Sapp, J. The New Foundations of Evolution: On the Tree of Life; Oxford University Press: Oxford, UK, 2009. [Google Scholar]
  30. Woese, C.R. On the evolution of cells. Proc. Natl. Acad. Sci. USA 2002, 99, 8742–8747. [Google Scholar] [CrossRef] [PubMed]
  31. Woese, C.R. Archaebacteria. Sci. Am. 1981, 244, 98–122. [Google Scholar] [CrossRef]
  32. Margulis, L. Symbiosis in Cell Evolution; W.H. Freeman Co.: London, UK, 1981. [Google Scholar]
  33. Margulis, L. Symbiosis and evolution. Sci. Am. 1971, 225, 48–57. [Google Scholar] [CrossRef] [PubMed]
  34. Margulis, L.; Sagan, D. Acquiring Genomes: A Theory of the Origins of Species; Perseus Books Group: Amherst, MA, USA, 2002. [Google Scholar]
  35. Margulis, L. Origin of Eukaryotic Cells; Yale University Press: New Haven, CT, USA, 1970. [Google Scholar]
  36. Foster, P.G.; Cox, C.J.; Embley, T.M. The primary divisions of life: A phylogenomic approach employing composition-heterogeneous methods. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364, 2197–2207. [Google Scholar] [CrossRef] [PubMed]
  37. Embley, T.M.; Martin, W. Eukaryotic evolution, changes and challenges. Nature 2006, 440, 623–630. [Google Scholar] [CrossRef] [PubMed]
  38. Lithgow, T.; Schneider, A. Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010, 365, 799–817. [Google Scholar] [CrossRef] [PubMed]
  39. Shiflett, A.M.; Johnson, P.J. Mitochondrion-related organelles in eukaryotic protists. Ann. Rev. Microbiol. 2010, 64, 409–429. [Google Scholar] [CrossRef] [PubMed]
  40. Woese, C.R. Endosymbionts and mitochondrial origins. J. Mol. Evol. 1977, 10, 93–96. [Google Scholar] [CrossRef] [PubMed]
  41. Esser, C.; Ahmadinejad, N.; Wiegand, C.; Rotte, C.; Sebastiani, F.; Gelius-Dietrich, G.; Henze, K.; Kretschmann, E.; Richly, E.; Leister, D.; et al. A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol. Biol. Evol. 2004, 21, 1643–1660. [Google Scholar] [CrossRef] [PubMed]
  42. Vesteg, M.; Krajcovic, J. Origin of eukaryotic cells as a symbiosis of parasitic alpha-proteobacteria in the periplasm of two-membrane-bounded sexual pre-karyotes. Commun. Integr. Biol. 2008, 1, 104–113. [Google Scholar] [CrossRef] [PubMed]
  43. Zablen, L.B.; Kissil, M.S.; Woese, C.R.; Buetow, D.E. Phylogenetic origin of the chloroplast and prokaryotic nature of its ribosomal RNA. Proc. Natl. Acad. Sci. USA 1975, 72, 2418–2422. [Google Scholar] [CrossRef] [PubMed]
  44. Bonen, L.; Doolittle, W.F. On the prokaryotic nature of red algal chloroplasts. Proc. Natl. Acad. Sci. USA 1975, 72, 2310–2314. [Google Scholar] [CrossRef] [PubMed]
  45. Green, B.R. Chloroplast genomes of photosynthetic eukaryotes. Plant J. 2011, 66, 34–44. [Google Scholar] [CrossRef] [PubMed]
  46. Cavalier-Smith, T. Chloroplast evolution: Secondary symbiogenesis and multiple losses. Curr. Biol. 2002, 12, R62–R64. [Google Scholar] [CrossRef]
  47. Krause, K. From chloroplasts to “cryptic” plastids: Evolution of plastid genomes in parasitic plants. Curr. Genet. 2008, 54, 111–121. [Google Scholar] [CrossRef] [PubMed]
  48. Thorsness, P.E.; Fox, T.D. Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Nature 1990, 346, 376–379. [Google Scholar] [CrossRef] [PubMed]
  49. Hazkani-Covo, E. Mitochondrial insertions into primate nuclear genomes suggest the use of numts as a tool for phylogeny. Mol. Biol. Evol. 2009, 26, 2175–2179. [Google Scholar] [CrossRef] [PubMed]
  50. Bachtrog, D.; Hornton, K.; Clark, A.; Andolfatto, P. Extensive introgression of mitochondrial DNA relative to nuclear genes in the Drosophila yakuba species group. Evolution 2006, 60, 292–302. [Google Scholar] [CrossRef] [PubMed]
  51. Adams, K.L.; Qiu, Y.L.; Stoutemyer, M.; Palmer, J.D. Punctuated evolution of mitochondrial gene content: High and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc. Natl. Acad. Sci. USA 2002, 99, 9905–9912. [Google Scholar] [CrossRef] [PubMed]
  52. Stegemann, S.; Hartmann, S.; Ruf, S.; Bock, R. High-frequency gene transfer from the chloroplast genome to the nucleus. Proc. Natl. Acad. Sci. USA 2003, 100, 8828–8833. [Google Scholar] [CrossRef] [PubMed]
  53. Rousseau-Gueutin, M.; Ayliffe, M.A.; Timmis, J.N. Conservation of plastid sequences in the plant nuclear genome for millions of years facilitates endosymbiotic evolution. Plant Physiol. 2011, 157, 2181–2193. [Google Scholar] [CrossRef] [PubMed]
  54. Keeling, P.J. The endosymbiotic origin, diversification and fate of plastids. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010, 365, 729–748. [Google Scholar] [CrossRef] [PubMed]
  55. Bock, R.; Timmis, J.N. Reconstructing evolution: Gene transfer from plastids to the nucleus. Bioessays 2008, 30, 556–566. [Google Scholar] [CrossRef] [PubMed]
  56. Ricchetti, M.; Tekaia, F.; Dujon, B. Continued colonization of the human genome by mitochondrial DNA. PLoS Biol. 2004, 2, e273. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  57. Lloyd, A.H.; Timmis, J.N. Endosybiotic evolution in action: Real-time observations of chloroplast to nucleus gene transfer. Mob. Genet. Elem. 2011, 1, 216–220. [Google Scholar] [CrossRef] [PubMed]
  58. Huang, C.Y.; Ayliffe, M.A.; Timmis, J.N. Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 2003, 422, 72–76. [Google Scholar] [CrossRef] [PubMed]
  59. Cullis, C.A.; Vorster, B.J.; van der Vyver, C.; Kunert, K.J. Transfer of genetic material between the chloroplast and nucleus: How is it related to stress in plants? Ann. Bot. 2009, 103, 625–633. [Google Scholar] [CrossRef] [PubMed]
  60. Roark, L.M.; Hui, A.Y.; Donnelly, L.; Birchler, J.A.; Newton, K.J. Recent and frequent insertions of chloroplast DNA into maize nuclear chromosomes. Cytogenet. Genome Res. 2010, 129, 17–23. [Google Scholar] [CrossRef] [PubMed]
  61. Cheng, X.; Ivessa, A.S. The migration of mitochondrial DNA fragments to the nucleus affects the chronological aging process of Saccharomyces cerevisiae. Aging Cell 2010, 9, 919–923. [Google Scholar] [CrossRef] [PubMed]
  62. Caro, P.; Gómez, J.; Arduini, A.; González-Sánchez, M.; González-García, M.; Borrás, C.; Viña, J.; Puertas, M.J.; Sastre, J.; Barja, G. Mitochondrial DNA sequences are present inside nuclear DNA in rat tissues and increase with age. Mitochondrion 2010, 10, 479–486. [Google Scholar] [CrossRef] [PubMed]
  63. Hazkani-Covo, E.; Zeller, R.M.; Martin, W. Molecular poltergeists: Mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet. 2010, 6, e1000834. [Google Scholar] [CrossRef] [PubMed]
  64. Ju, Y.S.; Tubio, J.M.; Mifsud, W.; Fu, B.; Davies, H.R.; Ramakrishna, M.; Li, Y.; Yates, L.; Gundem, G.; Tarpey, P.S.; et al. Frequent somatic transfer of mitochondrial DNA into the nuclear genome of human cancer cells. Genome Res. 2015, 25, 814–824. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Ricchetti, M.; Fairhead, C.; Dujon, B. Mitochondrial DNA repairs double-strand breaks in yeast chromosomes. Nature 1999, 402, 96–100. [Google Scholar] [CrossRef] [PubMed]
  66. Rodriguez-Moreno, L.; González, V.M.; Benjak, A.; Martí, M.C.; Puigdomènech, P.; Aranda, M.A.; Garcia-Mas, J. Determination of the melon chloroplast and mitochondrial genome sequences reveals that the largest reported mitochondrial genome in plants contains a significant amount of DNA having a nuclear origin. BMC Genom. 2011, 12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  67. Pietrokovski, S.; Trifonov, E.N. Imported sequences in the mitochondrial yeast genome identified by nucleotide linguistics. Gene 1992, 122, 129–137. [Google Scholar] [CrossRef]
  68. Adams, K.L.; Daley, D.O.; Whelan, J.; Palmer, J.D. Genes for two mitochondrial ribosomal proteins in flowering plants are derived from their chloroplast or cytosolic counterparts. Plant Cell 2002, 14, 931–943. [Google Scholar] [CrossRef] [PubMed]
  69. Koulintchenko, M.; Konstantinov, Y.; Dietrich, A. Plant mitochondria actively import DNA via the permeability transition pore complex. EMBO J. 2003, 22, 1245–1254. [Google Scholar] [CrossRef] [PubMed]
  70. Nozaki, H.; Matsuzaki, M.; Takahara, M.; Misumi, O.; Kuroiwa, H.; Hasegawa, M.; Shin-i, T.; Kohara, Y.; Ogasawara, N.; Kuroiwa, T. The phylogenetic position of red algae revealed by multiple nuclear genes from mitochondria-containing eukaryotes and an alternative hypothesis on the origin of plastids. J. Mol. Evol. 2003, 56, 485–497. [Google Scholar] [CrossRef] [PubMed]
  71. Jeyaprakash, A.; Hoy, M.A. First divergence time estimate of spiders, scorpions, mites and ticks (subphylum: Chelicerata) inferred from mitochondrial phylogeny. Exp. Appl. Acarol. 2009, 47, 1–18. [Google Scholar] [CrossRef] [PubMed]
  72. Bullerwell, C.E.; Gray, M.W. Evolution of the mitochondrial genome: Protist connections to animals, fungi and plants. Curr. Opin. Microbiol. 2004, 7, 528–534. [Google Scholar] [CrossRef] [PubMed]
  73. Burger, G.; Gray, M.W.; Lang, B.F. Mitochondrial genomes: Anything goes. Trends Genet. 2003, 19, 709–716. [Google Scholar] [CrossRef] [PubMed]
  74. Gray, M.W.; Lang, B.F.; Burger, G. Mitochondria of protists. Ann. Rev. Genet. 2004, 38, 477–524. [Google Scholar] [CrossRef] [PubMed]
  75. Gray, M.W.; Burger, G.; Lang, B.F. The origin and early evolution of mitochondria. Genome Biol. 2001, 2. [Google Scholar] [CrossRef]
  76. Gray, M.W.; Burger, G.; Lang, B.F. Mitochondrial evolution. Science 1999, 283, 1476–1481. [Google Scholar] [CrossRef] [PubMed]
