Two AP2/ERF transcription factors coregulate OsHAK1 to modulate potassium and cesium uptake in rice

Abstract The Group-I alkali metals potassium (K) and cesium (Cs) serve as an essential nutrient and a harmful element, respectively. In rice (Oryza sativa), the high-affinity K+ (HAK) transporter OsHAK1 contributes to K+ and Cs+ acquisition; however, its regulatory mechanism remains unclear. Here, we report 2 OsHAK1 regulators belonging to the APETALA2/ethylene responsive factor family, designated POTASSIUM TRANSPORTER REGULATOR 1/2 (KTR1/2). Low K+ suppresses KTR1 but induces KTR2 expression. KTR1 inhibits and KTR2 enhances OsHAK1 expression. KTR1-knockout increases and KTR2-knockout decreases K+ and Cs+ uptake. Notably, KTR2 activates KTR1 expression, and the single mutation of KTR2 has a similar effect as the double mutation of KTR1 and KTR2 in impairing rice growth and grain yield. Furthermore, OsHAK1 inactivation in ktr1 mutants or KTR2-overexpression lines reduces Cs+ content to a similar level as in the oshak1 mutant. Enhancing KTR2 expression driven by its native promoter increases grain yield and K+ uptake. Variation in K+ content in grain is associated with differences of K+ content in soils where rice accessions show a distinct combination of KTR1, KTR2, and OsHAK1 haplotypes. These results demonstrate that KTR1 and KTR2 play critical roles in the K+-mediated regulation of OsHAK1 expression, thus controlling K+ and Cs+ uptake and allowing rice to adapt to varying K+ supplies.