Pub Date : 2020-08-28eCollection Date: 2020-01-01DOI: 10.1186/s13227-020-00163-w
Guilherme Gainett, Prashant P Sharma
Background: The resurgence of interest in the comparative developmental study of chelicerates has led to important insights, such as the discovery of a genome duplication shared by spiders and scorpions, inferred to have occurred in the most recent common ancestor of Arachnopulmonata (a clade comprising the five arachnid orders that bear book lungs). Nonetheless, several arachnid groups remain understudied in the context of development and genomics, such as the order Amblypygi (whip spiders). The phylogenetic position of Amblypygi in Arachnopulmonata posits them as an interesting group to test the incidence of the proposed genome duplication in the common ancestor of Arachnopulmonata, as well as the degree of retention of duplicates over 450 Myr. Moreover, whip spiders have their first pair of walking legs elongated and modified into sensory appendages (a convergence with the antennae of mandibulates), but the genetic patterning of these antenniform legs has never been investigated.
Results: We established genomic resources and protocols for cultivation of embryos and gene expression assays by in situ hybridization to study the development of the whip spider Phrynus marginemaculatus. Using embryonic transcriptomes from three species of Amblypygi, we show that the ancestral whip spider exhibited duplications of all ten Hox genes. We deploy these resources to show that paralogs of the leg gap genes dachshund and homothorax retain arachnopulmonate-specific expression patterns in P. marginemaculatus. We characterize the expression of leg gap genes Distal-less, dachshund-1/2 and homothorax-1/2 in the embryonic antenniform leg and other appendages, and provide evidence that allometry, and by extension the antenniform leg fate, is specified early in embryogenesis.
Conclusion: This study is the first step in establishing P. marginemaculatus as a chelicerate model for modern evolutionary developmental study, and provides the first resources sampling whip spiders for comparative genomics. Our results suggest that Amblypygi share a genome duplication with spiders and scorpions, and set up a framework to study the genetic specification of antenniform legs. Future efforts to study whip spider development must emphasize the development of tools for functional experiments in P. marginemaculatus.
背景:人们对螯足类比较发育研究的兴趣再次升温,并由此获得了一些重要发现,例如发现了蜘蛛和蝎子共有的基因组复制,推断其发生在蛛形纲(Arachnopulmonata,由具有书肺的五个蛛形纲组成的一个支系)最近的共同祖先身上。然而,在发育和基因组学方面,一些蛛形纲类群的研究仍然不足,例如鞭蛛目(Amblypygi)。Amblypygi在蛛形纲中的系统发育位置使其成为一个有趣的类群,可用于检验蛛形纲共同祖先中基因组重复的发生率,以及重复基因在450 Myr以上的保留程度。此外,鞭蛛的第一对步行腿被拉长并被改造成感觉器官(与下颌动物的触角趋同),但这些触角状腿的遗传模式从未被研究过:结果:我们建立了基因组资源和胚胎培养规程,并通过原位杂交进行了基因表达测定,以研究鞭毛蛛的发育过程。我们利用三个Amblypygi物种的胚胎转录组表明,鞭毛蛛祖先的十个Hox基因都有重复。我们利用这些资源表明,腿间隙基因 dachshund 和 homothorax 的旁系亲属在 P. marginemaculatus 中保留了蛛形纲特有的表达模式。我们描述了腿间隙基因Distal-less、dachshund-1/2和homothorax-1/2在胚胎触角腿和其他附肢中的表达特征,并提供了证据,证明异型性以及触角腿的命运在胚胎发生早期就已确定:这项研究是将 P. marginemaculatus 确立为现代进化发育研究的螯足动物模型的第一步,并为比较基因组学提供了第一批鞭蛛样本资源。我们的研究结果表明,Amblypygi与蜘蛛和蝎子共享一个基因组复制,并为研究触角腿的基因规范建立了一个框架。今后研究鞭毛蛛发育的工作必须重视开发工具,以便在P. marginemaculatus中进行功能实验。
{"title":"Genomic resources and toolkits for developmental study of whip spiders (Amblypygi) provide insights into arachnid genome evolution and antenniform leg patterning.","authors":"Guilherme Gainett, Prashant P Sharma","doi":"10.1186/s13227-020-00163-w","DOIUrl":"10.1186/s13227-020-00163-w","url":null,"abstract":"<p><strong>Background: </strong>The resurgence of interest in the comparative developmental study of chelicerates has led to important insights, such as the discovery of a genome duplication shared by spiders and scorpions, inferred to have occurred in the most recent common ancestor of Arachnopulmonata (a clade comprising the five arachnid orders that bear book lungs). Nonetheless, several arachnid groups remain understudied in the context of development and genomics, such as the order Amblypygi (whip spiders). The phylogenetic position of Amblypygi in Arachnopulmonata posits them as an interesting group to test the incidence of the proposed genome duplication in the common ancestor of Arachnopulmonata, as well as the degree of retention of duplicates over 450 Myr. Moreover, whip spiders have their first pair of walking legs elongated and modified into sensory appendages (a convergence with the antennae of mandibulates), but the genetic patterning of these antenniform legs has never been investigated.</p><p><strong>Results: </strong>We established genomic resources and protocols for cultivation of embryos and gene expression assays by in situ hybridization to study the development of the whip spider <i>Phrynus marginemaculatus</i>. Using embryonic transcriptomes from three species of Amblypygi, we show that the ancestral whip spider exhibited duplications of all ten Hox genes. We deploy these resources to show that paralogs of the leg gap genes <i>dachshund</i> and <i>homothorax</i> retain arachnopulmonate-specific expression patterns in <i>P. marginemaculatus</i>. We characterize the expression of leg gap genes <i>Distal</i>-<i>less</i>, <i>dachshund</i>-<i>1/2</i> and <i>homothorax</i>-<i>1/2</i> in the embryonic antenniform leg and other appendages, and provide evidence that allometry, and by extension the antenniform leg fate, is specified early in embryogenesis.</p><p><strong>Conclusion: </strong>This study is the first step in establishing <i>P. marginemaculatus</i> as a chelicerate model for modern evolutionary developmental study, and provides the first resources sampling whip spiders for comparative genomics. Our results suggest that Amblypygi share a genome duplication with spiders and scorpions, and set up a framework to study the genetic specification of antenniform legs. Future efforts to study whip spider development must emphasize the development of tools for functional experiments in <i>P. marginemaculatus</i>.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":null,"pages":null},"PeriodicalIF":4.1,"publicationDate":"2020-08-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7455915/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38333971","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}
