Special Issue "Molecular Basis of Apomixis in Plants"

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Plant Genetics and Genomics".

Deadline for manuscript submissions: closed (10 June 2020) | Viewed by 24071

Special Issue Editor

Dr. Diego Hojsgaard
E-Mail Website
Guest Editor
Taxonomy & Evolutionary Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany
Interests: apomixis; evolution; genetics; genomics; hybridization; plant reproduction; polyploidy
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Sexual reproduction in plants is a highly complex, toughly regulated process leading to the creation of diaspores for a new generation: sexual seeds. Apomixis is the consequence of a concerted mechanism that exploits the sexual machinery and acts in a way to coordinate developmental pathways in the ovule to produce an asexual (clonal) seed. Altered sexual developments involve widely characterized functional and anatomical changes in meiosis, gametogenesis, and embryo and endosperm formation. In spite of recent progress uncovering specific genes related to apomixis-like phenotypes, the molecular basis and regulatory network of apomixis is still unknown. Different “traditional” and “innovative” genomics and metabolomics tools as well as rapid clearing and staining protocols and plant imaging technologies have been made available, which are facilitating developmental, genetic, and genome-wide analyses of nonmodel species, including apomictic plants. The forthcoming Special Issue aims to provide an up-to-date overview from cutting-edge molecular data on apomixis research and research using plant species displaying diverse changes on the sexual machinery. Likewise, the Special Issue will serve as a platform to explore the potential application of genome-editing approaches in apomixis research, and for discussion of most relevant hypotheses and presentation of novel ideas to improve our understanding of or resolve the still puzzled molecular basis of apomixis in plants.

Dr. Diego Hojsgaard
Guest Editor

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Keywords

  • Angiosperms
  • Meiosis
  • Gametogenesis
  • Unreduced gametes
  • Endosperm development
  • Clonal seeds
  • Genomics
  • Transcriptomics
  • Metabolomics
  • Genome editing

Published Papers (13 papers)

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Editorial

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Editorial
Molecular Basis of Apomixis in Plants
Genes 2021, 12(4), 576; https://doi.org/10.3390/genes12040576 - 16 Apr 2021
Viewed by 840
Abstract
Sexual reproduction in plants is a complex, stringently regulated process that leads to the creation of diaspores for a new generation: sexual seeds [...] Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)

