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Whole-Transcriptome Analysis Reveals Autophagy Is Involved in Early Senescence of zj-es Mutant Rice

Senescence is a necessary stage of plant growth and development, and the early senescence of rice will lead to yield reduction and quality decline. However, the mechanisms of rice senescence remain obscure. In this study, we characterized an early-senescence rice mutant, designated zj-es (ZheJing-ea...

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Autores principales: Sun, Jia, Liang, Weifang, Ye, Shenghai, Chen, Xinyu, Zhou, Yuhang, Lu, Jianfei, Shen, Ying, Wang, Xuming, Zhou, Jie, Yu, Chulang, Yan, Chengqi, Zheng, Bingsong, Chen, Jianping, Yang, Yong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9204060/
https://www.ncbi.nlm.nih.gov/pubmed/35720578
http://dx.doi.org/10.3389/fpls.2022.899054
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author Sun, Jia
Liang, Weifang
Ye, Shenghai
Chen, Xinyu
Zhou, Yuhang
Lu, Jianfei
Shen, Ying
Wang, Xuming
Zhou, Jie
Yu, Chulang
Yan, Chengqi
Zheng, Bingsong
Chen, Jianping
Yang, Yong
author_facet Sun, Jia
Liang, Weifang
Ye, Shenghai
Chen, Xinyu
Zhou, Yuhang
Lu, Jianfei
Shen, Ying
Wang, Xuming
Zhou, Jie
Yu, Chulang
Yan, Chengqi
Zheng, Bingsong
Chen, Jianping
Yang, Yong
author_sort Sun, Jia
collection PubMed
description Senescence is a necessary stage of plant growth and development, and the early senescence of rice will lead to yield reduction and quality decline. However, the mechanisms of rice senescence remain obscure. In this study, we characterized an early-senescence rice mutant, designated zj-es (ZheJing-early senescence), which was derived from the japonica rice cultivar Zhejing22. The mutant zj-es exhibited obvious early-senescence phenotype, such as collapsed chloroplast, lesions in leaves, declined fertility, plant dwarf, and decreased agronomic traits. The ZJ-ES gene was mapped in a 458 kb-interval between the molecular markers RM5992 and RM5813 on Chromosome 3, and analysis suggested that ZJ-ES is a novel gene controlling rice early senescence. Subsequently, whole-transcriptome RNA sequencing was performed on zj-es and its wild-type rice to dissect the underlying molecular mechanism for early senescence. Totally, 10,085 differentially expressed mRNAs (DEmRNAs), 1,253 differentially expressed lncRNAs (DElncRNAs), and 614 differentially expressed miRNAs (DEmiRNAs) were identified, respectively, in different comparison groups. Based on the weighted gene co-expression network analysis (WGCNA), the co-expression turquoise module was found to be the key for the occurrence of rice early senescence. Furthermore, analysis on the competing endogenous RNA (CeRNA) network revealed that 14 lncRNAs possibly regulated 16 co-expressed mRNAs through 8 miRNAs, and enrichment analysis showed that most of the DEmRNAs and the targets of DElncRNAs and DEmiRNAs were involved in reactive oxygen species (ROS)-triggered autophagy-related pathways. Further analysis showed that, in zj-es, ROS-related enzyme activities were markedly changed, ROS were largely accumulated, autophagosomes were obviously observed, cell death was significantly detected, and lesions were notably appeared in leaves. Totally, combining our results here and the remaining research, we infer that ROS-triggered autophagy induces the programmed cell death (PCD) and its coupled early senescence in zj-es mutant rice.
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spelling pubmed-92040602022-06-18 Whole-Transcriptome Analysis Reveals Autophagy Is Involved in Early Senescence of zj-es Mutant Rice Sun, Jia Liang, Weifang Ye, Shenghai Chen, Xinyu Zhou, Yuhang Lu, Jianfei Shen, Ying Wang, Xuming Zhou, Jie Yu, Chulang Yan, Chengqi Zheng, Bingsong Chen, Jianping Yang, Yong Front Plant Sci Plant Science Senescence is a necessary stage of plant growth and development, and the early senescence of rice will lead to yield reduction and quality decline. However, the mechanisms of rice senescence remain obscure. In this study, we characterized an early-senescence rice mutant, designated zj-es (ZheJing-early senescence), which was derived from the japonica rice cultivar Zhejing22. The mutant zj-es exhibited obvious early-senescence phenotype, such as collapsed chloroplast, lesions in leaves, declined fertility, plant dwarf, and decreased agronomic traits. The ZJ-ES gene was mapped in a 458 kb-interval between the molecular markers RM5992 and RM5813 on Chromosome 3, and analysis suggested that ZJ-ES is a novel gene controlling rice early senescence. Subsequently, whole-transcriptome RNA sequencing was performed on zj-es and its wild-type rice to dissect the underlying molecular mechanism for early senescence. Totally, 10,085 differentially expressed mRNAs (DEmRNAs), 1,253 differentially expressed lncRNAs (DElncRNAs), and 614 differentially expressed miRNAs (DEmiRNAs) were identified, respectively, in different comparison groups. Based on the weighted gene co-expression network analysis (WGCNA), the co-expression turquoise module was found to be the key for the occurrence of rice early senescence. Furthermore, analysis on the competing endogenous RNA (CeRNA) network revealed that 14 lncRNAs possibly regulated 16 co-expressed mRNAs through 8 miRNAs, and enrichment analysis showed that most of the DEmRNAs and the targets of DElncRNAs and DEmiRNAs were involved in reactive oxygen species (ROS)-triggered autophagy-related pathways. Further analysis showed that, in zj-es, ROS-related enzyme activities were markedly changed, ROS were largely accumulated, autophagosomes were obviously observed, cell death was significantly detected, and lesions were notably appeared in leaves. Totally, combining our results here and the remaining research, we infer that ROS-triggered autophagy induces the programmed cell death (PCD) and its coupled early senescence in zj-es mutant rice. Frontiers Media S.A. 2022-06-03 /pmc/articles/PMC9204060/ /pubmed/35720578 http://dx.doi.org/10.3389/fpls.2022.899054 Text en Copyright © 2022 Sun, Liang, Ye, Chen, Zhou, Lu, Shen, Wang, Zhou, Yu, Yan, Zheng, Chen and Yang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Sun, Jia
Liang, Weifang
Ye, Shenghai
Chen, Xinyu
Zhou, Yuhang
Lu, Jianfei
Shen, Ying
Wang, Xuming
Zhou, Jie
Yu, Chulang
Yan, Chengqi
Zheng, Bingsong
Chen, Jianping
Yang, Yong
Whole-Transcriptome Analysis Reveals Autophagy Is Involved in Early Senescence of zj-es Mutant Rice
title Whole-Transcriptome Analysis Reveals Autophagy Is Involved in Early Senescence of zj-es Mutant Rice
title_full Whole-Transcriptome Analysis Reveals Autophagy Is Involved in Early Senescence of zj-es Mutant Rice
title_fullStr Whole-Transcriptome Analysis Reveals Autophagy Is Involved in Early Senescence of zj-es Mutant Rice
title_full_unstemmed Whole-Transcriptome Analysis Reveals Autophagy Is Involved in Early Senescence of zj-es Mutant Rice
title_short Whole-Transcriptome Analysis Reveals Autophagy Is Involved in Early Senescence of zj-es Mutant Rice
title_sort whole-transcriptome analysis reveals autophagy is involved in early senescence of zj-es mutant rice
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9204060/
https://www.ncbi.nlm.nih.gov/pubmed/35720578
http://dx.doi.org/10.3389/fpls.2022.899054
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