Hongxia Zhao

Sex‐related adaptive responses to interaction of drought and salinity in Populus yunnanensis

We used Populus yunnanensis Dode., a native dioecious species in southwestern China, as a model species to study morphological, physiological, biochemical and ultrastructural responses to drought, salinity and their combination. Females exhibited more growth inhibition, gas exchange rate depression and reactive oxygen species (ROS) accumulation; higher lipid peroxide levels, lower osmotic adjustment capacity and ascorbate-glutathione cycle enzyme activities; and more damage to cell organelles than did males under drought, salinity and especially under their combination. In addition, we found sex-specific responses in total chlorophyll content (TC), carotenoid concentration and carbon isotope composition under different osmotic stresses. Our results indicated that: (1) females are more sensitive and suffer from greater negative effects than do males under drought, salinity and especially under their combination; (2) sexual differences in adaptive responses to drought, salinity and their combination are context dependent; and (3) sex-specific reactions under a combination of stresses are distinct from single-stress responses. Thus, these results provide evidence for adaptive differentiation between sexes in responses to osmotic stresses and in the sensitivity to environmental change.

Sex-related adaptive responses of Populus cathayana to photoperiod transitions.

Populus cathayana Rehd., a dioecious tree species, occupies a wide range of habitats in southwest China. Both males and females were grown under two regimes of photoperiod, from mid-length to short-day photoperiod (SD shift), or to long-day photoperiod (LD shift). SD shift triggered leaf senescence in both males and females by decreasing net photosynthesis rate (A), transpiration (E), and chlorophyll pigment (Chl), non-structural carbohydrate (NSC) and indoleacetic acid (IAA) contents, while increasing abscisic acid (ABA), malonaldehyde (MDA) and free proline (Pro) contents. The antioxidant enzyme (e.g. POD, CAT and SOD) activities and capability to maintain ultrastructural integrity also decreased under SD shift. Males exhibited faster leaf senescence than did females, as shown by greater decreases in A, E, Chl and IAA. However, males maintained a less senescent stage than did females, as indicated by higher values of A, Chl, NSC, IAA and antioxidant enzyme activities. Conversely, A, E, NSC and IAA contents and antioxidant enzyme activities were enhanced by lower O(2)(*-) in females, whereas reduced by higher O(2)(*-) in males under LD shift. Such sex-dependent responses of P. cathayana to photoperiod transitions showed that males and females possess different adaptabilities, which may relate to sex-specific leaf senescence speed under changing environments.

Different growth sensitivity to enhanced UV-B radiation between male and female Populus cathayana

We investigated sex-related morphological and physiological responses to enhanced UV-B radiation in the dioecious species Populus cathayana Rehd. Cuttings were subjected to two UV-B radiation regimes: ambient (4.5 kJ m⁻² day⁻¹) and enhanced (12.5 kJ m⁻² day⁻¹) biologically effective UV-B radiation for one growing season. Enhanced UV-B radiation was found to significantly decrease the shoot height and basal diameter and to reduce the leaf area, dry matter accumulation, net photosynthesis rate (P(n)), chlorophyll a/b ratio (Chl a/b) and anthocyanin content. Enhanced UV-B radiation also increased chlorophyll pigment, leaf nitrogen, malondialdehyde and abscisic acid (ABA) content, superoxide dismutase and peroxidase activities and UV-B-absorbing compounds. No significant effects of enhanced UV-B radiation were found on biomass allocation, gas exchange (except for P(n)), photochemical efficiency of photosystem II or water use efficiency. Moreover, different sensitivity to enhanced UV-B radiation between males and females was detected. Under enhanced UV-B radiation, males exhibited significantly higher basal diameter and leaf nitrogen, and lower Chl a/b, ABA content, UV-B-absorbing compounds, as well as less decrement of leaf area and dry matter accumulation than did females. However, no significant sexual differences in these traits were found under ambient UV-B radiation. Our results suggest that males may possess a greater UV-B resistance than do females, with males having a more efficient antioxidant system and higher anthocyanin content to alleviate UV-B penetration stress than females.

Sex-specific responses and tolerances of Populus cathayana to salinity

Responses of males and females to salinity were studied in order to reveal sex-specific adaptation and evolution in Populus cathayana Rehd cuttings. This dioecious tree species plays an important role in maintaining ecological stability and providing commercial raw material in southwest China. Female and male cuttings of P. cathayana were treated for about 1 month with 0, 75 and 150 mM NaCl. Plant growth traits, gas exchange parameters, chlorophyll pigments, intrinsic water use efficiency (WUEi), membrane system injuries, ion transport and ultrastructural morphology were assessed and compared between sexes. Salt stress caused less negative effects on the dry matter accumulation, growth rate of height, growth rate of stem base diameter, total number of leaves and photosynthetic abilities in males than in females. Relative electrolyte leakage increased more in females than in males under salinity stress. Soil salinity reduced the amounts of leaf chlorophyll a, chlorophyll b and total chlorophyll, and the chlorophyll a/b ratio more in females than in males. WUEi decreased in both sexes under salinity. Regarding the ultrastructural morphology, thylakoid swelling in chloroplasts and degrading structures in mitochondria were more frequent in females than in males. Moreover, females exhibited significantly higher Na(+) and Cl(-) concentrations in leaves and stems, but lower concentrations in roots than did males under salinity. In all, female cuttings of P. cathayana are more sensitive to salinity stress than males, which could be partially due to males having a better ability to restrain Na(+) transport from roots to shoots than do females.