  77. Sanchez-Puerta, M.V.; Cho, Y.; Mower, J.P.; Alverson, A.J.; Palmer, J.D. Frequent, phylogenetically local horizontal transfer of the cox1 group I Intron in flowering plant mitochondria. Mol. Biol. Evol. 2008, 25, 1762–1777. [Google Scholar] [CrossRef] [PubMed]
  78. Hikosaka, K.; Watanabe, Y.; Tsuji, N.; Kita, K.; Kishine, H.; Arisue, N.; Palacpac, N.M.; Kawazu, S.; Sawai, H.; Horii, T.; et al. Divergence of the mitochondrial genome structure in the apicomplexan parasites, Babesia and Theileria. Mol. Biol. Evol. 2010, 27, 1107–1116. [Google Scholar] [CrossRef] [PubMed]
  79. Hikosaka, K.; Watanabe, Y.; Kobayashi, F.; Waki, S.; Kita, K.; Tanabe, K. Highly conserved gene arrangement of the mitochondrial genomes of 23 Plasmodium species. Parasitol. Int. 2011, 60, 175–180. [Google Scholar] [CrossRef] [PubMed]
  80. Valach, M.; Farkas, Z.; Fricova, D.; Kovac, J.; Brejova, B.; Vinar, T.; Pfeiffer, I.; Kucsera, J.; Tomaska, L.; Lang, B.F.; et al. Evolution of linear chromosomes and multipartite genomes in yeast mitochondria. Nucleic Acids Res. 2011, 39, 4202–4219. [Google Scholar] [CrossRef] [PubMed]
  81. Smith, D.R.; Kayal, E.; Yanagihara, A.A.; Collins, A.G.; Pirro, S.; Keeling, P.J. First complete mitochondrial genome sequence from a box jellyfish reveals a highly fragmented linear architecture and insights into telomere evolution. Genome Biol. Evol. 2012, 4, 52–58. [Google Scholar] [CrossRef] [PubMed]
  82. Kayal, E.; Bentlage, B.; Collins, A.G.; Kayal, M.; Pirro, S.; Lavrov, D.V. Evolution of linear mitochondrial genomes in medusozoan cnidarians. Genome Biol. Evol. 2012, 4, 1–12. [Google Scholar] [CrossRef] [PubMed]
  83. Sloan, D.B.; Alverson, A.J.; Chuckalovcak, J.P.; Wu, M.; McCauley, D.E.; Palmer, J.D.; Taylor, D.R. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 2012, 10, e1001241. [Google Scholar] [CrossRef] [PubMed]
  84. Sloan, D.B.; Alverson, A.J.; Wu, M.; Palmer, J.D.; Taylor, D.R. Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus Silene. Genome Biol. Evol. 2012, 4, 294–306. [Google Scholar] [CrossRef] [PubMed]
  85. Hjort, K.; Goldberg, A.V.; Tsaousis, A.D.; Hirt, R.P.; Embley, T.M. Diversity and reductive evolution of mitochondria among microbial eukaryotes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010, 365, 713–727. [Google Scholar] [CrossRef] [PubMed]
  86. Marande, W.; Lukes, J.; Burger, G. Unique mitochondrial genome structure in diplonemids, the sister group of kinetoplastids. Eukaryot. Cell 2005, 4, 1137–1146. [Google Scholar] [CrossRef] [PubMed]
  87. Brown, W.M.; George, M., Jr.; Wilson, A.C. Rapid evolution of animal mitochondrial DNA. Proc. Natl. Acad. Sci. USA 1979, 76, 1967–1971. [Google Scholar] [CrossRef] [PubMed]
  88. Embley, T.M. Multiple secondary origins of the anaerobic lifestyle in eukaryotes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361, 1055–1067. [Google Scholar] [CrossRef] [PubMed]
  89. Van der Giezen, M. Hydrogenosomes and mitosomes: Conservation and evolution of functions. J. Eukaryot. Microbiol. 2009, 56, 221–231. [Google Scholar] [CrossRef] [PubMed]
  90. Hackstein, J.H.; Tjaden, J.; Huynen, M. Mitochondria, hydrogenosomes and mitosomes: Products of evolutionary tinkering! Curr. Genet. 2006, 50, 225–245. [Google Scholar] [CrossRef] [PubMed]
  91. Brouard, J.S.; Otis, C.; Lemieux, C.; Turmel, M. The exceptionally large chloroplast genome of the green alga Floydiella terrestris illuminates the evolutionary history of the Chlorophyceae. Genome Biol. Evol. 2010, 2, 240–256. [Google Scholar] [CrossRef] [PubMed]
  92. Magee, A.M.; Aspinall, S.; Rice, D.W.; Cusack, B.P.; Sémon, M.; Perry, A.S.; Stefanović, S.; Milbourne, D.; Barth, S.; Palmer, J.D.; et al. Localized hypermutation and associated gene losses in legume chloroplast genomes. Genome Res. 2010, 20, 1700–1710. [Google Scholar] [CrossRef] [PubMed]
  93. Wu, C.S.; Lin, C.P.; Hsu, C.Y.; Wang, R.J.; Chaw, S.M. Comparative chloroplast genomes of pinaceae: Insights into the mechanism of diversified genomic organizations. Genome Biol. Evol. 2011, 3, 309–319. [Google Scholar] [CrossRef] [PubMed]
  94. Wolf, P.G.; Der, J.P.; Duffy, A.M.; Davidson, J.B.; Grusz, A.L.; Pryer, K.M. The evolution of chloroplast genes and genomes in ferns. Plant Mol. Biol. 2011, 76, 251–261. [Google Scholar] [CrossRef] [PubMed]
  95. Reyes-Prieto, A.; Yoon, H.S.; Moustafa, A.; Yang, E.C.; Andersen, R.A.; Boo, S.M.; Nakayama, T.; Ishida, K.I.; Bhattacharya, D. Differential gene retention in plastids of common recent origin. Mol. Biol. Evol. 2010, 27, 1530–1537. [Google Scholar] [CrossRef] [PubMed]
  96. Gould, S.B.; Waller, R.F.; McFadden, G.I. Plastid evolution. Ann. Rev. Plant Biol. 2008, 59, 491–517. [Google Scholar] [CrossRef] [PubMed]
  97. Smith, D.R.; Lee, R.W. A plastid without a genome: Evidence from the nonphotosynthetic green alga Polytomella. Plant Physiol. 2014, 164, 1812–1819. [Google Scholar] [CrossRef] [PubMed]
  98. Stiller, J.W.; Huang, J.; Ding, Q.; Tian, J.; Goodwillie, C. Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses? BMC Genom. 2009, 10. [Google Scholar] [CrossRef] [PubMed]
  99. Revill, M.J.; Stanley, S.; Hibberd, J.M. Plastid genome structure and loss of photosynthetic ability in the parasitic genus Cuscuta. J. Exp. Bot. 2005, 56, 2477–2486. [Google Scholar] [CrossRef] [PubMed]
  100. Barbrook, A.C.; Howe, C.J.; Purton, S. Why are plastid genomes retained in non-photosynthetic organisms? Trends Plant Sci. 2006, 11, 101–108. [Google Scholar] [CrossRef] [PubMed]
  101. Baurain, D.; Brinkmann, H.; Petersen, J.; Rodríguez-Ezpeleta, N.; Stechmann, A.; Demoulin, V.; Roger, A.J.; Burger, G.; Lang, B.F.; Philippe, H. Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol. Biol. Evol. 2010, 27, 1698–1709. [Google Scholar] [CrossRef] [PubMed]
  102. Keeling, P.J. Chromalveolates and the evolution of plastids by secondary endosymbiosis. J. Eukaryot. Microbiol. 2009, 56, 1–8. [Google Scholar] [CrossRef] [PubMed]
  103. Archibald, J.M. Plastid evolution: Remnant algal genes in ciliates. Curr. Biol. 2008, 18, R663–R665. [Google Scholar] [CrossRef] [PubMed]
  104. Kutschera, U.; Niklas, K.J. Macroevolution via secondary endosymbiosis: A Neo-Goldschmidtian view of unicellular hopeful monsters and Darwin’s primordial intermediate form. Theory Biosci. 2008, 127, 277–289. [Google Scholar] [CrossRef] [PubMed]
  105. Zauner, S.; Lockhart, P.; Stoebe-Maier, B.; Gilson, P.; McFadden, G.I.; Maier, U.G. Differential gene transfers and gene duplications in primary and secondary endosymbioses. BMC Evol. Biol. 2006, 6. [Google Scholar] [CrossRef] [PubMed]
  106. Janouškovec, J.; Horák, A.; Oborník, M.; Lukeš, J.; Keeling, P.J. A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc. Natl. Acad. Sci. USA 2010, 107, 10949–10954. [Google Scholar] [CrossRef] [PubMed]
  107. Moore, C.E.; Archibald, J.M. Nucleomorph genomes. Ann. Rev. Genet. 2009, 43, 251–264. [Google Scholar] [CrossRef] [PubMed]
  108. Silver, T.D.; Koike, S.; Yabuki, A.; Kofuji, R.; Archibald, J.M.; Ishida, K.I. Phylogeny and nucleomorph karyotype diversity of chlorarachniophyte algae. J. Eukaryot. Microbiol. 2007, 54, 403–410. [Google Scholar] [CrossRef] [PubMed]
  109. Archibald, J.M. Nucleomorph genomes: Structure, function, origin and evolution. Bioessays 2007, 29, 392–402. [Google Scholar] [CrossRef] [PubMed]
  110. Maruyama, S.; Sugahara, J.; Kanai, A.; Nozaki, H. Permuted tRNA genes in the nuclear and nucleomorph genomes of photosynthetic eukaryotes. Mol. Biol. Evol. 2010, 27, 1070–1076. [Google Scholar] [CrossRef] [PubMed]
  111. Curtis, B.A.; Tanifuji, G.; Burki, F.; Gruber, A.; Irimia, M.; Maruyama, S.; Arias, M.C.; Ball, S.G.; Gile, G.H.; Hirakawa, Y.; et al. Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 2012, 492, 59–65. [Google Scholar] [CrossRef] [PubMed]
  112. Moore, C.E.; Curtis, B.; Mills, T.; Tanifuji, G.; Archibald, J.M. Nucleomorph genome sequence of the cryptophyte alga Chroomonas mesostigmatica CCMP1168 reveals lineage-specific gene loss and genome complexity. Genome Biol. Evol. 2012, 4, 1162–1175. [Google Scholar] [CrossRef] [PubMed]
  113. Cavalier-Smith, T. Nucleomorphs: Enslaved algal nuclei. Curr. Opin. Microbiol. 2002, 5, 612–619. [Google Scholar] [CrossRef]
  114. Trench, R.K.; Greene, R.W.; Bystrom, B.G. Chloroplasts as functional organelles in animal tissues. J. Cell Biol. 1969, 42, 404–417. [Google Scholar] [CrossRef] [PubMed]
  115. Händeler, K.; Grzymbowski, Y.P.; Krug, P.J.; Wägele, H. Functional chloroplasts in metazoan cells—A unique evolutionary strategy in animal life. Front. Zool. 2009, 6. [Google Scholar] [CrossRef] [PubMed]
  116. Serôdio, J.; Cruz, S.; Cartaxana, P.; Calado, R. Photophysiology of kleptoplasts: Photosynthetic use of light by chloroplasts living in animal cells. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014, 369. [Google Scholar] [CrossRef] [PubMed]
  117. Pierce, S.K.; Curtis, N.E. Cell biology of the chloroplast symbiosis in sacoglossan sea slugs. Int. Rev. Cell Mol. Biol. 2012, 293, 123–148. [Google Scholar] [PubMed]
  118. Baumgartner, F.A.; Pavia, H.; Toth, G.B. Acquired phototrophy through retention of functional chloroplasts increases growth efficiency of the sea slug Elysia viridis. PLoS ONE 2015, 10, e0120874. [Google Scholar] [CrossRef] [PubMed]
