Chemical communication between plant and microbe in the phyllosphere

The phyllosphere encompasses all above-ground plant surfaces, covering ~10 9 km 2 globally and hosting up to 10 26 microbial cells, yet its chemical ecology remains understudied compared to the rhizosphere. This review synthesizes recent advances in metabolite-mediated communication orchestrating phyllosphere microbiome assembly, function, and host feedback. Leaf structural traits, host immune genes, developmental stage, and fluctuating environmental drivers create spatiotemporal chemical niches that filter incoming microbes. We then examine four major classes of plant derived signals, including primary metabolites, secondary metabolites, phytohormones and volatile organic compounds, and we emphasize their dual roles. Microbial feedback occurs through phytohormone synthesis/catabolism, volatile and soluble effectors, and antimicrobial metabolites that collectively modulate plant immunity, growth, and stress tolerance while structuring inter-microbial competition. These bidirectional exchanges form a dynamic network where plants and microbes continuously negotiate cooperation and conflict under diurnal and seasonal oscillations. We outline translational prospects including probiotic foliar applications, metabolite priming, and breeding for beneficial consortia, while identifying key challenges in signal attribution, microbiota stabilization, and deciphering community-level crosstalk dynamics for sustainable crop protection. Chemical communication between plant and microbe in the phyllosphere Xuanxuan Ma 1,4, Li Ling 1,4, Bo Wang 1, Samiran Banerjee 2, Hai Nian 1, Qibin Ma 1*, Shuai Zhao 3 *, Tengxiang Lian 1* 1.Guangdong Basic Research Center of Excellence for Precise Breeding of Future Crops, Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Provincial Key Laboratory for the Development Biology and Environmental Adaptation of Agricultural Organisms, South China Institute for Soybean Innovation Research, College of Agriculture, South China Agricultural University, No.483 Wushan Road, Guangzhou, Guangdong 510642, China 2.Department of Microbiological Sciences, North Dakota State University (NDSU), Fargo, North Dakota, USA 3.State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, China 4. These authors contributed equally: Xuanxuan Ma, Li Ling Lead contact *Corresponding author. Email: [email protected]

The phyllosphere encompasses all above-ground plant surfaces, covering 10 26 microbial cells, yet its chemical ecology remains understudied compared to the rhizosphere. This review synthesizes recent advances in metabolite-mediated communication orchestrating phyllosphere microbiome assembly, function, and host feedback. Leaf structural traits, host immune genes, developmental stage, and fluctuating environmental drivers create spatiotemporal chemical niches that filter incoming microbes. We then examine four major classes of plant derived signals, including primary metabolites, secondary metabolites, phytohormones and volatile organic compounds, and we emphasize their dual roles. Microbial feedback occurs through phytohormone synthesis/catabolism, volatile and soluble effectors, and antimicrobial metabolites that collectively modulate plant immunity, growth, and stress tolerance while structuring inter-microbial competition. These bidirectional exchanges form a dynamic network where plants and microbes continuously negotiate cooperation and conflict under diurnal and seasonal oscillations. We outline translational prospects including probiotic foliar applications, metabolite priming, and breeding for beneficial consortia, while identifying key challenges in signal attribution, microbiota stabilization, and deciphering community-level crosstalk dynamics for sustainable crop protection. Key words: Phyllosphere microbiome, Chemical ecology, Metabolite-mediated communication, Plant–microbe interactions 1.Introduction The phyllosphere, the above-ground surfaces of plants, particularly the leaves, represents a dynamic interface between plants and their associated microbiota (Turner et al., 2013; Müller and Ruppel, 2014; Schlechter et al., 2019; Sohrabi et al., 2023). Unlike the nutrient-rich soil, the phyllosphere is an oligotrophic environment, exposed to fluctuating UV radiation, temperature extremes, and periodic desiccation (Dastogeer et al., 2020; Leveau, 2019). Despite these challenging conditions, it supports diverse microbial communities, including bacteria, fungi, yeasts, protists, archaea, and viruses (Mehlferber et al., 2023a; Rangel and Leveau, 2024). These microbial consortia are integral to host fitness, promoting plant growth and conferring resilience to environmental stressors, thereby underpinning the functional integrity of the phyllosphere ecosystem (Abadi et al., 2021; Ehau-Taumaunu and Hockett, 2023; Li et al., 2022a). Central to these interactions is chemical signaling, the primary mode of communication between plants and their microbial communities. Plants release a variety of metabolites and signaling molecules that influence microbial colonization, while microbes respond with their own chemical cues that can modulate plant physiology or affect neighboring microbes (Kefi et al., 2015; Liu et al., 2023; Morohoshi et al., 2009; Shao et al., 2023a; Y. Zhang et al., 2023). This intricate chemical dialogue is essential for regulating microbial populations and shaping the plant’s interactions