Persistent legacy effects on soil metagenomes facilitate plant adaptive responses to drought.

Both chronic and acute drought alter the composition and physiology of soil microbiomes, with implications for globally important processes including carbon cycling and plant productivity. When water is scarce, selection favors microbes with thicker peptidoglycan cell walls, sporulation ability, and constitutive osmolyte production (Schimel, Balser, and Wallenstein 2007)-but also the ability to degrade complex plant-derived polysaccharides, suggesting that the success of plants and microbes during drought are inextricably linked. However, communities vary enormously in their drought responses and subsequent interactions with plants. Hypothesized causes of this variation in drought resilience include soil texture, soil chemistry, and historical precipitation patterns that shaped the starting communities and their constituent species (Evans, Allison, and Hawkes 2022). Currently, the physiological and molecular mechanisms of microbial drought responses and microbe-dependent plant drought responses in diverse natural soils are largely unknown (de Vries et al. 2023). Here, we identify numerous microbial taxa, genes, and functions that characterize soil microbiomes with legacies of chronic water limitation. Soil microbiota from historically dry climates buffered plants from the negative effects of subsequent acute drought, but only for a wild grass species native to the same region, and not for domesticated maize. In particular, microbiota with a legacy of chronic water limitation altered the expression of a small subset of host genes in crown roots, which mediated the effect of acute drought on transpiration and intrinsic water use efficiency. Our results reveal how long-term exposure to water stress alters soil microbial communities at the metagenomic level, and demonstrate the resulting "legacy effects" on neighboring plants in unprecedented molecular and physiological detail.

Microbial Turnover and Dispersal Events Occur in Synchrony with Plant Phenology in the Perennial Evergreen Tree Crop Citrus sinensis.

Emerging research indicates that plant-associated microbes can alter plant developmental timing. However, it is unclear if host phenology affects microbial community assembly. Microbiome studies in annual or deciduous perennial plants face challenges in separating effects of tissue age from phenological driven effects on the microbiome. In contrast, evergreen perennial trees, like Citrus sinensis, retain leaves for years, allowing for uniform sampling of similarly aged leaves from the same developmental cohort. This aids in separating phenological effects on the microbiome from impacts due to annual leaf maturation/senescence. Here, we used this system to test the hypothesis that host phenology acts as a driver of microbiome composition. Citrus sinensis leaves and roots were sampled during seven phenological stages. Using amplicon-based sequencing, followed by diversity, phylogenetic, differential abundance, and network analyses, we examined changes in bacterial and fungal communities. Host phenological stage is the main determinant of microbiome composition, particularly within the foliar bacteriome. Microbial enrichment/depletion patterns suggest that microbial turnover and dispersal were driving these shifts. Moreover, a subset of community shifts were phylogenetically conserved across bacterial clades, suggesting that inherited traits contribute to microbe-microbe and/or plant-microbe interactions during specific phenophases. Plant phenology influences microbial community composition. These findings enhance understanding of microbiome assembly and identify microbes that potentially influence plant development and reproduction. IMPORTANCE Research at the forefront of plant microbiome studies indicates that plant-associated microbes can alter the timing of plant development (phenology). However, it is unclear if host phenological stage affects microbial community assembly. Microbiome studies in annual or deciduous perennial plants can face difficulty in separating effects of tissue age from phenological driven effects on the microbiome. Evergreen perennial plants, like sweet orange, maintain mature leaves for multiple years, allowing for uniform sampling of similarly aged tissue across host reproductive stages. Using this system, multiyear sampling, and high-throughput sequencing, we identified plant phenology as a major driver of microbiome composition, particularly within the leaf-associated bacterial communities. Distinct changes in microbial patterns suggest that microbial turnover and dispersal are mechanisms driving these community shifts. Additionally, closely related bacteria have similar abundance patterns across plant stages, indicating that inherited microbial traits may influence how bacteria respond to host developmental changes. Overall, this study illustrates that plant phenology does indeed govern microbiome seasonal shifts and identifies microbial candidates that may affect plant reproduction and development.

Microbial effects on plant phenology and fitness.

Plant development and the timing of developmental events (phenology) are tightly coupled with plant fitness. A variety of internal and external factors determine the timing and fitness consequences of these life-history transitions. Microbes interact with plants throughout their life history and impact host phenology. This review summarizes current mechanistic and theoretical knowledge surrounding microbe-driven changes in plant phenology. Overall, there are examples of microbes impacting every phenological transition. While most studies have focused on flowering time, microbial effects remain important for host survival and fitness across all phenological phases. Microbe-mediated changes in nutrient acquisition and phytohormone signaling can release plants from stressful conditions and alter plant stress responses inducing shifts in developmental events. The frequency and direction of phenological effects appear to be partly determined by the lifestyle and the underlying nature of a plant-microbe interaction (i.e., mutualistic or pathogenic), in addition to the taxonomic group of the microbe (fungi vs. bacteria). Finally, we highlight biases, gaps in knowledge, and future directions. This biotic source of plasticity for plant adaptation will serve an important role in sustaining plant biodiversity and managing agriculture under the pressures of climate change.