  119. Wägele, H.; Deusch, O.; Händeler, K.; Martin, R.; Schmitt, V.; Christa, G.; Pinzger, B.; Gould, S.B.; Dagan, T.; Klussmann-Kolb, A.; et al. Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes. Mol. Biol. Evol. 2011, 28, 699–706. [Google Scholar] [CrossRef] [PubMed]
  120. Muscatine, L.; Greene, R.W. Chloroplasts and algae as symbionts in molluscs. Int. Rev. Cytol. 1973, 36, 137–169. [Google Scholar] [PubMed]
  121. Green, B.J.; Li, W.Y.; Manhart, J.R.; Fox, T.C.; Summer, E.J.; Kennedy, R.A.; Pierce, S.K.; Rumpho, M.E. Mollusc-algal chloroplast endosymbiosis. Photosynthesis, thylakoid protein maintenance, and chloroplast gene expression continue for many months in the absence of the algal nucleus. Plant Physiol. 2000, 124, 331–342. [Google Scholar] [CrossRef] [PubMed]
  122. Gomez, F.; Lopez-Garcia, P.; Moreira, D. Molecular phylogeny of the ocelloid-bearing dinoflagellates Erythropsidinium and Warnowia (warnowiaceae, dinophyceae). J. Eukaryot. Microbiol. 2009, 56, 440–445. [Google Scholar] [CrossRef] [PubMed]
  123. Hoppenrath, M.; Bachvaroff, T.R.; Handy, S.M.; Delwiche, C.F.; Leander, B.S. Molecular phylogeny of ocelloid-bearing dinoflagellates (Warnowiaceae) as inferred from SSU and LSU rDNA sequences. BMC Evol. Biol. 2009, 9. [Google Scholar] [CrossRef] [PubMed]
  124. Gavelis, G.S.; Hayakawa, S.; White, R.A., III; Gojobori, T.; Suttle, C.A.; Keeling, P.J.; Leander, B.S. Eye-like ocelloids are built from different endosymbiotically acquired components. Nature 2015, 523, 204–207. [Google Scholar] [CrossRef] [PubMed]
  125. Hulse, J.H.; Spurgeon, D. Triticale. Sci. Am. 1974, 231, 72–80. [Google Scholar] [CrossRef]
  126. Bento, M.; Gustafson, P.; Viegas, W.; Silva, M. Genome merger: From sequence rearrangements in triticale to their elimination in wheat-rye addition lines. Theor. Appl. Genet. 2010, 121, 489–497. [Google Scholar] [CrossRef] [PubMed]
  127. Bento, M.; Pereira, H.S.; Rocheta, M.; Gustafson, P.; Viegas, W.; Silva, M. Polyploidization as a retraction force in plant genome evolution: Sequence rearrangements in triticale. PLoS ONE 2008, 3, e1402. [Google Scholar] [CrossRef] [PubMed]
  128. Bento, M.; Gustafson, J.P.; Viegas, W.; Silva, M. Size matters in Triticeae polyploids: Larger genomes have higher remodeling. Genome 2011, 54, 175–183. [Google Scholar] [PubMed]
  129. Anderson, E.; Stebbins, G.L., Jr. Hybridization as an evolutionary stimulus. Evolution 1954, 8, 378–388. [Google Scholar] [CrossRef]
  130. Stebbins, G.L. Cataclysmic Evolution. Sci. Am. 1951, 184, 54–59. [Google Scholar] [CrossRef]
  131. Ungerer, M.C.; Baird, S.J.; Pan, J.; Rieseberg, L.H. Rapid hybrid speciation in wild sunflowers. Proc. Natl. Acad. Sci. USA 1998, 95, 11757–11762. [Google Scholar] [CrossRef] [PubMed]
  132. Fuentes, I.; Stegemann, S.; Golczyk, H.; Karcher, D.; Bock, R. Horizontal genome transfer as an asexual path to the formation of new species. Nature 2014, 511, 232–235. [Google Scholar] [CrossRef] [PubMed]
  133. Véron, A.S.; Lemaitre, C.; Gautier, C.; Lacroix, V.; Sagot, M.F. Close 3D proximity of evolutionary breakpoints argues for the notion of spatial synteny. BMC Genom. 2011, 12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  134. Catchen, J.M.; Conery, J.S.; Postlethwait, J.H. Automated identification of conserved synteny after whole-genome duplication. Genome Res. 2009, 19, 1497–1505. [Google Scholar] [CrossRef] [PubMed]
  135. Tang, H. Synteny and collinearity in plant genomes. Science 2008, 320, 486–488. [Google Scholar] [CrossRef] [PubMed]
  136. Wolfe, K.H.; Shields, D.C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 1997, 387, 708–713. [Google Scholar] [CrossRef] [PubMed]
  137. Wolfe, K.H. Origin of the yeast whole-genome duplication. PLoS Biol. 2015, 13, e1002221. [Google Scholar] [CrossRef] [PubMed]
  138. Marcet-Houben, M.; Gabaldon, T. Beyond the whole-genome duplication: Phylogenetic evidence for an ancient interspecies hybridization in the baker’s yeast lineage. PLoS Biol. 2015, 13, e1002220. [Google Scholar] [CrossRef] [PubMed]
  139. Albertin, W.; Marullo, P. Polyploidy in fungi: Evolution after whole-genome duplication. Proc. Biol. Sci. 2012, 279, 2497–2509. [Google Scholar] [CrossRef] [PubMed]
  140. Aury, J.M. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 2006, 444, 171–178. [Google Scholar] [CrossRef] [PubMed]
  141. De Bodt, S.; Maere, S.; van de Peer, Y. Genome duplication and the origin of angiosperms. Trends Ecol. Evol. 2005, 20, 591–597. [Google Scholar] [CrossRef] [PubMed]
  142. Cui, L. Widespread genome duplications throughout the history of flowering plants. Genome Res. 2006, 16, 738–749. [Google Scholar] [CrossRef] [PubMed]
  143. Dehal, P.; Boore, J.L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 2005, 3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  144. Kasahara, M.; Naruse, K.; Sasaki, S.; Nakatani, Y.; Qu, W.; Ahsan, B.; Yamada, T.; Nagayasu, Y.; Doi, K.; Kasai, Y.; et al. The medaka draft genome and insights into vertebrate genome evolution. Nature 2007, 447, 714–719. [Google Scholar] [CrossRef] [PubMed]
  145. Kasahara, M. The 2R hypothesis: An update. Curr. Opin. Immunol. 2007, 19, 547–552. [Google Scholar] [CrossRef] [PubMed]
  146. Donoghue, P.C.J.; Purnell, M.A. Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 2005, 20, 312–319. [Google Scholar] [CrossRef] [PubMed]
  147. Hughes, T.; Liberles, D.A. Whole-genome duplications in the ancestral vertebrate are detectable in the distribution of gene family sizes of tetrapod species. J. Mol. Evol. 2008, 67, 343–357. [Google Scholar] [CrossRef] [PubMed]
  148. Meyer, A.; van de Peer, Y. From 2R to 3R: Evidence for a fish-specific genome duplication (FSGD). Bioessays 2005, 27, 937–945. [Google Scholar] [CrossRef] [PubMed]
  149. Glasauer, S.M.; Neuhauss, S.C. Whole-genome duplication in teleost fishes and its evolutionary consequences. Mol. Genet. Genom. 2014, 289, 1045–1060. [Google Scholar] [CrossRef] [PubMed]
  150. Metcalfe, C.J.; Bulazel, K.V.; Ferreri, G.C.; Schroeder-Reiter, E.; Wanner, G.; Rens, W.; Obergfell, C.; Eldridge, M.D.; O’Neill, R.J. Genomic instability within centromeres of interspecific marsupial hybrids. Genetics 2007, 177, 2507–2517. [Google Scholar] [CrossRef] [PubMed]
  151. Marfil, C.F.; Masuelli, R.W.; Davison, J.; Comai, L. Genomic instability in Solanum tuberosum × Solanum kurtzianum interspecific hybrids. Genome 2006, 49, 104–113. [Google Scholar] [PubMed]
  152. Han, F.P.; Fedak, G.; Ouellet, T.; Liu, B. Rapid genomic changes in interspecific and intergeneric hybrids and allopolyploids of Triticeae. Genome 2003, 46, 716–723. [Google Scholar] [CrossRef] [PubMed]
  153. King, M. Species Evolution: The Role of Chromosome Change; Cambridge University Press: Cambridge, UK, 1995. [Google Scholar]
  154. White, M.J. Chromosomes of the vertebrates. Evolution 1949, 3, 379–381. [Google Scholar] [CrossRef] [PubMed]
  155. Nie, W.; Wang, J.; Su, W.; Wang, D.; Tanomtong, A.; Perelman, P.L.; Graphodatsky, A.S.; Yang, F. Chromosomal rearrangements and karyotype evolution in carnivores revealed by chromosome painting. Heredity 2012, 108, 17–27. [Google Scholar] [CrossRef] [PubMed]
  156. Lim, J.K.; Simmons, M.J. Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. Bioessays 1994, 16, 269–275. [Google Scholar] [CrossRef] [PubMed]
  157. Mieczkowski, P.A.; Lemoine, F.J.; Petes, T.D. Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA Repair 2006, 5, 1010–1020. [Google Scholar] [CrossRef] [PubMed]
  158. Lonnig, W.E.; Saedler, H. Chromosome rearrangements and transposable elements. Ann. Rev Genet. 2002, 36, 389–410. [Google Scholar] [CrossRef] [PubMed]
  159. Zhang, J.; Yu, C.; Krishnaswamy, L.; Peterson, T. Transposable elements as catalysts for chromosome rearrangements. Methods Mol. Biol. 2011, 701, 315–326. [Google Scholar] [PubMed]
  160. Carbone, L.; Harris, R.A.; Gnerre, S.; Veeramah, K.R.; Lorente-Galdos, B.; Huddleston, J.; Meyer, T.J.; Herrero, J.; Roos, C.; Aken, B.; et al. Gibbon genome and the fast karyotype evolution of small apes. Nature 2014, 513, 195–201. [Google Scholar] [CrossRef] [PubMed]
  161. Syvanen, M.; Kado, C.I. Horizontal Gene Transfer, 2nd ed.; Academic Press: London, UK, 2002. [Google Scholar]
  162. Syvanen, M. Evolutionary implications of horizontal gene transfer. Ann. Rev. Genet. 2012, 46, 341–358. [Google Scholar] [CrossRef] [PubMed]
  163. Watanabe, T. Infectious drug resistance. Sci. Am. 1967, 217, 19–28. [Google Scholar] [CrossRef] [PubMed]
  164. Watanabe, T. Infective heredity of multiple drug resistance in bacteria. Bacteriol. Rev. 1963, 27, 87–115. [Google Scholar] [PubMed]
  165. Andam, C.P.; Fournier, G.P.; Gogarten, J.P. Multilevel populations and the evolution of antibiotic resistance through horizontal gene transfer. FEMS Microbiol. Rev. 2011, 35, 756–767. [Google Scholar] [CrossRef] [PubMed]
  166. Hastings, P.J.; Rosenberg, S.M.; Slack, A. Antibiotic-induced lateral transfer of antibiotic resistance. Trends Microbiol. 2004, 12, 401–404. [Google Scholar] [CrossRef] [PubMed]
  167. Hayes, W. The Genetics of Bacteria and Their Viruses, 2nd ed.; Blackwell: London, UK, 1968. [Google Scholar]
  168. DNA Insertion Elements, Plasmids and Episomes; Bukhari, A.I.; Shapiro, J.A.; Adhya, S.L. (Eds.) Cold Spring Harbor Press: Cold Spring Harbor, New York, NY, USA, 1977.
