EvodevoPub Date : 2023-07-27DOI: 10.1186/s13227-023-00216-w
Kohei Oguchi, Toru Miura
{"title":"Upregulation of Hox genes leading to caste-specific morphogenesis in a termite.","authors":"Kohei Oguchi, Toru Miura","doi":"10.1186/s13227-023-00216-w","DOIUrl":"https://doi.org/10.1186/s13227-023-00216-w","url":null,"abstract":"<p><strong>Background: </strong>In social insects, interactions among colony members trigger caste differentiation with morphological modifications. In termite caste differentiation, caste-specific morphologies (such as mandibles in soldiers, genital organs in reproductives or wings in alates) are well developed during post-embryonic development under endocrine controls (e.g., juvenile hormone and ecdysone). Since body part-specific morphogenesis in caste differentiation is hormonally regulated by global factors circulated throughout the body, positional information should be required for the caste-specific and also body part-specific morphogenesis. To identify factors providing the positional information, expression and functional analyses of eight Hox genes were carried out during the three types of caste differentiation (i.e., soldier, neotenic and alate differentiation) in a termite, Hodotermopsis sjostedti.</p><p><strong>Results: </strong>Spatio-temporal patterns of Hox gene expression during caste differentiation were elucidated by real-time qPCR, showing the caste-specific upregulations of Hox genes during the differentiation processes. Among eight Hox genes, Deformed (Dfd) was upregulated specifically in mandibles in soldier differentiation, abdominal-A (abd-A) and Abdominal-B (Abd-B) were upregulated in the abdomen in neotenic differentiation, while Sex-comb reduced (Scr) and Antennapedia (Antp) were upregulated during alate differentiation. Furthermore, RNAi knockdown of Dfd in soldier differentiation and of abd-A and Abd-B in neotenic differentiation distorted the modifications of caste-specific morphologies.</p><p><strong>Conclusions: </strong>Gene expression and functional analyses in this study revealed that, in the caste differentiation in termites, upregulation of Hox genes provide positional identities of body segments, resulting in the caste-specific morphogenesis. The acquisition of such developmental modifications would have enabled the evolution of sophisticated caste systems in termites.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":"14 1","pages":"12"},"PeriodicalIF":4.1,"publicationDate":"2023-07-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10375622/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10251491","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Expression and possible functions of a horizontally transferred glycosyl hydrolase gene, GH6-1, in Ciona embryogenesis.","authors":"Kun-Lung Li, Keisuke Nakashima, Kanako Hisata, Noriyuki Satoh","doi":"10.1186/s13227-023-00215-x","DOIUrl":"https://doi.org/10.1186/s13227-023-00215-x","url":null,"abstract":"<p><strong>Background: </strong>The Tunicata or Urochordata is the only animal group with the ability to synthesize cellulose directly and cellulose is a component of the tunic that covers the entire tunicate body. The genome of Ciona intestinalis type A contains a cellulose synthase gene, CesA, that it acquired via an ancient, horizontal gene transfer. CesA is expressed in embryonic epidermal cells and functions in cellulose production. Ciona CesA is composed of both a glycosyltransferase domain, GT2, and a glycosyl hydrolase domain, GH6, which shows a mutation at a key position and seems functionless. Interestingly, the Ciona genome contains a glycosyl hydrolase gene, GH6-1, in which the GH6 domain seems intact. This suggests expression and possible functions of GH6-1 during Ciona embryogenesis. Is GH6-1 expressed during embryogenesis? If so, in what tissues is the gene expressed? Does GH6-1 serve a function? If so, what is it? Answers to these questions may advance our understanding of evolution of this unique animal group.</p><p><strong>Results: </strong>Quantitative reverse transcription PCR and in situ hybridization revealed that GH6-1 is expressed in epidermis of tailbud embryos and in early swimming larvae, a pattern similar to that of CesA. Expression is downregulated at later stages and becomes undetectable in metamorphosed juveniles. The GH6-1 expression level is higher in the anterior-trunk region and caudal-tip regions of late embryos. Single-cell RNA sequencing analysis of the late tailbud stage showed that cells of three clusters with epidermal identity express GH6-1, and that some of them co-express CesA. TALEN-mediated genome editing was used to generate GH6-1 knockout Ciona larvae. Around half of TALEN-electroporated larvae showed abnormal development of adhesive papillae and altered distribution of surface cellulose. In addition, three-fourths of TALEN-electroporated animals failed to complete larval metamorphosis.</p><p><strong>Conclusions: </strong>This study showed that tunicate GH6-1, a gene that originated by horizontal gene transfer of a prokaryote gene, is recruited into the ascidian genome, and that it is expressed and functions in epidermal cells of ascidian embryos. Although further research is required, this observation demonstrates that both CesA and GH6-1 are involved in tunicate cellulose metabolism, impacting tunicate morphology and ecology.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":"14 1","pages":"11"},"PeriodicalIF":4.1,"publicationDate":"2023-07-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10334666/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10190707","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