with its microbiota. Recent advancements have shed light on how environmental,host and other factors influence the microbial communities in the phyllosphere, and the mechanisms through which plant-derived chemical signals regulate microbial populations are becoming increasingly understood (Liu et al., 2025; Z. Wang et al., 2023; Yin et al., 2024; Yuan et al., 2025). The growing recognition of the importance of phyllosphere chemical communication has raised new questions about its role in shaping plant-microbe interactions. As anthropogenic pressures, such as climate change and agricultural practices, increasingly disrupt microbial communities, understanding the mechanisms that govern these interactions is more critical than ever. Key scientific challenges remain, including the complex interplay between plant-derived signals and microbial responses, the effect of environmental factors on these interactions, and the cascading impacts of these chemical dialogues on plant immunity, stress tolerance, and overall growth. Addressing these gaps will not only advance our understanding of plant-microbe relationships but also open new avenues for improving agricultural practices and enhancing crop resilience in the face of environmental stressors. 2.Key Factors Shaping Phyllosphere Microbial Communities The phyllosphere acquires microorganisms from various sources, including soil, air, and neighboring plants, through vertical, horizontal, or mixed dispersal (Brown et al., 2020; Hardoim et al., 2012; Johnston-Monje et al., 2014; Maignien et al., 2014) (Mehlferber et al., 2023b) Unlike the more buffered rhizosphere, this open ecosystem selectively assembles microbial communities through multiple interdependent forces: host genetic constraints that filter colonizers, the dynamic spatiotemporal fluctuations that shape environmental heterogeneity and further intensify the complexity of phyllosphere metabolomics, and a physicochemical landscape shaped by intrinsic plant traits (Bao et al., 2020; Knief et al., 2010; Xu et al., 2022). These combined pressures create a metabolic theater where microbial survival hinges on adaptive chemical dialogues with the host （Figure.1） Figure 1 | Key drivers of phyllosphere microbial community assembly. Phyllosphere microbiota are shaped by multilevel factors, including environmental conditions (humidity, temperature, light), leaf structural traits, host immune and metabolic regulation, and plant developmental stage. These elements act as filters and modulators that influence microbial colonization, persistence, and interactions. Arrows indicate inhibitory (orange), selective or modulatory (blue), and bidirectional communicative (green dashed) effects. Icons represent microbes, pathogens, hormones, metabolites, and genetic material as defined in the key. 2.1 Leaf structural traits shaping microbial colonization Plant hosts exert substantial control over phyllosphere communities through the physical architecture and chemical composition of their leaves (Bodenhausen et al., 2014a; Li et al., 2018; Wagner et al., 2016). The cuticular wax layer, rich in very-long-chain fatty acids (VLCFAs) and their derivatives, functions as an impermeable barrier that protects aerial plant surfaces from environmental stress. functions both as an impermeable barrier and as a selective filter influencing microbial colonization (Lewandowska et al., 2020; Reisberg et al., 2013; Yeats and Rose, 2013). In Kentucky bluegrass, over‑expression of PpKCS6 boosts VLCFA (≥ C24) and alkane synthesis, markedly thickening the wax barrier, lowering surface permeability, and curbing trans‑cuticular water loss (Jiang et al., 2025); this wax environment change suppresses or reshapes the phyllosphere bacterial community, leading to the enrichment of certain taxa and the depletion of others (Lewandowska et al., 2020; Reisberg et al., 2013; Yeats and Rose, 2013). Trichomes introduce an additional layer of regulation (Kusstatscher et al., 2020a). Studies have shown that the decline in glandular trichome density drives substantial β‑cembrenediol exudation into the phyllosphere, which enriches Acidisoma, Ralstonia, Bradyrhizobium, and Alternaria populations while reducing the abundance of Pseudomonas (Shi et al., 2024). In chrysanthemum, trichome density and constitutive terpene production are coordinated by a CmMYC2–CmMYBML1 feedback module. CmMYC2 activates CmMYBML1, which in turn represses CmMYC2, leading to enhanced emission of monoterpenes and sesquiterpenes stored in glandular trichomes (Guan et al., 2024) . These terpenoids secreted by glandular trichomes possess specific chemical properties that not only selectively attract or inhibit certain bacteria, but may also serve as carbon sources for specific microbes; for example, Pseudomonas aeruginosa is capable of metabolizing acyclic terpenoids (Kusstatscher et al., 2020b). Leaf veins further modulate microbial assembly by governing metabolite fluxes. Copy‑number variation at OsNAL23 in rice disrupts ribosome biogenesis, down‑regulates YUCCA (auxin synthesis) and ARR (cytokinin signalling) genes, lowers indole‑3‑acetic acid, and increases vein density (Zhou et al., 2024). It has been evidenced that such densely packed veins enhance bacterial aggregation, network complexity, and community stability across diverse tree species (Yan et al., 2022). The densities of leaf veins and glandular trichomes are closely associated with the accumulation of surface exudates such as sugars, proteins, and secondary metabolites. The bases of trichomes and the microgrooves along leaf veins provide structural niches that facilitate the aggregation and release of these metabolites, enhancing their local accumulation and forming microhabitats that significantly promote bacterial colonization and community expansion (Thapa and Prasanna, 2018). Collectively, these structural attributes, cuticular waxes, trichomes, and vein architecture, interlock physical barriers, resource partitioning, and chemical signalling to establish the dynamic foundation on which phyllosphere microbes survive and function (Schäfer et al., 2023; Vorholt, 2012). 