Pub Date : 2020-08-10eCollection Date: 2020-01-01DOI: 10.1186/s13227-020-00161-y
Alexis R Lanza, Elaine C Seaver
Background: The clade of protostome animals known as the Spiralia (e.g., mollusks, annelids, nemerteans and polyclad flatworms) shares a highly conserved program of early development. This includes shared arrangement of cells in the early-stage embryo and fates of descendant cells into embryonic quadrants. In spiralian embryos, a single cell in the D quadrant functions as an embryonic organizer to pattern the body axes. The precise timing of the organizing signal and its cellular identity varies among spiralians. Previous experiments in the annelid Chaetopterus pergamentaceus Cuvier, 1830 demonstrated that the D quadrant possesses an organizing role in body axes formation; however, the molecular signal and exact cellular identity of the organizer were unknown.
Results: In this study, the timing of the signal and the specific signaling pathway that mediates organizing activity in C. pergamentaceus was investigated through short exposures to chemical inhibitors during early cleavage stages. Chemical interference of the Activin/Nodal pathway but not the BMP or MAPK pathways results in larvae that lack a detectable dorsal-ventral axis. Furthermore, these data show that the duration of organizing activity encompasses the 16 cell stage and is completed before the 32 cell stage.
Conclusions: The timing and molecular signaling pathway of the C. pergamentaceus organizer is comparable to that of another annelid, Capitella teleta, whose organizing signal is required through the 16 cell stage and localizes to micromere 2d. Since C. pergamentaceus is an early branching annelid, these data in conjunction with functional genomic investigations in C. teleta hint that the ancestral state of annelid dorsal-ventral axis patterning involved an organizing signal that occurs one to two cell divisions earlier than the organizing signal identified in mollusks, and that the signal is mediated by Activin/Nodal signaling. Our findings have significant evolutionary implications within the Spiralia, and furthermore suggest that global body patterning mechanisms may not be as conserved across bilaterians as was previously thought.
{"title":"Activin/Nodal signaling mediates dorsal-ventral axis formation before third quartet formation in embryos of the annelid <i>Chaetopterus pergamentaceus</i>.","authors":"Alexis R Lanza, Elaine C Seaver","doi":"10.1186/s13227-020-00161-y","DOIUrl":"10.1186/s13227-020-00161-y","url":null,"abstract":"<p><strong>Background: </strong>The clade of protostome animals known as the Spiralia (e.g., mollusks, annelids, nemerteans and polyclad flatworms) shares a highly conserved program of early development. This includes shared arrangement of cells in the early-stage embryo and fates of descendant cells into embryonic quadrants. In spiralian embryos, a single cell in the D quadrant functions as an embryonic organizer to pattern the body axes. The precise timing of the organizing signal and its cellular identity varies among spiralians. Previous experiments in the annelid <i>Chaetopterus pergamentaceus</i> Cuvier, 1830 demonstrated that the D quadrant possesses an organizing role in body axes formation; however, the molecular signal and exact cellular identity of the organizer were unknown.</p><p><strong>Results: </strong>In this study, the timing of the signal and the specific signaling pathway that mediates organizing activity in <i>C. pergamentaceus</i> was investigated through short exposures to chemical inhibitors during early cleavage stages. Chemical interference of the Activin/Nodal pathway but not the BMP or MAPK pathways results in larvae that lack a detectable dorsal-ventral axis. Furthermore, these data show that the duration of organizing activity encompasses the 16 cell stage and is completed before the 32 cell stage.</p><p><strong>Conclusions: </strong>The timing and molecular signaling pathway of the <i>C. pergamentaceus</i> organizer is comparable to that of another annelid, <i>Capitella teleta</i>, whose organizing signal is required through the 16 cell stage and localizes to micromere 2d. Since <i>C. pergamentaceus</i> is an early branching annelid, these data in conjunction with functional genomic investigations in <i>C. teleta</i> hint that the ancestral state of annelid dorsal-ventral axis patterning involved an organizing signal that occurs one to two cell divisions earlier than the organizing signal identified in mollusks, and that the signal is mediated by Activin/Nodal signaling. Our findings have significant evolutionary implications within the Spiralia, and furthermore suggest that global body patterning mechanisms may not be as conserved across bilaterians as was previously thought.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":null,"pages":null},"PeriodicalIF":4.1,"publicationDate":"2020-08-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7418201/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38259385","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}
Pub Date : 2020-08-10eCollection Date: 2020-01-01DOI: 10.1186/s13227-020-00160-z
Dewi Pramanik, Nemi Dorst, Niels Meesters, Marlies Spaans, Erik Smets, Monique Welten, Barbara Gravendeel
Background: Variation in shape and size of many floral organs is related to pollinators. Evolution of such organs is driven by duplication and modification of MADS-box and MYB transcription factors. We applied a combination of micro-morphological (SEM and micro 3D-CT scanning) and molecular techniques (transcriptome and RT-PCR analysis) to understand the evolution and development of the callus, stelidia and mentum, three highly specialized floral structures of orchids involved in pollination. Early stage and mature tissues were collected from flowers of the bee-pollinated Phalaenopsis equestris and Phalaenopsis pulcherrima, two species that differ in floral morphology: P. equestris has a large callus but short stelidia and no mentum, whereas P. pulcherrima has a small callus, but long stelidia and a pronounced mentum.
