Pentatricopeptide Repeat Gene-Mediated Mitochondrial RNA Editing Impacts on Rice Drought Tolerance

Zhi Luo; Jie Xiong; Hui Xia; Lei Wang; Guihua Hou; Zhaoyang Li; Jing Li; Hengling Zhou; Tianfei Li; Lijun Luo

doi:10.3389/fpls.2022.926285

Pentatricopeptide Repeat Gene-Mediated Mitochondrial RNA Editing Impacts on Rice Drought Tolerance

Front Plant Sci. 2022 Jul 19:13:926285. doi: 10.3389/fpls.2022.926285. eCollection 2022.

Authors

Zhi Luo^{1

2}, Jie Xiong^{1

2}, Hui Xia^{1

2

3}, Lei Wang^{1

3}, Guihua Hou^{1

2}, Zhaoyang Li^{1

2}, Jing Li^{1

2}, Hengling Zhou^{1

2}, Tianfei Li^{1

3}, Lijun Luo^{1

2

3}

Affiliations

¹ College of Plant Sciences & Technology, Huazhong Agricultural University, Wuhan, China.
² Shanghai Collaborative Innovation Center of Agri-Seeds (SCCAS), Shanghai Agrobiological Gene Center, Shanghai, China.
³ Key Laboratory of Grain Crop Genetic Resources Evaluation and Utilization, Ministry of Agriculture and Rural Affairs, Shanghai, China.

Abstract

Mitochondrial RNA editing plays crucial roles in the plant development and environmental adaptation. Pentatricopeptide repeat (PPR) genes, which are involved in the regulating mitochondrial RNA editing, are potential gene resources in the improvement of rice drought tolerance. In this study, we investigated genome-wide mitochondrial RNA editing in response to drought between upland and lowland rice. Responses of mitochondrial RNA editing to drought exhibit site-specific and genotype-specific patterns. We detected 22 and 57 ecotype-differentiated editing sites under well-watered and drought-treated conditions, respectively. Interestingly, the RNA editing efficiency was positively correlated with many agronomic traits, while it was negatively correlated with drought tolerance. We further selected two mitochondrial-localized PPR proteins, PPR035 and PPR406, to validate their functions in drought tolerance. PPR035 regulated RNA editing at rps4-926 and orfX-406, while PPR406 regulated RNA editing at orfX-355. The defectiveness in RNA editing at these sites had no apparent penalties in rice respiration and vegetative growth. Meanwhile, the knockout mutants of ppr035 and ppr406 show enhanced drought- and salt tolerance. PPR035 and PPR406 were under the balancing selection in upland rice and highly differentiated between upland and lowland rice ecotypes. The upland-dominant haplotypes of PPR035 and PPR406 shall contribute to the better drought tolerance in upland rice. They have great prospective in the improvement of rice drought tolerance.

Keywords: Oryza sativa; RNA editing; breeding; drought; mitochondria; pentatricopeptide repeats protein; upland rice.