Stress-induced nuclear translocation of ONAC023 improves drought and heat tolerance through multiple processes in rice.

Yu Chang, Yujie Fang, Jiahan Liu, Tiantian Ye, Xiaokai Li, Haifu Tu, Ying Ye, Yao Wang, Lizhong Xiong
Author Information
  1. Yu Chang: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  2. Yujie Fang: Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou, 225009, China. yjfang@yzu.edu.cn. ORCID
  3. Jiahan Liu: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  4. Tiantian Ye: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  5. Xiaokai Li: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  6. Haifu Tu: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  7. Ying Ye: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  8. Yao Wang: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  9. Lizhong Xiong: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China. lizhongx@mail.hzau.edu.cn. ORCID

Abstract

Drought and heat are major abiotic stresses frequently coinciding to threaten rice production. Despite hundreds of stress-related genes being identified, only a few have been confirmed to confer resistance to multiple stresses in crops. Here we report ONAC023, a hub stress regulator that integrates the regulations of both drought and heat tolerance in rice. ONAC023 positively regulates drought and heat tolerance at both seedling and reproductive stages. Notably, the functioning of ONAC023 is obliterated without stress treatment and can be triggered by drought and heat stresses at two layers. The expression of ONAC023 is induced in response to stress stimuli. We show that overexpressed ONAC23 is translocated to the nucleus under stress and evidence from protoplasts suggests that the dephosphorylation of the remorin protein OSREM1.5 can promote this translocation. Under drought or heat stress, the nuclear ONAC023 can target and promote the expression of diverse genes, such as OsPIP2;7, PGL3, OsFKBP20-1b, and OsSF3B1, which are involved in various processes including water transport, reactive oxygen species homeostasis, and alternative splicing. These results manifest that ONAC023 is fine-tuned to positively regulate drought and heat tolerance through the integration of multiple stress-responsive processes. Our findings provide not only an underlying connection between drought and heat responses, but also a promising candidate for engineering multi-stress-resilient rice.

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Grants

  1. U21A20207, 31930080, 31821005, and 32101666/National Natural Science Foundation of China (National Science Foundation of China)
  2. CARS-01-01/Earmarked Fund for China Agriculture Research System
  3. 2019M662657/China Postdoctoral Science Foundation

MeSH Term

Oryza
Plant Proteins
Droughts
Gene Expression Regulation, Plant
Thermotolerance
Cell Nucleus
Stress, Physiological
Plants, Genetically Modified
Seedlings
Heat-Shock Response
Reactive Oxygen Species

Chemicals

Plant Proteins
Reactive Oxygen Species

Word Cloud

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