  169. Daccord, A.; Ceccarelli, D.; Rodrigue, S.; Burrus, V. Comparative analysis of mobilizable genomic islands. J. Bacteriol. 2013, 195, 606–614. [Google Scholar] [CrossRef] [PubMed]
  170. Bellanger, X.; Payot, S.; Leblond-Bourget, N.; Guédon, G. Conjugative and mobilizable genomic islands in bacteria: Evolution and diversity. FEMS Microbiol. Rev. 2014, 38, 720–760. [Google Scholar] [CrossRef] [PubMed]
  171. Makarova, K.S.; Wolf, Y.I.; Snir, S.; Koonin, E.V. Defense islands in bacterial and archaeal genomes and prediction of novel defense systems. J. Bacteriol. 2011, 193, 6039–6056. [Google Scholar] [CrossRef] [PubMed]
  172. Van der Meer, J.R.; Sentchilo, V. Genomic islands and the evolution of catabolic pathways in bacteria. Curr. Opin. Biotechnol. 2003, 14, 248–254. [Google Scholar] [CrossRef]
  173. Hall, R.M. Integrons and gene cassettes: Hotspots of diversity in bacterial genomes. Ann. N.Y. Acad. Sci. 2012, 1267, 71–78. [Google Scholar] [CrossRef] [PubMed]
  174. Rowe-Magnus, D.A.; Mazel, D. The role of integrons in antibiotic resistance gene capture. Int. J. Med. Microbiol. 2002, 292, 115–125. [Google Scholar] [CrossRef] [PubMed]
  175. Rowe-Magnus, D.A.; Guérout, A.M.; Mazel, D. Super-integrons. Res. Microbiol. 1999, 150, 641–651. [Google Scholar] [CrossRef]
  176. Fluit, A.C.; Schmitz, F.J. Resistance integrons and super-integrons. Clin. Microbiol. Infect. 2004, 10, 272–288. [Google Scholar] [CrossRef] [PubMed]
  177. Escudero, J.A.; Loot, C.; Nivina, A.; Mazel, D. The integron: Adaptation on demand. Microbiol. Spectr. 2015, 3. [Google Scholar] [CrossRef] [PubMed]
  178. Rapa, R.A.; Labbate, M. The function of integron-associated gene cassettes in Vibrio species: The tip of the iceberg. Front. Microbiol. 2013, 4. [Google Scholar] [CrossRef] [PubMed]
  179. Sclafani, R.A. Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends Genet. 1998, 14, 442–444. [Google Scholar]
  180. Nelson-Sathi, S.; Sousa, F.L.; Roettger, M.; Lozada-Chávez, N.; Thiergart, T.; Janssen, A.; Bryant, D.; Landan, G.; Schönheit, P.; Siebers, B.; et al. Origins of major archaeal clades correspond to gene acquisitions from bacteria. Nature 2015, 517, 77–80. [Google Scholar] [CrossRef] [PubMed]
  181. Dodsworth, J.A.; Li, L.; Wei, S.; Hedlund, B.P.; Leigh, J.A.; de Figueiredo, P. Inter-domain conjugal transfer of DNA from bacteria to archaea. Appl. Environ. Microbiol. 2010, 76, 5644–5647. [Google Scholar] [CrossRef] [PubMed]
  182. Faguy, D.M.; Doolittle, W.F. Horizontal transfer of catalase-peroxidase genes between archaea and pathogenic bacteria. Trends Genet. 2000, 16, 196–197. [Google Scholar] [CrossRef]
  183. Koonin, E.V.; Wolf, Y.I. Genomics of bacteria and archaea: The emerging dynamic view of the prokaryotic world. Nucleic Acids Res. 2008, 36, 6688–6719. [Google Scholar] [CrossRef] [PubMed]
  184. Sonea, S.; Mathieu, L.G. Evolution of the genomic systems of prokaryotes and its momentous consequences. Int. Microbiol. 2001, 4, 67–71. [Google Scholar] [PubMed]
  185. Sonea, S.; Panisset, M. A New Bacteriology; Jones and Batlett: Boston, MA, USA, 1983. [Google Scholar]
  186. Sonea, S. A tentative unifying view of bacteria. Rev. Can. Biol. 1971, 30, 239–244. [Google Scholar] [PubMed]
  187. Sharon, I.; Battchikova, N.; Aro, E.M.; Giglione, C.; Meinnel, T.; Glaser, F.; Pinter, R.Y.; Breitbart, M.; Rohwer, F.; Béjà, O. Comparative metagenomics of microbial traits within oceanic viral communities. ISME J. 2011, 5, 1178–1190. [Google Scholar] [CrossRef] [PubMed]
  188. Kristensen, D.M.; Mushegian, A.R.; Dolja, V.V.; Koonin, E.V. New dimensions of the virus world discovered through metagenomics. Trends Microbiol. 2010, 18, 11–19. [Google Scholar] [CrossRef] [PubMed]
  189. Tamames, J.; Moya, A. Estimating the extent of horizontal gene transfer in metagenomic sequences. BMC Genom. 2008, 9. [Google Scholar] [CrossRef] [PubMed]
  190. Ufarte, L.; Potocki-Veronese, G.; Laville, E. Discovery of new protein families and functions: New challenges in functional metagenomics for biotechnologies and microbial ecology. Front. Microbiol. 2015, 6. [Google Scholar] [CrossRef] [PubMed]
  191. Wommack, K.E.; Nasko, D.J.; Chopyk, J.; Sakowski, E.G. Counts and sequences, observations that continue to change our understanding of viruses in nature. J. Microbiol. 2015, 53, 181–192. [Google Scholar] [CrossRef] [PubMed]
  192. Labonté, J.M.; Field, E.K.; Lau, M.; Chivian, D.; van Heerden, E.; Wommack, K.E.; Kieft, T.L.; Onstott, T.C.; Stepanauskas, R. Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population. Front. Microbiol. 2015, 6. [Google Scholar] [CrossRef] [PubMed]
  193. Mizuno, C.M.; Rodriguez-Valera, F.; Kimes, N.E.; Ghai, R. Expanding the marine virosphere using metagenomics. PLoS Genet. 2013, 9, e1003987. [Google Scholar] [CrossRef] [PubMed]
  194. Lopez, P.; Halary, S.; Bapteste, E. Highly divergent ancient gene families in metagenomic samples are compatible with additional divisions of life. Biol. Direct 2015, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  195. Moran, N.A.; Jarvik, T. Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 2010, 328, 624–627. [Google Scholar] [CrossRef] [PubMed]
  196. Jackson, D.J.; Macis, L.; Reitner, J.; Wörheide, G. A horizontal gene transfer supported the evolution of an early metazoan biomineralization strategy. BMC Evol. Biol. 2011, 11. [Google Scholar] [CrossRef] [PubMed]
  197. Altincicek, B.; Kovacs, J.L.; Gerardo, N.M. Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biol. Lett. 2012, 8, 253–257. [Google Scholar] [CrossRef] [PubMed]
  198. Lane, N. Energetics and genetics across the prokaryote-eukaryote divide. Biol. Direct 2011, 6. [Google Scholar] [CrossRef] [PubMed]
  199. Jaramillo, V.D.; Sukno, S.A.; Thon, M.R. Identification of horizontally transferred genes in the genus Colletotrichum reveals a steady tempo of bacterial to fungal gene transfer. BMC Genom. 2015, 16. [Google Scholar] [CrossRef] [PubMed]
  200. Zhu, B.; Zhou, Q.; Xie, G.; Zhang, G.; Zhang, X.; Wang, Y.; Sun, G.; Li, B.; Jin, G. Interkingdom gene transfer may contribute to the evolution of phytopathogenicity in Botrytis Cinerea. Evol. Bioinform. Online 2012, 8, 105–117. [Google Scholar] [CrossRef] [PubMed]
  201. Schönknecht, G.; Chen, W.H.; Ternes, C.M.; Barbier, G.G.; Shrestha, R.P.; Stanke, M.; Bräutigam, A.; Baker, B.J.; Banfield, J.F.; Garavito, R.M.; et al. Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 2013, 339, 1207–1210. [Google Scholar] [CrossRef] [PubMed]
  202. Bird, D.M.; Koltai, H. Plant parasitic nematodes: Habitats, hormones, and horizontally-acquired genes. J. Plant Growth Regul. 2000, 19, 183–194. [Google Scholar] [PubMed]
  203. Baldwin, J.G.; Nadler, S.A.; Adams, B.J. Evolution of plant parasitism among nematodes. Ann. Rev. Phytopathol. 2004, 42, 83–105. [Google Scholar] [CrossRef] [PubMed]
  204. Mitreva, M.; Smant, G.; Helder, J. Role of horizontal gene transfer in the evolution of plant parasitism among nematodes. Methods Mol. Biol. 2009, 532, 517–535. [Google Scholar] [PubMed]
  205. Danchin, E.G.; Rosso, M.N.; Vieira, P.; de Almeida-Engler, J.; Coutinho, P.M.; Henrissat, B.; Abad, P. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc. Natl. Acad. Sci. USA 2010, 107, 17651–17656. [Google Scholar] [CrossRef] [PubMed]
  206. Haegeman, A.; Jones, J.T.; Danchin, E.G. Horizontal gene transfer in nematodes: A catalyst for plant parasitism? Mol. Plant Microbe Interact. 2011, 24, 879–887. [Google Scholar] [CrossRef] [PubMed]
  207. Mayer, W.E.; Schuster, L.N.; Bartelmes, G.; Dieterich, C.; Sommer, R.J. Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover. BMC Evol. Biol. 2011, 11. [Google Scholar] [CrossRef] [PubMed]
  208. Danchin, E.G.; Rosso, M.N. Lateral gene transfers have polished animal genomes: Lessons from nematodes. Front. Cell. Infect. Microbiol. 2012, 2. [Google Scholar] [CrossRef] [PubMed]
  209. Yuan, J.B.; Zhang, X.J.; Liu, C.Z.; Wei, J.K.; Li, F.H.; Xiang, J.H. Horizontally transferred genes in the genome of Pacific white shrimp, Litopenaeus vannamei. BMC Evol. Biol. 2013, 13. [Google Scholar] [CrossRef] [PubMed]
  210. Sun, B.F.; Li, T.; Xiao, J.H.; Jia, L.Y.; Liu, L.; Zhang, P.; Murphy, R.W.; He, S.M.; Huang, D.W. Horizontal functional gene transfer from bacteria to fishes. Sci. Rep. 2015, 5. [Google Scholar] [CrossRef] [PubMed]
  211. Salzberg, S.L.; Hotopp, J.C.; Delcher, A.L.; Pop, M.; Smith, D.R.; Eisen, M.B.; Nelson, W.C. Serendipitous discovery of Wolbachia genomes in multiple Drosophila species. Genome Biol. 2005, 6. [Google Scholar] [CrossRef] [Green Version]
  212. Hotopp, J.C.D.; Clark, M.E.; Oliveira, D.C.; Foster, J.M.; Fischer, P.; Torres, M.C.M.; Giebel, J.D.; Kumar, N.; Ishmael, N.; Wang, S.; et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 2007, 317, 1753–1756. [Google Scholar] [CrossRef] [PubMed]
  213. Nikoh, N.; Tanaka, K.; Shibata, F.; Kondo, N.; Hizume, M.; Shimada, M.; Fukatsu, T. Wolbachia genome integrated in an insect chromosome: Evolution and fate of laterally transferred endosymbiont genes. Genome Res. 2008, 18, 272–280. [Google Scholar] [CrossRef] [PubMed]
  214. Nikoh, N.; Nakabachi, A. Aphids acquired symbiotic genes via lateral gene transfer. BMC Biol. 2009, 7. [Google Scholar] [CrossRef] [PubMed]
  215. Dunning Hotopp, J.C. Horizontal gene transfer between bacteria and animals. Trends Genet. 2011, 27, 157–163. [Google Scholar] [CrossRef] [PubMed]
  216. Klasson, L.; Kumar, N.; Bromley, R.; Sieber, K.; Flowers, M.; Ott, S.H.; Tallon, L.J.; Andersson, S.G.; Dunning Hotopp, J.C. Extensive duplication of the Wolbachia DNA in chromosome four of Drosophila ananassae. BMC Genom. 2014, 15. [Google Scholar] [CrossRef] [PubMed]
  217. Burstein, D.; Amaro, F.; Zusman, T.; Lifshitz, Z.; Cohen, O.; Gilbert, J.A.; Pupko, T.; Shuman, H.A.; Segal, G. Genomic analysis of 38 Legionella species identifies large and diverse effector repertoires. Nat. Genet. 2016, 48, 167–175. [Google Scholar] [CrossRef] [PubMed]