Research

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Article
Whether Gametophytes Are Reduced or Unreduced in Angiosperms Might Be Determined Metabolically
Genes 2020, 11(12), 1449; https://doi.org/10.3390/genes11121449 - 02 Dec 2020
Cited by 5 | Viewed by 2492
Abstract
In angiosperms, meiotic failure coupled with the formation of genetically unreduced gametophytes in ovules (apomeiosis) constitute major components of gametophytic apomixis. These aberrant developmental events are generally thought to be caused by mutation. However, efforts to locate the responsible mutations have failed. Herein, [...] Read more.
In angiosperms, meiotic failure coupled with the formation of genetically unreduced gametophytes in ovules (apomeiosis) constitute major components of gametophytic apomixis. These aberrant developmental events are generally thought to be caused by mutation. However, efforts to locate the responsible mutations have failed. Herein, we tested a fundamentally different hypothesis: apomeiosis is a polyphenism of meiosis, with meiosis and apomeiosis being maintained by different states of metabolic homeostasis. Microarray analyses of ovules and pistils were used to differentiate meiotic from apomeiotic processes in Boechera (Brassicaceae). Genes associated with translation, cell division, epigenetic silencing, flowering, and meiosis characterized sexual Boechera (meiotic). In contrast, genes associated with stress responses, abscisic acid signaling, reactive oxygen species production, and stress attenuation mechanisms characterized apomictic Boechera (apomeiotic). We next tested whether these metabolic differences regulate reproductive mode. Apomeiosis switched to meiosis when premeiotic ovules of apomicts were cultured on media that increased oxidative stress. These treatments included drought, starvation, and H2O2 applications. In contrast, meiosis switched to apomeiosis when premeiotic pistils of sexual plants were cultured on media that relieved oxidative stress. These treatments included antioxidants, glucose, abscisic acid, fluridone, and 5-azacytidine. High-frequency apomeiosis was initiated in all sexual species tested: Brassicaceae, Boechera stricta, Boechera exilis, and Arabidopsis thaliana; Fabaceae, Vigna unguiculata; Asteraceae, Antennaria dioica. Unreduced gametophytes formed from ameiotic female and male sporocytes, first division restitution dyads, and nucellar cells. These results are consistent with modes of reproduction and types of apomixis, in natural apomicts, being regulated metabolically. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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Article
Haploidy in Tobacco Induced by PsASGR-BBML Transgenes via Parthenogenesis
Genes 2020, 11(9), 1072; https://doi.org/10.3390/genes11091072 - 12 Sep 2020
Cited by 10 | Viewed by 1227
Abstract
Background: Engineering apomixis in sexually reproducing plants has been long desired because of the potential to fix hybrid vigor. Validating the functionality of genes originated from apomictic species that contribute to apomixis upon transfer to sexually reproducing species is an important step. The [...] Read more.
Background: Engineering apomixis in sexually reproducing plants has been long desired because of the potential to fix hybrid vigor. Validating the functionality of genes originated from apomictic species that contribute to apomixis upon transfer to sexually reproducing species is an important step. The PsASGR-BABYBOOM-like (PsASGR-BBML) gene from Pennisetum squamulatum confers parthenogenesis in this apomict, and its functionality was demonstrated in several sexually reproducing monocots but not in any dicots. Methods: We introduced the PsASGR-BBML gene regulated by egg cell-specific promoters, either AtDD45 or AtRKD2, into tobacco, and analyzed progeny of the transgenic lines resulting from self-pollination and crossing by flow cytometry. Results: We identified haploid progeny at a frequency lower than 1% in the AtDD45pro lines, while at a frequency of 9.3% for an octoploid (2n = 8x) AtRKD2pro line. Haploid production in the T2 generation, derived from the tetraploid T1 offspring of this original octoploid AtRKD2pro line, was also observed. Pollinated by homozygous transgenic tobacco carrying a DsRed marker gene, 4x progeny of the AtRKD2pro line yielded parthenogenetic embryos identified as DsRed negative. We verified that the DsRed negative seedlings recovered were haploid (2x). Conclusion: The PsASGR-BBML gene regulated by egg cell-specific promoters could enable parthenogenesis in tobacco, a dicotyledon species. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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Article
Efficient CRISPR/Cas9-Mediated Knockout of an Endogenous PHYTOENE DESATURASE Gene in T1 Progeny of Apomictic Hieracium Enables New Strategies for Apomixis Gene Identification
Genes 2020, 11(9), 1064; https://doi.org/10.3390/genes11091064 - 10 Sep 2020
Cited by 3 | Viewed by 2055
Abstract
