Rice phosphate transporter reduces the low phosphate response through jasmonate signaling

Abstract

Phosphorus (P) is an essential macronutrient for plant growth, and its deficiency severely limits crop productivity. The PHOSPHATE1 (PHO1) protein family, defined by an N-terminal SPX domain, four transmembrane (4TM) domains, and a C-terminal EXS domain, mediates phosphate (Pi) loading into the xylem for root-to-shoot transport. In rice, OsPHO1;2 is critical for Pi export, and loss-of-function mutants exhibit severe growth retardation and Pi deficiency symptoms despite sufficient external Pi. To dissect the functional contributions of PHO1 domains beyond Pi transport, we generated CRISPR/Cas9 rice lines expressing either the EXS domain containing part of the SPX domain (S-EXS) or the 4TM+EXS domains (T-EXS) of OsPHO1;2. Phenotypic analyses under Pi-sufficient and Pi-deficient conditions revealed that S-EXS lines displayed improved early growth compared to ospho1;2 mutants, despite similar shoot Pi levels. These plants exhibited reduced jasmonic acid accumulation and attenuated phosphate starvation responses, resembling wild-type hormone profiles. In contrast, T-EXS lines mirrored the growth defects of ospho1;2 mutants. Transcriptome profiling confirmed that defense and phosphate starvation pathways were less activated in S-EXS lines relative to mutants. However, both S-EXS and T-EXS lines retained seed development defects and reduced seed phosphorus content, consistent with ospho1;2 phenotypes. Heterozygous plants carrying one functional OsPHO1;2 allele exhibited normal growth and seed development, confirming the recessive nature of the mutation. Collectively, these findings demonstrate that the S-EXS domain of OsPHO1;2 promotes plant growth independently of Pi transport by modulating jasmonate signaling and suppressing phosphate starvation responses. This highlights a signaling role for PHO1 domains, offering new insights into Pi homeostasis and potential strategies for breeding Pi-efficient crops.