Evolution of sex-dependent mtDNA transmission in freshwater mussels (Bivalvia: Unionida)
Abstract Doubly uniparental inheritance (DUI) describes a mode of mtDNA transmission widespread in gonochoric freshwater mussels (Bivalvia: Palaeoheterodonta: Unionida). In this system, both female- and male-transmitted mtDNAs, named F and M respectively, coexist in the same species. In unionids, DU...
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Nature Portfolio
2017
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oai:doaj.org-article:e5b250e6c3024fa6babd37edc3f6bbb22021-12-02T11:40:50ZEvolution of sex-dependent mtDNA transmission in freshwater mussels (Bivalvia: Unionida)10.1038/s41598-017-01708-12045-2322https://doaj.org/article/e5b250e6c3024fa6babd37edc3f6bbb22017-05-01T00:00:00Zhttps://doi.org/10.1038/s41598-017-01708-1https://doaj.org/toc/2045-2322Abstract Doubly uniparental inheritance (DUI) describes a mode of mtDNA transmission widespread in gonochoric freshwater mussels (Bivalvia: Palaeoheterodonta: Unionida). In this system, both female- and male-transmitted mtDNAs, named F and M respectively, coexist in the same species. In unionids, DUI is strictly correlated to gonochorism and to the presence of the atypical open reading frames (ORFans) F-orf and M-orf, respectively inside F and M mtDNAs, which are hypothesized to participate in sex determination. However, DUI is not found in all three Unionida superfamilies (confirmed in Hyrioidea and Unionoidea but not in Etherioidea), raising the question of its origin in these bivalves. To reconstruct the co-evolution of DUI and of ORFans, we sequenced the mtDNAs of four unionids (two gonochoric with DUI, one gonochoric and one hermaphroditic without DUI) and of the related gonochoric species Neotrigonia margaritacea (Palaeoheterodonta: Trigoniida). Our analyses suggest that rearranged mtDNAs appeared early during unionid radiation, and that a duplicated and diverged atp8 gene evolved into the M-orf associated with the paternal transmission route in Hyrioidea and Unionoidea, but not in Etherioidea. We propose that novel mtDNA-encoded genes can deeply influence bivalve sex determining systems and the evolution of the mitogenomes in which they occur.Davide GuerraFederico PlazziDonald T. StewartArthur E. BoganWalter R. HoehSophie BretonNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 7, Iss 1, Pp 1-13 (2017) |
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Medicine R Science Q Davide Guerra Federico Plazzi Donald T. Stewart Arthur E. Bogan Walter R. Hoeh Sophie Breton Evolution of sex-dependent mtDNA transmission in freshwater mussels (Bivalvia: Unionida) |
description |
Abstract Doubly uniparental inheritance (DUI) describes a mode of mtDNA transmission widespread in gonochoric freshwater mussels (Bivalvia: Palaeoheterodonta: Unionida). In this system, both female- and male-transmitted mtDNAs, named F and M respectively, coexist in the same species. In unionids, DUI is strictly correlated to gonochorism and to the presence of the atypical open reading frames (ORFans) F-orf and M-orf, respectively inside F and M mtDNAs, which are hypothesized to participate in sex determination. However, DUI is not found in all three Unionida superfamilies (confirmed in Hyrioidea and Unionoidea but not in Etherioidea), raising the question of its origin in these bivalves. To reconstruct the co-evolution of DUI and of ORFans, we sequenced the mtDNAs of four unionids (two gonochoric with DUI, one gonochoric and one hermaphroditic without DUI) and of the related gonochoric species Neotrigonia margaritacea (Palaeoheterodonta: Trigoniida). Our analyses suggest that rearranged mtDNAs appeared early during unionid radiation, and that a duplicated and diverged atp8 gene evolved into the M-orf associated with the paternal transmission route in Hyrioidea and Unionoidea, but not in Etherioidea. We propose that novel mtDNA-encoded genes can deeply influence bivalve sex determining systems and the evolution of the mitogenomes in which they occur. |
format |
article |
author |
Davide Guerra Federico Plazzi Donald T. Stewart Arthur E. Bogan Walter R. Hoeh Sophie Breton |
author_facet |
Davide Guerra Federico Plazzi Donald T. Stewart Arthur E. Bogan Walter R. Hoeh Sophie Breton |
author_sort |
Davide Guerra |
title |
Evolution of sex-dependent mtDNA transmission in freshwater mussels (Bivalvia: Unionida) |
title_short |
Evolution of sex-dependent mtDNA transmission in freshwater mussels (Bivalvia: Unionida) |
title_full |
Evolution of sex-dependent mtDNA transmission in freshwater mussels (Bivalvia: Unionida) |
title_fullStr |
Evolution of sex-dependent mtDNA transmission in freshwater mussels (Bivalvia: Unionida) |
title_full_unstemmed |
Evolution of sex-dependent mtDNA transmission in freshwater mussels (Bivalvia: Unionida) |
title_sort |
evolution of sex-dependent mtdna transmission in freshwater mussels (bivalvia: unionida) |
publisher |
Nature Portfolio |
publishDate |
2017 |
url |
https://doaj.org/article/e5b250e6c3024fa6babd37edc3f6bbb2 |
work_keys_str_mv |
AT davideguerra evolutionofsexdependentmtdnatransmissioninfreshwatermusselsbivalviaunionida AT federicoplazzi evolutionofsexdependentmtdnatransmissioninfreshwatermusselsbivalviaunionida AT donaldtstewart evolutionofsexdependentmtdnatransmissioninfreshwatermusselsbivalviaunionida AT arthurebogan evolutionofsexdependentmtdnatransmissioninfreshwatermusselsbivalviaunionida AT walterrhoeh evolutionofsexdependentmtdnatransmissioninfreshwatermusselsbivalviaunionida AT sophiebreton evolutionofsexdependentmtdnatransmissioninfreshwatermusselsbivalviaunionida |
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