Most Hieracium subgenus Pilosella species are self-incompatible. Some undergo facultative apomixis where most seeds form asexually with a maternal genotype. Most embryo sacs develop by mitosis, without meiosis and seeds form without fertilization. Apomixis is controlled by dominant loci where recombination is suppressed. [...] Read more.
Most Hieracium subgenus Pilosella species are self-incompatible. Some undergo facultative apomixis where most seeds form asexually with a maternal genotype. Most embryo sacs develop by mitosis, without meiosis and seeds form without fertilization. Apomixis is controlled by dominant loci where recombination is suppressed. Loci deletion by γ-irradiation results in reversion to sexual reproduction. Targeted mutagenesis of genes at identified loci would facilitate causal gene identification. In this study, the efficacy of CRISPR/Cas9 editing was examined in apomictic Hieracium by targeting mutations in the endogenous PHYTOENE DESATURASE (PDS) gene using Agrobacterium-mediated leaf disk transformation. In three experiments, the expected albino dwarf-lethal phenotype, characteristic of PDS knockout, was evident in 11% of T0 plants, 31.4% were sectorial albino chimeras, and the remainder were green. The chimeric plants flowered. Germinated T1 seeds derived from apomictic reproduction in two chimeric plants were phenotyped and sequenced to identify PDS gene edits. Up to 86% of seeds produced albino seedlings with complete PDS knockout. This was attributed to continuing Cas9-mediated editing in chimeric plants during apomictic seed formation preventing Cas9 segregation from the PDS target. This successful demonstration of efficient CRISPR/Cas9 gene editing in apomictic Hieracium, enabled development of the discussed strategies for future identification of causal apomixis genes. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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Article
Genes Modulating the Increase in Sexuality in the Facultative Diplosporous Grass Eragrostis curvula under Water Stress Conditions
Genes 2020, 11(9), 969; https://doi.org/10.3390/genes11090969 - 21 Aug 2020
Cited by 8 | Viewed by 1037
Abstract
Eragrostis curvula presents mainly facultative genotypes that reproduce by diplosporous apomixis, retaining a percentage of sexual pistils that increase under drought and other stressful situations, indicating that some regulators activated by stress could be affecting the apomixis/sexual switch. Water stress experiments were performed [...] Read more.
Eragrostis curvula presents mainly facultative genotypes that reproduce by diplosporous apomixis, retaining a percentage of sexual pistils that increase under drought and other stressful situations, indicating that some regulators activated by stress could be affecting the apomixis/sexual switch. Water stress experiments were performed in order to associate the increase in sexual embryo sacs with the differential expression of genes in a facultative apomictic cultivar using cytoembryology and RNA sequencing. The percentage of sexual embryo sacs increased from 4 to 24% and 501 out of the 201,011 transcripts were differentially expressed (DE) between control and stressed plants. DE transcripts were compared with previous transcriptomes where apomictic and sexual genotypes were contrasted. The results point as candidates to transcripts related to methylation, ubiquitination, hormone and signal transduction pathways, transcription regulation and cell wall biosynthesis, some acting as a general response to stress and some that are specific to the reproductive mode. We suggest that a DNA glycosylase EcROS1-like could be demethylating, thus de-repressing a gene or genes involved in the sexuality pathways. Many of the other DE transcripts could be part of a complex mechanism that regulates apomixis and sexuality in this grass, the ones in the intersection between control/stress and apo/sex being the strongest candidates. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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Article
Genetic Dissection of Apomixis in Dandelions Identifies a Dominant Parthenogenesis Locus and Highlights the Complexity of Autonomous Endosperm Formation
Genes 2020, 11(9), 961; https://doi.org/10.3390/genes11090961 - 20 Aug 2020
Cited by 5 | Viewed by 1881
Abstract
Apomixis in the common dandelion (Taraxacum officinale) consists of three developmental components: diplospory (apomeiosis), parthenogenesis, and autonomous endosperm development. The genetic basis of diplospory, which is inherited as a single dominant factor, has been previously elucidated. To uncover the genetic basis [...] Read more.
