Evolutionary history of glucose-6-phosphatase encoding genes in vertebrate lineages: towards a better understanding of the functions of multiple duplicates

Abstract Background Glucose-6-phosphate (G6pc) is a key enzyme involved in the regulation of the glucose homeostasis. The present study aims at revisiting and clarifying the evolutionary history of g6pc genes in vertebrates. Results g6pc duplications happened by successive rounds of whole genome dup...

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Main Authors: Lucie Marandel, Stéphane Panserat, Elisabeth Plagnes-Juan, Eva Arbenoits, José Luis Soengas, Julien Bobe
Format: Article
Language:English
Published: BMC 2017-05-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-017-3727-1
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author Lucie Marandel
Stéphane Panserat
Elisabeth Plagnes-Juan
Eva Arbenoits
José Luis Soengas
Julien Bobe
author_facet Lucie Marandel
Stéphane Panserat
Elisabeth Plagnes-Juan
Eva Arbenoits
José Luis Soengas
Julien Bobe
author_sort Lucie Marandel
collection DOAJ
description Abstract Background Glucose-6-phosphate (G6pc) is a key enzyme involved in the regulation of the glucose homeostasis. The present study aims at revisiting and clarifying the evolutionary history of g6pc genes in vertebrates. Results g6pc duplications happened by successive rounds of whole genome duplication that occurred during vertebrate evolution. g6pc duplicated before or around Osteichthyes/Chondrichthyes radiation, giving rise to g6pca and g6pcb as a consequence of the second vertebrate whole genome duplication. g6pca was lost after this duplication in Sarcopterygii whereas both g6pca and g6pcb then duplicated as a consequence of the teleost-specific whole genome duplication. One g6pca duplicate was lost after this duplication in teleosts. Similarly one g6pcb2 duplicate was lost at least in the ancestor of percomorpha. The analysis of the evolution of spatial expression patterns of g6pc genes in vertebrates showed that all g6pc were mainly expressed in intestine and liver whereas teleost-specific g6pcb2 genes were mainly and surprisingly expressed in brain and heart. g6pcb2b, one gene previously hypothesised to be involved in the glucose intolerant phenotype in trout, was unexpectedly up-regulated (as it was in liver) by carbohydrates in trout telencephalon without showing significant changes in other brain regions. This up-regulation is in striking contrast with expected glucosensing mechanisms suggesting that its positive response to glucose relates to specific unknown processes in this brain area. Conclusions Our results suggested that the fixation and the divergence of g6pc duplicated genes during vertebrates’ evolution may lead to adaptive novelty and probably to the emergence of novel phenotypes related to glucose homeostasis.
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spelling doaj.art-a996fa067505448c9a93cbc8f8934f122022-12-22T01:24:11ZengBMCBMC Genomics1471-21642017-05-0118111310.1186/s12864-017-3727-1Evolutionary history of glucose-6-phosphatase encoding genes in vertebrate lineages: towards a better understanding of the functions of multiple duplicatesLucie Marandel0Stéphane Panserat1Elisabeth Plagnes-Juan2Eva Arbenoits3José Luis Soengas4Julien Bobe5INRA, UPPA, UMR 1419 Nutrition, Metabolism, AquacultureINRA, UPPA, UMR 1419 Nutrition, Metabolism, AquacultureINRA, UPPA, UMR 1419 Nutrition, Metabolism, AquacultureINRA, UPPA, UMR 1419 Nutrition, Metabolism, AquacultureDepartamento de Bioloxía Funcional e Ciencias da Saúde, Laboratorio de Fisioloxía Animal, Facultade de Bioloxía, Universidade de VigoINRA, UR1037 LPGP, Campus de BeaulieuAbstract Background Glucose-6-phosphate (G6pc) is a key enzyme involved in the regulation of the glucose homeostasis. The present study aims at revisiting and clarifying the evolutionary history of g6pc genes in vertebrates. Results g6pc duplications happened by successive rounds of whole genome duplication that occurred during vertebrate evolution. g6pc duplicated before or around Osteichthyes/Chondrichthyes radiation, giving rise to g6pca and g6pcb as a consequence of the second vertebrate whole genome duplication. g6pca was lost after this duplication in Sarcopterygii whereas both g6pca and g6pcb then duplicated as a consequence of the teleost-specific whole genome duplication. One g6pca duplicate was lost after this duplication in teleosts. Similarly one g6pcb2 duplicate was lost at least in the ancestor of percomorpha. The analysis of the evolution of spatial expression patterns of g6pc genes in vertebrates showed that all g6pc were mainly expressed in intestine and liver whereas teleost-specific g6pcb2 genes were mainly and surprisingly expressed in brain and heart. g6pcb2b, one gene previously hypothesised to be involved in the glucose intolerant phenotype in trout, was unexpectedly up-regulated (as it was in liver) by carbohydrates in trout telencephalon without showing significant changes in other brain regions. This up-regulation is in striking contrast with expected glucosensing mechanisms suggesting that its positive response to glucose relates to specific unknown processes in this brain area. Conclusions Our results suggested that the fixation and the divergence of g6pc duplicated genes during vertebrates’ evolution may lead to adaptive novelty and probably to the emergence of novel phenotypes related to glucose homeostasis.http://link.springer.com/article/10.1186/s12864-017-3727-1TeleostsDuplicated genesSarcopterygiiActinopterygiitroutglucose
spellingShingle Lucie Marandel
Stéphane Panserat
Elisabeth Plagnes-Juan
Eva Arbenoits
José Luis Soengas
Julien Bobe
Evolutionary history of glucose-6-phosphatase encoding genes in vertebrate lineages: towards a better understanding of the functions of multiple duplicates
BMC Genomics
Teleosts
Duplicated genes
Sarcopterygii
Actinopterygii
trout
glucose
title Evolutionary history of glucose-6-phosphatase encoding genes in vertebrate lineages: towards a better understanding of the functions of multiple duplicates
title_full Evolutionary history of glucose-6-phosphatase encoding genes in vertebrate lineages: towards a better understanding of the functions of multiple duplicates
title_fullStr Evolutionary history of glucose-6-phosphatase encoding genes in vertebrate lineages: towards a better understanding of the functions of multiple duplicates
title_full_unstemmed Evolutionary history of glucose-6-phosphatase encoding genes in vertebrate lineages: towards a better understanding of the functions of multiple duplicates
title_short Evolutionary history of glucose-6-phosphatase encoding genes in vertebrate lineages: towards a better understanding of the functions of multiple duplicates
title_sort evolutionary history of glucose 6 phosphatase encoding genes in vertebrate lineages towards a better understanding of the functions of multiple duplicates
topic Teleosts
Duplicated genes
Sarcopterygii
Actinopterygii
trout
glucose
url http://link.springer.com/article/10.1186/s12864-017-3727-1
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