Results: Our results show the stelidia develop from early primordial stages, whereas the callus and mentum develop later. In combination, the micro 3D-CT scan analysis and gene expression analyses show that the callus is of mixed petaloid-staminodial origin, the stelidia of staminodial origin, and the mentum of mixed sepaloid-petaloid-staminodial origin. SEP clade 1 copies are expressed in the larger callus of P. equestris, whereas AP3 clade 1 and AGL6 clade 1 copies are expressed in the pronounced mentum and long stelidia of P. pulcherrima. AP3 clade 4, PI-, AGL6 clade 2 and PCF clade 1 copies might have a balancing role in callus and gynostemium development. There appears to be a trade-off between DIV clade 2 expression with SEP clade 1 expression in the callus, on the one hand, and with AP3 clade 1 and AGL6 clade 1 expression in the stelidia and mentum on the other.
Conclusions: We detected differential growth and expression of MADS box AP3/PI-like, AGL6-like and SEP-like, and MYB DIV-like gene copies in the callus, stelidia and mentum of two species of Phalaenopsis, of which these floral structures are very differently shaped and sized. Our study provides a first glimpse of the evolutionary developmental mechanisms driving adaptation of Phalaenopsis flowers to different pollinators by providing combined micro-morphological and molecular evidence for a possible sepaloid-petaloid-staminodial origin of the orchid mentum.
{"title":"Evolution and development of three highly specialized floral structures of bee-pollinated <i>Phalaenopsis</i> species.","authors":"Dewi Pramanik, Nemi Dorst, Niels Meesters, Marlies Spaans, Erik Smets, Monique Welten, Barbara Gravendeel","doi":"10.1186/s13227-020-00160-z","DOIUrl":"https://doi.org/10.1186/s13227-020-00160-z","url":null,"abstract":"<p><strong>Background: </strong>Variation in shape and size of many floral organs is related to pollinators. Evolution of such organs is driven by duplication and modification of MADS-box and MYB transcription factors. We applied a combination of micro-morphological (SEM and micro 3D-CT scanning) and molecular techniques (transcriptome and RT-PCR analysis) to understand the evolution and development of the callus, stelidia and mentum, three highly specialized floral structures of orchids involved in pollination. Early stage and mature tissues were collected from flowers of the bee-pollinated <i>Phalaenopsis equestris</i> and <i>Phalaenopsis pulcherrima</i>, two species that differ in floral morphology: <i>P. equestris</i> has a large callus but short stelidia and no mentum, whereas <i>P. pulcherrima</i> has a small callus, but long stelidia and a pronounced mentum.</p><p><strong>Results: </strong>Our results show the stelidia develop from early primordial stages, whereas the callus and mentum develop later. In combination, the micro 3D-CT scan analysis and gene expression analyses show that the callus is of mixed petaloid-staminodial origin, the stelidia of staminodial origin, and the mentum of mixed sepaloid-petaloid-staminodial origin. <i>SEP</i> clade 1 copies are expressed in the larger callus of <i>P. equestris</i>, whereas <i>AP3</i> clade 1 and <i>AGL6</i> clade 1 copies are expressed in the pronounced mentum and long stelidia of <i>P. pulcherrima. AP3</i> clade 4, <i>PI</i>-, <i>AGL6</i> clade 2 and <i>PCF</i> clade 1 copies might have a balancing role in callus and gynostemium development. There appears to be a trade-off between <i>DIV</i> clade 2 expression with <i>SEP</i> clade 1 expression in the callus, on the one hand, and with <i>AP3</i> clade 1 and <i>AGL6</i> clade 1 expression in the stelidia and mentum on the other.</p><p><strong>Conclusions: </strong>We detected differential growth and expression of MADS box <i>AP3/PI</i>-like, <i>AGL</i>6-like and <i>SEP</i>-like, and MYB <i>DIV</i>-like gene copies in the callus, stelidia and mentum of two species of <i>Phalaenopsis,</i> of which these floral structures are very differently shaped and sized. Our study provides a first glimpse of the evolutionary developmental mechanisms driving adaptation of <i>Phalaenopsis</i> flowers to different pollinators by providing combined micro-morphological and molecular evidence for a possible sepaloid-petaloid-staminodial origin of the orchid mentum.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":null,"pages":null},"PeriodicalIF":4.1,"publicationDate":"2020-08-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s13227-020-00160-z","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38263310","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}
Pub Date : 2020-08-03eCollection Date: 2020-01-01DOI: 10.1186/s13227-020-00162-x
Christopher J Johnson, Florian Razy-Krajka, Alberto Stolfi
Background: The evolution of vertebrate smooth muscles is obscured by lack of identifiable smooth muscle-like cells in tunicates, the invertebrates most closely related to vertebrates. A recent evolutionary model was proposed in which smooth muscles arose before the last bilaterian common ancestor, and were later diversified, secondarily lost or modified in the branches leading to extant animal taxa. However, there is currently no data from tunicates to support this scenario.
