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尾索动物中大量的基因丢失和功能重排扩展了脊索动物Wnt家族进化的边界。

Massive Gene Loss and Function Shuffling in Appendicularians Stretch the Boundaries of Chordate Wnt Family Evolution.

作者信息

Martí-Solans Josep, Godoy-Marín Hector, Diaz-Gracia Miriam, Onuma Takeshi A, Nishida Hiroki, Albalat Ricard, Cañestro Cristian

机构信息

Departament de Genètica, Microbiologia i Estadística, Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain.

Department of Biological Sciences, Graduate School of Science, Osaka University, Osaka, Japan.

出版信息

Front Cell Dev Biol. 2021 Jun 9;9:700827. doi: 10.3389/fcell.2021.700827. eCollection 2021.


DOI:10.3389/fcell.2021.700827
PMID:34179025
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC8220140/
Abstract

Gene loss is a pervasive source of genetic variation that influences species evolvability, biodiversity and the innovation of evolutionary adaptations. To better understand the evolutionary patterns and impact of gene loss, here we investigate as a case study the evolution of the wingless (Wnt) family in the appendicularian tunicate , an emergent EvoDevo model characterized by its proneness to lose genes among chordates. Genome survey and phylogenetic analyses reveal that only four of the thirteen Wnt subfamilies have survived in -Wnt5, Wnt10, Wnt11, and Wnt16,-representing the minimal Wnt repertoire described in chordates. While the loss of Wnt4 and Wnt8 likely occurred in the last common ancestor of tunicates, representing therefore a synapomorphy of this subphylum, the rest of losses occurred during the evolution of appendicularians. This work provides the first complete Wnt developmental expression atlas in a tunicate and the first insights into the evolution of Wnt developmental functions in appendicularians. Our work highlights three main evolutionary patterns of gene loss: (1) conservation of ancestral Wnt expression domains not affected by gene losses; (2) function shuffling among Wnt paralogs accompanied by gene losses; and (3) extinction of Wnt expression in certain embryonic directly correlated with gene losses. Overall our work reveals that in contrast to "conservative" pattern of evolution of cephalochordates and vertebrates, shows an even more radical "liberal" evolutionary pattern than that described ascidian tunicates, stretching the boundaries of the malleability of Wnt family evolution in chordates.

摘要

基因丢失是遗传变异的一个普遍来源,它影响物种的进化能力、生物多样性以及进化适应的创新。为了更好地理解基因丢失的进化模式及其影响,我们以尾海鞘纲被囊动物中的无翅(Wnt)家族进化为例进行研究,尾海鞘纲是一种新兴的进化发育生物学(EvoDevo)模型,其特点是在脊索动物中易于丢失基因。基因组调查和系统发育分析表明,在13个Wnt亚家族中只有4个得以保留,即Wnt5、Wnt10、Wnt11和Wnt16,这代表了脊索动物中描述的最小Wnt基因库。虽然Wnt4和Wnt8的丢失可能发生在被囊动物的最后一个共同祖先中,因此代表了该亚门的一个共衍征,但其余的丢失发生在尾海鞘纲的进化过程中。这项工作提供了首个被囊动物完整的Wnt发育表达图谱,并首次深入了解了尾海鞘纲中Wnt发育功能的进化。我们的工作突出了基因丢失的三种主要进化模式:(1)未受基因丢失影响的祖先Wnt表达域的保守性;(2)Wnt旁系同源基因之间的功能洗牌并伴有基因丢失;(3)某些胚胎中Wnt表达的消失与基因丢失直接相关。总体而言,我们的工作表明,与头索动物和脊椎动物的“保守”进化模式相反,尾海鞘纲显示出比被描述的海鞘更为激进的“自由”进化模式,拓展了脊索动物中Wnt家族进化可塑性的边界。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/518e/8220140/c25efbcf21b4/fcell-09-700827-g005.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/518e/8220140/114b613ffce4/fcell-09-700827-g001.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/518e/8220140/76e3ba4bdf18/fcell-09-700827-g002.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/518e/8220140/65c3b410e71c/fcell-09-700827-g003.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/518e/8220140/6648f9853037/fcell-09-700827-g004.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/518e/8220140/c25efbcf21b4/fcell-09-700827-g005.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/518e/8220140/114b613ffce4/fcell-09-700827-g001.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/518e/8220140/76e3ba4bdf18/fcell-09-700827-g002.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/518e/8220140/65c3b410e71c/fcell-09-700827-g003.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/518e/8220140/6648f9853037/fcell-09-700827-g004.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/518e/8220140/c25efbcf21b4/fcell-09-700827-g005.jpg

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[1]
Massive Gene Loss and Function Shuffling in Appendicularians Stretch the Boundaries of Chordate Wnt Family Evolution.

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[2]
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[3]
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[4]
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[5]
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[6]
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[8]
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[3]
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[4]
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[5]
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[6]
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[7]
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[8]
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本文引用的文献

[1]
Less Is More, Natural Loss-of-Function Mutation Is a Strategy for Adaptation.

Plant Commun. 2020-11-9

[2]
Gene Loss Predictably Drives Evolutionary Adaptation.

Mol Biol Evol. 2020-10-1

[3]
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Proc Natl Acad Sci U S A. 2020-2-6

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Nat Ecol Evol. 2020-1-28

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Oikopleura dioica: An Emergent Chordate Model to Study the Impact of Gene Loss on the Evolution of the Mechanisms of Development.

Results Probl Cell Differ. 2019

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Wnt evolution and function shuffling in liberal and conservative chordate genomes.

Genome Biol. 2018-7-25

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A genomics approach reveals insights into the importance of gene losses for mammalian adaptations.

Nat Commun. 2018-3-23

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Evidence for a centrosome-attracting body like structure in germ-soma segregation during early development, in the urochordate Oikopleura dioica.

BMC Dev Biol. 2018-2-27

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