  218. Bork, P. Hundreds of ankyrin-like repeats in functionally diverse proteins: Mobile modules that cross phyla horizontally? Proteins 1993, 17, 363–374. [Google Scholar] [CrossRef] [PubMed]
  219. De Felipe, K.S.; Pampou, S.; Jovanovic, O.S.; Pericone, C.D.; Senna, F.Y.; Kalachikov, S.; Shuman, H.A. Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J. Bacteriol. 2005, 187, 7716–7726. [Google Scholar] [CrossRef] [PubMed]
  220. De la Casa-Esperon, E. Horizontal transfer and the evolution of host-pathogen interactions. Int. J. Evol. Biol. 2012, 2012. [Google Scholar] [CrossRef] [PubMed]
  221. Gomez-Valero, L.; Rusniok, C.; Jarraud, S.; Vacherie, B.; Rouy, Z.; Barbe, V.; Medigue, C.; Etienne, J.; Buchrieser, C. Extensive recombination events and horizontal gene transfer shaped the Legionella pneumophila genomes. BMC Genom. 2011, 12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  222. Ensminger, A.W. Legionella pneumophila, armed to the hilt: Justifying the largest arsenal of effectors in the bacterial world. Curr. Opin. Microbiol. 2015, 29, 74–80. [Google Scholar] [CrossRef] [PubMed]
  223. Jernigan, K.K.; Bordenstein, S.R. Ankyrin domains across the Tree of Life. PeerJ 2014, 2. [Google Scholar] [CrossRef] [PubMed]
  224. Rennoll-Bankert, K.E.; Dumler, J.S. Lessons from Anaplasma phagocytophilum: Chromatin remodeling by bacterial effectors. Infect. Disorders Drug Targets 2012, 12, 380–387. [Google Scholar] [CrossRef]
  225. Al-Khodor, S.; Price, C.T.; Kalia, A.; Kwaik, Y.A. Functional diversity of ankyrin repeats in microbial proteins. Trends Microbiol. 2010, 18, 132–139. [Google Scholar] [CrossRef] [PubMed]
  226. Habyarimana, F.; Price, C.T.; Santic, M.; Al-Khodor, S.; Kwaik, Y.A. Molecular characterization of the Dot/Icm-translocated AnkH and AnkJ eukaryotic-like effectors of Legionella pneumophila. Infect. Immun. 2010, 78, 1123–1134. [Google Scholar] [CrossRef] [PubMed]
  227. Voth, D.E. ThANKs for the repeat: Intracellular pathogens exploit a common eukaryotic domain. Cell. Logist. 2011, 1, 128–132. [Google Scholar] [CrossRef] [PubMed]
  228. Dubreuil, R.; Segev, N. Bringing host-cell takeover by pathogenic bacteria to center stage. Cell. Logist. 2011, 1, 120–124. [Google Scholar] [CrossRef] [PubMed]
  229. Gomez-Valero, L.; Rusniok, C.; Cazalet, C.; Buchrieser, C. Comparative and functional genomics of legionella identified eukaryotic like proteins as key players in host-pathogen interactions. Front. Microbiol. 2011, 2. [Google Scholar] [CrossRef] [PubMed]
  230. Gomez-Valero, L.; Buchrieser, C. Genome dynamics in Legionella: The basis of versatility and adaptation to intracellular replication. Cold Spring Harb. Perspect. Med. 2013, 3. [Google Scholar] [CrossRef] [PubMed]
  231. Keeling, P.J.; Palmer, J.D. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 2008, 9, 605–618. [Google Scholar] [CrossRef] [PubMed]
  232. Andersson, J.O.; Sjögren, Å.M.; Davis, L.A.; Embley, T.M.; Roger, A.J. Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr. Biol. 2003, 13, 94–104. [Google Scholar] [CrossRef]
  233. Alsmark, U.C.; Sicheritz-Ponten, T.; Foster, P.G.; Hirt, R.P.; Embley, T.M. Horizontal gene transfer in eukaryotic parasites: A case study of Entamoeba histolytica and Trichomonas vaginalis. Methods Mol. Biol. 2009, 532, 489–500. [Google Scholar] [PubMed]
  234. Alsmark, C.; Foster, P.G.; Sicheritz-Ponten, T.; Nakjang, S.; Embley, T.M.; Hirt, R.P. Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes. Genome Biol. 2013, 14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  235. Xi, Z.; Wang, Y.; Bradley, R.K.; Sugumaran, M.; Marx, C.J.; Rest, J.S.; Davis, C.C. Massive mitochondrial gene transfer in a parasitic flowering plant clade. PLoS Genet. 2013, 9, e1003265. [Google Scholar] [CrossRef] [PubMed]
  236. Hao, W.; Richardson, A.O.; Zheng, Y.; Palmer, J.D. Gorgeous mosaic of mitochondrial genes created by horizontal transfer and gene conversion. Proc. Natl. Acad. Sci. USA 2010, 107, 21576–21581. [Google Scholar] [CrossRef] [PubMed]
  237. Bergthorsson, U.; Adams, K.L.; Thomason, B.; Palmer, J.D. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 2003, 424, 197–201. [Google Scholar] [CrossRef] [PubMed]
  238. Stegemann, S.; Keuthe, M.; Greiner, S.; Bock, R. Horizontal transfer of chloroplast genomes between plant species. Proc. Natl. Acad. Sci. USA 2012, 109, 2434–2438. [Google Scholar] [CrossRef] [PubMed]
  239. Pace, J.K.; Gilbert, C.; Clark, M.S.; Feschotte, C. Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods. Proc. Natl. Acad. Sci. USA 2008, 105, 17023–17028. [Google Scholar] [CrossRef] [PubMed]
  240. Fortune, P.M.; Roulin, A.; Panaud, O. Horizontal transfer of transposable elements in plants. Commun. Integr. Biol. 2008, 1, 74–77. [Google Scholar] [CrossRef] [PubMed]
  241. Thomas, J.; Schaack, S.; Pritham, E.J. Pervasive horizontal transfer of rolling-circle transposons among animals. Genome Biol. Evol. 2010, 2, 656–664. [Google Scholar] [CrossRef] [PubMed]
  242. Bartolome, C.; Bello, X.; Maside, X. Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes. Genome Biol. 2009, 10. [Google Scholar] [CrossRef] [PubMed]
  243. Novick, P.; Smith, J.; Ray, D.; Boissinot, S. Independent and parallel lateral transfer of DNA transposons in tetrapod genomes. Gene 2010, 449, 85–94. [Google Scholar] [CrossRef] [PubMed]
  244. Wallau, G.L.; Ortiz, M.F.; Loreto, E.L. Horizontal transposon transfer in eukarya: Detection, bias, and perspectives. Genome Biol. Evol. 2012, 4, 689–699. [Google Scholar] [CrossRef] [PubMed]
  245. Ivancevic, A.M.; Walsh, A.M.; Kortschak, R.D.; Adelson, D.L. Jumping the fine LINE between species: Horizontal transfer of transposable elements in animals catalyses genome evolution. Bioessays 2013, 35, 1071–1082. [Google Scholar] [CrossRef] [PubMed]
  246. Kondrashov, F.A.; Koonin, E.V.; Morgunov, I.G.; Finogenova, T.V.; Kondrashova, M.N. Evolution of glyoxylate cycle enzymes in Metazoa: Evidence of multiple horizontal transfer events and pseudogene formation. Biol. Direct 2006, 1. [Google Scholar] [CrossRef] [PubMed]
  247. Rogers, M.; Keeling, P.J. Lateral transfer and recompartmentalization of Calvin cycle enzymes of plants and algae. J. Mol. Evol. 2004, 58, 367–375. [Google Scholar] [CrossRef] [PubMed]
  248. Christin, P.A.; Wallace, M.J.; Clayton, H.; Edwards, E.J.; Furbank, R.T.; Hattersley, P.W.; Sage, R.F.; Macfarlane, T.D.; Ludwig, M. Multiple photosynthetic transitions, polyploidy, and lateral gene transfer in the grass subtribe Neurachninae. J. Exp. Bot. 2012, 63, 6297–6308. [Google Scholar] [CrossRef] [PubMed]
  249. Graham, L.A.; Lougheed, S.C.; Ewart, K.V.; Davies, P.L. Lateral transfer of a lectin-like antifreeze protein gene in fishes. PLoS ONE 2008, 3, e2616. [Google Scholar] [CrossRef] [PubMed]
  250. Heliconius Genome Consortium. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 2012, 487, 94–98. [Google Scholar]
  251. Xi, Z.; Bradley, R.K.; Wurdack, K.J.; Wong, K.; Sugumaran, M.; Bomblies, K.; Rest, J.S.; Davis, C.C. Horizontal transfer of expressed genes in a parasitic flowering plant. BMC Genom. 2012, 13. [Google Scholar] [CrossRef] [PubMed]
  252. Houck, M.A.; Clark, J.B.; Peterson, K.R.; Kidwell, M.G. Possible horizontal transfer of Drosophila genes by the mite Proctolaelaps regalis. Science 1991, 253, 1125–1128. [Google Scholar] [CrossRef] [PubMed]
  253. Gilbert, C.; Schaack, S.; Pace, J.K., II; Brindley, P.J.; Feschotte, C. A role for host-parasite interactions in the horizontal transfer of transposons across phyla. Nature 2010, 464, 1347–1350. [Google Scholar] [CrossRef] [PubMed]
  254. Barteneva, N.S.; Maltsev, N.; Vorobjev, I.A. Microvesicles and intercellular communication in the context of parasitism. Front. Cell. Infect. Microbiol. 2013, 3. [Google Scholar] [CrossRef] [PubMed]
  255. Qiu, H.; Yoon, H.S.; Bhattacharya, D. Algal endosymbionts as vectors of horizontal gene transfer in photosynthetic eukaryotes. Front. Plant Sci. 2013, 4. [Google Scholar] [CrossRef] [PubMed]
  256. Taylor, M.; Mediannikov, O.; Raoult, D.; Greub, G. Endosymbiotic bacteria associated with nematodes, ticks and amoebae. FEMS Immunol. Med. Microbiol. 2012, 64, 21–31. [Google Scholar] [CrossRef] [PubMed]
  257. Sandström, J.P.; Russell, J.A.; White, J.P.; Moran, N.A. Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol. Ecol. 2001, 10, 217–228. [Google Scholar] [CrossRef] [PubMed]
  258. Raychoudhury, R.; Baldo, L.; Oliveira, D.C.; Werren, J.H. Modes of acquisition of Wolbachia: Horizontal transfer, hybrid introgression, and codivergence in the Nasonia species complex. Evolution 2009, 63, 165–183. [Google Scholar] [CrossRef] [PubMed]
  259. Oliver, K.M.; Degnan, P.H.; Burke, G.R.; Moran, N.A. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Ann. Rev. Entomol. 2010, 55, 247–266. [Google Scholar] [CrossRef] [PubMed]
  260. Bozzaro, S.; Eichinger, L. The professional phagocyte Dictyostelium discoideum as a model host for bacterial pathogens. Curr. Drug Targets 2011, 12, 942–954. [Google Scholar] [CrossRef] [PubMed]
  261. Chien, M.; Morozova, I.; Shi, S.; Sheng, H.; Chen, J.; Gomez, S.M.; Asamani, G.; Hill, K.; Nuara, J.; Feder, M.; et al. The genomic sequence of the accidental pathogen Legionella pneumophila. Science 2004, 305, 1966–1968. [Google Scholar] [CrossRef] [PubMed]
  262. Steinert, M. Pathogen-host interactions in Dictyostelium, Legionella, Mycobacterium and other pathogens. Semin. Cell Dev. Biol. 2011, 22, 70–76. [Google Scholar] [CrossRef] [PubMed]
  263. Huws, S.A.; Morley, R.J.; Jones, M.V.; Brown, M.R.; Smith, A.W. Interactions of some common pathogenic bacteria with Acanthamoeba polyphaga. FEMS Microbiol. Lett. 2008, 282, 258–265. [Google Scholar] [CrossRef] [PubMed]
