Genome-wide association study uncovers a novel gene responsible for rice seedling submergence tolerance

Submergence tolerance is crucial for the direct seeding of rice, yet long-term domestication and breeding have inadvertently reduced the adaptability of cultivated rice to submergence stress. Here, we identify a nucleic acid excision repair protein-encoding gene qSHS5 as an essential regulator of seedling height under submergence through a genome-wide association study in 322 rice accessions. Disruption of qSHS5 in mutants resulted in seedling growth inhibition under submergence, while growth remains comparable to wild-type under normal conditions. This inhibition is primarily due to decreased cell number resulting from G1 phase cell cycle arrest. Further investigation showed that levels of reactive oxygen species (ROS), O₂ ^- and H₂O₂ significantly increased, and DNA damage was aggravated in qshs5 mutants under submergence. Additionally, we find the submergence-tolerant haplotype qSHS5^H4 has been progressively lost, while the elite haplotype qSHS5^H3 has been largely overlooked during the breeding of semi-dwarf and high-yield in rice. Importantly, we demonstrate that combining qSHS5^H3 with the semi-dwarfing haplotype SD1^H1 exhibited high yield without compromising submergence tolerance, offering significant potential for future breeding programmes targeting direct seeding cultivation. This study not only identifies a novel superior allele but also provides valuable insights for future improvement of rice cultivation, particularly under climate change-induced submergence for direct seeding.