Down-regulation of the rice HRS1 HOMOLOG3 transcriptional repressor gene due to N deficiency directly co-activates ammonium and phosphate transporter genes

J Exp Bot. 2025 Jan 10;76(2):461-477. doi: 10.1093/jxb/erae440.

Abstract

Rice HRS1 HOMOLOG3 (OsHHO3) acts as a transcriptional repressor of AMMONIUM TRANSPORTER1 (OsAMT1) genes in rice; thus, reduced OsHHO3 expression in nitrogen (N)-deficient environments promotes ammonium uptake. In this study, we show that OsHHO3 also functions as a repressor of a specific subset of phosphate (Pi) transporter (PT) genes involved in the uptake and root-to-shoot translocation of Pi, including OsPT2, OsPT4, and OsPHO1;1. Disruption of OsHHO3 increased Pi uptake and Pi contents in shoots and roots, while overexpression of OsHHO3 caused the opposite effects. Furthermore, phosphorus (P) deficiency slightly decreased OsHHO3 expression, up-regulating a specific subset of PT genes. However, N deficiency was more effective than P deficiency in suppressing OsHHO3 expression in roots, and unlike N deficiency-dependent activation of PT genes under the control of OsHHO3, the P deficiency-dependent activation of OsAMT1 genes was minimal. Interestingly, the simultaneous deficiency of both N and P promoted the OsHHO3-regulated expression of PT genes more significantly than the deficiency of either N or P, but diminished the expression of genes regulated by OsPHR2, a master regulator of Pi starvation-responsive transcriptional activation. Phenotypic analysis revealed that the inactivation and overexpression of OsHHO3 improved and reduced plant growth, respectively, under N-deficient and P-deficient conditions. These results indicate that OsHHO3 regulates a specific subset of PT genes independently of OsPHR2-mediated regulation and plays a critical role in the adaptation to diverse N and P environments.

Keywords: Nitrogen deficiency; OsHHO3; phosphate deficiency; phosphate transporter; rice; transcriptional repressor.

MeSH terms

  • Ammonium Compounds / metabolism
  • Cation Transport Proteins / genetics
  • Cation Transport Proteins / metabolism
  • Down-Regulation*
  • Gene Expression Regulation, Plant*
  • Nitrogen* / deficiency
  • Nitrogen* / metabolism
  • Oryza* / genetics
  • Oryza* / metabolism
  • Phosphate Transport Proteins* / genetics
  • Phosphate Transport Proteins* / metabolism
  • Phosphates / deficiency
  • Phosphates / metabolism
  • Plant Proteins* / genetics
  • Plant Proteins* / metabolism
  • Plant Roots / genetics
  • Plant Roots / growth & development
  • Plant Roots / metabolism

Substances

  • Plant Proteins
  • Phosphate Transport Proteins
  • Nitrogen
  • ammonium transporters, plant
  • Cation Transport Proteins
  • Phosphates
  • Ammonium Compounds