  264. Douesnard-Malo, F.; Daigle, F. Increased persistence of Salmonella enterica serovar Typhi in the presence of Acanthamoeba castellanii. Appl. Environ. Microbiol. 2011, 77, 7640–7646. [Google Scholar] [CrossRef] [PubMed]
  265. Yousuf, F.A.; Siddiqui, R.; Khan, N.A. Acanthamoeba castellanii of the T4 genotype is a potential environmental host for Enterobacter aerogenes and Aeromonas hydrophila. Parasites Vectors 2013, 6. [Google Scholar] [CrossRef] [PubMed]
  266. Jeon, K.W. Genetic and physiological interactions in the amoeba-bacteria symbiosis. J. Eukaryot. Microbiol. 2004, 51, 502–508. [Google Scholar] [CrossRef] [PubMed]
  267. Charpentier, X.; Kay, E.; Schneider, D.; Shuman, H.A. Antibiotics and UV radiation induce competence for natural transformation in Legionella pneumophila. J. Bacteriol. 2011, 193, 1114–1121. [Google Scholar] [CrossRef] [PubMed]
  268. Sun, Y.; Bernardy, E.E.; Hammer, B.K.; Miyashiro, T. Competence and natural transformation in vibrios. Mol. Microbiol. 2013, 89, 583–595. [Google Scholar] [CrossRef] [PubMed]
  269. Kovács, Á.T.; Smits, W.K.; Mirończuk, A.M.; Kuipers, O.P. Ubiquitous late competence genes in Bacillus species indicate the presence of functional DNA uptake machineries. Environ. Microbiol. 2009, 11, 1911–1922. [Google Scholar] [CrossRef] [PubMed]
  270. Benam, A.V.; Lång, E.; Alfsnes, K.; Fleckenstein, B.; Rowe, A.D.; Hovland, E.; Ambur, O.H.; Frye, S.A.; Tønjum, T. Structure-function relationships of the competence lipoprotein ComL and SSB in meningococcal transformation. Microbiology 2011, 157, 1329–1342. [Google Scholar] [CrossRef] [PubMed]
  271. Crochu, S.; Cook, S.; Attoui, H.; Charrel, R.N.; de Chesse, R.; Belhouchet, M.; Lemasson, J.J.; de Micco, P.; de Lamballerie, X. Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes. J. Gen. Virol. 2004, 85, 1971–1980. [Google Scholar] [CrossRef] [PubMed]
  272. Tanne, E.; Sela, I. Occurrence of a DNA sequence of a non-retro RNA virus in a host plant genome and its expression: Evidence for recombination between viral and host RNAs. Virology 2005, 332, 614–622. [Google Scholar] [CrossRef] [PubMed]
  273. Frank, A.C.; Wolfe, K.H. Evolutionary capture of viral and plasmid DNA by yeast nuclear chromosomes. Eukaryot. Cell 2009, 8, 1521–1531. [Google Scholar] [CrossRef] [PubMed]
  274. Roiz, D.; Vázquez, A.; Seco, M.P.S.; Tenorio, A.; Rizzoli, A. Detection of novel insect flavivirus sequences integrated in Aedes albopictus (Diptera: Culicidae) in Northern Italy. Virol. J. 2009, 6. [Google Scholar] [CrossRef] [PubMed]
  275. Taylor, D.J.; Leach, R.W.; Bruenn, J. Filoviruses are ancient and integrated into mammalian genomes. BMC Evol. Biol. 2010, 10. [Google Scholar] [CrossRef] [PubMed]
  276. Belyi, V.A.; Levine, A.J.; Skalka, A.M. Sequences from ancestral single-stranded DNA viruses in vertebrate genomes: The Parvoviridae and Circoviridae are more than 40 to 50 million years old. J. Virol. 2010, 84, 12458–12462. [Google Scholar] [CrossRef] [PubMed]
  277. Belyi, V.A.; Levine, A.J.; Skalka, A.M. Unexpected inheritance: Multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog. 2010, 6, e1001030. [Google Scholar] [CrossRef] [PubMed]
  278. Horie, M.; Honda, T.; Suzuki, Y.; Kobayashi, Y.; Daito, T.; Oshida, T.; Ikuta, K.; Jern, P.; Gojobori, T.; Coffin, J.M.; et al. Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 2010, 463, 84–87. [Google Scholar] [CrossRef] [PubMed]
  279. Iskra-Caruana, M.L.; Baurens, F.C.; Gayral, P.; Chabannes, M. A four-partner plant-virus interaction: Enemies can also come from within. Mol. Plant Microbe Interact. 2010, 23, 1394–1402. [Google Scholar] [CrossRef] [PubMed]
  280. Kapoor, A.; Simmonds, P.; Lipkin, W.I. Discovery and characterization of mammalian endogenous parvoviruses. J. Virol. 2010, 84, 12628–12635. [Google Scholar] [CrossRef] [PubMed]
  281. Katzourakis, A.; Gifford, R.J. Endogenous viral elements in animal genomes. PLoS Genet. 2010, 6, e1001191. [Google Scholar] [CrossRef] [PubMed]
  282. Liu, H.; Fu, Y.; Jiang, D.; Li, G.; Xie, J.; Cheng, J.; Peng, Y.; Ghabrial, S.A.; Yi, X. Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J. Virol. 2010, 84, 11876–11887. [Google Scholar] [CrossRef] [PubMed]
  283. Horie, M.; Tomonaga, K. Non-retroviral fossils in vertebrate genomes. Viruses 2011, 3, 1836–1848. [Google Scholar] [CrossRef] [PubMed]
  284. Chiba, S.; Kondo, H.; Tani, A.; Saisho, D.; Sakamoto, W.; Kanematsu, S.; Suzuki, N. Widespread endogenization of genome sequences of non-retroviral RNA viruses into plant genomes. PLoS Pathog. 2011, 7, e1002146. [Google Scholar] [CrossRef] [PubMed]
  285. Liu, H.; Fu, Y.; Xie, J.; Cheng, J.; Ghabrial, S.A.; Li, G.; Peng, Y.; Yi, X.; Jiang, D. Widespread endogenization of densoviruses and parvoviruses in animal and human genomes. J. Virol. 2011, 85, 9863–9876. [Google Scholar] [CrossRef] [PubMed]
  286. Holmes, E.C. The evolution of endogenous viral elements. Cell Host Microbe 2011, 10, 368–377. [Google Scholar] [CrossRef] [PubMed]
  287. Feschotte, C.; Gilbert, C. Endogenous viruses: Insights into viral evolution and impact on host biology. Nat. Rev. Genet. 2012, 13, 283–296. [Google Scholar] [CrossRef] [PubMed]
  288. Cui, J.; Holmes, E.C. Endogenous RNA viruses of plants in insect genomes. Virology 2012, 427, 77–79. [Google Scholar] [CrossRef] [PubMed]
  289. Geuking, M.B.; Weber, J.; Dewannieux, M.; Gorelik, E.; Heidmann, T.; Hengartner, H.; Zinkernagel, R.M.; Hangartner, L. Recombination of retrotransposon and exogenous RNA virus results in nonretroviral cDNA integration. Science 2009, 323, 393–396. [Google Scholar] [CrossRef] [PubMed]
  290. Bill, C.A.; Summers, J. Genomic DNA double-strand breaks are targets for hepadnaviral DNA integration. Proc. Natl. Acad. Sci. USA 2004, 101, 11135–11140. [Google Scholar] [CrossRef] [PubMed]
  291. Hu, X.; Lin, J.; Xie, Q.; Ren, J.; Chang, Y.; Wu, W.; Xia, Y. DNA double-strand breaks, potential targets for HBV integration. J. Huazhong Univ. Sci. Technol. Med. Sci. 2010, 30, 265–270. [Google Scholar] [CrossRef] [PubMed]
  292. Koonin, E.V.; Dolja, V.V. Virus world as an evolutionary network of viruses and capsidless selfish elements. Microbiol. Mol. Biol. Rev. 2014, 78, 278–303. [Google Scholar] [CrossRef] [PubMed]
  293. Abroi, A. A protein domain-based view of the virosphere-host relationship. Biochimie 2015, 119, 231–243. [Google Scholar] [CrossRef] [PubMed]
  294. Yoosuf, N.; Yutin, N.; Colson, P.; Shabalina, S.A.; Pagnier, I.; Robert, C.; Azza, S.; Klose, T.; Wong, J.; Rossmann, M.G.; et al. Related giant viruses in distant locations and different habitats: Acanthamoeba polyphaga moumouvirus represents a third lineage of the Mimiviridae that is close to the megavirus lineage. Genome Biol. Evol. 2012, 4, 1324–1330. [Google Scholar] [CrossRef] [PubMed]
  295. Claverie, J.-M.; Abergel, C. The concept of virus in the post-megavirus era. In Viruses: Essential Agents of Life; Witzany, G., Ed.; Springer: Dordrecht, The Netherlands, 2012; pp. 187–202. [Google Scholar]
  296. Piacente, F.; de Castro, C.; Jeudy, S.; Molinaro, A.; Salis, A.; Damonte, G.; Bernardi, C.; Abergel, C.; Tonetti, M.G. Giant virus Megavirus chilensis encodes the biosynthetic pathway for uncommon acetamido sugars. J. Biol. Chem. 2014, 289, 24428–24439. [Google Scholar] [CrossRef] [PubMed]
  297. Filee, J.; Pouget, N.; Chandler, M. Phylogenetic evidence for extensive lateral acquisition of cellular genes by Nucleocytoplasmic large DNA viruses. BMC Evol. Biol. 2008, 8. [Google Scholar] [CrossRef] [PubMed]
  298. Filee, J. Lateral gene transfer, lineage-specific gene expansion and the evolution of Nucleo Cytoplasmic Large DNA viruses. J. Invertebrate Pathol. 2009, 101, 169–171. [Google Scholar] [CrossRef] [PubMed]
  299. Filee, J.; Chandler, M. Gene exchange and the origin of giant viruses. Intervirology 2010, 53, 354–361. [Google Scholar] [CrossRef] [PubMed]
  300. Filee, J. Route of NCLDV evolution: The genomic accordion. Curr. Opin. Virol. 2013, 3, 595–599. [Google Scholar] [CrossRef] [PubMed]
  301. Boyer, M.; Yutin, N.; Pagnier, I.; Barrassi, L.; Fournous, G.; Espinosa, L.; Robert, C.; Azza, S.; Sun, S.; Rossmann, M.G.; et al. Giant Marseillevirus highlights the role of Amoebae as a melting pot in emergence of chimeric microorganisms. Proc. Natl. Acad. Sci. USA 2009, 106, 21848–21853. [Google Scholar] [CrossRef] [PubMed]
  302. Colson, P.; Gimenez, G.; Boyer, M.; Fournous, G.; Raoult, D. The giant Cafeteria roenbergensis virus that infects a widespread marine phagocytic protist is a new member of the fourth domain of life. PLoS ONE 2011, 6, e18935. [Google Scholar] [CrossRef] [PubMed]
  303. Saisongkorh, W.; Robert, C.; la Scola, B.; Raoult, D.; Rolain, J.M. Evidence of transfer by conjugation of type IV secretion system genes between Bartonella species and Rhizobium radiobacter in amoeba. PLoS ONE 2010, 5, e12666. [Google Scholar] [CrossRef] [PubMed]
  304. McClure, M.A. Evolution of the DUT gene: Horizontal transfer between host and pathogen in all three domains of life. Curr. Protein Pept. Sci. 2001, 2, 313–324. [Google Scholar] [CrossRef] [PubMed]
  305. Metcalf, J.A.; Funkhouser-Jones, L.J.; Brileya, K.; Reysenbach, A.L.; Bordenstein, S.R. Antibacterial gene transfer across the tree of life. eLife 2014, 3. [Google Scholar] [CrossRef] [PubMed]
  306. Doolittle, R.F.; Bork, P. Evolutionarily mobile modules in proteins. Sci. Am. 1993, 269, 50–56. [Google Scholar] [CrossRef] [PubMed]
  307. Lander, E.S.; Linton, L.M.; Birren, B.; Nusbaum, C.; Zody, M.C.; Baldwin, J.; Devon, K.; Dewar, K.; Doyle, M.; FitzHugh, W.; et al. Initial sequencing and analysis of the human genome. Nature 2001, 409, 860–921. [Google Scholar] [CrossRef] [PubMed]
  308. Schmitz, J.; Brosius, J. Exonization of transposed elements: A challenge and opportunity for evolution. Biochimie 2011, 93, 1928–1934. [Google Scholar] [CrossRef] [PubMed]
