Phosphoproteomic and Metabolomic Analyses Reveal Sexually Differential Regulatory Mechanisms in Poplar to Nitrogen Deficiency

Nitrogen (N) is a key factor impacting physiological processes in plants. Many proteins have been investigated in male and female poplars under N limitation. However, little is known about sex differences in the protein modifications and metabolites that occur in poplar leaves in response to N deficiency. In this study, as compared to N-deficient males, N-deficient females suffered greater damage from N deficiency, including chloroplast disorganization and lipid peroxidation of cellular membranes. Male poplars had greater osmotic adjustment ability than did females, allowing greater accumulation of soluble metabolites. In addition, as compared to that in N-deficient males, glycolysis was less suppressed in N-deficient females for increased enzyme activities to consume excess energy. Moreover, we found that pronounced protein phosphorylation occurred during carbon metabolism and substance transport processes in both sexes of poplar under N-limiting conditions. Sex-specific metabolites mainly included intermediates in glycolysis, amino acids, and phenylpropanoid-derived metabolites. This study provides new molecular evidence that female poplars suffer greater negative effects from N deficiency than do male poplars.