Expression of NK cluster genes in the onychophoran Euperipatoides rowelli : implications for the evolution of NK family genes in nephrozoans

Understanding the evolution and development of morphological traits of the last common bilaterian ancestor is a major goal of the evo-devo discipline. The reconstruction of this "urbilaterian" is mainly based on comparative studies of common molecular patterning mechanisms in recent model...

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Published inEvoDevo Vol. 9; no. 1; p. 17
Main Authors Treffkorn, Sandra, Kahnke, Laura, Hering, Lars, Mayer, Georg
Format Journal Article
LanguageEnglish
Published England BioMed Central Ltd 18.07.2018
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Abstract Understanding the evolution and development of morphological traits of the last common bilaterian ancestor is a major goal of the evo-devo discipline. The reconstruction of this "urbilaterian" is mainly based on comparative studies of common molecular patterning mechanisms in recent model organisms. The NK homeobox genes are key players in many of these molecular pathways, including processes regulating mesoderm, heart and neural development. Shared features seen in the expression patterns of NK genes have been used to determine the ancestral bilaterian characters. However, the commonly used model organisms provide only a limited view on the evolution of these molecular pathways. To further investigate the ancestral roles of NK cluster genes, we analyzed their expression patterns in the onychophoran . We identified nine transcripts of NK cluster genes in , including single copies of , , , , , and , and two copies of . All of these genes except for and are expressed in different mesodermal organs and tissues in embryos of , including the anlagen of somatic musculature and the heart. Furthermore, we found distinct expression patterns of , , , and in the developing nervous system. The same holds true for the NKL gene , which does not belong to the NK cluster but is a related gene playing a role in neural patterning. Surprisingly, , and are additionally expressed in a segment polarity-like pattern early in development-a feature that has been otherwise reported only from annelids. Our results indicate that the NK cluster genes were involved in mesoderm and neural development in the last common ancestor of bilaterians or at least nephrozoans (i.e., bilaterians to the exclusion of xenacoelomorphs). By comparing our data from an onychophoran to those from other bilaterians, we critically review the hypothesis of a complex "urbilaterian" with a segmented body, a pulsatile organ or heart, and a condensed mediolaterally patterned nerve cord.
AbstractList BACKGROUNDUnderstanding the evolution and development of morphological traits of the last common bilaterian ancestor is a major goal of the evo-devo discipline. The reconstruction of this "urbilaterian" is mainly based on comparative studies of common molecular patterning mechanisms in recent model organisms. The NK homeobox genes are key players in many of these molecular pathways, including processes regulating mesoderm, heart and neural development. Shared features seen in the expression patterns of NK genes have been used to determine the ancestral bilaterian characters. However, the commonly used model organisms provide only a limited view on the evolution of these molecular pathways. To further investigate the ancestral roles of NK cluster genes, we analyzed their expression patterns in the onychophoran Euperipatoides rowelli. RESULTSWe identified nine transcripts of NK cluster genes in E. rowelli, including single copies of NK1, NK3, NK4, NK5, Msx, Lbx and Tlx, and two copies of NK6. All of these genes except for NK6.1 and NK6.2 are expressed in different mesodermal organs and tissues in embryos of E. rowelli, including the anlagen of somatic musculature and the heart. Furthermore, we found distinct expression patterns of NK3, NK5, NK6, Lbx and Msx in the developing nervous system. The same holds true for the NKL gene NK2.2, which does not belong to the NK cluster but is a related gene playing a role in neural patterning. Surprisingly, NK1, Msx and Lbx are additionally expressed in a segment polarity-like pattern early in development-a feature that has been otherwise reported only from annelids. CONCLUSIONOur results indicate that the NK cluster genes were involved in mesoderm and neural development in the last common ancestor of bilaterians or at least nephrozoans (i.e., bilaterians to the exclusion of xenacoelomorphs). By comparing our data from an onychophoran to those from other bilaterians, we critically review the hypothesis of a complex "urbilaterian" with a segmented body, a pulsatile organ or heart, and a condensed mediolaterally patterned nerve cord.
