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

ABSTRACT: Drought and heat are major abiotic stresses frequently coinciding to threaten rice production. Although hundreds of stress-related genes have been identified in the past two decades, very few genes have been confirmed to confer resistance to multiple stresses in crops. Here we report ONAC023, identified through NAC-centered gene regulatory network and genetic association analyses, is a hub stress-regulator that integrates the regulations of both drought and heat tolerance in rice. The loss-of-function mutant of ONAC023 showed significantly increased sensitivity to drought and heat stresses, whereas the overexpression of ONAC023 confers drought and heat tolerance at both seedling and reproductive stages. Notably, drought and heat stresses activated the function of ONAC023 not only by the induction of ONAC023 transcript but also by the nuclear accumulation of ONAC023 protein through a remorin-importin-α-assisted translocation. Under drought or heat stress, ONAC023 can directly target and promote the expression of functionally diverse downstream genes, such as OsPIP2;7, PGL3, OsFKBP20-1b, and OsSF3B1, which are involved in various stress-responsive processes including water transport, reactive oxygen species homeostasis, and alternative splicing (AS). Furthermore, genome-wide AS profiling revealed that the loss of ONAC023 function led to alternation of the encoding outcomes of thousands of AS transcripts under drought and heat stresses. These results manifested 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.

ORGANISM(S): Oryza sativa Japonica Group

PROVIDER: GSE183241 | GEO | 2024/06/13

REPOSITORIES: GEO

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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.

Project description:Drought is one of the major abiotic stresses threatening rice (Oryza sativa) production worldwide. Drought resistance is controlled by multiple genes, and therefore, a multi-gene genetic engineering strategy is theoretically useful for improving drought resistance. However, the experimental evidence for such a strategy is still lacking. In this study, a few drought-responsive genes from rice were assembled by a multiple-round site-specific assembly (MISSA) system, and the constructs were introduced into the rice cultivar KY131 via Agrobacterium-mediated transformation. The transgenic lines of the multi-gene and corresponding single-gene constructs were pre-evaluated for drought resistance. We found that the co-overexpression of two genes, encoding a constitutively active form of a bZIP transcription factor (OsbZIP46CA1) and a protein kinase (SAPK6) involved in the abscisic acid (ABA) signaling pathway, showed significantly enhanced drought resistance compared with the single-gene transgenic lines and the negative transgenic plants. Single-copy lines of this bi-gene combination (named XL22) and the corresponding single-gene lines were further evaluated for drought resistance in the field using agronomical traits. The results showed that XL22 exhibited greater yield, biomass, spikelet number, and grain number under moderate drought stress conditions. The seedling survival rate of XL22 and the single-gene overexpressors after drought stress treatment also supported the drought resistance results. Furthermore, expression profiling by RNA-Seq revealed that many genes involved in the stress response were specifically up-regulated in the drought-treated XL22 lines and some of the stress-related genes activated in CA1-OE and SAPK6-OE were distinct, which could partially explain the different performances of these lines with respect to drought resistance. In addition, the XL22 seedlings showed improved tolerance to heat and cold stresses. Our results demonstrate that the multi-gene assembly in an appropriate combination may be a promising approach in the genetic improvement of drought resistance.

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

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