EvodevoPub Date : 2023-06-16DOI: 10.1186/s13227-023-00214-y
Abdull Jesus Massri, Brennan McDonald, Gregory A Wray, David R McClay
{"title":"Feedback circuits are numerous in embryonic gene regulatory networks and offer a stabilizing influence on evolution of those networks.","authors":"Abdull Jesus Massri, Brennan McDonald, Gregory A Wray, David R McClay","doi":"10.1186/s13227-023-00214-y","DOIUrl":"https://doi.org/10.1186/s13227-023-00214-y","url":null,"abstract":"<p><p>The developmental gene regulatory networks (dGRNs) of two sea urchin species, Lytechinus variegatus (Lv) and Strongylocentrotus purpuratus (Sp), have remained remarkably similar despite about 50 million years since a common ancestor. Hundreds of parallel experimental perturbations of transcription factors with similar outcomes support this conclusion. A recent scRNA-seq analysis suggested that the earliest expression of several genes within the dGRNs differs between Lv and Sp. Here, we present a careful reanalysis of the dGRNs in these two species, paying close attention to timing of first expression. We find that initial expression of genes critical for cell fate specification occurs during several compressed time periods in both species. Previously unrecognized feedback circuits are inferred from the temporally corrected dGRNs. Although many of these feedbacks differ in location within the respective GRNs, the overall number is similar between species. We identify several prominent differences in timing of first expression for key developmental regulatory genes; comparison with a third species indicates that these heterochronies likely originated in an unbiased manner with respect to embryonic cell lineage and evolutionary branch. Together, these results suggest that interactions can evolve even within highly conserved dGRNs and that feedback circuits may buffer the effects of heterochronies in the expression of key regulatory genes.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":"14 1","pages":"10"},"PeriodicalIF":4.1,"publicationDate":"2023-06-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10273620/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10034859","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
EvodevoPub Date : 2023-05-06DOI: 10.1186/s13227-023-00213-z
Haeli J Lomheim, Lizet Reyes Rodas, Lubna Mulla, Layla Freeborn, Dennis A Sun, Sheri A Sanders, Meredith E Protas
{"title":"Transcriptomic analysis of cave, surface, and hybrid samples of the isopod Asellus aquaticus and identification of chromosomal location of candidate genes for cave phenotype evolution.","authors":"Haeli J Lomheim, Lizet Reyes Rodas, Lubna Mulla, Layla Freeborn, Dennis A Sun, Sheri A Sanders, Meredith E Protas","doi":"10.1186/s13227-023-00213-z","DOIUrl":"10.1186/s13227-023-00213-z","url":null,"abstract":"<p><strong>Background: </strong>Transcriptomic methods can be used to elucidate genes and pathways responsible for phenotypic differences between populations. Asellus aquaticus is a freshwater isopod crustacean with surface- and cave-dwelling ecomorphs that differ greatly in multiple phenotypes including pigmentation and eye size. Multiple genetic resources have been generated for this species, but the genes and pathways responsible for cave-specific characteristics have not yet been identified. Our goal was to generate transcriptomic resources in tandem with taking advantage of the species' ability to interbreed and generate hybrid individuals.</p><p><strong>Results: </strong>We generated transcriptomes of the Rakov Škocjan surface population and the Rak Channel of Planina Cave population that combined Illumina short-read assemblies and PacBio Iso-seq long-read sequences. We investigated differential expression at two different embryonic time points as well as allele-specific expression of F<sub>1</sub> hybrids between cave and surface individuals. RNAseq of F<sub>2</sub> hybrids, as well as genotyping of a backcross, allowed for positional information of multiple candidate genes from the differential expression and allele-specific analyses.</p><p><strong>Conclusions: </strong>As expected, genes involved in phototransduction and ommochrome synthesis were under-expressed in the cave samples as compared to the surface samples. Allele-specific expression analysis of F<sub>1</sub> hybrids identified genes with cave-biased (cave allele has higher mRNA levels than the surface allele) and surface-biased expression (surface allele has higher mRNA levels than the cave allele). RNAseq of F<sub>2</sub> hybrids allowed for multiple genes to be placed to previously mapped genomic regions responsible for eye and pigmentation phenotypes. In the future, these transcriptomic resources will guide prioritization of candidates for functional analysis.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":"14 1","pages":"9"},"PeriodicalIF":4.1,"publicationDate":"2023-05-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10163715/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9605535","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
EvodevoPub Date : 2023-05-05DOI: 10.1186/s13227-023-00211-1
Zachary D Root, David Jandzik, Claire Gould, Cara Allen, Margaux Brewer, Daniel M Medeiros