2.2 Immune regulation and fine-tuned selection Beyond these broad filters, plants exert a finer control on phyllosphere microbiota through immune signaling and targeted defense responses (Keppler et al., 2025; Legein et al., 2020a). This immune surveillance not only protects against pathogens but also influences the composition of the commensal community by affecting microbial survival and growth. For instance, a defect in the regulation of programmed cell death in CAD1 (as observed in the S205F mutant ben3 ) disrupts the host’s balance control over endophytic microbiota, leading to abnormal overgrowth of Proteobacteria and partial niche loss of Firmicutes from the community (Chen et al., 2020). MIN7 mediates vesicle trafficking to maintain apoplastic homeostasis, while CERK1 activates immune responses by recognizing pathogen-associated molecular patterns. Functional defects in these genes lead to impaired cell wall integrity barriers and trigger tissue damage caused by microbial overproliferation (Chen et al., 2020). RbohD, an NADPH oxidase, sustains robust ROS signaling; mutants lacking RbohD exhibit imbalanced immunity and phyllosphere dysbiosis, characterized by a decline in beneficial bacteria and over-proliferation of Xanthomonas, ultimately disrupting the community structure (Pfeilmeier et al., 2024). Beyond immune regulation, a plant’s metabolic state also profoundly influences its phyllosphere microbial composition (Pang et al., 2021; Y. Zhang et al., 2023). These metabolites create a unique microenvironment on the leaf surface. Not only do these metabolites provide carbon and nitrogen sources for microorganisms (Schlechter et al., 2023), but they also release functional secondary metabolites that serve as signals. In this way, plants establish specific ”chemical niches” that guide the colonization and cooperative interactions of beneficial microbes (Lajoie et al., 2020a). For example, In wheat, host genetic variation drives accumulation of the phenylpropanoid DIMBOA-Glc. This compound enriches Pseudomonas spp. in a dose-dependent manner and correlates with increased phyllosphere antibiotic resistance gene (ARG) abundance, indicating a microbiome shift toward a more ARG-enriched community (Xiang et al., n.d.). In rice, the OsPAL02 gene (involved in lignin biosynthesis) encodes an enzyme that catalyzes the synthesis of 4-hydroxycinnamic acid (4-HCA), which specifically enriches Pseudomonas spp. and inhibits the proliferation of pathogens, reducing susceptibility to leaf blight (Su et al., 2024). Notably, plants may also regulate their phyllosphere microbiome through unconventional genetic signaling molecules such as RNAs and small peptides (Sundararajan et al., 2025). Stable RNA molecules, including full-length tRNAs and tRNA-derived fragments (tRFs), have been detected on the leaf surface of Arabidopsis thaliana . These RNAs can form condensates in the presence of Ca²⁺, which enhances their stability. It is speculated that such RNAs may influence phyllosphere microbial communities through a potential cross-kingdom signaling mechanism (Borniego et al., 2025). Similarly, the application of small peptides to tea leaves was found to reduce bacterial diversity but increase fungal diversity in the tea phyllosphere, while also enriching certain beneficial microbes as core community members (H. Chen et al., 2023) . Although research on these non-traditional signals is still in its early stages, these findings suggest that plants may employ non-coding RNAs and small peptides to establish a more complex chemical communication system with their microbiota. 2.3 Developmental stage dependent reassembly of the phyllosphere microbiome The composition of the phyllosphere microbiota is not static over the lifespan of a leaf, but shifts with leaf age and developmental stage (Geyer et al., 2024; Lan et al., 2024a). Young, expanding tobacco leaves exhibit limited metabolic activity and reduced structural complexity, resulting in low microbial diversity and simplified community functions. Some reported that phyllosphere bacterial communities at this stage are dominated by fast-growing taxa, while oligotrophic genera such as Acinetobacter begin to proliferate as they exploit diverse carbon sources (Gao et al., 2023). As photosynthetic output intensifies during leaf maturation, increased availability of soluble sugars, amino acids, and secondary metabolites reshapes the microbial niche . In tobacco, this transition is marked by a gradual replacement of early Proteobacteria by Firmicutes and Bacteroidetes, with community functions shifting toward stress resilience and host adaptation (Gao et al., 2023). A similar metabolite-mediated selection is observed in tea plants, where early-stage accumulation of theophylline promotes the enrichment of Flavobacterium and Myriangium, while later accumulation of EGCG suppresses Pseudomonas via ROS-associated stress and favors beneficial microbes such as Parabacteroides and Mortierella (Tan et al., 2025). During senescence, cell wall disassembly releases abundant nutrients; leaching diminishes oligotrophic Methylobacterium, whereas actinomycetes such as Streptomyces secrete extracellular hydrolases that accelerate organic matter turnover, increasing stochasticity yet maintaining overall phyllosphere homeostasis (Lan et al., 2024b). Stage‑specific metabolites thus drive a recruit–screen–replace cycle, enabling plants to dynamically assemble and reshape their leaf microbiomes throughout development. 