Litsea Males Are Better Adapted to Pb Stress Than Females by Modulating Photosynthesis and Pb Subcellular Distribution

Abstract

Litsea cubeba Pers., a dioecious species, is an important tree species for the bioenergy industry with great potential for lead (Pb)-polluted soil phytoremediation. However, the sex-specific morphological and physiological characteristics of L. cubeba under Pb stress remain largely unknown. In this study, L. cubeba was used as a study model to identify sex differences in leaf traits, chlorophyll, photosynthetic gas parameters, chlorophyll fluorescence, Pb subcellular distribution, and photosynthesis-related nutrient contents in chloroplasts and cell nuclei under three different Pb concentrations [0 (CK), 1 (P1), 2 (P2), and 3 (P3) mmol/kg]. The results indicate that Pb stress significantly decreases photosynthetic leaf pigments in both sexes, mainly caused by changes in Ca, Mg, and Mn contents. Furthermore, L. cubeba male plants exhibited greater adaptability to Pb stress by enlarging their leaf area, enhancing photosynthesis and excess light energy in the form of heat dissipation when compared to female plants. Notably, we observed that more Pb reached the organelle fraction and damaged chloroplasts and mitochondria in female leaves under high-level Pb treatments compared to those of the opposite sex. Transcriptome analysis demonstrated that Pb stress could significantly up-regulate more genes involved in photosynthetic antenna proteins and photosynthesis pathways in male leaves than in female leaves. Taken together, L. cubeba male plants are clearly more resistant to Pb toxicity than female plants—at least under the described Pb treatments—which is most likely due to differences in Pb allocation. This research offers a theoretical foundation for the utilization of male and female L. cubeba as suitable plants for the remediation of Pb-polluted soil.