Methods and results: Here, we show that the axial columnar cells, a unique cell type in the adhesive larval papillae of the tunicate Ciona, are enriched for orthologs of vertebrate smooth/non-muscle-specific effectors of contractility, in addition to developing from progenitors that express conserved cardiomyocyte regulatory factors. We show that these cells contract during the retraction of the Ciona papillae during larval settlement and metamorphosis.
Conclusions: We propose that the axial columnar cells of Ciona are a myoepithelial cell type required for transducing external stimuli into mechanical forces that aid in the attachment of the motile larva to its final substrate. Furthermore, they share developmental and functional features with vertebrate myoepithelial cells, vascular smooth muscle cells, and cardiomyocytes. We discuss these findings in the context of the proposed models of vertebrate smooth muscle and cardiomyocyte evolution.
{"title":"Expression of smooth muscle-like effectors and core cardiomyocyte regulators in the contractile papillae of <i>Ciona</i>.","authors":"Christopher J Johnson, Florian Razy-Krajka, Alberto Stolfi","doi":"10.1186/s13227-020-00162-x","DOIUrl":"10.1186/s13227-020-00162-x","url":null,"abstract":"<p><strong>Background: </strong>The evolution of vertebrate smooth muscles is obscured by lack of identifiable smooth muscle-like cells in tunicates, the invertebrates most closely related to vertebrates. A recent evolutionary model was proposed in which smooth muscles arose before the last bilaterian common ancestor, and were later diversified, secondarily lost or modified in the branches leading to extant animal taxa. However, there is currently no data from tunicates to support this scenario.</p><p><strong>Methods and results: </strong>Here, we show that the axial columnar cells, a unique cell type in the adhesive larval papillae of the tunicate <i>Ciona,</i> are enriched for orthologs of vertebrate smooth/non-muscle-specific effectors of contractility, in addition to developing from progenitors that express conserved cardiomyocyte regulatory factors. We show that these cells contract during the retraction of the <i>Ciona</i> papillae during larval settlement and metamorphosis.</p><p><strong>Conclusions: </strong>We propose that the axial columnar cells of <i>Ciona</i> are a myoepithelial cell type required for transducing external stimuli into mechanical forces that aid in the attachment of the motile larva to its final substrate. Furthermore, they share developmental and functional features with vertebrate myoepithelial cells, vascular smooth muscle cells, and cardiomyocytes. We discuss these findings in the context of the proposed models of vertebrate smooth muscle and cardiomyocyte evolution.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":null,"pages":null},"PeriodicalIF":4.1,"publicationDate":"2020-08-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7397655/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38246441","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}
Pub Date : 2020-07-11eCollection Date: 2020-01-01DOI: 10.1186/s13227-020-00159-6
William R Jeffery
The small teleost fish Astyanax mexicanus has emerged as an outstanding model for studying many biological topics in the context of evolution. A major attribute is conspecific surface dwelling (surface fish) and blind cave dwelling (cavefish) morphs that can be raised in the laboratory and spawn large numbers of transparent and synchronously developing embryos. More than 30 cavefish populations have been discovered, mostly in northeastern Mexico, and some are thought to have evolved independently from surface fish ancestors, providing excellent models of parallel and convergent evolution. Cavefish have evolved eye and pigmentation regression, as well as modifications in brain morphology, behaviors, heart regenerative capacity, metabolic processes, and craniofacial organization. Thus, the Astyanax model provides researchers with natural "mutants" to study life in the challenging cave environment. The application of powerful genetic approaches based on hybridization between the two morphs and between the different cavefish populations are key advantages for deciphering the developmental and genetic mechanisms regulating trait evolution. QTL analysis has revealed the genetic architectures of gained and lost traits. In addition, some cavefish traits resemble human diseases, offering novel models for biomedical research. Astyanax research is supported by genome assemblies, transcriptomes, tissue and organ transplantation, gene manipulation and editing, and stable transgenesis, and benefits from a welcoming and interactive research community that conducts integrated community projects and sponsors the International Astyanax Meeting (AIM).
