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The Loss-Function of the Male Sterile Gene ZmMs33/ZmGPAT6 Results in Severely Oxidative Stress and Metabolic Disorder in Maize Anthers

In plants, oxidative stress and metabolic reprogramming frequently induce male sterility, however our knowledge of the underlying molecular mechanism is far from complete. Here, a maize genic male-sterility (GMS) mutant (ms33-6038) with a loss-of-function of the ZmMs33 gene encoding glycerol-3-phosp...

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Autores principales: Li, Ziwen, Liu, Shuangshuang, Zhu, Taotao, An, Xueli, Wei, Xun, Zhang, Juan, Wu, Suowei, Dong, Zhenying, Long, Yan, Wan, Xiangyuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9367433/
https://www.ncbi.nlm.nih.gov/pubmed/35954161
http://dx.doi.org/10.3390/cells11152318
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author Li, Ziwen
Liu, Shuangshuang
Zhu, Taotao
An, Xueli
Wei, Xun
Zhang, Juan
Wu, Suowei
Dong, Zhenying
Long, Yan
Wan, Xiangyuan
author_facet Li, Ziwen
Liu, Shuangshuang
Zhu, Taotao
An, Xueli
Wei, Xun
Zhang, Juan
Wu, Suowei
Dong, Zhenying
Long, Yan
Wan, Xiangyuan
author_sort Li, Ziwen
collection PubMed
description In plants, oxidative stress and metabolic reprogramming frequently induce male sterility, however our knowledge of the underlying molecular mechanism is far from complete. Here, a maize genic male-sterility (GMS) mutant (ms33-6038) with a loss-of-function of the ZmMs33 gene encoding glycerol-3-phosphate acyltransferase 6 (GPAT6) displayed severe deficiencies in the development of a four-layer anther wall and microspores and excessive reactive oxygen species (ROS) content in anthers. In ms33-6038 anthers, transcriptome analysis identified thousands of differentially expressed genes that were functionally enriched in stress response and primary metabolism pathways. Further investigation revealed that 64 genes involved in ROS production, scavenging, and signaling were specifically changed in expression levels in ms33-6038 anthers compared to the other five investigated GMS lines. The severe oxidative stress triggered premature tapetal autophagy and metabolic reprogramming mediated mainly by the activated SnRK1-bZIP pathway, as well as the TOR and PP2AC pathways, proven by transcriptome analysis. Furthermore, 20 reported maize GMS genes were altered in expression levels in ms33-6038 anthers. The excessive oxidative stress and the metabolic reprogramming resulted in severe phenotypic deficiencies in ms33-6038 anthers. These findings enrich our understanding of the molecular mechanisms by which ROS and metabolic homeostasis impair anther and pollen development in plants.
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spelling pubmed-93674332022-08-12 The Loss-Function of the Male Sterile Gene ZmMs33/ZmGPAT6 Results in Severely Oxidative Stress and Metabolic Disorder in Maize Anthers Li, Ziwen Liu, Shuangshuang Zhu, Taotao An, Xueli Wei, Xun Zhang, Juan Wu, Suowei Dong, Zhenying Long, Yan Wan, Xiangyuan Cells Article In plants, oxidative stress and metabolic reprogramming frequently induce male sterility, however our knowledge of the underlying molecular mechanism is far from complete. Here, a maize genic male-sterility (GMS) mutant (ms33-6038) with a loss-of-function of the ZmMs33 gene encoding glycerol-3-phosphate acyltransferase 6 (GPAT6) displayed severe deficiencies in the development of a four-layer anther wall and microspores and excessive reactive oxygen species (ROS) content in anthers. In ms33-6038 anthers, transcriptome analysis identified thousands of differentially expressed genes that were functionally enriched in stress response and primary metabolism pathways. Further investigation revealed that 64 genes involved in ROS production, scavenging, and signaling were specifically changed in expression levels in ms33-6038 anthers compared to the other five investigated GMS lines. The severe oxidative stress triggered premature tapetal autophagy and metabolic reprogramming mediated mainly by the activated SnRK1-bZIP pathway, as well as the TOR and PP2AC pathways, proven by transcriptome analysis. Furthermore, 20 reported maize GMS genes were altered in expression levels in ms33-6038 anthers. The excessive oxidative stress and the metabolic reprogramming resulted in severe phenotypic deficiencies in ms33-6038 anthers. These findings enrich our understanding of the molecular mechanisms by which ROS and metabolic homeostasis impair anther and pollen development in plants. MDPI 2022-07-27 /pmc/articles/PMC9367433/ /pubmed/35954161 http://dx.doi.org/10.3390/cells11152318 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Li, Ziwen
Liu, Shuangshuang
Zhu, Taotao
An, Xueli
Wei, Xun
Zhang, Juan
Wu, Suowei
Dong, Zhenying
Long, Yan
Wan, Xiangyuan
The Loss-Function of the Male Sterile Gene ZmMs33/ZmGPAT6 Results in Severely Oxidative Stress and Metabolic Disorder in Maize Anthers
title The Loss-Function of the Male Sterile Gene ZmMs33/ZmGPAT6 Results in Severely Oxidative Stress and Metabolic Disorder in Maize Anthers
title_full The Loss-Function of the Male Sterile Gene ZmMs33/ZmGPAT6 Results in Severely Oxidative Stress and Metabolic Disorder in Maize Anthers
title_fullStr The Loss-Function of the Male Sterile Gene ZmMs33/ZmGPAT6 Results in Severely Oxidative Stress and Metabolic Disorder in Maize Anthers
title_full_unstemmed The Loss-Function of the Male Sterile Gene ZmMs33/ZmGPAT6 Results in Severely Oxidative Stress and Metabolic Disorder in Maize Anthers
title_short The Loss-Function of the Male Sterile Gene ZmMs33/ZmGPAT6 Results in Severely Oxidative Stress and Metabolic Disorder in Maize Anthers
title_sort loss-function of the male sterile gene zmms33/zmgpat6 results in severely oxidative stress and metabolic disorder in maize anthers
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9367433/
https://www.ncbi.nlm.nih.gov/pubmed/35954161
http://dx.doi.org/10.3390/cells11152318
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