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Abstract

In eukaryotic cells, lipid droplets (LDs) serve as energy reservoirs by storing triacylglycerols (TAGs). Lipases such as sugar-dependent 1 (SDP1) break down LDs to release free fatty acids (FAs), which are then transported into peroxisomes via peroxisomal ABC-transporter 1 (PXA1) for β-oxidation. Previous studies have established that SDP1-derived FAs act as the primary energy source during essential physiological processes, including seed germination and energy deprivation under prolonged darkness. Here, we show that in poplar 84K (Populus alba × Populus tremula var. glandulosa), SDP1-generated FAs not only fuel β-oxidation but also contribute to cuticle formation, a vital protective layer preventing water loss. Genetic disruption of PagSDP1 resulted in increased TAG accumulation but a thinner cuticle with reduced cutin, leading to drought hypersensitivity. Conversely, PagPXA1 knockout increased cuticular thickness and drought resistance, suggesting that blocking peroxisomal entry redirects acyl chains toward cutin biosynthesis. Intriguingly, drought stress accentuates this metabolic reprogramming; under water deficit, LD-derived FAs not only bolster cutin levels but also fuel the wax biosynthetic machinery—a shift not observed under normal conditions. Furthermore, we identified the transcription factor PagABI5 as a master regulator of this partitioning. PagABI5 directly binds to the promoters of PagSDP1a and PagPXA1s, activating the former to mobilize LDs while suppressing the latter to prioritize structural lipid production over catabolic breakdown. Our findings reveal a role for LD homeostasis in structural lipid assembly, providing a sophisticated model for how trees modulate metabolic flux to enhance environmental resilience.