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A quantitative proteomic analysis of the molecular mechanism underlying fertility conversion in thermo-sensitive genetic male sterility line AnnongS-1

BACKGROUND: Thermo-sensitive genetic male sterile (TGMS) lines have been widely used in two-line hybrid rice breeding. The two-line hybrids have increased rice yields substantially. However, the effect of environmental temperatures on the fertility conversion is still not fully clear. In this study,...

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Detalles Bibliográficos
Autores principales: Wang, Siyao, Tian, Qingyuan, Zhou, Shiqi, Mao, Dandan, Chen, Liangbi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6371510/
https://www.ncbi.nlm.nih.gov/pubmed/30744566
http://dx.doi.org/10.1186/s12870-019-1666-5
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author Wang, Siyao
Tian, Qingyuan
Zhou, Shiqi
Mao, Dandan
Chen, Liangbi
author_facet Wang, Siyao
Tian, Qingyuan
Zhou, Shiqi
Mao, Dandan
Chen, Liangbi
author_sort Wang, Siyao
collection PubMed
description BACKGROUND: Thermo-sensitive genetic male sterile (TGMS) lines have been widely used in two-line hybrid rice breeding. The two-line hybrids have increased rice yields substantially. However, the effect of environmental temperatures on the fertility conversion is still not fully clear. In this study, we performed a tandem mass tag (TMT)-based proteomic analysis on the anthers of the TGMS line AnnongS-1 grown under permissive (low) temperature (21 °C) and restrictive (high) temperature (> 26 °C) conditions in an attempt to explore the effect of temperature on the fertility of the male sterile line. RESULTS: After the AnnongS-1 plants were induced under either permissive or restrictive conditions, morphological observations and I(2)-KI staining confirmed that the pollen grains formed under high temperature conditions were abortive while those formed under low temperature developed normally. In comparison to the plants grown under permissive conditions, the restrictive high-temperature conditions led to the differential accumulation of 89 proteins in the anthers, of which 46 were increased in abundance and 43 were decreased in abundance. Most of the subcellular compartments of the anther cells had one or more proteins that had been differentially accumulated, with the cytoplasm and chloroplast having the greatest accumulations. More than 40% of the differentially abundant proteins (DAPs) were enzymes involved in photosynthesis, energy metabolism, biosynthesis and catabolism of cellular components, metabolic regulation, defense and stress, etc. The DAPs related to protein metabolism accounted for the largest proportion (21.35%), followed by those related to defense and stress (12.36%), metabolic regulation (10.11%) and carbohydrate metabolism (8.99%), indicating that such biological processes in anther cells were more susceptible to high temperature stress. CONCLUSIONS: The restrictive temperature induction caused fertility-sterility conversion in the TGMS line AnnongS-1 mainly by adversely affecting the metabolism of protein, carbohydrate and energy, and decreasing the abundances of important proteins closely related to defense and stress, thereby impeding the growth and development of the pollen and weakening the overall defense and ability to endure stress of AnnongS-1. These data are helpful for deepening our understanding of the molecular mechanism underlying fertility conversion in TGMS lines. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1666-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-63715102019-02-21 A quantitative proteomic analysis of the molecular mechanism underlying fertility conversion in thermo-sensitive genetic male sterility line AnnongS-1 Wang, Siyao Tian, Qingyuan Zhou, Shiqi Mao, Dandan Chen, Liangbi BMC Plant Biol Research Article BACKGROUND: Thermo-sensitive genetic male sterile (TGMS) lines have been widely used in two-line hybrid rice breeding. The two-line hybrids have increased rice yields substantially. However, the effect of environmental temperatures on the fertility conversion is still not fully clear. In this study, we performed a tandem mass tag (TMT)-based proteomic analysis on the anthers of the TGMS line AnnongS-1 grown under permissive (low) temperature (21 °C) and restrictive (high) temperature (> 26 °C) conditions in an attempt to explore the effect of temperature on the fertility of the male sterile line. RESULTS: After the AnnongS-1 plants were induced under either permissive or restrictive conditions, morphological observations and I(2)-KI staining confirmed that the pollen grains formed under high temperature conditions were abortive while those formed under low temperature developed normally. In comparison to the plants grown under permissive conditions, the restrictive high-temperature conditions led to the differential accumulation of 89 proteins in the anthers, of which 46 were increased in abundance and 43 were decreased in abundance. Most of the subcellular compartments of the anther cells had one or more proteins that had been differentially accumulated, with the cytoplasm and chloroplast having the greatest accumulations. More than 40% of the differentially abundant proteins (DAPs) were enzymes involved in photosynthesis, energy metabolism, biosynthesis and catabolism of cellular components, metabolic regulation, defense and stress, etc. The DAPs related to protein metabolism accounted for the largest proportion (21.35%), followed by those related to defense and stress (12.36%), metabolic regulation (10.11%) and carbohydrate metabolism (8.99%), indicating that such biological processes in anther cells were more susceptible to high temperature stress. CONCLUSIONS: The restrictive temperature induction caused fertility-sterility conversion in the TGMS line AnnongS-1 mainly by adversely affecting the metabolism of protein, carbohydrate and energy, and decreasing the abundances of important proteins closely related to defense and stress, thereby impeding the growth and development of the pollen and weakening the overall defense and ability to endure stress of AnnongS-1. These data are helpful for deepening our understanding of the molecular mechanism underlying fertility conversion in TGMS lines. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1666-5) contains supplementary material, which is available to authorized users. BioMed Central 2019-02-11 /pmc/articles/PMC6371510/ /pubmed/30744566 http://dx.doi.org/10.1186/s12870-019-1666-5 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Wang, Siyao
Tian, Qingyuan
Zhou, Shiqi
Mao, Dandan
Chen, Liangbi
A quantitative proteomic analysis of the molecular mechanism underlying fertility conversion in thermo-sensitive genetic male sterility line AnnongS-1
title A quantitative proteomic analysis of the molecular mechanism underlying fertility conversion in thermo-sensitive genetic male sterility line AnnongS-1
title_full A quantitative proteomic analysis of the molecular mechanism underlying fertility conversion in thermo-sensitive genetic male sterility line AnnongS-1
title_fullStr A quantitative proteomic analysis of the molecular mechanism underlying fertility conversion in thermo-sensitive genetic male sterility line AnnongS-1
title_full_unstemmed A quantitative proteomic analysis of the molecular mechanism underlying fertility conversion in thermo-sensitive genetic male sterility line AnnongS-1
title_short A quantitative proteomic analysis of the molecular mechanism underlying fertility conversion in thermo-sensitive genetic male sterility line AnnongS-1
title_sort quantitative proteomic analysis of the molecular mechanism underlying fertility conversion in thermo-sensitive genetic male sterility line annongs-1
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6371510/
https://www.ncbi.nlm.nih.gov/pubmed/30744566
http://dx.doi.org/10.1186/s12870-019-1666-5
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