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Genomics and Evolution of Sauropsid Traits in the Genomics Era

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

Deadline for manuscript submissions: closed (15 November 2021) | Viewed by 13365

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Special Issue Editors

Dr. Matthew Greenwold

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Guest Editor

Department of Biology, University of Texas at Tyler, Tyler, TX 75708, USA
Interests: genome; molecular evolution; bird; feather; algae; bioinformatics

Prof. Dr. Roger Sawyer

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Guest Editor

Department of Biological Sciences, University of South Carolina, Columbia, SC 29205, USA

Special Issue Information

Dear Colleagues,

Birds have diversified to all habitats on earth, which concurrently has led to the evolution of multiple diverse and unique traits. Feathers are perhaps the most noticeable characteristic due to their vibrant colors and morphological diversity. Understanding the genetics behind the evolution of the sauropsid epidermis, feathers, and other traits such as vision, speech, and flight has been accelerated with the explosion of avian genomes in 2014 (Zhang et al. 2014). In that same year, Strasser et al. (2014) identified and characterized the chicken epidermal differentiation complex, which is a genomic locus containing over eighty genes that encode for proteins comprising the epidermis and epidermal appendages. This as well as many other studies highlight how genomics is invigorating the study of sauropsid evolution. We invite colleagues who are investigating the genetics of sauropsid traits using bird and reptile comparative genomics and other genetic methods to contribute to this Special Edition of Genes.

Dr. Matthew Greenwold
Prof. Dr. Roger Sawyer
Guest Editors

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Keywords

bird
genome
comparative genomics
integument
skin
feathers
scales
beta keratin

Published Papers (5 papers)

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Research

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13 pages, 10184 KiB

Open AccessArticle

Identification of Chicken Transglutaminase 1 and In Situ Localization of Transglutaminase Activity in Avian Skin and Esophagus

by Attila Placido Sachslehner, Marta Surbek, Julia Lachner, Surya Paudel and Leopold Eckhart

Genes 2021, 12(10), 1565; https://doi.org/10.3390/genes12101565 - 30 Sep 2021

Cited by 4 | Viewed by 2229

Abstract

Transglutaminase 1 (TGM1) is a membrane-anchored enzyme that cross-links proteins during terminal differentiation of epidermal and esophageal keratinocytes in mammals. The current genome assembly of the chicken, which is a major model for avian skin biology, does not include an annotated region corresponding to TGM1. To close this gap of knowledge about the genetic control of avian cornification, we analyzed RNA-sequencing reads from organotypic chicken skin and identified TGM1 mRNA. By RT-PCR, we demonstrated that TGM1 is expressed in the skin and esophagus of chickens. The cysteine-rich sequence motif required for palmitoylation and membrane anchorage is conserved in the chicken TGM1 protein, and differentiated chicken keratinocytes display membrane-associated transglutaminase activity. Expression of TGM1 and prominent transglutaminase activity in the esophageal epithelium was also demonstrated in the zebra finch. Altogether, the results of this study indicate that TGM1 is conserved among birds and suggest that chicken keratinocytes may be a useful model for the study of TGM1 in non-mammalian cornification. Full article

(This article belongs to the Special Issue Genomics and Evolution of Sauropsid Traits in the Genomics Era)

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15 pages, 33305 KiB

Open AccessArticle

Regional Specific Differentiation of Integumentary Organs: Regulation of Gene Clusters within the Avian Epidermal Differentiation Complex and Impacts of SATB2 Overexpression

by Gee-Way Lin, Yung-Chih Lai, Ya-Chen Liang, Randall B. Widelitz, Ping Wu and Cheng-Ming Chuong

Genes 2021, 12(8), 1291; https://doi.org/10.3390/genes12081291 - 23 Aug 2021

Cited by 5 | Viewed by 2574

Abstract

The epidermal differentiation complex (EDC) encodes a group of unique proteins expressed in late epidermal differentiation. The EDC gave integuments new physicochemical properties and is critical in evolution. Recently, we showed β-keratins, members of the EDC, undergo gene cluster switching with overexpression of SATB2 (Special AT-rich binding protein-2), considered a chromatin regulator. We wondered whether this unique regulatory mechanism is specific to β-keratins or may be derived from and common to EDC members. Here we explore (1) the systematic expression patterns of non-β-keratin EDC genes and their preferential expression in different skin appendages during development, (2) whether the expression of non-β-keratin EDC sub-clusters are also regulated in clusters by SATB2. We analyzed bulk RNA-seq and ChIP-seq data and also evaluated the disrupted expression patterns caused by overexpressing SATB2. The results show that the expression of whole EDDA and EDQM sub-clusters are possibly mediated by enhancers in E14-feathers. Overexpressing SATB2 down-regulates the enriched EDCRP sub-cluster in feathers and the EDCH sub-cluster in beaks. These results reveal the potential of complex epigenetic regulation activities within the avian EDC, implying transcriptional regulation of EDC members acting at the gene and/or gene cluster level in a temporal and skin regional-specific fashion, which may contribute to the evolution of diverse avian integuments. Full article

(This article belongs to the Special Issue Genomics and Evolution of Sauropsid Traits in the Genomics Era)

