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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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-06-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.899054/full |
| _version_ | 1811336200972140544 |
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| author | Jia Sun Jia Sun Weifang Liang Weifang Liang Shenghai Ye Xinyu Chen Xinyu Chen Yuhang Zhou Yuhang Zhou Jianfei Lu Ying Shen Xuming Wang Jie Zhou Chulang Yu Chengqi Yan Bingsong Zheng Jianping Chen Jianping Chen Yong Yang |
| author_facet | Jia Sun Jia Sun Weifang Liang Weifang Liang Shenghai Ye Xinyu Chen Xinyu Chen Yuhang Zhou Yuhang Zhou Jianfei Lu Ying Shen Xuming Wang Jie Zhou Chulang Yu Chengqi Yan Bingsong Zheng Jianping Chen Jianping Chen Yong Yang |
| author_sort | Jia Sun |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-13T17:36:02Z |
| format | Article |
| id | doaj.art-4e575a65a5bb4e56b48157d0e51d1ac3 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-13T17:36:02Z |
| publishDate | 2022-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-4e575a65a5bb4e56b48157d0e51d1ac32022-12-22T02:37:22ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-06-011310.3389/fpls.2022.899054899054Whole-Transcriptome Analysis Reveals Autophagy Is Involved in Early Senescence of zj-es Mutant RiceJia Sun0Jia Sun1Weifang Liang2Weifang Liang3Shenghai Ye4Xinyu Chen5Xinyu Chen6Yuhang Zhou7Yuhang Zhou8Jianfei Lu9Ying Shen10Xuming Wang11Jie Zhou12Chulang Yu13Chengqi Yan14Bingsong Zheng15Jianping Chen16Jianping Chen17Yong Yang18College of Life Science, Fujian A&F University, Fuzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology for Plant Protection, Ministry of Agriculture, and Rural Affairs, Zhejiang Provincial Key Laboratory of Biotechnology for Plant Protection, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Science, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology for Plant Protection, Ministry of Agriculture, and Rural Affairs, Zhejiang Provincial Key Laboratory of Biotechnology for Plant Protection, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Science, Hangzhou, ChinaCollege of Plant Protection, Yunnan Agricultural University, Kunming, ChinaInstitute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology for Plant Protection, Ministry of Agriculture, and Rural Affairs, Zhejiang Provincial Key Laboratory of Biotechnology for Plant Protection, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Science, Hangzhou, ChinaCollege of Plant Protection, Shenyang Agricultural University, Shenyang, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology for Plant Protection, Ministry of Agriculture, and Rural Affairs, Zhejiang Provincial Key Laboratory of Biotechnology for Plant Protection, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Science, Hangzhou, ChinaState Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou, ChinaZhejiang Plant Protection, Quarantine and Pesticide Management Station, Hangzhou, ChinaZhejiang Plant Protection, Quarantine and Pesticide Management Station, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology for Plant Protection, Ministry of Agriculture, and Rural Affairs, Zhejiang Provincial Key Laboratory of Biotechnology for Plant Protection, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Science, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology for Plant Protection, Ministry of Agriculture, and Rural Affairs, Zhejiang Provincial Key Laboratory of Biotechnology for Plant Protection, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Science, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology for Plant Protection, Ministry of Agriculture, and Rural affairs, Zhejiang Provincial Key Laboratory of Biotechnology for Plant Protection, Institute of Plant Virology, Ningbo University, Ningbo, ChinaInstitute of Biotechnology, Ningbo Academy of Agricultural Science, Ningbo, ChinaState Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology for Plant Protection, Ministry of Agriculture, and Rural Affairs, Zhejiang Provincial Key Laboratory of Biotechnology for Plant Protection, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Science, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology for Plant Protection, Ministry of Agriculture, and Rural affairs, Zhejiang Provincial Key Laboratory of Biotechnology for Plant Protection, Institute of Plant Virology, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology for Plant Protection, Ministry of Agriculture, and Rural Affairs, Zhejiang Provincial Key Laboratory of Biotechnology for Plant Protection, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Science, Hangzhou, ChinaSenescence 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.https://www.frontiersin.org/articles/10.3389/fpls.2022.899054/fullwhole-transcriptomeautophagyROScell deathearly senescence |
| spellingShingle | Jia Sun Jia Sun Weifang Liang Weifang Liang Shenghai Ye Xinyu Chen Xinyu Chen Yuhang Zhou Yuhang Zhou Jianfei Lu Ying Shen Xuming Wang Jie Zhou Chulang Yu Chengqi Yan Bingsong Zheng Jianping Chen Jianping Chen Yong Yang Whole-Transcriptome Analysis Reveals Autophagy Is Involved in Early Senescence of zj-es Mutant Rice Frontiers in Plant Science whole-transcriptome autophagy ROS cell death early senescence |
| 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 | whole-transcriptome autophagy ROS cell death early senescence |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.899054/full |
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