Apomixis in the common dandelion (Taraxacum officinale) consists of three developmental components: diplospory (apomeiosis), parthenogenesis, and autonomous endosperm development. The genetic basis of diplospory, which is inherited as a single dominant factor, has been previously elucidated. To uncover the genetic basis of the remaining components, a cross between a diploid sexual seed parent and a triploid apomictic pollen donor was made. The resulting 95 triploid progeny plants were genotyped with co-dominant simple-sequence repeat (SSR) markers and phenotyped for apomixis as a whole and for the individual apomixis components using Nomarski Differential Interference Contrast (DIC) microscopy of cleared ovules and seed flow cytometry. From this, a new SSR marker allele was discovered that was closely linked to parthenogenesis and unlinked to diplospory. The segregation of apomixis as a whole does not differ significantly from a three-locus model, with diplospory and parthenogenesis segregating as unlinked dominant loci. Autonomous endosperm is regularly present without parthenogenesis, suggesting that the parthenogenesis locus does not also control endosperm formation. However, the high recovery of autonomous endosperm is inconsistent with this phenotype segregating as the third dominant locus. These results highlight the genetic complexity underlying apomixis in the dandelion and underline the challenge of introducing autonomous apomixis into sexual crops. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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Article
The Role of APOSTART in Switching between Sexuality and Apomixis in Poa pratensis
Genes 2020, 11(8), 941; https://doi.org/10.3390/genes11080941 - 14 Aug 2020
Cited by 5 | Viewed by 1917
Abstract
The production of seeds without sex is considered the holy grail of plant biology. The transfer of apomixis to various crop species has the potential to transform plant breeding, since it will allow new varieties to retain valuable traits thorough asexual reproduction. Therefore, [...] Read more.
The production of seeds without sex is considered the holy grail of plant biology. The transfer of apomixis to various crop species has the potential to transform plant breeding, since it will allow new varieties to retain valuable traits thorough asexual reproduction. Therefore, a greater molecular understanding of apomixis is fundamental. In a previous work we identified a gene, namely APOSTART, that seemed to be involved in this asexual mode of reproduction, which is very common in Poa pratensis L., and here we present a detailed work aimed at clarifying its role in apomixis. In situ hybridization showed that PpAPOSTART is expressed in reproductive tissues from pre-meiosis to embryo development. Interestingly, it is expressed early in few nucellar cells of apomictic individuals possibly switching from a somatic to a reproductive cell as in aposporic apomixis. Moreover, out of 13 APOSTART members, we identified one, APOSTART_6, as specifically expressed in flower tissue. APOSTART_6 also exhibited delayed expression in apomictic genotypes when compared with sexual types. Most importantly, the SCAR (Sequence Characterized Amplified Region) derived from the APOSTART_6 sequence completely co-segregated with apomixis. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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Article
Chasing the Apomictic Factors in the Ranunculus auricomus Complex: Exploring Gene Expression Patterns in Microdissected Sexual and Apomictic Ovules
Genes 2020, 11(7), 728; https://doi.org/10.3390/genes11070728 - 30 Jun 2020
Cited by 9 | Viewed by 1251
Abstract
Apomixis, the asexual reproduction via seeds, is associated to polyploidy and hybridization. To identify possible signatures of apomixis, and possible candidate genes underlying the shift from sex to apomixis, microarray-based gene expression patterns of live microdissected ovules at four different developmental stages were [...] Read more.
Apomixis, the asexual reproduction via seeds, is associated to polyploidy and hybridization. To identify possible signatures of apomixis, and possible candidate genes underlying the shift from sex to apomixis, microarray-based gene expression patterns of live microdissected ovules at four different developmental stages were compared between apomictic and sexual individuals of the Ranunculus auricomus complex. Following predictions from previous work on mechanisms underlying apomixis penetrance and expressivity in the genus, gene expression patterns were classified into three categories based on their relative expression in apomicts compared to their sexual parental ancestors. We found evidence of misregulation and differential gene expression between apomicts and sexuals, with the highest number of differences detected during meiosis progression and emergence of aposporous initial (AI) cells, a key developmental stage in the ovule of apomicts where a decision between divergent reproductive pathways takes place. While most of the differentially expressed genes (DEGs) could not be annotated, gene expression was classified into transgressive, parent of origin and ploidy effects. Genes related to gametogenesis and meiosis demonstrated patterns reflective of transgressive and genome dosage effects, which support the hypothesis of a dominant factor controlling apomixis in Ranunculus and modulated by secondary modifiers. Three genes with probable functions in sporogenesis and gametogenesis development are identified and characterized for future studies. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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Review

