C4 plants respond to phosphate starvation differently than C3 plants

Abstract C4 photosynthesis concentrates CO2 around RUBISCO, thereby decreasing photorespiration and leading to greater productivity. C4 photosynthesis evolved several times independently in different plant families including monocots and dicots. Beside changes in carbon fixation, C4 plants have also evolved several alterations in nitrogen and sulfur nutrition, leading to a better nitrogen use efficiency. Here, we utilized C3 and C4 species from two model systems, Flaveria and Panicum, to ask whether the evolution of C4 photosynthesis also affected phosphate homeostasis. The accumulation of phosphate within the plant shifted from the roots to the shoots with the evolution of C4, which can probably be explained by the higher demand of phosphate for completing the C4 cycle. A limitation of carbon assimilation by phosphate availability was shown solely for the C4 dicot plant, indicating a higher sensitivity to the starvation. Metabolic responses to phosphate limitation, including accumulation of amino acids, TCA cycle intermediates, as well as starch, were genus or species specific, rather than associated with the photosynthesis type. The expression of key phosphate starvation response genes was induced in all species by phosphate deficiency, while the high induction of microRNA399 coupled with a repression of PHOSPHATE 2 (PHO2) was especially prominent in the C4 monocot. Thus, it seems that C4 photosynthesis increases the demand for phosphate in the leaves and C4 plants either respond more strongly to phosphate deficiency than C3 plants or experience inhibition of photosynthesis.