{"title":"Cartilage diversification and modularity drove the evolution of the ancestral vertebrate head skeleton.","authors":"Zachary D Root, David Jandzik, Claire Gould, Cara Allen, Margaux Brewer, Daniel M Medeiros","doi":"10.1186/s13227-023-00211-1","DOIUrl":"10.1186/s13227-023-00211-1","url":null,"abstract":"<p><p>The vertebrate head skeleton has evolved a myriad of forms since their divergence from invertebrate chordates. The connection between novel gene expression and cell types is therefore of importance in this process. The transformation of the jawed vertebrate (gnathostome) head skeleton from oral cirri to jointed jaw elements required a diversity of cartilages as well as changes in the patterning of these tissues. Although lampreys are a sister clade to gnathostomes, they display skeletal diversity with distinct gene expression and histologies, a useful model for addressing joint evolution. Specifically, the lamprey tissue known as mucocartilage has noted similarities with the jointed elements of the mandibular arch in jawed vertebrates. We thus asked whether the cells in lamprey mucocartilage and gnathostome joint tissue could be considered homologous. To do this, we characterized new genes that are involved in gnathostome joint formation and characterized the histochemical properties of lamprey skeletal types. We find that most of these genes are minimally found in mucocartilage and are likely later innovations, but we do identify new activity for gdf5/6/7b in both hyaline and mucocartilage, supporting its role as a chondrogenic regulator. Contrary to previous works, our histological assays do not find any perichondrial fibroblasts surrounding mucocartilage, suggesting that mucocartilage is non-skeletogenic tissue that is partially chondrified. Interestingly, we also identify new histochemical features of the lamprey otic capsule that diverge from normal hyaline. Paired with our new insights into lamprey mucocartilage, we propose a broader framework for skeletal evolution in which an ancestral soxD/E and gdf5/6/7 network directs mesenchyme along a spectrum of cartilage-like features.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":"14 1","pages":"8"},"PeriodicalIF":4.1,"publicationDate":"2023-05-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10161429/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9424662","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Early expression onset of tissue-specific effector genes during the specification process in sea urchin embryos.","authors":"Shumpei Yamakawa, Atsuko Yamazaki, Yoshiaki Morino, Hiroshi Wada","doi":"10.1186/s13227-023-00210-2","DOIUrl":"https://doi.org/10.1186/s13227-023-00210-2","url":null,"abstract":"<p><strong>Background: </strong>In the course of animal developmental processes, various tissues are differentiated through complex interactions within the gene regulatory network. As a general concept, differentiation has been considered to be the endpoint of specification processes. Previous works followed this view and provided a genetic control scheme of differentiation in sea urchin embryos: early specification genes generate distinct regulatory territories in an embryo to express a small set of differentiation driver genes; these genes eventually stimulate the expression of tissue-specific effector genes, which provide biological identity to differentiated cells, in each region. However, some tissue-specific effector genes begin to be expressed in parallel with the expression onset of early specification genes, raising questions about the simplistic regulatory scheme of tissue-specific effector gene expression and the current concept of differentiation itself.</p><p><strong>Results: </strong>Here, we examined the dynamics of effector gene expression patterns during sea urchin embryogenesis. Our transcriptome-based analysis indicated that many tissue-specific effector genes begin to be expressed and accumulated along with the advancing specification GRN in the distinct cell lineages of embryos. Moreover, we found that the expression of some of the tissue-specific effector genes commences before cell lineage segregation occurs.</p><p><strong>Conclusions: </strong>Based on this finding, we propose that the expression onset of tissue-specific effector genes is controlled more dynamically than suggested in the previously proposed simplistic regulation scheme. Thus, we suggest that differentiation should be conceptualized as a seamless process of accumulation of effector expression along with the advancing specification GRN. This pattern of effector gene expression may have interesting implications for the evolution of novel cell types.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":"14 1","pages":"7"},"PeriodicalIF":4.1,"publicationDate":"2023-04-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10131483/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9359686","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
EvodevoPub Date : 2023-04-19DOI: 10.1186/s13227-023-00212-0
Noura Jabr, Paul Gonzalez, Kevin M Kocot, Christopher B Cameron
