Metabolic and physiological analyses reveal that Populus cathayana males adopt an energy-saving strategy to cope with phosphorus deficiency.

Dioecious trees have evolved sex-specific adaptation strategies to cope with inorganic phosphorus (Pi) limitation. Yet, little is known about the effects of Pi limitation on plant metabolism, particularly in dioecious woody plants. To identify potential gender-specific metabolites appearing in response to Pi limitation in poplars, we studied the metabolic and ionomic responses in the roots and leaves of Populus cathayana Rehd males and females exposed to a 60-day period of Pi deficiency. Besides significant decreases in phosphorus contents in both Pi-deficient roots and leaves, the calcium level decreased significantly and the sulfur content increased significantly in Pi-deficient male roots, while the zinc and ferrum contents increased significantly in Pi-deficient female roots. Inorganic P deficiency caused a smaller change in the abscisic acid content, but a significant increase in the jasmonic acid content was detected in both leaves and roots. Salicylic acid significantly decreased under Pi deficiency in male leaves and female roots. Changes were found in phospholipids and phosphorylated metabolites (e.g., fructose-6-phosphate, glycerol-3-phosphate, glucose-6-phosphate, phosphoric acid and inositol-1-phosphate) in roots and leaves. Both P. cathayana males and females relied on inorganic pyrophosphate-dependent but not on Pi-dependent glycolysis under Pi-deficient conditions. Sex-specific metabolites in leaves were primarily in the category of primary metabolites (e.g., amino acids), while in roots primarily in the category of secondary metabolites (e.g., organic acids) and sugars. The metabolome analysis revealed that sexually different pathways occurred mainly in amino acid metabolism, and the tissue-related differences were in the shikimate pathway and glycolysis. We observed changes in carbon flow, reduced root biomass and increased amino acid contents in P. cathayana males but not in females, which indicated that males have adopted an energy-saving strategy to adapt to Pi deficiency. Thus, this study provides new insights into sex-specific metabolic responses to Pi deficiency.