The OsWRKY72–OsAAT30/OsGSTU26 module mediates reactive oxygen species scavenging to drive heterosis for salt tolerance in hybrid rice

Author:

Liu Citao1ORCID,Mao Bigang2ORCID,Zhang Yanxia3ORCID,tian Lei4ORCID,Ma Biao3ORCID,Chen Zhuo5ORCID,Wei Zhongwei2ORCID,Li Aifu6ORCID,Shao Ye2ORCID,Cheng Gongye1ORCID,Li Lingling1ORCID,Li Wenyu1ORCID,Zhang Di1ORCID,Ding Xiaoping1ORCID,Peng Jiangxiang7ORCID,Peng Yulin2ORCID,He Jiwai1ORCID,Ye Nenghui1ORCID,Yuan Dingyang2ORCID,Chu Chengcai3ORCID,Duan Meijuan1ORCID

Affiliation:

1. Hunan Provincial Key Laboratory of Stress Biology, College of Agriculture Hunan Agricultural University Changsha 410128 China

2. State Key Laboratory of Hybrid Rice Hunan Hybrid Rice Research Center Changsha 410125 China

3. College of Agriculture South China Agricultural University Guangzhou 510642 China

4. State Key Laboratory of Wheat and Maize Crop Science, Center for Crop Genome Engineering, College of Agronomy Henan Agricultural University Zhengzhou 450002 China

5. College of Horticulture Fujian Agriculture and Forestry University Fuzhou 350002 China

6. Department of Computational Medicine and Bioinformatics University of Michigan Ann Arbor, MI 48109 USA

7. Biobin Data Science Co., Ltd. Changsha 410221 China

Abstract

ABSTRACTHybrid rice (Oryza sativa) generally outperforms its inbred parents in yield and stress tolerance, a phenomenon termed heterosis, but the underlying mechanism is not completely understood. Here, we combined transcriptome, proteome, physiological, and heterosis analyses to examine the salt response of super hybrid rice Chaoyou1000 (CY1000). In addition to surpassing the mean values for its two parents (mid‐parent heterosis), CY1000 exhibited a higher reactive oxygen species scavenging ability than both its parents (over‐parent heterosis or heterobeltiosis). Nonadditive expression and allele‐specific gene expression assays showed that the glutathione S‐transferase gene OsGSTU26 and the amino acid transporter gene OsAAT30 may have major roles in heterosis for salt tolerance, acting in an overdominant fashion in CY1000. Furthermore, we identified OsWRKY72 as a common transcription factor that binds and regulates OsGSTU26 and OsAAT30. The salt‐sensitive phenotypes were associated with the OsWRKY72paternal genotype or the OsAAT30maternal genotype in core rice germplasm varieties. OsWRKY72paternal specifically repressed the expression of OsGSTU26 under salt stress, leading to salinity sensitivity, while OsWRKY72maternal specifically repressed OsAAT30, resulting in salinity tolerance. These results suggest that the OsWRKY72–OsAAT30/OsGSTU26 module may play an important role in heterosis for salt tolerance in an overdominant fashion in CY1000 hybrid rice, providing valuable clues to elucidate the mechanism of heterosis for salinity tolerance in hybrid rice.

Funder

National Natural Science Foundation of China

Publisher

Wiley

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