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Reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato

BACKGROUND: Hybrid vigor is highly valued in the agricultural industry. Male sterility is an important trait for crop breeding. Pollen development is under strict control of both gametophytic and sporophytic factors, and defects in this process can result in male sterility. Both in the dicot Arabido...

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Autores principales: Yu, Shi-Xia, Feng, Qiang-Nan, Xie, Hong-Tao, Li, Sha, Zhang, Yan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5399379/
https://www.ncbi.nlm.nih.gov/pubmed/28427341
http://dx.doi.org/10.1186/s12870-017-1025-3
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author Yu, Shi-Xia
Feng, Qiang-Nan
Xie, Hong-Tao
Li, Sha
Zhang, Yan
author_facet Yu, Shi-Xia
Feng, Qiang-Nan
Xie, Hong-Tao
Li, Sha
Zhang, Yan
author_sort Yu, Shi-Xia
collection PubMed
description BACKGROUND: Hybrid vigor is highly valued in the agricultural industry. Male sterility is an important trait for crop breeding. Pollen development is under strict control of both gametophytic and sporophytic factors, and defects in this process can result in male sterility. Both in the dicot Arabidopsis and in the moncot rice, proper timing of programmed cell death (PCD) in the tapetum ensures pollen development. Dynamic ROS levels have been reported to control tapetal PCD, and thus pollen development, in Arabidopsis and rice. However, it was unclear whether it is evolutionarily conserved, as only those two distantly related species were studied. RESULTS: Here, we performed histological analyses of anther development of two economically important dicot species, tobacco and tomato. We identified the same ROS amplitude during anther development in these two species and found that dynamic ROS levels correlate with the initiation and progression of tapetal PCD. We further showed that manipulating ROS levels during anther development severely impaired pollen development, resulting in partial male sterility. Finally, real-time quantitative PCR showed that several tobacco and tomato RBOHs, encoding NADPH oxidases, are preferentially expressed in anthers. CONCLUSION: This study demonstrated evolutionarily conserved ROS amplitude during anther development by examining two commercially important crop species in the Solanaceae. Manipulating ROS amplitude through genetic interference of RBOHs therefore may provide a practical way to generate male sterile plants. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-017-1025-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-53993792017-04-24 Reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato Yu, Shi-Xia Feng, Qiang-Nan Xie, Hong-Tao Li, Sha Zhang, Yan BMC Plant Biol Research Article BACKGROUND: Hybrid vigor is highly valued in the agricultural industry. Male sterility is an important trait for crop breeding. Pollen development is under strict control of both gametophytic and sporophytic factors, and defects in this process can result in male sterility. Both in the dicot Arabidopsis and in the moncot rice, proper timing of programmed cell death (PCD) in the tapetum ensures pollen development. Dynamic ROS levels have been reported to control tapetal PCD, and thus pollen development, in Arabidopsis and rice. However, it was unclear whether it is evolutionarily conserved, as only those two distantly related species were studied. RESULTS: Here, we performed histological analyses of anther development of two economically important dicot species, tobacco and tomato. We identified the same ROS amplitude during anther development in these two species and found that dynamic ROS levels correlate with the initiation and progression of tapetal PCD. We further showed that manipulating ROS levels during anther development severely impaired pollen development, resulting in partial male sterility. Finally, real-time quantitative PCR showed that several tobacco and tomato RBOHs, encoding NADPH oxidases, are preferentially expressed in anthers. CONCLUSION: This study demonstrated evolutionarily conserved ROS amplitude during anther development by examining two commercially important crop species in the Solanaceae. Manipulating ROS amplitude through genetic interference of RBOHs therefore may provide a practical way to generate male sterile plants. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-017-1025-3) contains supplementary material, which is available to authorized users. BioMed Central 2017-04-20 /pmc/articles/PMC5399379/ /pubmed/28427341 http://dx.doi.org/10.1186/s12870-017-1025-3 Text en © The Author(s). 2017 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
Yu, Shi-Xia
Feng, Qiang-Nan
Xie, Hong-Tao
Li, Sha
Zhang, Yan
Reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato
title Reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato
title_full Reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato
title_fullStr Reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato
title_full_unstemmed Reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato
title_short Reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato
title_sort reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5399379/
https://www.ncbi.nlm.nih.gov/pubmed/28427341
http://dx.doi.org/10.1186/s12870-017-1025-3
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