Nucleolar DEAD-Box RNA Helicase TOGR1 Regulates Thermotolerant Growth as a Pre-rRNA Chaperone in Rice

Plants have evolved a considerable number of intrinsic tolerance strategies to acclimate to ambient temperature increase. However, their molecular mechanisms remain largely obscure. Here we report a DEAD-box RNA helicase, TOGR1 (Thermotolerant Growth Required1), prerequisite for rice growth themotolerance. Regulated by both temperature and the circadian clock, its expression is tightly coupled to daily temperature fluctuations and its helicase activities directly promoted by temperature increase. Located in the nucleolus and associated with the small subunit (SSU) pre-rRNA processome, TOGR1 maintains a normal rRNA homeostasis at high temperature. Natural variation in its transcript level is positively correlated with plant height and its overexpression significantly improves rice growth under hot conditions. Our findings reveal a novel molecular mechanism of RNA helicase as a key chaperone for rRNA homeostasis required for rice thermotolerant growth and provide a potential strategy to breed heat-tolerant crops by modulating the expression of TOGR1 and its orthologs.
Author Summary Global warming is increasingly posing negative impacts on crop productivity. In this study, we report a nucleolar-located RNA helicase TOGR1 for thermotolerant growth in rice. TOGR1 maintains pre-rRNA homeostasis under high temperature by securing a proper pre-rRNA structure via elevating its helicase activity. Its expression is high temperature inducible with an afternoon peak expression, consistent with a high temperature anticipation of the circadian clock. Transcriptome analysis revealed that TOGR1 is essential in coordinating primary metabolisms to support thermotolerant growth. Importantly, an enhanced expression of TOGR1 significantly increased biomass of rice. Our findings reveal a novel role of a RNA helicase in thermotolerance and provide a potential strategy to breed heat-tolerant rice cultivars and possibly other heat-tolerant crops.