{"title":"The embryology, metamorphosis, and muscle development of Schizocardium karankawa sp. nov. (Enteropneusta) from the Gulf of Mexico.","authors":"Noura Jabr, Paul Gonzalez, Kevin M Kocot, Christopher B Cameron","doi":"10.1186/s13227-023-00212-0","DOIUrl":"https://doi.org/10.1186/s13227-023-00212-0","url":null,"abstract":"<p><p>Schizocardium karankawa sp. nov. has been collected from subtidal muds of the Laguna Madre, Texas, and the Mississippi coast, Gulf of Mexico. The Texas population is reproductive from early February to mid-April. Gametes are liberated by a small incision in a gonad. Oocyte germinal vesicle breakdown is increased in the presence of sperm, and the highest fertilization success was in the artificial seawater Jamarin U. Manually dechorionated embryos develop normally. Development was asynchronous via a tornaria larva, metamorphosis and maintained to the juvenile worm 6 gill-pore stage. Phalloidin-labeled late-stage tornaria revealed retractor muscles that connect the pericardial sac with the apical tuft anteriorly, the oesophagus ventrally, and muscle cells of the early mesocoels. The muscle development of early juvenile worms began with dorso-lateral trunk muscles, lateral trunk bands, and sphincters around the gill pores and anus. Adult worms are characterized by a stomochord that bifurcates anteriorly into paired vermiform processes, gill bars that extend almost the entire dorsal to ventral branchial region resulting in a narrow ventral hypobranchial ridge, and an elaborate epibranchial organ with six zones of discrete cell types. The trunk has up to three rows of liver sacs, and lateral gonads. The acorn worm evo-devo model species Saccoglossus kowalevskii, Ptychodera flava, and Schizocardium californicum are phylogenetically distant with disparate life histories. S. karnakawa from S. californicum are phylogenetically close, and differences between them that become apparent as adult worms include the number of gill pores and hepatic sacs, and elaborations of the heart-kidney-stomochord complex. An important challenge for evolutionary developmental biology is to form links from phylogenetically distant and large-scale differences to phylogenetically close and small-scale differences. This description of the embryology, development, and adult morphology of S. karankawa permits investigations into how acorn worm development evolves at fine scales.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":"14 1","pages":"6"},"PeriodicalIF":4.1,"publicationDate":"2023-04-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10114407/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9773349","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
EvodevoPub Date : 2023-04-06DOI: 10.1186/s13227-023-00209-9
Yuxiu Xia, Pin Huan, Baozhong Liu
{"title":"Shell field morphogenesis in the polyplacophoran mollusk Acanthochitona rubrolineata.","authors":"Yuxiu Xia, Pin Huan, Baozhong Liu","doi":"10.1186/s13227-023-00209-9","DOIUrl":"https://doi.org/10.1186/s13227-023-00209-9","url":null,"abstract":"<p><strong>Background: </strong>The polyplacophoran mollusks (chitons) possess serially arranged shell plates. This feature is unique among mollusks and believed to be essential to explore the evolution of mollusks as well as their shells. Previous studies revealed several cell populations in the dorsal epithelium (shell field) of polyplacophoran larvae and their roles in the formation of shell plates. Nevertheless, they provide limited molecular information, and shell field morphogenesis remains largely uninvestigated.</p><p><strong>Results: </strong>In the present study, we investigated shell field development in the chiton Acanthochitona rubrolineata based on morphological characteristics and molecular patterns. A total of four types of tissue could be recognized from the shell field of A. rubrolineata. The shell field comprised not only the centrally located, alternatively arranged plate fields and ridges, but also the tissues surrounding them, which were the precursors of the girdle and we termed as the girdle field. The girdle field exhibited a concentric organization composed of two circularly arranged tissues, and spicules were only developed in the outer circle. Dynamic engrailed expression and F-actin (filamentous actin) distributions revealed relatively complicated morphogenesis of the shell field. The repeated units (plate fields and ridges) were gradually established in the shell field, seemingly different from the manners used in the segmentation of Drosophila or vertebrates. The seven repeated ridges also experienced different modes of ontogenesis from each other. In the girdle field, the presumptive spicule-formation cells exhibited different patterns of F-actin aggregations as they differentiate.</p><p><strong>Conclusions: </strong>These results reveal the details concerning the structure of polyplacophoran shell field as well as its morphogenesis. They would contribute to exploring the mechanisms of polyplacophoran shell development and molluscan shell evolution.