Understanding the evolution and development of morphological traits of the last common bilaterian ancestor is a major goal of the evo-devo discipline. The reconstruction of this "urbilaterian" is mainly based on comparative studies of common molecular patterning mechanisms in recent model organisms. The NK homeobox genes are key players in many of these molecular pathways, including processes regulating mesoderm, heart and neural development. Shared features seen in the expression patterns of NK genes have been used to determine the ancestral bilaterian characters. However, the commonly used model organisms provide only a limited view on the evolution of these molecular pathways. To further investigate the ancestral roles of NK cluster genes, we analyzed their expression patterns in the onychophoran . We identified nine transcripts of NK cluster genes in , including single copies of , , , , , and , and two copies of . All of these genes except for and are expressed in different mesodermal organs and tissues in embryos of , including the anlagen of somatic musculature and the heart. Furthermore, we found distinct expression patterns of , , , and in the developing nervous system. The same holds true for the NKL gene , which does not belong to the NK cluster but is a related gene playing a role in neural patterning. Surprisingly, , and are additionally expressed in a segment polarity-like pattern early in development-a feature that has been otherwise reported only from annelids. Our results indicate that the NK cluster genes were involved in mesoderm and neural development in the last common ancestor of bilaterians or at least nephrozoans (i.e., bilaterians to the exclusion of xenacoelomorphs). By comparing our data from an onychophoran to those from other bilaterians, we critically review the hypothesis of a complex "urbilaterian" with a segmented body, a pulsatile organ or heart, and a condensed mediolaterally patterned nerve cord.
Abstract Background Understanding the evolution and development of morphological traits of the last common bilaterian ancestor is a major goal of the evo-devo discipline. The reconstruction of this “urbilaterian” is mainly based on comparative studies of common molecular patterning mechanisms in recent model organisms. The NK homeobox genes are key players in many of these molecular pathways, including processes regulating mesoderm, heart and neural development. Shared features seen in the expression patterns of NK genes have been used to determine the ancestral bilaterian characters. However, the commonly used model organisms provide only a limited view on the evolution of these molecular pathways. To further investigate the ancestral roles of NK cluster genes, we analyzed their expression patterns in the onychophoran Euperipatoides rowelli. Results We identified nine transcripts of NK cluster genes in E. rowelli, including single copies of NK1, NK3, NK4, NK5, Msx, Lbx and Tlx, and two copies of NK6. All of these genes except for NK6.1 and NK6.2 are expressed in different mesodermal organs and tissues in embryos of E. rowelli, including the anlagen of somatic musculature and the heart. Furthermore, we found distinct expression patterns of NK3, NK5, NK6, Lbx and Msx in the developing nervous system. The same holds true for the NKL gene NK2.2, which does not belong to the NK cluster but is a related gene playing a role in neural patterning. Surprisingly, NK1, Msx and Lbx are additionally expressed in a segment polarity-like pattern early in development—a feature that has been otherwise reported only from annelids. Conclusion Our results indicate that the NK cluster genes were involved in mesoderm and neural development in the last common ancestor of bilaterians or at least nephrozoans (i.e., bilaterians to the exclusion of xenacoelomorphs). By comparing our data from an onychophoran to those from other bilaterians, we critically review the hypothesis of a complex “urbilaterian” with a segmented body, a pulsatile organ or heart, and a condensed mediolaterally patterned nerve cord.
ArticleNumber 17
Audience Academic
Author Mayer, Georg
Kahnke, Laura
Hering, Lars
Treffkorn, Sandra
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  givenname: Laura
  surname: Kahnke
  fullname: Kahnke, Laura
  organization: Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Str. 40, 34132 Kassel, Germany
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  givenname: Lars
  surname: Hering
  fullname: Hering, Lars
  organization: Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Str. 40, 34132 Kassel, Germany
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  givenname: Georg
  surname: Mayer
  fullname: Mayer, Georg
  organization: Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Str. 40, 34132 Kassel, Germany
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30026904$$D View this record in MEDLINE/PubMed
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Issue 1
Keywords Homeobox genes
Mesoderm development
NK-linked genes
Urbilaterian
Gene expression
Velvet worms
Nephrozoa
Onychophora
NK genes
Language English
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Snippet Understanding the evolution and development of morphological traits of the last common bilaterian ancestor is a major goal of the evo-devo discipline. The...
BackgroundUnderstanding the evolution and development of morphological traits of the last common bilaterian ancestor is a major goal of the evo-devo...
BACKGROUNDUnderstanding the evolution and development of morphological traits of the last common bilaterian ancestor is a major goal of the evo-devo...
Abstract Background Understanding the evolution and development of morphological traits of the last common bilaterian ancestor is a major goal of the evo-devo...
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StartPage 17
SubjectTerms Analysis
Arthropods
Caenorhabditis elegans
Developmental biology
Drosophila
Embryos
Euperipatoides rowelli
Evolution
Evolutionary genetics
Gene expression
Genetic aspects
Genomes
Heart
Homeobox
Homeobox genes
Insects
Mesoderm
Morphology
Nervous system
NK genes
NK-linked genes
Onychophora
Pattern formation
Phylogenetics
Polarity
Velvet worms
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Title Expression of NK cluster genes in the onychophoran Euperipatoides rowelli : implications for the evolution of NK family genes in nephrozoans
URI https://www.ncbi.nlm.nih.gov/pubmed/30026904
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