Perkins, A. M. | Search bioRxiv

bioRxiv2025

Functional memory of drought affects leaf chemical defenses and microbial interactions in aspen

Drought is an increasingly important driver of tree mortality, but its long-term impacts on trait expression remain poorly understood. Leaves are a key interface at which trees respond to abiotic stress, and foliar traits such as chemical defenses and microbial communities may play an important role in determining post-drought resilience. Here, we tested whether prior-year drought leaves a persistent imprint on leaf traits in Populus tremuloides. Using a three-year common garden experiment with controlled water limitation, we measured two major classes of defensive phenolics--salicinoid phenolic glycosides (SPGs) and condensed tannins (CTs)--alongside foliar fungal community composition. SPG concentrations increased and CTs declined in response to prior-year drought, with these effects persisting across growing seasons. While overall fungal community composition remained relatively stable, we detected shifts in the relative abundance of individual amplicon sequence variants (ASVs), particularly within potentially pathogenic lineages, associated with drought history. These findings provide evidence that drought leaves a legacy in leaf chemistry and microbial colonization, with potential consequences for how trees tolerate future abiotic and biotic stress. Our results highlight the importance of incorporating foliar trait legacies into models of forest resilience under climate change. Significance StatementTrees are known to exhibit long-term responses to drought, but whether such legacy effects extend to annually renewed tissues like leaves remains unclear. Our findings reveal that prior-year drought alters both chemical defenses and microbial associations in newly formed leaves, demonstrating a form of physiological memory. This work uncovers a novel mechanism by which trees integrate past environmental stress into future interactions, with implications for understanding forest resilience under climate change.

plant biology↗

bioRxiv2025

Persistent trade-offs balance competition and colonization across centuries

Microbial competition drives rapid adaptation, often forcing organisms to specialize in new ecological niches. Adaptations that improve competitive ability can reduce performance in other environments creating trade-offs. Whether such trade-offs persist in nature--or are eroded as lineages adapt through compensatory changes--remains largely unknown. Here we show that a trade-off between competitive ability and host colonization has been stably maintained in natural Pseudomonas populations for centuries. Wild plant-pathogenic Pseudomonas compete using tailocins--phage-derived molecular weapons that bind to specific cell-surface receptors. Genomic surveys and functional assays reveal that the most broadly lethal tailocins remain rare--while the tailocins production increases competitive killing, it also compromises plant colonization. We determine that the polymorphisms behind this trade-off are not transient -- historical genomes spanning two centuries show that the trade-off has been maintained for at least 10-10 generations. Our results demonstrate that, in natural populations, a trade-off between competition and pathogenicity is fundamental and not easily overcome. SignificanceWhen a microbe colonizes a host, it must both establish infection and outcompete other organisms. Short-term experiments show that gains in competitive ability can reduce colonization, creating trade-offs, but whether microbes resolve these conflicts over long evolutionary timescales is unknown. We show that a trade-off between competitive killing and host colonization has been stably maintained for centuries in natural Pseudomonas populations infecting Arabidopsis thaliana. Tailocins--phage-derived weapons--provide strong competitive advantages, yet their production reduces colonization success, explaining why the most broadly lethal variants remain rare. Genomic surveys and historical genomes spanning two centuries reveal that the polymorphisms underlying this trade-off have persisted across 10-10 generations. Understanding such long-lived constraints can inform antimicrobial strategies that exploit evolutionary trade-offs.

evolutionary biology↗