Phosphate Starvation-Induced CORNICHON HOMOLOG 5 as Endoplasmic Reticulum Cargo Receptor for PHT1 Transporters in Arabidopsis

Inorganic phosphate (Pi) is essential for plant growth and is acquired and distributed by the plasma membrane PHOSPHATE TRANSPORTER 1 proteins (PHT1s). Enhancing the abundance of PHT1s at the cell surface thus ensures plant productivity and sustainable agriculture. CORNICHON HOMOLOG proteins (CNIHs) are conserved eukaryotic cargo receptors that mediate the selective endoplasmic reticulum (ER) export of membrane proteins. In this study, we identified the Arabidopsis thaliana CNIH5 (AtCNIH5) as a Pi starvation-inducible gene, preferentially expressed in vascular tissues and outer root cell layers above the meristem. AtCNIH5 co-localizes to the AtSAR1A/AtSEC16A/AtSEC24A-labeled ER exit sites and interacts with AtPHT1;1. Loss of AtCNIH5 confers reduced shoot Pi levels under Pi sufficiency due to the reduced translocation of Pi from roots to shoots, as well as decreased Pi uptake under Pi deficiency. The cnih5 mutant exhibits decreased abundance of AtPHT1s but increased PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 (AtPHF1), which enables the ER exit of PHT1s. The cnih5 mutant also shows a lower plasma membrane targeting efficiency of split-GFP tagged-AtPHT1;1 in the root hair and the epidermis within the root transition/elongation zone. Consistently, dysfunctional AtCNIH5 exerts a suppressive effect on the growth of phf1 and alleviates Pi toxicity in the Pi overaccumulator pho2. However, the in vivo protein-protein interaction and degradation assays indicated that AtCNIH5 is not a direct target of AtPHO2. Our findings unveil that AtCNIH5 is a low Pi-responsive ER cargo receptor that interplays with AtPHF1 to promote the plasma membrane targeting of AtPHT1s in a cell-type-dependent manner.