{"title":"<i>Astyanax</i> surface and cave fish morphs.","authors":"William R Jeffery","doi":"10.1186/s13227-020-00159-6","DOIUrl":"10.1186/s13227-020-00159-6","url":null,"abstract":"<p><p>The small teleost fish <i>Astyanax mexicanus</i> has emerged as an outstanding model for studying many biological topics in the context of evolution. A major attribute is conspecific surface dwelling (surface fish) and blind cave dwelling (cavefish) morphs that can be raised in the laboratory and spawn large numbers of transparent and synchronously developing embryos. More than 30 cavefish populations have been discovered, mostly in northeastern Mexico, and some are thought to have evolved independently from surface fish ancestors, providing excellent models of parallel and convergent evolution. Cavefish have evolved eye and pigmentation regression, as well as modifications in brain morphology, behaviors, heart regenerative capacity, metabolic processes, and craniofacial organization. Thus, the <i>Astyanax</i> model provides researchers with natural \"mutants\" to study life in the challenging cave environment. The application of powerful genetic approaches based on hybridization between the two morphs and between the different cavefish populations are key advantages for deciphering the developmental and genetic mechanisms regulating trait evolution. QTL analysis has revealed the genetic architectures of gained and lost traits. In addition, some cavefish traits resemble human diseases, offering novel models for biomedical research. <i>Astyanax</i> research is supported by genome assemblies, transcriptomes, tissue and organ transplantation, gene manipulation and editing, and stable transgenesis, and benefits from a welcoming and interactive research community that conducts integrated community projects and sponsors the International Astyanax Meeting (AIM).</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":null,"pages":null},"PeriodicalIF":4.1,"publicationDate":"2020-07-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7353729/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38168717","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}
Pub Date : 2020-07-01eCollection Date: 2020-01-01DOI: 10.1186/s13227-020-00158-7
James G Umen
The transition of life from single cells to more complex multicellular forms has occurred at least two dozen times among eukaryotes and is one of the major evolutionary transitions, but the early steps that enabled multicellular life to evolve and thrive remain poorly understood. Volvocine green algae are a taxonomic group that is uniquely suited to investigating the step-wise acquisition of multicellular organization. The multicellular volvocine species Volvox carteri exhibits many hallmarks of complex multicellularity including complete germ-soma division of labor, asymmetric cell divisions, coordinated tissue-level morphogenesis, and dimorphic sexes-none of which have obvious analogs in its closest unicellular relative, the model alga Chlamydomonas reinhardtii. Here, I summarize some of the key questions and areas of study that are being addressed with Volvox carteri and how increasing genomic information and methodologies for volvocine algae are opening up the entire group as an integrated experimental system for exploring the evolution of multicellularity and more.
{"title":"Volvox and volvocine green algae.","authors":"James G Umen","doi":"10.1186/s13227-020-00158-7","DOIUrl":"https://doi.org/10.1186/s13227-020-00158-7","url":null,"abstract":"<p><p>The transition of life from single cells to more complex multicellular forms has occurred at least two dozen times among eukaryotes and is one of the major evolutionary transitions, but the early steps that enabled multicellular life to evolve and thrive remain poorly understood. Volvocine green algae are a taxonomic group that is uniquely suited to investigating the step-wise acquisition of multicellular organization. The multicellular volvocine species <i>Volvox carteri</i> exhibits many hallmarks of complex multicellularity including complete germ-soma division of labor, asymmetric cell divisions, coordinated tissue-level morphogenesis, and dimorphic sexes-none of which have obvious analogs in its closest unicellular relative, the model alga <i>Chlamydomonas reinhardtii</i>. Here, I summarize some of the key questions and areas of study that are being addressed with <i>Volvox carteri</i> and how increasing genomic information and methodologies for volvocine algae are opening up the entire group as an integrated experimental system for exploring the evolution of multicellularity and more.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":null,"pages":null},"PeriodicalIF":4.1,"publicationDate":"2020-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s13227-020-00158-7","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38120455","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}
Background: Interpretation of the floral structure of Zingiberaceae has long concentrated on the relationships of the androecial members. It suggested that labellum is composed of two structures rather than three or five, and glands are interpreted either as gynoecial part or as androecial members.
Methods: Serial sections were used to observe the vasculature of normal and two-staminate flowers in Alpinia intermedia 'shengzhen'. Floral diagrams were drawn to interpret the morphological category of the floral organs and the relationships of the androecial members. Androecial vascular bundles were associated with carpellary dorsal bundles (CDBs) and parietal bundles (PBs) in a Zingiberales phylogeny setting using ancestral state reconstruction.
Results: Anatomical observations demonstrate that the fertile stamen(s) incorporate parietal bundles both in normal and two-staminate flowers. The three appendages represent the three members of the outer whorl of the androecium, while the labellum represents the inner whorl of the androecium in the two-staminate flower. Reconstruction of the origin of the vascular system in the androecium suggests that the outer whorl of androecium receives its vascular supply from the CDBs, and the inner whorl of androecium receives from the PBs in both the basal banana group and the more derived ginger clade.
