Nitrogen (N) is a key nutrient impacting plant growth and physiological processes. However, the supply of N is often not sufficient to meet the requirements of trees in many terrestrial ecosystems. Because of differences in production costs, male and female plants have evolved different stress resistance strategies for N limitation. However, little is known about differential gene expression according to sex in poplars responding to N limitation. To explore sex-related constitutive defenses, Populus cathayana Rehder transcriptomic, proteomic and metabolic analyses were performed on the roots of male and female Populus cathayana. We detected 16,816 proteins and 37,286 transcripts, with 2797 overlapping proteins and mRNAs in the roots. In combination with the identification of 90 metabolites, we found that N deficiency greatly altered gene expression related to N metabolism as well as carbohydrate metabolism, secondary metabolism and stress-related processes in both sexes. Nitrogen-deficient P. cathayana females exhibited greater root biomass and less inhibition of citric acid production and glycolysis as well as higher secondary metabolic activity and abscisic acid contents than N-deficient P. cathayana males. Interestingly, males presented a better osmotic adjustment ability and higher expression of resistance genes, suggesting that P. cathayana males exhibit a better stress tolerance ability and can invest fewer resources in defense compared with females. Therefore, our study provides new molecular evidence that P. cathayana males and females adopt different resistance strategies to cope with N deficiency in their roots.

Salicaceae plants are dioecious woody plants. Previous studies have shown that male individuals are more tolerant to water deficiency than females for male‐biased poplars. However, Salix paraplesia is a female‐biased species in nature. It is still unknown whether female willows are more tolerant to drought stress than males. To better understand the sexually different tolerance to water deficiency in willows, a greenhouse experiment combined with a field investigation was conducted, and physiological traits were tested in male and female S. paraplesia under a drought‐stressed condition (50% of soil water capacity). Our field investigation showed that S. paraplesia was a species with female‐biased sex ratio along altitude gradients (2,400 m, 2,600 m and 2,800 m) in their natural habitats. Our results showed that the height growth, biomass accumulation, total chlorophyll pigment content ( TChl ), and the net photosynthetic rate were higher in female willows than in males at the low and middle altitudes (2,400 m and 2,600 m) rather than at a high altitude (2,800 m) under well‐watered conditions. Under drought‐stressed conditions, the growth, biomass, and photosynthesis were greatly inhibited in both sexes, while females showed higher biomass and TChl content and suffered less negative effects than did males. Particularly, females that originated from a high altitude showed lower leaf relative electrolyte leakage, malondialdehyde content, and less disorder of chloroplast ultrastructures but a higher peroxidase activity (POD) than that of males. Therefore, S. paraplesia females exhibited a better drought tolerance and self‐protective ability than males from high altitude. There is a reason to speculate that the population structure of S. paraplesia at a high altitude would be likely to further female biases with the increased drought intensity in the alpine regions.

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.

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