Sexual dimorphism in poplar plants: Resource trade-offs and sex-specific strategic responses during leaf senescence

Leaf senescence is a critical developmental transition that drives nutrient remobilization, profoundly impacting plant fitness and forest productivity. In dioecious plants, divergent reproductive costs drive sex-specific life-history strategies, yet how these fundamental differences are rewired at the senescence level remains largely unknown. Here, integrating physiological, hormonal, metabolomic, and transcriptomic analyses, we reveal a striking sexual dimorphism in the senescence trajectories of the perennial tree Populus deltoides. Males execute a "fast-recycling" strategy characterized by accelerated canopy yellowing, massive reactive oxygen species (ROS) bursts, rapid nitrogen export, and synergistic surges in abscisic acid (ABA) and salicylic acid (SA), which collectively support enhanced vegetative growth. In contrast, females adopt a "maintenance-and-defense" strategy, retaining higher chlorophyll levels and mitigating oxidative stress through enhanced antioxidant metabolism to prolong leaf longevity. By constructing hierarchical regulatory networks, we identify a male-biased HD-ZIP/MYB transcriptional cascade that acts as a master amplifier of senescence signals and is associated with downstream effector genes (such as PLIP2, ATGAP1, and ASG1) involved in lipid degradation and cell death. Our findings provide a comprehensive multi-omics framework demonstrating that sex shapes the fundamental paradigm of leaf senescence, highlighting an evolutionary trade-off between rapid nutrient remobilization and prolonged organ maintenance.