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17 pages, 3645 KiB

Open AccessArticle

Evolution of an Epidermal Differentiation Complex (EDC) Gene Family in Birds

by Anthony Davis and Matthew J. Greenwold

Genes 2021, 12(5), 767; https://doi.org/10.3390/genes12050767 - 18 May 2021

Cited by 10 | Viewed by 2420

Abstract

The transition of amniotes to a fully terrestrial lifestyle involved the adaptation of major molecular innovations to the epidermis, often in the form of epidermal appendages such as hair, scales and feathers. Feathers are diverse epidermal structures of birds, and their evolution has played a key role in the expansion of avian species to a wide range of lifestyles and habitats. As with other epidermal appendages, feather development is a complex process which involves many different genetic and protein elements. In mammals, many of the genetic elements involved in epidermal development are located at a specific genetic locus known as the epidermal differentiation complex (EDC). Studies have identified a homologous EDC locus in birds, which contains several genes expressed throughout epidermal and feather development. A family of avian EDC genes rich in aromatic amino acids that also contain MTF amino acid motifs (EDAAs/EDMTFs), that includes the previously reported histidine-rich or fast-protein (HRP/fp), an important marker in feather development, has expanded significantly in birds. Here, we characterize the EDAA gene family in birds and investigate the evolutionary history and possible functions of EDAA genes using phylogenetic and sequence analyses. We provide evidence that the EDAA gene family originated in an early archosaur ancestor, and has since expanded in birds, crocodiles and turtles, respectively. Furthermore, this study shows that the respective amino acid compositions of avian EDAAs are characteristic of structural functions associated with EDC genes and feather development. Finally, these results support the hypothesis that the genes of the EDC have evolved through tandem duplication and diversification, which has contributed to the evolution of the intricate avian epidermis and epidermal appendages. Full article

(This article belongs to the Special Issue Genomics and Evolution of Sauropsid Traits in the Genomics Era)

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11 pages, 2483 KiB

Open AccessFeature PaperArticle

The Trichohyalin-Like Protein Scaffoldin Is Expressed in the Multilayered Periderm during Development of Avian Beak and Egg Tooth

by Veronika Mlitz, Marcela Hermann, Maria Buchberger, Erwin Tschachler and Leopold Eckhart

Genes 2021, 12(2), 248; https://doi.org/10.3390/genes12020248 - 10 Feb 2021

Cited by 5 | Viewed by 2345

Abstract

Scaffoldin, an S100 fused-type protein (SFTP) with high amino acid sequence similarity to the mammalian hair follicle protein trichohyalin, has been identified in reptiles and birds, but its functions are not yet fully understood. Here, we investigated the expression pattern of scaffoldin and cornulin, a related SFTP, in the developing beaks of birds. We determined the mRNA levels of both SFTPs by reverse transcription polymerase chain reaction (RT-PCR) in the beak and other ectodermal tissues of chicken (Gallus gallus) and quail (Coturnix japonica) embryos. Immunohistochemical staining was performed to localize scaffoldin in tissues. Scaffoldin and cornulin were expressed in the beak and, at lower levels, in other embryonic tissues of both chickens and quails. Immunohistochemistry revealed scaffoldin in the peridermal compartment of the egg tooth, a transitory cornified protuberance (caruncle) on the upper beak which breaks the eggshell during hatching. Furthermore, scaffoldin marked a multilayered peridermal structure on the lower beak. The results of this study suggest that scaffoldin plays an evolutionarily conserved role in the development of the avian beak with a particular function in the morphogenesis of the egg tooth. Full article

(This article belongs to the Special Issue Genomics and Evolution of Sauropsid Traits in the Genomics Era)

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Review

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19 pages, 5199 KiB

Open AccessFeature PaperReview

Structures of the ß-Keratin Filaments and Keratin Intermediate Filaments in the Epidermal Appendages of Birds and Reptiles (Sauropsids)

by David A.D. Parry

Genes 2021, 12(4), 591; https://doi.org/10.3390/genes12040591 - 17 Apr 2021

Cited by 4 | Viewed by 2884

Abstract

The epidermal appendages of birds and reptiles (the sauropsids) include claws, scales, and feathers. Each has specialized physical properties that facilitate movement, thermal insulation, defence mechanisms, and/or the catching of prey. The mechanical attributes of each of these appendages originate from its fibril-matrix texture, where the two filamentous structures present, i.e., the corneous ß-proteins (CBP or ß-keratins) that form 3.4 nm diameter filaments and the α-fibrous molecules that form the 7–10 nm diameter keratin intermediate filaments (KIF), provide much of the required tensile properties. The matrix, which is composed of the terminal domains of the KIF molecules and the proteins of the epidermal differentiation complex (EDC) (and which include the terminal domains of the CBP), provides the appendages, with their ability to resist compression and torsion. Only by knowing the detailed structures of the individual components and the manner in which they interact with one another will a full understanding be gained of the physical properties of the tissues as a whole. Towards that end, newly-derived aspects of the detailed conformations of the two filamentous structures will be discussed and then placed in the context of former knowledge. Full article

(This article belongs to the Special Issue Genomics and Evolution of Sauropsid Traits in the Genomics Era)

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