  309. Gilbert, W. The exon theory of genes. Cold Spring Harb. Symp. Quant. Biol. 1987, 52, 901–905. [Google Scholar] [CrossRef] [PubMed]
  310. Gilbert, W. DNA sequencing and gene structure. Science 1981, 214, 1305–1312. [Google Scholar] [CrossRef] [PubMed]
  311. Liu, M.; Grigoriev, A. Protein domains correlate strongly with exons in multiple eukaryotic genomes—Evidence of exon shuffling? Trends Genet. 2004, 20, 399–403. [Google Scholar] [CrossRef] [PubMed]
  312. Xing, Y.; Lee, C. Alternative splicing and RNA selection pressure—Evolutionary consequences for eukaryotic genomes. Nat. Rev. Genet. 2006, 7, 499–509. [Google Scholar] [CrossRef] [PubMed]
  313. Barbosa-Morais, N.L.; Irimia, M.; Pan, Q.; Xiong, H.Y.; Gueroussov, S.; Lee, L.J.; Slobodeniuc, V.; Kutter, C.; Watt, S.; Çolak, R.; et al. The evolutionary landscape of alternative splicing in vertebrate species. Science 2012, 338, 1587–1593. [Google Scholar] [CrossRef] [PubMed]
  314. Hassan, M.A.; Saeij, J.P. Incorporating alternative splicing and mRNA editing into the genetic analysis of complex traits. Bioessays 2014, 36, 1032–1040. [Google Scholar] [CrossRef] [PubMed]
  315. Kornblihtt, A.R.; Schor, I.E.; Alló, M.; Dujardin, G.; Petrillo, E.; Muñoz, M.J. Alternative splicing: A pivotal step between eukaryotic transcription and translation. Nat. Rev. Mol. Cell Biol. 2013, 14, 153–165. [Google Scholar] [CrossRef] [PubMed]
  316. Kalsotra, A.; Cooper, T.A. Functional consequences of developmentally regulated alternative splicing. Nat. Rev. Genet. 2011, 12, 715–729. [Google Scholar] [CrossRef] [PubMed]
  317. Ast, G. How did alternative splicing evolve? Nat. Rev. Genet. 2004, 5, 773–782. [Google Scholar] [CrossRef] [PubMed]
  318. Chen, M.; Manley, J.L. Mechanisms of alternative splicing regulation: Insights from molecular and genomics approaches. Nat. Rev. Mol. Cell Biol. 2009, 10, 741–754. [Google Scholar] [CrossRef] [PubMed]
  319. Mudge, J.M.; Frankish, A.; Fernandez-Banet, J.; Alioto, T.; Derrien, T.; Howald, C.; Reymond, A.; Guigó, R.; Hubbard, T.; Harrow, J. The origins, evolution, and functional potential of alternative splicing in vertebrates. Mol. Biol. Evol. 2011, 28, 2949–2959. [Google Scholar] [CrossRef] [PubMed]
  320. Kawashima, T.; Kawashima, S.; Tanaka, C.; Murai, M.; Yoneda, M.; Putnam, N.H.; Rokhsar, D.S.; Kanehisa, M.; Satoh, N.; Wada, H. Domain shuffling and the evolution of vertebrates. Genome Res. 2009, 19, 1393–1403. [Google Scholar] [CrossRef] [PubMed]
  321. Kaessmann, H.; Zöllner, S.; Nekrutenko, A.; Li, W.H. Signatures of domain shuffling in the human genome. Genome Res. 2002, 12, 1642–1650. [Google Scholar] [CrossRef] [PubMed]
  322. Van Rijk, A.; Bloemendal, H. Molecular mechanisms of exon shuffling: Illegitimate recombination. Genetica 2003, 118, 245–249. [Google Scholar] [CrossRef] [PubMed]
  323. Franca, G.S.; Cancherini, D.V.; de Souza, S.J. Evolutionary history of exon shuffling. Genetica 2012, 140, 249–257. [Google Scholar] [CrossRef] [PubMed]
  324. Sorek, R. The birth of new exons: Mechanisms and evolutionary consequences. RNA 2007, 13, 1603–1608. [Google Scholar] [CrossRef] [PubMed]
  325. Liu, L.Y.; Charng, Y.C. Genome-wide survey of ds exonization to enrich transcriptomes and proteomes in plants. Evolut. Bioinform. Online 2012, 8, 575–587. [Google Scholar]
  326. Huda, A.; Bushel, P.R. Widespread exonization of transposable elements in human coding sequences is associated with epigenetic regulation of transcription. Transcriptomics Open Access 2013, 1. [Google Scholar] [CrossRef]
  327. Bacher, J.M.; Reiss, B.D.; Ellington, A.D. Anticipatory evolution and DNA shuffling. Genome Biol. 2002, 3. [Google Scholar] [CrossRef]
  328. Stemmer, W.P. DNA shuffling by random fragmentation and reassembly: In vitro recombination for molecular evolution. Proc. Natl. Acad. Sci. USA 1994, 91, 10747–10751. [Google Scholar] [CrossRef] [PubMed]
  329. Stemmer, W.P. Rapid evolution of a protein in vitro by DNA shuffling. Nature 1994, 370, 389–391. [Google Scholar] [CrossRef] [PubMed]
  330. Ejima, Y.; Yang, L. Trans mobilization of genomic DNA as a mechanism for retrotransposon-mediated exon shuffling. Hum. Mol. Genet. 2003, 12, 1321–1328. [Google Scholar] [CrossRef] [PubMed]
  331. Jiang, N.; Bao, Z.; Zhang, X.; Eddy, S.R.; Wessler, S.R. Pack-MULE transposable elements mediate gene evolution in plants. Nature 2004, 431, 569–573. [Google Scholar] [CrossRef] [PubMed]
  332. Morgante, M.; Brunner, S.; Pea, G.; Fengler, K.; Zuccolo, A.; Rafalski, A. Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat. Genet. 2005, 37, 997–1002. [Google Scholar] [CrossRef] [PubMed]
  333. Lisch, D. Pack-MULEs: Theft on a massive scale. Bioessays 2005, 27, 353–355. [Google Scholar] [CrossRef] [PubMed]
  334. Damert, A.; Raiz, J.; Horn, A.V.; Löwer, J.; Wang, H.; Xing, J.; Batzer, M.A.; Löwer, R.; Schumann, G.G. 5’-Transducing SVA retrotransposon groups spread efficiently throughout the human genome. Genome Res. 2009, 19, 1992–2008. [Google Scholar] [CrossRef] [PubMed]
  335. Hancks, D.C.; Ewing, A.D.; Chen, J.E.; Tokunaga, K.; Kazazian, H.H., Jr. Exon-trapping mediated by the human retrotransposon SVA. Genome Res. 2009, 19, 1983–1991. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  336. Elrouby, N.; Bureau, T.E. Bs1, a new chimeric gene formed by retrotransposon-mediated exon shuffling in maize. Plant Physiol. 2010, 153, 1413–1424. [Google Scholar] [CrossRef] [PubMed]
  337. Jiang, N.; Ferguson, A.A.; Slotkin, R.K.; Lisch, D. Pack-Mutator-like transposable elements (Pack-MULEs) induce directional modification of genes through biased insertion and DNA acquisition. Proc. Natl. Acad. Sci. USA 2011, 108, 1537–1542. [Google Scholar] [CrossRef] [PubMed]
  338. Moran, J.V.; DeBerardinis, R.J.; Kazazian, H.H., Jr. Exon shuffling by L1 retrotransposition. Science 1999, 283, 1530–1534. [Google Scholar] [CrossRef] [PubMed]
  339. Hiller, R.; Hetzer, M.; Schweyen, R.J.; Mueller, M.W. Transposition and exon shuffling by group II intron RNA molecules in pieces. J. Mol. Biol. 2000, 297, 301–308. [Google Scholar] [CrossRef] [PubMed]
  340. Kolkman, J.A.; Stemmer, W.P. Directed evolution of proteins by exon shuffling. Nat. Biotechnol. 2001, 19, 423–428. [Google Scholar] [CrossRef] [PubMed]
  341. Piriyapongsa, J.; Polavarapu, N.; Borodovsky, M.; McDonald, J. Exonization of the LTR transposable elements in human genome. BMC Genom. 2007, 8. [Google Scholar] [CrossRef] [PubMed]
  342. Schwartz, S.; Gal-Mark, N.; Kfir, N.; Oren, R.; Kim, E.; Ast, G. Alu exonization events reveal features required for precise recognition of exons by the splicing machinery. PLoS Comput. Biol. 2009, 5, e1000300. [Google Scholar] [CrossRef] [PubMed]
  343. Sela, N.; Mersch, B.; Hotz-Wagenblatt, A.; Ast, G. Characteristics of transposable element exonization within human and mouse. PLoS ONE 2010, 5, e10907. [Google Scholar] [CrossRef] [PubMed]
  344. Krull, M.; Brosius, J.; Schmitz, J. Alu-SINE exonization: En route to protein-coding function. Mol. Biol. Evol. 2005, 22, 1702–1711. [Google Scholar] [CrossRef] [PubMed]
  345. Möller-Krull, M.; Zemann, A.; Roos, C.; Brosius, J.; Schmitz, J. Beyond DNA: RNA editing and steps toward Alu exonization in primates. J. Mol. Biol. 2008, 382, 601–609. [Google Scholar] [CrossRef] [PubMed]
  346. Zemojtel, T.; Penzkofer, T.; Schultz, J.; Dandekar, T.; Badge, R.; Vingron, M. Exonization of active mouse L1s: A driver of transcriptome evolution? BMC Genom. 2007, 8. [Google Scholar] [CrossRef] [PubMed]
  347. Dobzhansky, T. Genetics and the Origin of Species; Columbia University Press: New York, NY, USA, 1937. [Google Scholar]
  348. Marino-Ramirez, L.; Lewis, K.C.; Landsman, D.; Jordan, I.K. Transposable elements donate lineage-specific regulatory sequences to host genomes. Cytogenetic Genome Res. 2005, 110, 333–341. [Google Scholar] [CrossRef] [PubMed]
  349. Wang, T.; Zeng, J.; Lowe, C.B.; Sellers, R.G.; Salama, S.R.; Yang, M.; Burgess, S.M.; Brachmann, R.K.; Haussler, D. Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc. Natl. Acad. Sci. USA 2007, 104, 18613–18618. [Google Scholar] [CrossRef] [PubMed]
  350. Wang, J.; Bowen, N.J.; Mariño-Ramírez, L.; Jordan, I.K. A c-Myc regulatory subnetwork from human transposable element sequences. Mol. Biosyst. 2009, 5, 1831–1839. [Google Scholar] [CrossRef] [PubMed]
  351. Kunarso, G.; Chia, N.Y.; Jeyakani, J.; Hwang, C.; Lu, X.; Chan, Y.S.; Ng, H.H.; Bourque, G. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 2010, 42, 631–634. [Google Scholar] [CrossRef] [PubMed]
  352. Xie, D.; Chen, C.C.; Ptaszek, L.M.; Xiao, S.; Cao, X.; Fang, F.; Ng, H.H.; Lewin, H.A.; Cowan, C.; Zhong, S. Rewirable gene regulatory networks in the preimplantation embryonic development of three mammalian species. Genome Res. 2010, 20, 804–815. [Google Scholar] [CrossRef] [PubMed]
  353. Feschotte, C. Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 2008, 9, 397–405. [Google Scholar] [CrossRef] [PubMed]
  354. David, L.; Stolovicki, E.; Haziz, E.; Braun, E. Inherited adaptation of genome-rewired cells in response to a challenging environment. HFSP J. 2010, 4, 131–141. [Google Scholar] [CrossRef] [PubMed]
  355. Scannell, D.R.; Wolfe, K. Rewiring the transcriptional regulatory circuits of cells. Genome Biol. 2004, 5. [Google Scholar] [CrossRef] [PubMed]
  356. Shou, C.; Bhardwaj, N.; Lam, H.Y.; Yan, K.K.; Kim, P.M.; Snyder, M.; Gerstein, M.B. Measuring the evolutionary rewiring of biological networks. PLoS Comput. Biol. 2011, 7, e1001050. [Google Scholar] [CrossRef] [PubMed]
  357. Lowe, C.B.; Kellis, M.; Siepel, A.; Raney, B.J.; Clamp, M.; Salama, S.R.; Kingsley, D.M.; Lindblad-Toh, K.; Haussler, D. Three periods of regulatory innovation during vertebrate evolution. Science 2011, 333, 1019–1024. [Google Scholar] [CrossRef] [PubMed]
