The Lineage-Specific Evolution of Aquaporin Gene Clusters Facilitated Tetrapod Terrestrial Adaptation
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Author
Finn, Roderick Nigel
Hlidberg, Jón Baldur
Cutler, Christopher P.
Publication date
2014-11-26ISSN
1932-6203
Abstract
A major physiological barrier for aquatic organisms adapting to terrestrial life is dessication in the aerial environment. This barrier was nevertheless overcome by the Devonian ancestors of extant Tetrapoda, but the origin of specific molecular mechanisms that solved this water problem remains largely unknown. Here we show that an ancient aquaporin gene cluster evolved specifically in the sarcopterygian lineage, and subsequently diverged into paralogous forms of AQP2, -5, or -6 to mediate water conservation in extant Tetrapoda. To determine the origin of these apomorphic genomic traits, we combined aquaporin sequencing from jawless and jawed vertebrates with broad taxon assembly of .2,000 transcripts
amongst 131 deuterostome genomes and developed a model based upon Bayesian inference that traces their convergent roots to stem subfamilies in basal Metazoa and Prokaryota. This approach uncovered an unexpected diversity of aquaporins in every lineage investigated, and revealed that the vertebrate
superfamily consists of 17 classes of aquaporins (Aqp0 - Aqp16). The oldest orthologs associated with water conservation in modern Tetrapoda are traced to a cluster of three aqp2-like genes in Actinistia that likely arose .500 Ma through duplication of an aqp0-like gene present in a jawless ancestor. In sea lamprey, we show that aqp0 first arose in a protocluster comprised of a novel aqp14 paralog and a fused aqp01 gene. To corroborate these findings, we conducted phylogenetic analyses of five syntenic nuclear receptor subfamilies, which, together with observations of extensive genome rearrangements, support the coincident loss of ancestral aqp2-like orthologs in Actinopterygii. We thus conclude that the divergence of sarcopterygian-specific aquaporin gene clusters was permissive for the evolution of water conservation mechanisms that facilitated tetrapod terrestrial adaptation.
Document Type
Article
Document version
Published version
Language
English
Subject (CDU)
639 - Hunting. Fishing. Fish breeding
Pages
38
Publisher
Public Library of Science
Is part of
PLoS ONE
Citation
Finn, Roderick Nigel, François Chauvigné, Jón Baldur Hlidberg, Christopher P. Cutler, and Joan Cerdà. 2014. "The Lineage-Specific Evolution Of Aquaporin Gene Clusters Facilitated Tetrapod Terrestrial Adaptation". Plos ONE 9 (11): e113686. doi:10.1371/journal.pone.0113686.
Grant agreement number
MICINN/Programa Nacional de Proyectos de Investigación Fundamental/AGL2010-15597/ES/AQUAPORINAS TESTICULARES DURANTE LA ESPERMATOGENESIS DE PECES MARINOS Y LA ACTIVACION Y PERMEABILIDAD ESPERMATICA/
Program
Aqüicultura
This item appears in the following Collection(s)
- ARTICLES CIENTÍFICS [2838]
Except where otherwise noted, this item's license is described as http://creativecommons.org/licenses/by/4.0/