Sexually different physiological responses of Populus cathayana to nitrogen and phosphorus deficiencies

Previous studies have shown that there are significant sexual differences in the morphological and physiological responses of Populus cathayana Rehder under stressful conditions. However, little is known about sex-specific differences in responses to nutrient deficiencies. In this study, the effects of nitrogen (N) and phosphorus (P) deficiencies on the morphological, physiological and chloroplast ultrastructural traits of P. cathayana males and females were investigated. The results showed that N and P deficiencies significantly decreased plant growth, foliar N and P contents, chlorophyll content, photosynthesis, and instantaneous photosynthetic N- and P-use efficiencies (PNUE and PPUE) in both sexes. Males had higher photosynthesis, higher PNUE and PPUE rates, and a lower accumulation of plastoglobules in chloroplasts than did females when exposed to N- and P-deficiency conditions. Nitrogen-deficient males had higher glutamate dehydrogenase and peroxidase activities, and a more intact chloroplast ultrastructure, but less starch accumulation than did N-deficient females. Phosphorus-deficient males had higher nitrate reductase, glutamine synthetase and acid phosphatase activities, but a lower foliar N : P ratio and less PSII damage than did P-deficient females. These results suggest that N and P deficiencies cause greater negative effects on females than on males, and that the different sexes of P. cathayana may employ different strategies to cope with N and P deficiencies.

Sex-related and stage-dependent source-to-sink transition in Populus cathayana grown at elevated CO2 and elevated temperature

Dioecious plants, which comprise more than 14,620 species, account for an important component of terrestrial ecosystems. Hence, understanding the sexually dimorphic responses in balancing carbon (C) supply and demand under elevated CO(2) is important for understanding leaf sink-to-source transitions. Here we investigate sex-related responses of the dioecious Populus cathayana Rehd. to elevated CO(2) and elevated temperature. The plants were grown in environmentally controlled growth chambers at two CO(2) enrichment regimes (350 ± 20 and 700 ± 20 μmol mol(-1)) with two temperature levels, elevated by 0 and 2 ± 0.2 °C (compared with the out-of-chamber environment). Plant growth characteristics, carbohydrate accumulation, C and nitrogen (N) allocation, photosynthetic capacity, N use efficiency and the morphology of mesophyll cells were investigated in the developing leaves (DLs) and expanded leaves (ELs) of both males and females. Elevated CO(2) enhanced plant growth and photosynthetic capacity in DLs of both males and females, and induced the male ELs to have a greater leaf mass production, net photosynthesis rate (P(n)), chlorophyll a/b ratio (Chl a/b), soluble protein level (SP), photosynthetic N use efficiency and soluble sugar level compared with females at the same leaf stage. Elevated temperature enhanced source activities and N uptake status during CO(2) enrichment, and the combined treatment induced males to be more responsive than females in sink capacities, especially in ELs, probably due to greater N acquisition from other plant parts. Our findings showed that elevated CO(2) increases the sink capacities of P. cathayana seedlings, and elevated temperature enhances the stimulation effect of elevated CO(2) on plant growth. Male ELs were found to play an important role in N acquisition from roots and stems under decreasing N in total leaves under elevated CO(2). Knowledge of the sex-specific leaf adaptability to warming climate can help us to understand sex-related source-to-sink transitions in dioecious plant species.

iTRAQ-based quantitative proteomic analysis gives insight into sexually different metabolic processes of poplars under nitrogen and phosphorus deficiencies

Male and female poplars (Populus cathayana Rehd.) respond differently to nitrogen (N) and phosphorus (P) deficiencies. In this study, an iTRAQ‐based quantitative proteomic analysis was performed. N and P deficiencies caused 189 and 144 proteins to change in abundance in males and 244 and 464 in females, respectively. Compared to N‐ and P‐deficient males, both N‐ and P‐deficient females showed a wider range of changes in proteins that are involved in amino acid, carbohydrate and protein metabolism, and the sexual differences were significant. When comparing the effects of N‐ and P‐deficiencies, N‐deficient females expressed more changes in proteins that are involved in stress responses and gene expression regulation, while P‐deficient females showed more changes in proteins that are involved in energy and lipid metabolism, stress responses and gene expression regulation. The quantitative RT‐PCR analysis of stress‐related proteins showed that males have a better expression correlation between mRNA and protein levels than do females. This study shows that P. cathayana females are more sensitive and have more rapid metabolic mechanisms when responding to N and P deficiencies than do males, and P deficiency has a wider range of effects on females than does N deficiency.