2.4 Environmental factors influencing phyllosphere microbial dynamics Moisture and temperature sculpt a shifting mosaic of phyllosphere “oases,” and recent work is clarifying the underlying molecular levers. In natural Arabidopsis populations, specific allelic variation in the immune gene ACD6 interacts with drought conditions to modulate the composition of core phyllosphere microbiota (Karasov et al., 2024). In parallel, long-term water limitation in five forage grasses reduces overall microbial diversity while leaving Gammaproteobacteria dominant (Bechtold et al., 2021). Sudden increases in leaf surface humidity can create transient aqueous microhabitats that boost microbial proliferation and shift community structure toward moisture adapted taxa (Smets et al., 2023). However, Arabidopsis mutants defective in leaf water balance exhibit uncontrolled bacterial proliferation and leaf necrosis under high humidity stress (Xin et al., 2016). Temperature adds another selective tier (Faticov et al., 2021). Elevated temperature alters carbon and nitrogen assimilation in leaves, resulting in an increased C:N ratio. This shift selectively filters phyllosphere microbial communities, notably shaping the trophic strategies of organic carbon–dependent fungi such as Ascomycota (Sangiorgio et al., 2024; X. Wang et al., 2023). Seasonal fluctuations reinforce this pattern (Zhang et al., 2022). In warm, carbohydrate‑rich months favor carbon-metabolizing Pseudomonas, whereas cold seasons shift the microbial community toward stress-tolerant taxa such as Ascomycota and Actinobacteria (Postiglione et al., 2022). Thus, fluctuating water availability and thermal stress interact with plant physiology to filter microbial partners. Although microbes are highly sensitive to individual environmental factors, their integrated ecological responses to the interaction of multiple factors remain insufficiently understood and require further investigation. Light regimes impose an additional, dual-layer filter on microbes via direct irradiation and plant-mediated chemistry (Carvalho and Castillo, 2018). UV‑B screens out sensitive taxa, the proportion of UV‑tolerant strains within the peanut phyllosphere increases markedly, with pigmented bacteria exhibiting a pronounced competitive advantage (Peredo and Simmons, 2018). Beyond direct effects,sub‑lethal UV‑A, however, acts through the plant: current research indicates that UV - A irradiation stimulates both the Calvin cycle and phosphoenolpyruvate transport. This enhances the availability of precursors for phenylpropanoid and terpenoid biosynthesis, it elevating flavonoid and phenolic exudation that remodel microbial interaction networks (Zha et al., 2024). Visible light intensity influences phyllosphere communities mainly through metabolic shifts. In lettuce, high light intensity promotes the accumulation of soluble proteins and chlorophyll, induces the expression of sulfur- and carbon-cycling genes (e.g., mdh and glyA), and functionally selects for microbial taxa capable of utilizing these altered leaf substrates (Kong et al., 2024). Light quality is equally potent; a low red to far-red ratio activates the phytochrome pathway, triggers shade-avoidance growth, and promotes the dominance of IAA-producing Bacillus and Pseudomonas species (O’Rourke et al., 2025). Laboratory LED studies also reveal a direct microbial response, with Pseudomonas exposed to light exhibiting significant changes in its utilization patterns of metabolic substrates (Gharaie et al., 2017). Although studies on the influence of light on microbial communities have made initial progress, the dynamic interplay among light-driven circadian rhythms, fluctuations in carbon source availability, and the assembly of phyllosphere microbiota remains poorly understood. Furthermore, the role of plant-derived metabolites as biochemical intermediaries in orchestrating these processes is still unclear, warranting further investigation into how light-mediated metabolic shifts shape phyllosphere microbial ecology. 