Interdependent Iron and Phosphorus Availability Controls Photosynthesis Through Retrograde Signaling

Abstract

Iron deficiency hampers photosynthesis and is associated with chlorosis. We recently showed that iron deficiency-induced chlorosis depends on phosphorus availability. How plants integrate these cues to control chlorophyll accumulation is unknown. Here, we show that iron limitation downregulates photosynthesis genes in a phosphorus-dependent manner. Using transcriptomics and genome-wide association analysis, we identify two genes, a chloroplastic ascorbate transporter (PHT4;4) and a nuclear transcription factor (bZIP58), which prevent the downregulation of photosynthesis genes leading to the stay-green phenotype under iron-phosphorus deficiency. Joint limitation of these nutrients induces ascorbate accumulation by activating expression of an ascorbate biosynthesis gene, VTC4, which requires bZIP58. Exogenous ascorbate prevents iron deficiency-induced chlorosis in vtc4 mutants, but not in bzip58 or pht4;4. Our study demonstrates chloroplastic ascorbate transport is essential for preventing the downregulation of photosynthesis genes under iron-phosphorus combined deficiency. These findings uncover a molecular pathway coordinating chloroplast-nucleus communication to adapt photosynthesis to nutrient availability.