Integrated omic analysis provides insights into the molecular regulation of stress tolerance by partial root-zone drying in rice

Minhua Zhao; Canghao Du; Jian Zeng; Zhihong Gao; Yongyong Zhu; Jinfei Wang; Yupeng Zhang; Zetao Zhu; Yaqiong Wang; Mingjie Chen; Yuesheng Wang; Junli Chang; Guangxiao Yang; Guangyuan He; Yin Li; Xiaoyuan Chen

doi:10.3389/fpls.2023.1156514

Integrated omic analysis provides insights into the molecular regulation of stress tolerance by partial root-zone drying in rice

Front Plant Sci. 2023 Jun 9:14:1156514. doi: 10.3389/fpls.2023.1156514. eCollection 2023.

Authors

Affiliations

¹ Henry Fok School of Biology and Agriculture, Guangdong Engineering Technology Research Center for Efficient Utilization of Water and Soil Resources in North Region, Shaoguan University, Shaoguan, Guangdong, China.
² The Genetic Engineering International Cooperation Base of Chinese Ministry of Science and Technology, Key Laboratory of Molecular Biophysics of Chinese Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, China.

Abstract

Partial root-zone drying (PRD) is an effective water-saving irrigation strategy that improves stress tolerance and facilitates efficient water use in several crops. It has long been considered that abscisic acid (ABA)-dependent drought resistance may be involved during partial root-zone drying. However, the molecular mechanisms underlying PRD-mediated stress tolerance remain unclear. It's hypothesized that other mechanisms might contribute to PRD-mediated drought tolerance. Here, rice seedlings were used as a research model and the complex transcriptomic and metabolic reprogramming processes were revealed during PRD, with several key genes involved in osmotic stress tolerance identified by using a combination of physiological, transcriptome, and metabolome analyses. Our results demonstrated that PRD induces transcriptomic alteration mainly in the roots but not in the leaves and adjusts several amino-acid and phytohormone metabolic pathways to maintain the balance between growth and stress response compared to the polyethylene glycol (PEG)-treated roots. Integrated analysis of the transcriptome and metabolome associated the co-expression modules with PRD-induced metabolic reprogramming. Several genes encoding the key transcription factors (TFs) were identified in these co-expression modules, highlighting several key TFs, including TCP19, WRI1a, ABF1, ABF2, DERF1, and TZF7, involved in nitrogen metabolism, lipid metabolism, ABA signaling, ethylene signaling, and stress regulation. Thus, our work presents the first evidence that molecular mechanisms other than ABA-mediated drought resistance are involved in PRD-mediated stress tolerance. Overall, our results provide new insights into PRD-mediated osmotic stress tolerance, clarify the molecular regulation induced by PRD, and identify genes useful for further improving water-use efficiency and/or stress tolerance in rice.

Keywords: RNA-Seq; metabolomics; omics analysis; osmotic stress; partial root-zone drying (PRD); regulation of gene expression; rice; transcription factors.

Grants and funding

This work was supported by the Guangdong Basic and Applied Basic Research Foundation (2018A030307075, 2021A1515011236, 2023A1515011736, 2023A1515010336), Guangdong Science and Technology Program (2019B121201004), Research Platform Project of Education Department of Guangdong Province (2020KCKXTD037, 2021GCZX001, 2022ZDZX4047), National Innovative Training Program for College Students (202110576016), National Natural Science Foundation of China (32272126, 31901537), the Fundamental Research Funds for Central Universities, HUST (2021XXJS070, 3004170157), Wuhan Knowledge Innovation Project (2022020801010073) and the Opening fund of Guangdong Provincial Key Laboratory of Utilization and Conservation of Food and Medicinal Resources in Northern Region (FMR2022001Z).