3.Metabolite-Mediated Plant-Microbiome Interactions: A Key to Shaping phyllosphere Microbial Communities In the phyllosphere environment, as the physical contact between plants and microbes is limited to surface interactions, chemicals become the primary medium for communication between the two. Table 1 summarizes the major classes of plant-derived chemicals on leaves, their microbial targets, and the resultant community and host outcomes prior to the detailed sections below. Table 1. Plant-derived chemical cues shaping phyllosphere microbiota and host outcomes | Chemical class | Representative molecules | Source on leaf | Mode of release | Microbial effect | Community outcome | Plant outcome | Key refs | | Primary metabolites | Sugars, amino acids, organic acids | Cuticle, guttation droplets, trichomes | Passive leakage, exudation | Nutrient supply | Enrichment of metabolically competent taxa | Facilitate commensal colonization | Schlechter et al., 2019; Zhang et al., 2023 | | Secondary metabolites | Phenolics, flavonoids, terpenoids, alkaloids | Epidermis, trichomes | Accumulation or release upon tissue damage | Antimicrobial action, quorum-sensing interference | Host-specific filtering, niche partitioning | Defence barrier, ecological gatekeeping | Erb & Kliebenstein, 2020; De Mandal et al., 2023 | | Hormones | SA, JA, ET, ABA, IAA, CK | Endogenous signaling gradients | Stress-induced secretion, local exudation | Alter microbial stress tolerance, modulate signaling | Shifts in abundance of core taxa | Induced PR proteins, ROS burst, stomatal closure | Karasov et al., 2024; Pang et al., 2021 | | VOCs | α-/β-pinene, limonene, linalool, isoprene | Leaf mesophyll & epidermis | Volatilization | Signaling, antimicrobial, alternative carbon source | Enrichment of VOC-adapted taxa (e.g., Sphingomonas ) | ISR, pathogen suppression | Huang et al., 2023; Xin et al., 2016 | 3.1 Nutritional and Primary Metabolites Unlike the rhizosphere (root zone), where plants deliberately secrete abundant nutrients to attract microorganisms, the phyllosphere is an oligotrophic (nutrient-poor) environment (Hu et al., 2023; Yusuf et al., 2025). Nevertheless, plants do release primary metabolites (e.g. sugars, amino acids, and organic acids) onto leaf surfaces through processes such as diffusion from epidermal cells, secretion by glandular trichomes, guttation, or leaching of cellular contents during rain events (Ossola and Farmer, 2024a; Schlechter et al., 2019b; Shakir et al., 2021). These compounds are essential for supporting microbial growth on leaves, and carbon sources are highly limiting. For example, in tea plants ( Camellia sinensis ), the significant increase in sucrose and D-glucose-6-phosphate levels can selectively promote the proliferation of Bacillus species capable of methanol metabolism, markedly enhancing their colonization efficiency on the leaf surface (Chen et al., 2024). In the phyllosphere of Arabidopsis, mutation of phosphoribosylpyrophosphate synthetase (PRS) enhances microbial colonization by upregulating the phosphoketolase (PKT) pathway, thereby reallocating carbon resources from nucleotide biosynthesis to methanol assimilation (C. Zhang et al., 2024)。 3.2 Secondary Metabolites and Defense Compounds In addition to acquiring essential nutrients, plants synthesize a multitude of secondary metabolites that serve primarily defensive and signaling roles (Yang et al., 2025). These compounds often accumulate on leaf surfaces as a chemical barrier, which both pathogens and commensal microbes must adapt to. During pathogen attack or environmental stress, plants dramatically increase the secretion of antimicrobial compounds such as phenolics, flavonoids, tannins, alkaloids, and terpenoids (Erb and Kliebenstein, 2020; George and Brandl, 2021). These defenses can either diffuse directly onto the leaf surface or be stored in epidermal cells and released upon tissue damage, where they inhibit microbial growth and even disrupt microbial quorum sensing (De Mandal and Jeon, 2023). In this way, secondary metabolites act as phyllosphere “gatekeepers” that protect the leaf habitat. Secondary metabolites can also modulate microbial behavior. Analyses suggest that upon pathogen infection, poplar actively remodels the phyllosphere microenvironment through metabolic reprogramming. In more resistant genotypes, the concentration of organic acids increases significantly, which may modulate nutrient availability or local pH conditions, thereby indirectly shaping microbial habitat suitability and promoting the enrichment of antagonistic bacteria such as Pseudomonas (L. Zhang et al., 2023) . Different tree species release specific secondary metabolites, such as terpenoids and phenylpropanoids, which function as antimicrobial agents or signaling molecules. These compounds create chemically defined niches where only microbes with the corresponding metabolic capacities (e.g., Methylobacterium extorquens, Burkholderia ) can survive and establish. This selective filtering shapes host-specific microbial assemblages and reflects a process of adaptive matching between plant metabolism and phyllosphere microbiota (Lajoie et al., 2020b). This phenomenon also occurs in microbial interactions. In a co-culture of two phyllosphere isolates from Ferula leaves ( Streptomyces LBM_605 and Rhodococcus LBM_791), physical contact and shifts in strain abundance activated a previously silent resistomycin biosynthetic gene cluster in the Streptomyces. The production of this antibiotic is thought to give Streptomyces a competitive advantage and help maintain community balance (Huang et al., 2025). Through these multifaceted roles, plant secondary metabolites help establish and sustain a healthy phyllosphere microbiome, promoting beneficial plant–microbe interactions while defending against potential threats. 