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

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. Besides the stress-induced expression, ONAC023 also exhibits cytoplasm-nucleus transport via a remorin-importin-α-assisted pathway regulated by the stress-dependent dephosphorylation of OsREM1.5. 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.

INSTRUMENT(S): LTQ Orbitrap Velos

ORGANISM(S): Oryza Sativa (rice)

TISSUE(S): Plant Cell, Leaf

SUBMITTER: Yu Chang

LAB HEAD: Lizhong Xiong

PROVIDER: PXD046729 | Pride | 2024-06-13

REPOSITORIES: Pride

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Project description:Rice is susceptible to both heat and drought stress, in particular during flowering and grain filling, when both grain yield and quality may be severely compromised. However, under field conditions, these two stresses rarely occur separately. Under well-watered conditions, plants avoid heat stress by transpirational cooling, while this is not possible under drought conditions. Although investigating combined heat and drought stress is clearly more agronomically relevant than analyzing the effects of the single stresses, only a few studies of this stress combination, in particular under field conditions, have been published. Furthermore, little is known about how plants respond during recovery from drought stress, which also determines plant survival. To address these knowledge gaps, three rice cultivars differing in heat and drought tolerance were grown in the field under control and drought conditions in three consecutive years. Drought was applied either during flowering or during early grain filling, resulting in simultaneous heat stress, leading to reduced grain yield and quality. Analysis by gas chromatography-mass spectrometry (GC-MS) showed distinct metabolic profiles for the three investigated organs (flag leaves, flowering spikelets, developing seeds). The metabolic responses of the plants also strongly differed between cultivars and organs, and between stress and rewatering conditions. Correlation analysis identified potential metabolic markers for grain yield and quality under combined heat and drought stress from stress- and rewatering-regulated metabolites and from metabolites with constitutive differences between the cultivars. These results show that GC-MS can resolve metabolic responses to combined heat and drought stress and subsequent rewatering in different organs of field-grown rice. The metabolite profiles can be used to identify potential marker metabolites for yield stability and grain quality that are expected to improve breeding efforts towards climate change resilient rice.

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

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