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

Abstract

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.

Sexual Dimorphism in the Chemical Composition of Male and Female in the Dioecious Tree, Juniperus communis L., Growing under Different Nutritional Conditions

“…Male individuals can adopt an energy-saving strategy when they grow in nutrient deficient conditions [43]. In our current study, however, a significant interaction between soil fertilization treatment and sex in the concentration of carbohydrates was not observed, contrary to our second hypothesis.…”

Metabolic alterations provide insights into Stylosanthes roots responding to phosphorus deficiency

“…Under P-limiting conditions, P-containing metabolites, such as nucleic acid, phospholipids and phosphorylated sugars, can be scavenged to release Pi and maintain P homeostasis in plant cells [60]. It has been shown that phosphorylated sugars are reduced by P deficiency in various plants, such as Arabidopsis [37], barley [40], white lupin (Lupinus albus) [61] and Populus cathayana [62]. Similarly, the accumulation of 6 phosphorylated sugars were decreased in P-deficient stylo roots (Fig.…”

Metabolic alterations provide insights into Stylosanthes roots responding to phosphorus deficiency

“…Under P-limiting conditions, P-containing metabolites, such as nucleic acid, phospholipids and phosphorylated sugars, can be scavenged to release Pi and maintain P homeostasis in plant cells [59]. It has been shown that phosphorylated sugars are reduced by P deficiency in various plants, such as Arabidopsis [37], barley [40], white lupin (Lupinus albus) [60] and Populus cathayana [61]. Similarly, the accumulation of 6 phosphorylated sugars were decreased in Pdeficient stylo roots (Fig.…”