3.3 Plant Hormones as Signals in the Phyllosphere Plant hormones operate as chemical gatekeepers on the leaf, selectively sculpting the phyllosphere microbiome. Salicylic acid (SA) signalling promotes the deposition of pathogenesis-related proteins and activates an NADPH oxidase-mediated reactive oxygen species (ROS) burst. This immune response imposes broad stress on non-pathogenic microbes, particularly inhibiting the growth of Gram-negative bacteria that typically dominate the leaf surface, such as γ-Proteobacteria . Concurrently, SA activation frees ecological microniches, facilitating the colonization of rare genera such as Aeribacillus and Granulicella (Vincent et al., 2022). Ethylene signaling influences the colonization and selection process of microorganisms by modulating the host’s leaf surface structures and the secretion of defense-related metabolites. In the ethylene-insensitive mutant ein2, bacteria of the genus Variovorax are significantly enriched, indicating that under normal conditions ethylene exerts a negative regulatory effect on this group. Loss of signal perception removes this inhibitory effect, thereby promoting its expansion and colonization in the phyllosphere (Bodenhausen et al., 2014b) Growth‑linked hormones add a second layer of screening. Leaf‑dwelling Pseudomonas convert host tryptophan to indole‑3‑acetic acid (IAA) via the trp gene cluster; the resulting auxin promotes plant cell expansion and modulates host developmental processes, contributing to enhanced plant growth and colonization efficiency. Cytokinin (CK) signalling remodels the phyllosphere microenvironment by regulating the composition of leaf surface metabolites and structural features. Through chemically mediated selection, it enriches Bacillus species with antimicrobial properties and enhances their adhesion, biofilm formation, and colonization capacity. This, in turn, triggers plant immune responses and improves resistance against foliar pathogens such as Pseudomonas syringae and Botrytis cinerea (Gupta et al., 2022). Elevated auxin levels in Eucommia ulmoides leaves correlate with the enrichment of abundant phyllosphere taxa, including Actinobacteriota, likely via modulation of host traits such as leaf structure, alkaloid content, and antioxidant activity (Shao et al., 2024). Hormonal gradients thus provide a dynamic, molecularly precise filter that determines which microbial partners prosper on the phyllosphere. 3.4 Volatile Organic Compounds Regulate Phyllosphere Microbial Communities via Dual Mechanisms Higher plants emit numerous small lipophilic molecules with high vapor pressure, known as volatile organic compounds (VOCs) (Bergman et al., 2025). These volatiles play a dual role in plant–microbe interactions: on one hand, they act as signaling molecules in pathogen recognition and defense responses, and on the other hand, they serve as carbon sources for symbiotic microbes, aiding in their colonization of the phyllosphere. This ”dual functionality” makes VOCs key chemical mediators by which plants actively shape the structure and function of the phyllosphere microbiome (Farré-Armengol et al., 2016; Hammerbacher et al., 2019; Quintana‐Rodriguez et al., 2015; Rosenkranz and Schnitzler, 2016). For example, in Citrus medica ‘Fingered’, monoterpenes such as α-pinene, β-pinene, and linalool were identified as dominant volatile organic compounds (VOCs) in leaf emissions under pathogen-associated conditions. These VOCs may function as selective chemical signals that either serve as metabolic substrates or exert antimicrobial and signaling effects, thereby facilitating the specific colonization and enrichment of microbial taxa such as Actinomycetospora and Sphingomonas, which are capable of adapting to or exhibiting chemotactic responses toward high-VOC environments on the leaf surface (Wang et al., 2022). Consistent with VOC‑mediated defense functions, overexpression of OsTPS19 in rice enhances accumulation of (S)‑limonene, which inhibits Magnaporthe oryzae spore germination and significantly increases blast disease resistance (Chen et al., 2018). Plant volatiles can induce systemic acquired resistance. Arabidopsis thaliana exposed to a blend of α-pinene and β-pinene showed elevated expression of AZI1 ( AZELAIC ACID INDUCED 1 ) and related regulatory genes, thereby triggering a systemic defense response (Riedlmeier et al., 2017).In addition to their role as signaling molecules, certain volatile organic compounds (VOCs), such as isoprene, can be metabolized by phyllosphere microbes as energy sources, forming a type of metabolic mutualism. Studies have shown that Variovorax bacteria can utilize plant-emitted isoprene as a carbon source to support their colonization on the leaf surface (Crombie et al., 2018). Taken together, VOCs exemplify the remarkable capacity of plants to chemically sculpt phyllosphere microbial communities. Future research should continue to explore the diverse structures and functions of VOCs, as well as their potential in plant health management, particularly in enhancing pathogen detection, selecting for beneficial symbionts, and restoring microbial ecological balance. Beyond host-derived metabolites, the phyllosphere microbiota itself acts as an active source of chemical cues. These reciprocal exchanges between plants and microbes form feedback loops that stabilize communities and fine-tune host physiology. Figure 2 summarizes the dual directions of these interactions and provides a conceptual bridge to the following section on microbial contributions. Figure 2 | Bidirectional interactions between plant metabolites and phyllosphere microbes. The assembly and stability of phyllosphere microbial communities are shaped by bidirectional exchanges