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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...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
MDPI
2022
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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. |
format | Online Article Text |
id | pubmed-9367433 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | MDPI |
record_format | MEDLINE/PubMed |
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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