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How did a duplicated gene copy evolve into a restorer-of-fertility gene in a plant? The case of Oma1

Restorer-of-fertility (Rf) is a suppressor of cytoplasmic male sterility (CMS), a mitochondrion-encoded trait that has been reported in many plant species. The occurrence of CMS is considered to be independent in each lineage; hence, the question of how Rf evolved was raised. Sugar beet Rf resembles...

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Autores principales: Arakawa, Takumi, Sugaya, Hajime, Katsuyama, Takaya, Honma, Yujiro, Matsui, Katsunori, Matsuhira, Hiroaki, Kuroda, Yosuke, Kitazaki, Kazuyoshi, Kubo, Tomohiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6894571/
https://www.ncbi.nlm.nih.gov/pubmed/31827833
http://dx.doi.org/10.1098/rsos.190853
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author Arakawa, Takumi
Sugaya, Hajime
Katsuyama, Takaya
Honma, Yujiro
Matsui, Katsunori
Matsuhira, Hiroaki
Kuroda, Yosuke
Kitazaki, Kazuyoshi
Kubo, Tomohiko
author_facet Arakawa, Takumi
Sugaya, Hajime
Katsuyama, Takaya
Honma, Yujiro
Matsui, Katsunori
Matsuhira, Hiroaki
Kuroda, Yosuke
Kitazaki, Kazuyoshi
Kubo, Tomohiko
author_sort Arakawa, Takumi
collection PubMed
description Restorer-of-fertility (Rf) is a suppressor of cytoplasmic male sterility (CMS), a mitochondrion-encoded trait that has been reported in many plant species. The occurrence of CMS is considered to be independent in each lineage; hence, the question of how Rf evolved was raised. Sugar beet Rf resembles Oma1, a gene for quality control of the mitochondrial inner membrane. Oma1 homologues comprise a small gene family in the sugar beet genome, unlike Arabidopsis and other eukaryotes. The sugar beet sequence that best matched Arabidopsis atOma1 was named bvOma1; sugar beet Rf (RF1-Oma1) was another member. During anther development, atOma1 mRNA was detected from the tetrad to the microspore stages, whereas bvOma1 mRNA was detected at the microspore stage and RF1-Oma1 mRNA was detected during the meiosis and tetrad stages. A transgenic study revealed that, whereas RF1-Oma1 can bind to a CMS-specific protein and alter the higher-order structure of the CMS-specific protein complex, neither bvOma1 nor atOma1 show such activity. We favour the hypothesis that an ancestral Oma1 gene duplicated to form a small gene family, and that one of the copies evolved and acquired a novel expression pattern and protein function as an Rf, i.e. RF1-Oma1 evolved via neofunctionalization.
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spelling pubmed-68945712019-12-11 How did a duplicated gene copy evolve into a restorer-of-fertility gene in a plant? The case of Oma1 Arakawa, Takumi Sugaya, Hajime Katsuyama, Takaya Honma, Yujiro Matsui, Katsunori Matsuhira, Hiroaki Kuroda, Yosuke Kitazaki, Kazuyoshi Kubo, Tomohiko R Soc Open Sci Genetics and Genomics Restorer-of-fertility (Rf) is a suppressor of cytoplasmic male sterility (CMS), a mitochondrion-encoded trait that has been reported in many plant species. The occurrence of CMS is considered to be independent in each lineage; hence, the question of how Rf evolved was raised. Sugar beet Rf resembles Oma1, a gene for quality control of the mitochondrial inner membrane. Oma1 homologues comprise a small gene family in the sugar beet genome, unlike Arabidopsis and other eukaryotes. The sugar beet sequence that best matched Arabidopsis atOma1 was named bvOma1; sugar beet Rf (RF1-Oma1) was another member. During anther development, atOma1 mRNA was detected from the tetrad to the microspore stages, whereas bvOma1 mRNA was detected at the microspore stage and RF1-Oma1 mRNA was detected during the meiosis and tetrad stages. A transgenic study revealed that, whereas RF1-Oma1 can bind to a CMS-specific protein and alter the higher-order structure of the CMS-specific protein complex, neither bvOma1 nor atOma1 show such activity. We favour the hypothesis that an ancestral Oma1 gene duplicated to form a small gene family, and that one of the copies evolved and acquired a novel expression pattern and protein function as an Rf, i.e. RF1-Oma1 evolved via neofunctionalization. The Royal Society 2019-11-06 /pmc/articles/PMC6894571/ /pubmed/31827833 http://dx.doi.org/10.1098/rsos.190853 Text en © 2019 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Genetics and Genomics
Arakawa, Takumi
Sugaya, Hajime
Katsuyama, Takaya
Honma, Yujiro
Matsui, Katsunori
Matsuhira, Hiroaki
Kuroda, Yosuke
Kitazaki, Kazuyoshi
Kubo, Tomohiko
How did a duplicated gene copy evolve into a restorer-of-fertility gene in a plant? The case of Oma1
title How did a duplicated gene copy evolve into a restorer-of-fertility gene in a plant? The case of Oma1
title_full How did a duplicated gene copy evolve into a restorer-of-fertility gene in a plant? The case of Oma1
title_fullStr How did a duplicated gene copy evolve into a restorer-of-fertility gene in a plant? The case of Oma1
title_full_unstemmed How did a duplicated gene copy evolve into a restorer-of-fertility gene in a plant? The case of Oma1
title_short How did a duplicated gene copy evolve into a restorer-of-fertility gene in a plant? The case of Oma1
title_sort how did a duplicated gene copy evolve into a restorer-of-fertility gene in a plant? the case of oma1
topic Genetics and Genomics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6894571/
https://www.ncbi.nlm.nih.gov/pubmed/31827833
http://dx.doi.org/10.1098/rsos.190853
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