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Review
How to Become an Apomixis Model: The Multifaceted Case of Paspalum
Genes 2020, 11(9), 974; https://doi.org/10.3390/genes11090974 - 21 Aug 2020
Cited by 8 | Viewed by 1183
Abstract
In the past decades, the grasses of the Paspalum genus have emerged as a versatile model allowing evolutionary, genetic, molecular, and developmental studies on apomixis as well as successful breeding applications. The rise of such an archetypal system progressed through integrative phases, which [...] Read more.
In the past decades, the grasses of the Paspalum genus have emerged as a versatile model allowing evolutionary, genetic, molecular, and developmental studies on apomixis as well as successful breeding applications. The rise of such an archetypal system progressed through integrative phases, which were essential to draw conclusions based on solid standards. Here, we review the steps adopted in Paspalum to establish the current body of knowledge on apomixis and provide model breeding programs for other agronomically important apomictic crops. In particular, we discuss the need for previous detailed cytoembryological and cytogenetic germplasm characterization; the establishment of sexual and apomictic materials of identical ploidy level; the development of segregating populations useful for inheritance analysis, positional mapping, and epigenetic control studies; the development of omics data resources; the identification of key molecular pathways via comparative gene expression studies; the accurate molecular characterization of genomic loci governing apomixis; the in-depth functional analysis of selected candidate genes in apomictic and model species; the successful building of a sexual/apomictic combined breeding scheme. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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Review
A Reappraisal of the Evolutionary and Developmental Pathway of Apomixis and Its Genetic Control in Angiosperms
Genes 2020, 11(8), 859; https://doi.org/10.3390/genes11080859 - 28 Jul 2020
Cited by 9 | Viewed by 1436
Abstract
Apomixis sensu stricto (agamospermy) is asexual reproduction by seed. In angiosperms it represents an easy byway of life cycle renewal through gamete-like cells that give rise to maternal embryos without ploidy reduction (meiosis) and ploidy restitution (syngamy). The origin of apomixis still represents [...] Read more.
Apomixis sensu stricto (agamospermy) is asexual reproduction by seed. In angiosperms it represents an easy byway of life cycle renewal through gamete-like cells that give rise to maternal embryos without ploidy reduction (meiosis) and ploidy restitution (syngamy). The origin of apomixis still represents an unsolved problem, as it may be either evolved from sex or the other way around. This review deals with a reappraisal of the origin of apomixis in order to deepen knowledge on such asexual mode of reproduction which seems mainly lacking in the most basal angiosperm orders (i.e., Amborellales, Nymphaeales and Austrobaileyales, also known as ANA-grade), while it clearly occurs in different forms and variants in many unrelated families of monocots and eudicots. Overall findings strengthen the hypothesis that apomixis as a whole may have evolved multiple times in angiosperm evolution following different developmental pathways deviating to different extents from sexuality. Recent developments on the genetic control of apomixis in model species are also presented and adequately discussed in order to shed additional light on the antagonist theories of gain- and loss-of-function over sexuality. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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Review
Controlling Apomixis: Shared Features and Distinct Characteristics of Gene Regulation
Genes 2020, 11(3), 329; https://doi.org/10.3390/genes11030329 - 20 Mar 2020
Cited by 30 | Viewed by 3028
Abstract
In higher plants, sexual and asexual reproduction through seeds (apomixis) have evolved as alternative strategies. As apomixis leads to the formation of clonal offspring, its great potential for agricultural applications has long been recognized. However, the genetic basis and the molecular control underlying [...] Read more.
In higher plants, sexual and asexual reproduction through seeds (apomixis) have evolved as alternative strategies. As apomixis leads to the formation of clonal offspring, its great potential for agricultural applications has long been recognized. However, the genetic basis and the molecular control underlying apomixis and its evolutionary origin are to date not fully understood. Both in sexual and apomictic plants, reproduction is tightly controlled by versatile mechanisms regulating gene expression, translation, and protein abundance and activity. Increasing evidence suggests that interrelated pathways including epigenetic regulation, cell-cycle control, hormonal pathways, and signal transduction processes are relevant for apomixis. Additional molecular mechanisms are being identified that involve the activity of DNA- and RNA-binding proteins, such as RNA helicases which are increasingly recognized as important regulators of reproduction. Together with other factors including non-coding RNAs, their association with ribosomes is likely to be relevant for the formation and specification of the apomictic reproductive lineage. Subsequent seed formation appears to involve an interplay of transcriptional activation and repression of developmental programs by epigenetic regulatory mechanisms. In this review, insights into the genetic basis and molecular control of apomixis are presented, also taking into account potential relations to environmental stress, and considering aspects of evolution. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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Other