Conclusions: The present study adds to a growing body of literature suggesting that the anatomy of abnormal flowers may not provide enough evidence for elucidating the relationships of the androecial members, and help us to better understand how the vascular system is constructed during the androecial petaloidy evolution.
{"title":"Can the anatomy of abnormal flowers elucidate relationships of the androecial members in the ginger (Zingiberaceae)?","authors":"Xiumei Li, Tian Fan, Pu Zou, Wenhu Zhang, Xiuju Wu, Yixin Zhang, Jingping Liao","doi":"10.1186/s13227-020-00157-8","DOIUrl":"10.1186/s13227-020-00157-8","url":null,"abstract":"<p><strong>Background: </strong>Interpretation of the floral structure of Zingiberaceae has long concentrated on the relationships of the androecial members. It suggested that labellum is composed of two structures rather than three or five, and glands are interpreted either as gynoecial part or as androecial members.</p><p><strong>Methods: </strong>Serial sections were used to observe the vasculature of normal and two-staminate flowers in <i>Alpinia intermedia</i> 'shengzhen'. Floral diagrams were drawn to interpret the morphological category of the floral organs and the relationships of the androecial members. Androecial vascular bundles were associated with carpellary dorsal bundles (CDBs) and parietal bundles (PBs) in a Zingiberales phylogeny setting using ancestral state reconstruction.</p><p><strong>Results: </strong>Anatomical observations demonstrate that the fertile stamen(s) incorporate parietal bundles both in normal and two-staminate flowers. The three appendages represent the three members of the outer whorl of the androecium, while the labellum represents the inner whorl of the androecium in the two-staminate flower. Reconstruction of the origin of the vascular system in the androecium suggests that the outer whorl of androecium receives its vascular supply from the CDBs, and the inner whorl of androecium receives from the PBs in both the basal banana group and the more derived ginger clade.</p><p><strong>Conclusions: </strong>The present study adds to a growing body of literature suggesting that the anatomy of abnormal flowers may not provide enough evidence for elucidating the relationships of the androecial members, and help us to better understand how the vascular system is constructed during the androecial petaloidy evolution.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":null,"pages":null},"PeriodicalIF":4.1,"publicationDate":"2020-06-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7285767/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38047287","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}
Pub Date : 2020-06-02eCollection Date: 2020-01-01DOI: 10.1186/s13227-020-00156-9
Jasmin Camacho, Rachel Moon, Samantha K Smith, Jacky D Lin, Charles Randolph, John J Rasweiler, Richard R Behringer, Arhat Abzhanov
Background: Skull diversity in the neotropical leaf-nosed bats (Phyllostomidae) evolved through a heterochronic process called peramorphosis, with underlying causes varying by subfamily. The nectar-eating (subfamily Glossophaginae) and blood-eating (subfamily Desmondontinae) groups originate from insect-eating ancestors and generate their uniquely shaped faces and skulls by extending the ancestral ontogenetic program, appending new developmental stages and demonstrating peramorphosis by hypermorphosis. However, the fruit-eating phyllostomids (subfamilies Carollinae and Stenodermatinae) adjust their craniofacial development by speeding up certain developmental processes, displaying peramorphosis by acceleration. We hypothesized that these two forms of peramorphosis detected by our morphometric studies could be explained by differential growth and investigated cell proliferation during craniofacial morphogenesis.
Results: We obtained cranial tissues from four wild-caught bat species representing a range of facial diversity and labeled mitotic cells using immunohistochemistry. During craniofacial development, all bats display a conserved spatiotemporal distribution of proliferative cells with distinguishable zones of elevated mitosis. These areas were identified as modules by the spatial distribution analysis. Ancestral state reconstruction of proliferation rates and patterns in the facial module between species provided support, and a degree of explanation, for the developmental mechanisms underlying the two models of peramorphosis. In the long-faced species, Glossophaga soricina, whose facial shape evolved by hypermorphosis, cell proliferation rate is maintained at lower levels and for a longer period of time compared to the outgroup species Miniopterus natalensis. In both species of studied short-faced fruit bats, Carollia perspicillata and Artibeus jamaicensis, which evolved under the acceleration model, cell proliferation rate is increased compared to the outgroup.
Conclusions: This is the first study which links differential cellular proliferation and developmental modularity with heterochronic developmental changes, leading to the evolution of adaptive cranial diversity in an important group of mammals.
