Natural variation in a K+-preferring HKT transporter contributes to wheat shoot K+ accumulation and tolerance

Soil salinity can adversely affect crop growth and yield, and an improved understanding of the genetic factors that confer salt tolerance could inform breeding strategies to engineer salt-tolerant crops and improve productivity. Here, a group of K+-preferring HKT transporters, TaHKT8, TaHKT9 and TaHKT10, were identified and negatively regulate the wheat shoot K+ accumulation and salt tolerance. A genome-wide association study (GWAS) and candidate gene association analysis further revealed that TaHKT9-B substantially underlies the natural variation of wheat shoot K+ accumulation under saline soil conditions. Specifically, an auxin responsive element (ARE) within an 8-bp insertion in the promoter of TaHKT9-B is strongly associated with shoot K+ content among wheat accessions. This ARE can be directly bound by TaARF4 for transcriptional activation of TaHKT9-B, which subsequently attenuates shoot K+ accumulation and salt tolerance. Moreover, the tae-miR390/TaTAS3/TaARF4 pathway was identified to regulate the salt-induced root development and salt tolerance in wheat. Taken together, our study describes the genetic basis and accompanying mechanism driving phenotypic variation in wheat shoot K+ accumulation and salt tolerance. The identified tae-miR390/TaTAS3/TaARF4/TaHKT9-B module is an important regulator in wheat subjected to salt stress, which provides the potentially important genetic resources for breeders to improve wheat salt tolerance.