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":" ","pages":"15"},"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":" ","pages":"14"},"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":" ","pages":"13"},"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":" ","pages":"12"},"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":" ","pages":"11"},"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":" ","pages":"10"},"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":" ","pages":"9"},"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}
Pub Date : 2020-03-26eCollection Date: 2020-01-01DOI: 10.1186/s13227-020-00151-0
Uri Frank, Matthew L Nicotra, Christine E Schnitzler
Hydractinia, a genus of colonial marine cnidarians, has been used as a model organism for developmental biology and comparative immunology for over a century. It was this animal where stem cells and germ cells were first studied. However, protocols for efficient genetic engineering have only recently been established by a small but interactive community of researchers. The animal grows well in the lab, spawns daily, and its relatively short life cycle allows genetic studies. The availability of genomic tools and resources opens further opportunities for research using this animal. Its accessibility to experimental manipulation, growth- and cellular-plasticity, regenerative ability, and resistance to aging and cancer place Hydractinia as an emerging model for research in many biological and environmental disciplines.
{"title":"The colonial cnidarian <i>Hydractinia</i>.","authors":"Uri Frank, Matthew L Nicotra, Christine E Schnitzler","doi":"10.1186/s13227-020-00151-0","DOIUrl":"https://doi.org/10.1186/s13227-020-00151-0","url":null,"abstract":"<p><p><i>Hydractinia</i>, a genus of colonial marine cnidarians, has been used as a model organism for developmental biology and comparative immunology for over a century. It was this animal where stem cells and germ cells were first studied. However, protocols for efficient genetic engineering have only recently been established by a small but interactive community of researchers. The animal grows well in the lab, spawns daily, and its relatively short life cycle allows genetic studies. The availability of genomic tools and resources opens further opportunities for research using this animal. Its accessibility to experimental manipulation, growth- and cellular-plasticity, regenerative ability, and resistance to aging and cancer place <i>Hydractinia</i> as an emerging model for research in many biological and environmental disciplines.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":" ","pages":"7"},"PeriodicalIF":4.1,"publicationDate":"2020-03-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s13227-020-00151-0","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"37784266","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 : 2020-03-20eCollection Date: 2020-01-01DOI: 10.1186/s13227-020-00152-z
Hiroki Oda, Yasuko Akiyama-Oda
The common house spider Parasteatoda tepidariorum, belonging to the Chelicerata in the phylum Arthropoda, has emerged as an experimental system for studying mechanisms of development from an evolutionary standpoint. In this article, we review the distinct characteristics of P. tepidariorum, the major research questions relevant to this organism, and the available key methods and resources. P. tepidariorum has a relatively short lifecycle and, once mated, periodically lays eggs. The morphogenetic field of the P. tepidariorum embryo is cellular from an early stage and exhibits stepwise symmetry-breaking events and stripe-forming processes that are associated with body axes formation and segmentation, respectively, before reaching the arthropod phylotypic stage. Self-regulatory capabilities of the embryonic field are a prominent feature in P. tepidariorum. The mechanisms and logic underlying the evolvability of heritable patterning systems at the phylum level could be one of the major avenues of research investigated using this animal. The sequenced genome reveals whole genome duplication (WGD) within chelicerates, which offers an invertebrate platform for investigating the potential roles of WGD in animal diversification and evolution. The development and evolution of lineage-specific organs, including the book lungs and the union of spinnerets and silk glands, are attractive subjects of study. Studies using P. tepidariorum can benefit from the use of parental RNA interference, microinjection applications (including cell labeling and embryonic RNA interference), multicolor fluorescence in situ hybridization, and laser ablation as well as rich genomic and transcriptomic resources. These techniques enable functional gene discoveries and the uncovering of cellular and molecular insights.
{"title":"The common house spider <i>Parasteatoda tepidariorum</i>.","authors":"Hiroki Oda, Yasuko Akiyama-Oda","doi":"10.1186/s13227-020-00152-z","DOIUrl":"https://doi.org/10.1186/s13227-020-00152-z","url":null,"abstract":"<p><p>The common house spider <i>Parasteatoda tepidariorum,</i> belonging to the Chelicerata in the phylum Arthropoda, has emerged as an experimental system for studying mechanisms of development from an evolutionary standpoint. In this article, we review the distinct characteristics of <i>P. tepidariorum</i>, the major research questions relevant to this organism, and the available key methods and resources. <i>P. tepidariorum</i> has a relatively short lifecycle and, once mated, periodically lays eggs. The morphogenetic field of the <i>P. tepidariorum</i> embryo is cellular from an early stage and exhibits stepwise symmetry-breaking events and stripe-forming processes that are associated with body axes formation and segmentation, respectively, before reaching the arthropod phylotypic stage. Self-regulatory capabilities of the embryonic field are a prominent feature in <i>P. tepidariorum</i>. The mechanisms and logic underlying the evolvability of heritable patterning systems at the phylum level could be one of the major avenues of research investigated using this animal. The sequenced genome reveals whole genome duplication (WGD) within chelicerates, which offers an invertebrate platform for investigating the potential roles of WGD in animal diversification and evolution. The development and evolution of lineage-specific organs, including the book lungs and the union of spinnerets and silk glands, are attractive subjects of study. Studies using <i>P. tepidariorum</i> can benefit from the use of parental RNA interference, microinjection applications (including cell labeling and embryonic RNA interference), multicolor fluorescence in situ hybridization, and laser ablation as well as rich genomic and transcriptomic resources. These techniques enable functional gene discoveries and the uncovering of cellular and molecular insights.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":" ","pages":"6"},"PeriodicalIF":4.1,"publicationDate":"2020-03-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s13227-020-00152-z","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"37765724","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}