of chemical signals. On the one hand, host-derived metabolites exert direct effects by enriching commensal diversity and suppressing pathogen proliferation, and indirect effects by supporting nutrient cycling and optimizing metabolic allocation, thereby strengthening microbial network stability. On the other hand, resident microbes feed back on host physiology through three principal routes: (i) modulation of plant hormone homeostasis, where microbial biosynthesis or catabolism of hormones such as auxin and ethylene rebalances plant hormones and affects developmental and immune signaling; (ii) signal exchange, in which microbial cues alter host gene expression and reshape the physicochemical environment of the leaf surface and (iii) biological antagonism, in which beneficial taxa secrete antimicrobial compounds that limit pathogen invasion and reinforce niche exclusion. Together, these reciprocal processes underpin cooperative as well as competitive dynamics, ultimately linking phyllosphere community function to plant health. Icons denote metabolites (colored dots), microbes (cells), and interaction types (arrows). 4.Microbial Chemical Feedback to the Host Plant Chemical feedback from the phyllosphere microbiome is as influential as the plant‑to‑microbe signals described earlier. Epiphytic bacteria and fungi release phytohormones, volatile cues, siderophores, quorum‑quenching enzymes and antibiotics that reshape host physiology, recalibrate immune set‑points and modulate stress tolerance (Yang et al., 2024). These compounds can amplify defence (induced systemic resistance), loosen or tighten stomata, alter carbon allocation and even redirect plant development, turning the leaf surface into a chemically co‑governed niche rather than a host‑dominated arena. 4.1 Microbial Production of Phytohormones and Growth Regulators Many phyllosphere microbes are capable of synthesizing plant hormones, thereby regulating the plant’s hormonal balance. Within the endophytic bacterial community of tomato leaves, several isolates such as Bacillus methylotrophicus, Pseudomonas spp ., and Pantoea spp. exhibited the ability to produce indole-3-acetic acid (IAA) and siderophores. These strains demonstrated in vitro antagonistic activity against phytopathogens and concurrently promoted plant growth (Romero et al., 2016). This microbially produced auxin can diffuse into plant tissues and become part of the plant’s total auxin pool, potentially affecting plant cell elongation, division, and differentiation (C.-Y. Chen et al., 2023; Timofeeva et al., 2024). Beyond synthesizing hormones, microbes can also degrade or modify plant hormones to influence plant physiology. A notable mechanism is the production of the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase by certain phyllosphere bacteria (e.g., Paraburkholderia dioscoreae Msb3). This deaminase breaks down the ethylene precursor ACC, thereby lowering ethylene levels in the plant and alleviating ethylene-induced growth inhibition (Herpell et al., 2023). By lowering ethylene, a hormone that in excess stunts growth and triggers early ageing, these microbes ease plant stress and often extend both growth and lifespan (Arun K. et al., 2020). Another intriguing interaction is that some phyllosphere bacteria can catabolize auxin itself as a sole carbon and nitrogen source; for example, Pseudomonas putida strain 1290 is able to utilize IAA as its only growth substrate (Leveau and Lindow, 2005). By depleting auxin on the leaf surface, these bacteria may cause plant cell walls to remain more rigid (since auxin typically promotes cell wall loosening), thereby increasing the retention of nutrients in the phyllosphere (Majda and Robert, 2018; Thomas et al., 2024). This represents a beneficial feedback loop: the microbe helps the host plant cope with stress and remain healthier, while the plants sustained health provides a continued habitat for the microbe. By modulating plant hormone levels in these ways, phyllosphere microbes can either promote plant growth and stress resilience or manipulate plant tissues for their own advantage, depending on the context and concentration of the hormonal signals (Sohrabi et al., 2023b). Importantly, plants are capable of perceiving and responding to these microbe-derived hormones, though not always consciously. The intricate interplay between microbial hormones and plant hormonal signaling is a frontier of plant-microbe interaction research, promising to reveal how symbiotic microbes fine-tune plant physiology from the leaf surface and provide new insights. 4.2 Microbial Volatiles and Soluble Signals Microbial metabolites are not mere by-products; they act as mobile signals that allow epiphytes to modulate both the host and surrounding microbial communities. Volatile organic compounds (VOCs) diffuse through the laminar boundary layer, extending their chemical influence beyond the producer within a certain range. A well-studied example is 2,3-butanediol from Enterobacter aerogenes, which primes salicylic- and jasmonic-acid pathways and elicits induced systemic resistance throughout the leaf canopy (D’Alessandro et al., 2014). Similarly, 3-methyl-1-butanol released by the tomato phyllosphere bacterium Enterobacter cloacae TR1 suppresses Botrytis cinerea, effectively fumigating the phyllosphere with a biologically active volatile (Chaouachi et al., 2021). Unlike contact-dependent antimicrobial compounds, these volatiles