Evolution of sexes from an ancestral mating-type specification pathway.

Male and female sexes have evolved repeatedly in eukaryotes but the origins of dimorphic sexes and their relationship to mating types in unicellular species are not understood. Volvocine algae include isogamous species such as Chlamydomonas reinhardtii, with two equal-sized mating types, and oogamou...

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Autores principales:	Sa Geng, Peter De Hoff, James G Umen
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2014
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/99d54382a8374ec98527395821f9dbca
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spelling	oai:doaj.org-article:99d54382a8374ec98527395821f9dbca2021-11-25T05:33:03ZEvolution of sexes from an ancestral mating-type specification pathway.1544-91731545-788510.1371/journal.pbio.1001904https://doaj.org/article/99d54382a8374ec98527395821f9dbca2014-07-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/25003332/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Male and female sexes have evolved repeatedly in eukaryotes but the origins of dimorphic sexes and their relationship to mating types in unicellular species are not understood. Volvocine algae include isogamous species such as Chlamydomonas reinhardtii, with two equal-sized mating types, and oogamous multicellular species such as Volvox carteri with sperm-producing males and egg-producing females. Theoretical work predicts genetic linkage of a gamete cell-size regulatory gene(s) to an ancestral mating-type locus as a possible step in the evolution of dimorphic gametes, but this idea has not been tested. Here we show that, contrary to predictions, a single conserved mating locus (MT) gene in volvocine algae-MID, which encodes a RWP-RK domain transcription factor-evolved from its ancestral role in C. reinhardtii as a mating-type specifier, to become a determinant of sperm and egg development in V. carteri. Transgenic female V. carteri expressing male MID produced functional sperm packets during sexual development. Transgenic male V. carteri with RNA interference (RNAi)-mediated knockdowns of VcMID produced functional eggs, or self-fertile hermaphrodites. Post-transcriptional controls were found to regulate cell-type-limited expression and nuclear localization of VcMid protein that restricted its activity to nuclei of developing male germ cells and sperm. Crosses with sex-reversed strains uncoupled sex determination from sex chromosome identity and revealed gender-specific roles for male and female mating locus genes in sexual development, gamete fitness and reproductive success. Our data show genetic continuity between the mating-type specification and sex determination pathways of volvocine algae, and reveal evidence for gender-specific adaptations in the male and female mating locus haplotypes of Volvox. These findings will enable a deeper understanding of how a master regulator of mating-type determination in an ancestral unicellular species was reprogrammed to control sexually dimorphic gamete development in a multicellular descendant.Sa GengPeter De HoffJames G UmenPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 12, Iss 7, p e1001904 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Sa Geng Peter De Hoff James G Umen Evolution of sexes from an ancestral mating-type specification pathway.
description	Male and female sexes have evolved repeatedly in eukaryotes but the origins of dimorphic sexes and their relationship to mating types in unicellular species are not understood. Volvocine algae include isogamous species such as Chlamydomonas reinhardtii, with two equal-sized mating types, and oogamous multicellular species such as Volvox carteri with sperm-producing males and egg-producing females. Theoretical work predicts genetic linkage of a gamete cell-size regulatory gene(s) to an ancestral mating-type locus as a possible step in the evolution of dimorphic gametes, but this idea has not been tested. Here we show that, contrary to predictions, a single conserved mating locus (MT) gene in volvocine algae-MID, which encodes a RWP-RK domain transcription factor-evolved from its ancestral role in C. reinhardtii as a mating-type specifier, to become a determinant of sperm and egg development in V. carteri. Transgenic female V. carteri expressing male MID produced functional sperm packets during sexual development. Transgenic male V. carteri with RNA interference (RNAi)-mediated knockdowns of VcMID produced functional eggs, or self-fertile hermaphrodites. Post-transcriptional controls were found to regulate cell-type-limited expression and nuclear localization of VcMid protein that restricted its activity to nuclei of developing male germ cells and sperm. Crosses with sex-reversed strains uncoupled sex determination from sex chromosome identity and revealed gender-specific roles for male and female mating locus genes in sexual development, gamete fitness and reproductive success. Our data show genetic continuity between the mating-type specification and sex determination pathways of volvocine algae, and reveal evidence for gender-specific adaptations in the male and female mating locus haplotypes of Volvox. These findings will enable a deeper understanding of how a master regulator of mating-type determination in an ancestral unicellular species was reprogrammed to control sexually dimorphic gamete development in a multicellular descendant.
format	article
author	Sa Geng Peter De Hoff James G Umen
author_facet	Sa Geng Peter De Hoff James G Umen
author_sort	Sa Geng
title	Evolution of sexes from an ancestral mating-type specification pathway.
title_short	Evolution of sexes from an ancestral mating-type specification pathway.
title_full	Evolution of sexes from an ancestral mating-type specification pathway.
title_fullStr	Evolution of sexes from an ancestral mating-type specification pathway.
title_full_unstemmed	Evolution of sexes from an ancestral mating-type specification pathway.
title_sort	evolution of sexes from an ancestral mating-type specification pathway.
publisher	Public Library of Science (PLoS)
publishDate	2014
url	https://doaj.org/article/99d54382a8374ec98527395821f9dbca
work_keys_str_mv	AT sageng evolutionofsexesfromanancestralmatingtypespecificationpathway AT peterdehoff evolutionofsexesfromanancestralmatingtypespecificationpathway AT jamesgumen evolutionofsexesfromanancestralmatingtypespecificationpathway
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Evolution of sexes from an ancestral mating-type specification pathway.

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