{"title":"Differential cellular proliferation underlies heterochronic generation of cranial diversity in phyllostomid bats.","authors":"Jasmin Camacho, Rachel Moon, Samantha K Smith, Jacky D Lin, Charles Randolph, John J Rasweiler, Richard R Behringer, Arhat Abzhanov","doi":"10.1186/s13227-020-00156-9","DOIUrl":"10.1186/s13227-020-00156-9","url":null,"abstract":"<p><strong>Background: </strong>Skull diversity in the neotropical leaf-nosed bats (Phyllostomidae) evolved through a heterochronic process called peramorphosis, with underlying causes varying by subfamily. The nectar-eating (subfamily Glossophaginae) and blood-eating (subfamily Desmondontinae) groups originate from insect-eating ancestors and generate their uniquely shaped faces and skulls by extending the ancestral ontogenetic program, appending new developmental stages and demonstrating peramorphosis by hypermorphosis. However, the fruit-eating phyllostomids (subfamilies Carollinae and Stenodermatinae) adjust their craniofacial development by speeding up certain developmental processes, displaying peramorphosis by acceleration. We hypothesized that these two forms of peramorphosis detected by our morphometric studies could be explained by differential growth and investigated cell proliferation during craniofacial morphogenesis.</p><p><strong>Results: </strong>We obtained cranial tissues from four wild-caught bat species representing a range of facial diversity and labeled mitotic cells using immunohistochemistry. During craniofacial development, all bats display a conserved spatiotemporal distribution of proliferative cells with distinguishable zones of elevated mitosis. These areas were identified as modules by the spatial distribution analysis. Ancestral state reconstruction of proliferation rates and patterns in the facial module between species provided support, and a degree of explanation, for the developmental mechanisms underlying the two models of peramorphosis. In the long-faced species, <i>Glossophaga soricina</i>, whose facial shape evolved by hypermorphosis, cell proliferation rate is maintained at lower levels and for a longer period of time compared to the outgroup species <i>Miniopterus natalensis</i>. In both species of studied short-faced fruit bats, <i>Carollia perspicillata</i> and <i>Artibeus jamaicensis</i>, which evolved under the acceleration model, cell proliferation rate is increased compared to the outgroup.</p><p><strong>Conclusions: </strong>This is the first study which links differential cellular proliferation and developmental modularity with heterochronic developmental changes, leading to the evolution of adaptive cranial diversity in an important group of mammals.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":null,"pages":null},"PeriodicalIF":4.1,"publicationDate":"2020-06-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7268441/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38027800","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}
Pub Date : 2020-05-27eCollection Date: 2020-01-01DOI: 10.1186/s13227-020-00155-w
Robert D Reed, Jayne E Selegue, Linlin Zhang, Craig R Brunetti
Background: The diversity of butterfly color patterns can be attributed to a relatively small number of pattern elements that are homologous across Lepidoptera. Although genes involved in patterning some of these elements have been identified, the development of several major elements remains poorly understood. To identify genes underlying wing pupal cuticle markings and wing margin color patterns, we examined expression of the candidate transcription factors Engrailed/Invected (En/Inv), Distal-less (Dll), Cubitus interruptus (Ci), and Spalt in two nymphalids: Junonia coenia and Bicyclus anynana.
Results: We found that En/Inv, Dll, and Ci mark domains on the J. coenia last-instar forewing disc that closely correspond to the position and shape of pupal cuticle markings. We also found that Spalt demarcates wing margin color patterns in both J. coenia and B. anynana, and that CRISPR/Cas9 deletions in the spalt gene result in reduction and loss of wing margin color patterns in J. coenia. These data demonstrate a role for spalt in promoting wing margin color patterning, in addition to its previously described role in eyespot patterning.
Conclusion: Our observations support the model that a core set of regulatory genes are redeployed multiple times, and in multiple roles, during butterfly wing pattern development. Of these genes, spalt is of special interest as it plays a dual role in both eyespot and margin color pattern development.
{"title":"Transcription factors underlying wing margin color patterns and pupal cuticle markings in butterflies.","authors":"Robert D Reed, Jayne E Selegue, Linlin Zhang, Craig R Brunetti","doi":"10.1186/s13227-020-00155-w","DOIUrl":"https://doi.org/10.1186/s13227-020-00155-w","url":null,"abstract":"<p><strong>Background: </strong>The diversity of butterfly color patterns can be attributed to a relatively small number of pattern elements that are homologous across Lepidoptera. Although genes involved in patterning some of these elements have been identified, the development of several major elements remains poorly understood. To identify genes underlying wing pupal cuticle markings and wing margin color patterns, we examined expression of the candidate transcription factors Engrailed/Invected (En/Inv), Distal-less (Dll), Cubitus interruptus (Ci), and Spalt in two nymphalids: <i>Junonia coenia</i> and <i>Bicyclus anynana</i>.</p><p><strong>Results: </strong>We found that En/Inv, Dll, and Ci mark domains on the <i>J. coenia</i> last-instar forewing disc that closely correspond to the position and shape of pupal cuticle markings. We also found that Spalt demarcates wing margin color patterns in both <i>J. coenia</i> and <i>B. anynana</i>, and that CRISPR/Cas9 deletions in the <i>spalt</i> gene result in reduction and loss of wing margin color patterns in <i>J. coenia</i>. These data demonstrate a role for <i>spalt</i> in promoting wing margin color patterning, in addition to its previously described role in eyespot patterning.</p><p><strong>Conclusion: </strong>Our observations support the model that a core set of regulatory genes are redeployed multiple times, and in multiple roles, during butterfly wing pattern development. Of these genes, <i>spalt</i> is of special interest as it plays a dual role in both eyespot and margin color pattern development.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":null,"pages":null},"PeriodicalIF":4.1,"publicationDate":"2020-05-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s13227-020-00155-w","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38027799","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}
Pub Date : 2020-04-22eCollection Date: 2020-01-01DOI: 10.1186/s13227-020-00154-x
Jessica Hernandez, Leslie Pick, Katie Reding
Background: Much has been learned about basic biology from studies of insect model systems. The pre-eminent insect model system, Drosophila melanogaster, is a holometabolous insect with a derived mode of segment formation. While additional insect models have been pioneered in recent years, most of these fall within holometabolous lineages. In contrast, hemimetabolous insects have garnered less attention, although they include agricultural pests, vectors of human disease, and present numerous evolutionary novelties in form and function. The milkweed bug, Oncopeltus fasciatus (order: Hemiptera)-close outgroup to holometabolous insects-is an emerging model system. However, comparative studies within this order are limited as many phytophagous hemipterans are difficult to stably maintain in the lab due to their reliance on fresh plants, deposition of eggs within plant material, and long development time from embryo to adult.