  358. Jurka, J.; Bao, W.; Kojima, K.K.; Kohany, O.; Yurka, M.G. Distinct groups of repetitive families preserved in mammals correspond to different periods of regulatory innovations in vertebrates. Biol. Direct 2012, 7. [Google Scholar] [CrossRef] [PubMed]
  359. Huda, A.; Mariño-Ramírez, L.; Landsman, D.; Jordan, I.K. Repetitive DNA elements, nucleosome binding and human gene expression. Gene 2009, 436, 12–22. [Google Scholar] [CrossRef] [PubMed]
  360. Jordan, I.K.; Rogozin, I.B.; Glazko, G.V.; Koonin, E.V. Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet. 2003, 19, 68–72. [Google Scholar] [CrossRef]
  361. Jurka, J.; Kapitonov, V.V.; Kohany, O.; Jurka, M.V. Repetitive sequences in complex genomes: Structure and evolution. Ann. Rev. Genom. Hum. Genet. 2007, 8, 241–259. [Google Scholar] [CrossRef] [PubMed]
  362. Jurka, J.; Bao, W.; Kojima, K.K. Families of transposable elements, population structure and the origin of species. Biol. Direct 2011, 6. [Google Scholar] [CrossRef] [PubMed]
  363. Sternberg, R.V.; Shapiro, J.A. How repeated retroelements format genome function. Cytogenet. Genome Res. 2005, 110, 108–116. [Google Scholar] [CrossRef] [PubMed]
  364. Gorbunova, V.; Boeke, J.D.; Helfand, S.L.; Sedivy, J.M. Human genomics. Sleeping dogs of the genome. Science 2014, 346, 1187–1188. [Google Scholar] [PubMed]
  365. Jern, P.; Coffin, J.M. Effects of retroviruses on host genome function. Ann. Rev. Genet. 2008, 42, 709–732. [Google Scholar] [CrossRef] [PubMed]
  366. Cornelis, G.; Heidmann, O.; Degrelle, S.A.; Vernochet, C.; Lavialle, C.; Letzelter, C.; Bernard-Stoecklin, S.; Hassanin, A.; Mulot, B.; Guillomot, M.; et al. Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants. Proc. Natl. Acad. Sci. USA 2013, 110, E828–E837. [Google Scholar] [CrossRef] [PubMed]
  367. Lavialle, C.; Cornelis, G.; Dupressoir, A.; Esnault, C.; Heidmann, O.; Vernochet, C.; Heidmann, T. Paleovirology of “syncytins”, retroviral env genes exapted for a role in placentation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368. [Google Scholar] [CrossRef] [PubMed]
  368. Dupressoir, A.; Lavialle, C.; Heidmann, T. From ancestral infectious retroviruses to bona fide cellular genes: Role of the captured syncytins in placentation. Placenta 2012, 33, 663–671. [Google Scholar] [CrossRef] [PubMed]
  369. Esnault, C.; Priet, S.; Ribet, D.; Vernochet, C.; Bruls, T.; Lavialle, C.; Weissenbach, J.; Heidmann, T. A placenta-specific receptor for the fusogenic, endogenous retrovirus-derived, human syncytin-2. Proc. Natl. Acad. Sci. USA 2008, 105, 17532–17537. [Google Scholar] [CrossRef] [PubMed]
  370. Chuong, E.B. Retroviruses facilitate the rapid evolution of the mammalian placenta. Bioessays 2013, 35, 853–861. [Google Scholar] [CrossRef] [PubMed]
  371. Macaulay, E.C.; Weeks, R.J.; Andrews, S.; Morison, I.M. Hypomethylation of functional retrotransposon-derived genes in the human placenta. Mamm. Genome 2011, 22, 722–735. [Google Scholar] [CrossRef] [PubMed]
  372. Macaulay, E.C.; Roberts, H.E.; Cheng, X.; Jeffs, A.R.; Baguley, B.C.; Morison, I.M. Retrotransposon hypomethylation in melanoma and expression of a placenta-specific gene. PLoS ONE 2014, 9, e95840. [Google Scholar] [CrossRef] [PubMed]
  373. Renfree, M.B.; Suzuki, S.; Kaneko-Ishino, T. The origin and evolution of genomic imprinting and viviparity in mammals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368. [Google Scholar] [CrossRef] [PubMed]
  374. Lynch, V.J.; Nnamani, M.C.; Kapusta, A.; Brayer, K.; Plaza, S.L.; Mazur, E.C.; Emera, D.; Sheikh, S.Z.; Grützner, F.; Bauersachs, S.; et al. Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep. 2015, 10. [Google Scholar] [CrossRef] [PubMed]
  375. Kapusta, A.; Kronenberg, Z.; Lynch, V.J.; Zhuo, X.; Ramsay, L.; Bourque, G.; Yandell, M.; Feschotte, C. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet. 2013, 9, e1003470. [Google Scholar] [CrossRef] [PubMed]
  376. Lynch, V.J.; Leclerc, R.D.; May, G.; Wagner, G.P. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet. 2011, 43, 1154–1159. [Google Scholar] [CrossRef] [PubMed]
  377. Emera, D.; Wagner, G.P. Transposable element recruitments in the mammalian placenta: Impacts and mechanisms. Briefings Funct. Genom. 2012, 11, 267–276. [Google Scholar] [CrossRef] [PubMed]
  378. Emera, D.; Casola, C.; Lynch, V.J.; Wildman, D.E.; Agnew, D.; Wagner, G.P. Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol. Biol. Evol. 2012, 29, 239–247. [Google Scholar] [CrossRef] [PubMed]
  379. Goke, J.; Lu, X.; Chan, Y.S.; Ng, H.H.; Ly, L.H.; Sachs, F.; Szczerbinska, I. Dynamic transcription of distinct classes of endogenous retroviral elements marks specific populations of early human embryonic cells. Cell Stem Cell 2015, 16, 135–141. [Google Scholar] [CrossRef] [PubMed]
  380. Grow, E.J.; Flynn, R.A.; Chavez, S.L.; Bayless, N.L.; Wossidlo, M.; Wesche, D.J.; Martin, L.; Ware, C.B.; Blish, C.A.; Chang, H.Y.; et al. Intrinsic retroviral reactivation in human preimplantation embryos and pluripotent cells. Nature 2015, 522, 221–225. [Google Scholar] [CrossRef] [PubMed]
  381. Kigami, D.; Minami, N.; Takayama, H.; Imai, H. MuERV-L is one of the earliest transcribed genes in mouse one-cell embryos. Biol. Reprod. 2003, 68, 651–654. [Google Scholar] [CrossRef] [PubMed]
  382. Hutchins, A.P.; Pei, D. Transposable elements at the center of the crossroads between embryogenesis, embryonic stem cells, reprogramming, and long non-coding RNAs. Sci. Bull. 2015, 60, 1722–1733. [Google Scholar] [CrossRef] [PubMed]
  383. Loewer, S.; Cabili, M.N.; Guttman, M.; Loh, Y.H.; Thomas, K.; Park, I.H.; Garber, M.; Curran, M.; Onder, T.; Agarwal, S.; et al. Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat. Genet. 2010, 42, 1113–1117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  384. Kelley, D.; Rinn, J. Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol. 2012, 13. [Google Scholar] [CrossRef] [PubMed]
  385. Ng, S.Y.; Stanton, L.W. Long non-coding RNAs in stem cell pluripotency. Wiley Interdiscip. Rev. RNA 2013, 4, 121–128. [Google Scholar] [CrossRef] [PubMed]
  386. Narva, E.; Rahkonen, N.; Emani, M.R.; Lund, R.; Pursiheimo, J.P.; Nästi, J.; Autio, R.; Rasool, O.; Denessiouk, K.; Lähdesmäki, H.; et al. RNA-binding protein L1TD1 interacts with LIN28 via RNA and is required for human embryonic stem cell self-renewal and cancer cell proliferation. Stem Cells 2012, 30, 452–460. [Google Scholar] [CrossRef] [PubMed]
  387. Glinsky, G.V. Transposable elements and DNA methylation create in embryonic stem cells human-specific regulatory sequences associated with distal enhancers and noncoding RNAs. Genome Biol. Evol. 2015, 7, 1432–1454. [Google Scholar] [CrossRef] [PubMed]
  388. Kim, D.H.; Marinov, G.K.; Pepke, S.; Singer, Z.S.; He, P.; Williams, B.; Schroth, G.P.; Elowitz, M.B.; Wold, B.J. Single-cell transcriptome analysis reveals dynamic changes in lncRNA expression during reprogramming. Cell Stem Cell 2015, 16, 88–101. [Google Scholar] [CrossRef] [PubMed]
  389. Fort, A.; Hashimoto, K.; Yamada, D.; Salimullah, M.; Keya, C.A.; Saxena, A.; Bonetti, A.; Voineagu, I.; Bertin, N.; Kratz, A.; et al. Deep transcriptome profiling of mammalian stem cells supports a regulatory role for retrotransposons in pluripotency maintenance. Nat. Genet. 2014, 46, 558–566. [Google Scholar] [CrossRef] [PubMed]
  390. Schlesinger, S.; Goff, S.P. Retroviral transcriptional regulation and embryonic stem cells: War and peace. Mol. Cell. Biol. 2015, 35, 770–777. [Google Scholar] [CrossRef] [PubMed]
  391. Huo, J.S.; Zambidis, E.T. Pivots of pluripotency: The roles of non-coding RNA in regulating embryonic and induced pluripotent stem cells. Biochim. Biophys. Acta 2013, 1830, 2385–2394. [Google Scholar] [CrossRef] [PubMed]
  392. Hadjiargyrou, M.; Delihas, N. The intertwining of transposable elements and non-coding RNAs. Int. J. Mol. Sci. 2013, 14, 13307–13328. [Google Scholar] [CrossRef] [PubMed]
  393. Kapusta, A.; Feschotte, C. Volatile evolution of long noncoding RNA repertoires: Mechanisms and biological implications. Trends Genet. 2014, 30, 439–452. [Google Scholar] [CrossRef] [PubMed]
  394. Johnson, R.; Guigo, R. The RIDL hypothesis: Transposable elements as functional domains of long noncoding RNAs. RNA 2014, 20, 959–976. [Google Scholar] [CrossRef] [PubMed]
  395. Guttman, M.; Rinn, J.L. Modular regulatory principles of large non-coding RNAs. Nature 2012, 482, 339–346. [Google Scholar] [CrossRef] [PubMed]
  396. Roberts, J.T.; Cardin, S.E.; Borchert, G.M. Burgeoning evidence indicates that microRNAs were initially formed from transposable element sequences. Mob. Genet. Elem. 2014, 4, e29255. [Google Scholar] [CrossRef] [PubMed]
  397. Gifford, W.D.; Pfaff, S.L.; Macfarlan, T.S. Transposable elements as genetic regulatory substrates in early development. Trends Cell Biol. 2013, 23, 218–226. [Google Scholar] [CrossRef] [PubMed]
  398. Piriyapongsa, J.; Marino-Ramirez, L.; Jordan, I.K. Origin and evolution of human microRNAs from transposable elements. Genetics 2007, 176, 1323–1337. [Google Scholar] [CrossRef] [PubMed]
  399. Piriyapongsa, J.; Jordan, I.K. Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 2008, 14, 814–821. [Google Scholar] [CrossRef] [PubMed]

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Shapiro, J.A. Nothing in Evolution Makes Sense Except in the Light of Genomics: Read–Write Genome Evolution as an Active Biological Process. Biology 2016, 5, 27.

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Shapiro JA. Nothing in Evolution Makes Sense Except in the Light of Genomics: Read–Write Genome Evolution as an Active Biological Process. Biology. 2016; 5(2):27.

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Shapiro, James A. 2016. "Nothing in Evolution Makes Sense Except in the Light of Genomics: Read–Write Genome Evolution as an Active Biological Process" Biology 5, no. 2: 27.

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