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

Jia Sun; Weifang Liang; Shenghai Ye; Xinyu Chen; Yuhang Zhou; Jianfei Lu; Ying Shen; Xuming Wang; Jie Zhou; Chulang Yu; Chengqi Yan; Bingsong Zheng; Jianping Chen; Yong Yang

doi:10.3389/fpls.2022.899054

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

Front Plant Sci. 2022 Jun 3:13:899054. doi: 10.3389/fpls.2022.899054. eCollection 2022.

Authors

Jia Sun^{1

2}, Weifang Liang^{2

3}, Shenghai Ye⁴, Xinyu Chen^{2

5}, Yuhang Zhou^{2

6}, Jianfei Lu⁷, Ying Shen⁷, Xuming Wang², Jie Zhou², Chulang Yu⁸, Chengqi Yan⁹, Bingsong Zheng⁶, Jianping Chen^{2

8}, Yong Yang²

Affiliations

¹ College of Life Science, Fujian A&F University, Fuzhou, China.
² State 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, China.
³ College of Plant Protection, Yunnan Agricultural University, Kunming, China.
⁴ Institute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural Sciences, Hangzhou, China.
⁵ College of Plant Protection, Shenyang Agricultural University, Shenyang, China.
⁶ State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou, China.
⁷ Zhejiang Plant Protection, Quarantine and Pesticide Management Station, Hangzhou, China.
⁸ State 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, China.
⁹ Institute of Biotechnology, Ningbo Academy of Agricultural Science, Ningbo, China.

Abstract

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.

Keywords: ROS; autophagy; cell death; early senescence; whole-transcriptome.