Discussion
Can We Use Gene-Editing to Induce Apomixis in Sexual Plants?
Genes 2020, 11(7), 781; https://doi.org/10.3390/genes11070781 - 12 Jul 2020
Cited by 9 | Viewed by 2490
Abstract
Apomixis, the asexual formation of seeds, is a potentially valuable agricultural trait. Inducing apomixis in sexual crop plants would, for example, allow breeders to fix heterosis in hybrid seeds and rapidly generate doubled haploid crop lines. Molecular models explain the emergence of functional [...] Read more.
Apomixis, the asexual formation of seeds, is a potentially valuable agricultural trait. Inducing apomixis in sexual crop plants would, for example, allow breeders to fix heterosis in hybrid seeds and rapidly generate doubled haploid crop lines. Molecular models explain the emergence of functional apomixis, i.e., apomeiosis + parthenogenesis + endosperm development, as resulting from a combination of genetic or epigenetic changes that coordinate altered molecular and developmental steps to form clonal seeds. Apomixis-like features and synthetic clonal seeds have been induced with limited success in the sexual plants rice and maize by using gene editing to mutate genes related to meiosis and fertility or via egg-cell specific expression of embryogenesis genes. Inducing functional apomixis and increasing the penetrance of apomictic seed production will be important for commercial deployment of the trait. Optimizing the induction of apomixis with gene editing strategies that use known targets as well as identifying alternative targets will be possible by better understanding natural genetic variation in apomictic species. With the growing availability of genomic data and precise gene editing tools, we are making substantial progress towards engineering apomictic crops. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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Opinion
Apomixis Technology: Separating the Wheat from the Chaff
Genes 2020, 11(4), 411; https://doi.org/10.3390/genes11040411 - 10 Apr 2020
Cited by 15 | Viewed by 1747
Abstract
Projections indicate that current plant breeding approaches will be unable to incorporate the global crop yields needed to deliver global food security. Apomixis is a disruptive innovation by which a plant produces clonal seeds capturing heterosis and gene combinations of elite phenotypes. Introducing [...] Read more.
Projections indicate that current plant breeding approaches will be unable to incorporate the global crop yields needed to deliver global food security. Apomixis is a disruptive innovation by which a plant produces clonal seeds capturing heterosis and gene combinations of elite phenotypes. Introducing apomixis into hybrid cultivars is a game-changing development in the current plant breeding paradigm that will accelerate the generation of high-yield cultivars. However, apomixis is a developmentally complex and genetically multifaceted trait. The central problem behind current constraints to apomixis breeding is that the genomic configuration and molecular mechanism that initiate apomixis and guide the formation of a clonal seed are still unknown. Today, not a single explanation about the origin of apomixis offer full empirical coverage, and synthesizing apomixis by manipulating individual genes has failed or produced little success. Overall evidence suggests apomixis arise from a still unknown single event molecular mechanism with multigenic effects. Disentangling the genomic basis and complex genetics behind the emergence of apomixis in plants will require the use of novel experimental approaches benefiting from Next Generation Sequencing technologies and targeting not only reproductive genes, but also the epigenetic and genomic configurations associated with reproductive phenotypes in homoploid sexual and apomictic carriers. A comprehensive picture of most regulatory changes guiding apomixis emergence will be central for successfully installing apomixis into the target species by exploiting genetic modification techniques. Full article
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
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