Genome-Wide Association Study Identifies the Serine/Threonine Kinase ClSIK1 for Low Nitrogen Tolerance in Watermelon...

Plants have evolved multiple complex mechanisms enabling them to adapt to low nitrogen (LN) stress via increased nitrogen use efficiency (NUE) as nitrogen deficiency in soil is a major factor limiting plant growth and development. However, the adaptive process and evolutionary roles of LN tolerance-related genes in plants remain largely unknown. In this study, we resequenced 191 watermelon accessions and examined their phenotypic differences related to LN tolerance. A major gene ClSIK1 encoding a serine/threonine protein kinase involved in the response to LN stress was identified on chromosome 11 using genome-wide association study and RNA-Seq analysis. According to a functional analysis, ClSIK1 overexpression can increase the root area, total biomass, NUE and LN tolerance by manipulating multiple nitrogen-metabolized genes. Interestingly, the desirable LN-tolerant haplotype ClSIK1^HapC was detected in only one wild relative (Citrullus mucosospermus) and likely gradually lost during watermelon domestication and improvement. This study clarified the regulatory effects of ClSIK1 on NUE and adaptations to LN stress, which also identifying valuable haplotypes-resolved gene variants for molecular design breeding of 'green' watermelon varieties highly tolerant to LN stress.