Defense-related callose synthase<i>PMR4</i>promotes root hair callose deposition and adaptation to phosphate deficiency in<i>Arabidopsis thaliana</i>

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<jats:title>Summary</jats:title><jats:p>Plants acquire phosphorus (P) primarily as inorganic phosphate (Pi) from the soil. Under Pi deficiency, plants induce an array of physiological and morphological responses, termed phosphate starvation response (PSR), thereby increasing Pi acquisition and use efficiency. However, the mechanisms by which plants adapt to Pi deficiency remain to be elucidated. Here, we report that deposition of a β-1,3-glucan polymer called callose is induced in<jats:italic>Arabidopsis thaliana</jats:italic>root hairs under Pi deficiency, in a manner independent of PSR-regulating<jats:italic>PHR1/PHL1</jats:italic>transcription factors and<jats:italic>LPR1/LPR2</jats:italic>ferroxidases. Genetic studies revealed<jats:italic>PMR4</jats:italic>(<jats:italic>GSL5</jats:italic>) callose synthase being required for the callose deposition in Pi-depleted root hairs. Loss of<jats:italic>PMR4</jats:italic>also reduces Pi acquisition in shoots and plant growth under low Pi conditions. The defects are not recovered by simultaneous disruption of<jats:italic>SID2</jats:italic>, mediating defense-associated salicylic acid (SA) biosynthesis, excluding SA defense activation from the cause of the observed<jats:italic>pmr4</jats:italic>phenotypes. Grafting experiments and characterization of plants expressing<jats:italic>PMR4</jats:italic>specifically in root hair cells suggest that a PMR4 pool in the cell type contributes to shoot growth under Pi deficiency. Our findings thus suggest an important role for<jats:italic>PMR4</jats:italic>in plant adaptation to Pi deficiency.</jats:p><jats:sec><jats:title>Significance statement</jats:title><jats:p>We reveal that PMR4 callose synthase mediates callose deposition in root hairs under phosphate (Pi) deficiency, without requiring Pi starvation response regulators<jats:italic>PHR1/PHL1</jats:italic>or<jats:italic>LPR1/LPR2</jats:italic>. The loss of the callose deposition is accompanied by decreases in Pi acquisition and plant growth in<jats:italic>pmr4</jats:italic>. Root hair cell-specific<jats:italic>PMR4</jats:italic>expression restores callose deposition in root hairs and shoot growth under Pi deficiency, indicating a critical role for root hair callose in plant adaptation to Pi deficiency.</jats:p></jats:sec>

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