A heat stress responsive NAC transcription factor heterodimer plays key roles in rice grain filling

Abstract

High temperature often leads to the failure of grain filling in rice (Oryza sativa) to cause yield loss, while the mechanism is not well elucidated yet. Here, we report that two seed-specific NAM/ATAF/CUC domain transcription factors, ONAC127 and ONAC129, are responsive to heat stress and involved in the grain filling process of rice. ONAC127 and ONAC129 are dominantly expressed in the pericarp and can form a heterodimer during rice grain filling. CRISPR/Cas9 induced mutants and overexpression lines were then generated to investigate the functions of these two transcription factors. Interestingly, both knock-out and overexpression plants showed incomplete grain filling and shrunken grains, which became more severe under heat stress. Transcriptome analysis revealed that ONAC127 and ONAC129 mainly regulate stimulus response and nutrient transport. ChIP-seq analysis identified that the direct targets of ONAC127 and ONAC129 in developing rice seeds include monosaccharide transporter OsMST6, sugar transporter OsSWEET4, calmodulin-like protein OsMSR2 and AP2/ERF factor OsEATB. These results suggest that ONAC127 and ONAC129 may regulate grain filling through affecting sugar transportation and abiotic stress responses. Overall, this study demonstrates a transcriptional regulatory network involving ONAC127 and ONAC129 and coordinating multiple pathways to modulate seed development and heat stress response at rice reproductive stage.

Starch biosynthesis in cereal endosperms: An updated review over the last decade

“…In the linked region of rice chromosome 11, a gene cluster encoding four NAC members (ONAC025, ONAC127, ONAC128, and ONAC129) was identified ( Fang et al., 2008 ). ONAC127 and ONAC129 are not directly involved in starch synthesis in the rice endosperm, but they do form heterodimers that participate in apoplastic transport and the heat stress response to regulate rice grain filling, including starch accumulation ( Ren et al., 2021 ). In wheat, the endosperm-specific TaNAC019 was also found to regulate glutenin and starch accumulation by directly activating the expression of relevant genes ( Liu et al., 2020 ; Gao et al., 2021 ).…”

Current Understanding of Leaf Senescence in Rice

“…For instance, high temperature during the grain-filling stage can cause a nearly 50% reduction in rice yield [ 138 ], and heat-tolerance studies in rice have mainly focused on the reproductive stage due to its high sensitivity and critical influence on grain yield [ 139 ]. Plants respond to high temperature through the activation of the heat shock TFs (HSFs) or other stress-related genes [ 140 , 141 ]. Heat stress-responsive two NAC TFs, ONAC127, and ONAC129 are specifically expressed in the pericarp of rice seeds [ 141 ].…”

“…Plants respond to high temperature through the activation of the heat shock TFs (HSFs) or other stress-related genes [ 140 , 141 ]. Heat stress-responsive two NAC TFs, ONAC127, and ONAC129 are specifically expressed in the pericarp of rice seeds [ 141 ]. They are involved in the apoplasmic transport of photosynthates for starch accumulation during grain filling as a heterodimer.…”

Can omics deliver temperature resilient ready-to-grow crops?

“…Incomplete filling and shrunken caryopsis were observed in CRISPR-induced mutants. In short, ONAC127 and ONAC129, along with multiple pathways (sugar transportation), regulate caryopsis filling, including monosaccharide transporter OsMST6, sugar transporter OsSWEET4, calmodulin-like protein OsMSR2, AP2/ERF, OsEATB, cell wall construction, and nutrient transport under HS [66]. In tomato, CRISPRmediated Simapk3 mutant unveiled improved tolerance to HS, less cell damage and wilting, lower ROS contents, increasing antioxidant activity, and the higher expression of genes encoding heat shock factors/proteins (HSFs and HSPs) that mainly regulates HS [133].…”