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":"14 1","pages":"5"},"PeriodicalIF":4.1,"publicationDate":"2023-04-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10080879/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9651486","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Stability in gene expression and body-plan development leads to evolutionary conservation.","authors":"Yui Uchida, Hiroyuki Takeda, Chikara Furusawa, Naoki Irie","doi":"10.1186/s13227-023-00208-w","DOIUrl":"https://doi.org/10.1186/s13227-023-00208-w","url":null,"abstract":"<p><strong>Background: </strong>Phenotypic evolution is mainly explained by selection for phenotypic variation arising from factors including mutation and environmental noise. Recent theoretical and experimental studies have suggested that phenotypes with greater developmental stability tend to have a constant phenotype and gene expression level within a particular genetic and environmental condition, and this positively correlates with stronger evolutionary conservation, even after the accumulation of genetic changes. This could reflect a novel mechanism that contributes to evolutionary conservation; however, it remains unclear whether developmental stability is the cause, or whether at least it contributes to their evolutionary conservation. Here, using Japanese medaka lines, we tested experimentally whether developmental stages and gene expression levels with greater stability led to their evolutionary conservation.</p><p><strong>Results: </strong>We first measured the stability of each gene expression level and developmental stage (defined here as the whole embryonic transcriptome) in the inbred F0 medaka population. We then measured their evolutionary conservation in the F3 generation by crossing the F0 line with the distantly related Japanese medaka line (Teradomori), followed by two rounds of intra-generational crossings. The results indicated that the genes and developmental stages that had smaller variations in the F0 generation showed lower diversity in the hybrid F3 generation, which implies a causal relationship between stability and evolutionary conservation.</p><p><strong>Conclusions: </strong>These findings suggest that the stability in phenotypes, including the developmental stages and gene expression levels, leads to their evolutionary conservation; this most likely occurs due to their low potential to generate phenotypic variation. In addition, since the highly stable developmental stages match with the body-plan-establishment stage, it also implies that the developmental stability potentially contributed to the strict conservation of animal body plan.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":"14 1","pages":"4"},"PeriodicalIF":4.1,"publicationDate":"2023-03-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10015717/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9121472","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
EvodevoPub Date : 2023-02-10DOI: 10.1186/s13227-022-00206-4
Erik Díaz-Valenzuela, Daniel Hernández-Ríos, Angélica Cibrián-Jaramillo
{"title":"The role of non-additive gene action on gene expression variation in plant domestication.","authors":"Erik Díaz-Valenzuela, Daniel Hernández-Ríos, Angélica Cibrián-Jaramillo","doi":"10.1186/s13227-022-00206-4","DOIUrl":"https://doi.org/10.1186/s13227-022-00206-4","url":null,"abstract":"<p><strong>Background: </strong>Plant domestication is a remarkable example of rapid phenotypic transformation of polygenic traits, such as organ size. Evidence from a handful of study cases suggests this transformation is due to gene regulatory changes that result in non-additive phenotypes. Employing data from published genetic crosses, we estimated the role of non-additive gene action in the modulation of transcriptional landscapes in three domesticated plants: maize, sunflower, and chili pepper. Using A. thaliana, we assessed the correlation between gene regulatory network (GRN) connectivity properties, transcript abundance variation, and gene action. Finally, we investigated the propagation of non-additive gene action in GRNs.</p><p><strong>Results: </strong>We compared crosses between domesticated plants and their wild relatives to a set of control crosses that included a pair of subspecies evolving under natural selection and a set of inbred lines evolving under domestication. We found abundance differences on a higher portion of transcripts in crosses between domesticated-wild plants relative to the control crosses. These transcripts showed non-additive gene action more often in crosses of domesticated-wild plants than in our control crosses. This pattern was strong for genes associated with cell cycle and cell fate determination, which control organ size. We found weak but significant negative correlations between the number of targets of trans-acting genes (Out-degree) and both the magnitude of transcript abundance difference a well as the absolute degree of dominance. Likewise, we found that the number of regulators that control a gene's expression (In-degree) is weakly but negatively correlated with the magnitude of transcript abundance differences. We observed that dominant-recessive gene action is highly propagable through GRNs. Finally, we found that transgressive gene action is driven by trans-acting regulators showing additive gene action.</p><p><strong>Conclusions: </strong>Our study highlights the role of non-additive gene action on modulating domestication-related traits, such as organ size via regulatory divergence. We propose that GRNs are shaped by regulatory changes at genes with modest connectivity, which reduces the effects of antagonistic pleiotropy. Finally, we provide empirical evidence of the propagation of non-additive gene action in GRNs, which suggests a transcriptional epistatic model for the control of polygenic traits, such as organ size.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":"14 1","pages":"3"},"PeriodicalIF":4.1,"publicationDate":"2023-02-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9912502/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10683414","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}