Results: Here we present the harlequin bug, Murgantia histrionica, as a new hemipteran model species. Murgantia-a member of the stink bug family Pentatomidae which shares a common ancestor with Oncopeltus ~ 200 mya-is easy to rear in the lab, produces a large number of eggs, and is amenable to molecular genetic techniques. We use Murgantia to ask whether Pair-Rule Genes (PRGs) are deployed in ways similar to holometabolous insects or to Oncopeltus. Specifically, PRGs even-skipped, odd-skipped, paired and sloppy-paired are initially expressed in PR-stripes in Drosophila and a number of holometabolous insects but in segmental-stripes in Oncopeltus. We found that these genes are likewise expressed in segmental-stripes in Murgantia, while runt displays partial PR-character in both species. Also like Oncopeltus, E75A is expressed in a clear PR-pattern in blastoderm- and germband-stage Murgantia embryos, although it plays no role in segmentation in Drosophila. Thus, genes diagnostic of the split between holometabolous insects and Oncopeltus are expressed in an Oncopeltus-like fashion during Murgantia development.
Conclusions: The similarity in gene expression between Murgantia and Oncopeltus suggests that Oncopeltus is not a sole outlier species in failing to utilize orthologs of Drosophila PRGs for PR-patterning. Rather, strategies deployed for PR-patterning, including the use of E75A in the PRG-network, are likely conserved within Hemiptera, and possibly more broadly among hemimetabolous insects.
{"title":"<i>Oncopeltus</i>-like gene expression patterns in <i>Murgantia histrionica</i>, a new hemipteran model system, suggest ancient regulatory network divergence.","authors":"Jessica Hernandez, Leslie Pick, Katie Reding","doi":"10.1186/s13227-020-00154-x","DOIUrl":"https://doi.org/10.1186/s13227-020-00154-x","url":null,"abstract":"<p><strong>Background: </strong>Much has been learned about basic biology from studies of insect model systems. The pre-eminent insect model system, <i>Drosophila melanogaster</i>, is a holometabolous insect with a derived mode of segment formation. While additional insect models have been pioneered in recent years, most of these fall within holometabolous lineages. In contrast, hemimetabolous insects have garnered less attention, although they include agricultural pests, vectors of human disease, and present numerous evolutionary novelties in form and function. The milkweed bug, <i>Oncopeltus fasciatus</i> (order: Hemiptera)-close outgroup to holometabolous insects-is an emerging model system. However, comparative studies within this order are limited as many phytophagous hemipterans are difficult to stably maintain in the lab due to their reliance on fresh plants, deposition of eggs within plant material, and long development time from embryo to adult.</p><p><strong>Results: </strong>Here we present the harlequin bug, <i>Murgantia histrionica</i>, as a new hemipteran model species. <i>Murgantia</i>-a member of the stink bug family Pentatomidae which shares a common ancestor with <i>Oncopeltus</i> ~ 200 mya-is easy to rear in the lab, produces a large number of eggs, and is amenable to molecular genetic techniques. We use <i>Murgantia</i> to ask whether Pair-Rule Genes (PRGs) are deployed in ways similar to holometabolous insects or to <i>Oncopeltus</i>. Specifically, PRGs <i>even</i>-<i>skipped, odd</i>-<i>skipped, paired</i> and <i>sloppy</i>-<i>paired</i> are initially expressed in PR-stripes in <i>Drosophila</i> and a number of holometabolous insects but in segmental-stripes in <i>Oncopeltus</i>. We found that these genes are likewise expressed in segmental-stripes in <i>Murgantia,</i> while <i>runt</i> displays partial PR-character in both species. Also like <i>Oncopeltus</i>, <i>E75A</i> is expressed in a clear PR-pattern in blastoderm- and germband-stage <i>Murgantia</i> embryos, although it plays no role in segmentation in <i>Drosophila</i>. Thus, genes diagnostic of the split between holometabolous insects and <i>Oncopeltus</i> are expressed in an <i>Oncopeltus</i>-like fashion during <i>Murgantia</i> development.</p><p><strong>Conclusions: </strong>The similarity in gene expression between <i>Murgantia</i> and <i>Oncopeltus</i> suggests that <i>Oncopeltus</i> is not a sole outlier species in failing to utilize orthologs of <i>Drosophila</i> PRGs for PR-patterning. Rather, strategies deployed for PR-patterning, including the use of <i>E75A</i> in the PRG-network, are likely conserved within Hemiptera, and possibly more broadly among hemimetabolous insects.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":null,"pages":null},"PeriodicalIF":4.1,"publicationDate":"2020-04-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s13227-020-00154-x","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"37874081","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}