spread over the leaf surface and penetrate microscopic crevices that bacteria themselves cannot reach, creating a wide protective halo around beneficial microbes. Importantly, not all microbial signals that affect the plant are volatile; many are soluble compounds that can still diffuse through the leaf surface or be sensed at the interface, although their range of action is limited (Ossola and Farmer, 2024b; Thomas et al., 2024). Pseudomonas species, including phyllosphere-associated strains, can acquire iron under iron-limited conditions by producing multiple siderophores such as NRPS-dependent pyoverdine and NIS-dependent achromobactin (Berti and Thomas, 2009; Owen and Ackerley, 2011). Due to the specificity of siderophore–receptor interactions, differences among community members in their ability to utilize the same siderophore can lead to uneven resource allocation at the community level, thereby modulating ecological niches and reshaping community structure (Gu et al., 2025). A recent study revealed that 3-hydroxydecanoic acid (3-OH-C10:0) secreted by bacteria from Arabidopsis leaves is perceived by the LORE receptor, whose homomerization is essential for triggering ROS bursts and PTI. Natural variation in the receptor’s dimerization capacity among species determines their immune sensitivity (Eschrig et al., 2024). Phyllosphere biocontrol strains associated with disease-resistant tomatoes can secrete lytic enzymes, and plants “eavesdrop” on their products to activate immune responses (Shao et al., 2023b). Community enzymes can even weaponise pathogen structures: a citrus core bacterium expresses β-mannosidase that cleaves Phyllosticta cell wall thereby weakening the pathogen’s structural integrity (Li et al., 2022b). Overall, the chemical footprint that microbes leave on leaves constitutes a rich source of cues that plants can detect and interpret. VOCs and soluble metabolites generate a feedback loop in which microbial chemistry modulates plant signalling, and the ensuing plant responses reshape the microbial community. This bidirectional exchange remains an underexplored lever for phyllosphere engineering. 4.3 Antagonistic Metabolites and Microbial Warfare Intense resource competition on the leaf surface drives many epiphytes to deploy antimicrobial metabolites, turning microbial rivalries into an auxiliary layer of plant defence (Aachath and Rupawalla, n.d.; Schlechter et al., 2019c).Chemical antagonism can be even more direct: 2,4-di-tert-butylphenol secreted by Aspergillus cvjetkovicii neutralizes ROS-dependent pathogenicity in Rhizoctonia solani and represses bZIP-activated AMT1 transcription, thereby enhancing rice resistance (Fan et al., 2024). As classic phyllosphere inhabitants, Pseudomonas spp. deploy an expanded antimicrobial arsenal comprising phenazines, safracin, and cyclic lipopeptides that suppress the fire blight pathogen Erwinia amylovora on aerial tissues (Dagher et al., 2021; Legein et al., 2020b; Santos Kron et al., 2020) Ecologically, such “microbial warfare” reallocates space and nutrients, often in the plant’s favour but occasionally at the cost of collateral beneficials. Evidence suggests that plants release niche specific nutrients to selectively foster antagonistic metabolite producing microbes, indicating active recruitment of microbial bodyguards. Thus, leaf-borne antagonistic metabolites illustrate a three-way alliance: microbes combat one another for their own advantage, yet their rivalry ultimately reinforces host protection and maintains community balance. 4.4 MAMPs and Induction of Plant Immunity Microbe-associated molecular patterns (MAMPs) provide an energetically economical route by which the leaf microbiota modulates host immunity. Flagellin fragments, LPS, chitin, and lipopeptides are constitutively exposed during colonization and are perceived by plasma-membrane pattern-recognition receptors (PRRs), leading to MAMP-triggered immunity (MTI), a broad-spectrum yet tunable defense state (Kim et al., 2020; Lü et al., 2022a). MTI can be viewed as a third, self-adjusting filter that complements structural barriers and nutrient chemistry, allowing plants to discriminate between allies and enemies without incurring the high metabolic cost of a full defense response. Low MAMP “loads” supplied by commensals induce only basal MAPK activity and ROS, thereby priming immunity without penalizing growth, whereas higher loads or unfamiliar epitopes amplify the cascade to activate antimicrobial proteins and phenylpropanoid metabolism (Cheng et al., 2021; Entila et al., 2024a; Watkins et al., 2024; M. Zhang et al., 2024). Selected mechanisms exemplify this graded response. In the phyllosphere, the conserved flagellin-derived peptide flg22 is recognized by the plasma membrane-localized PRR FLS2, which assembles a signaling complex with the co-receptor BAK1 (Colaianni et al., 2021). Upon activation, this complex recruits the receptor-like cytoplasmic kinase BIK1, which directly phosphorylates the NADPH oxidase RBOHD (Li et al., 2014) and the cation channels CNGC2/4, thereby coordinating extracellular ROS production and Ca²⁺ influx (Bai et al., 2023). The resulting ROS not only activate MAPK cascades such as MPK3/MPK6 and downstream WRKY transcription factors to induce defense gene expression (Tian et al., 2019), but also regulate guard cell ion fluxes and turgor, promoting stomatal closure to restrict pathogen entry (Arnaud et al., 2023). These immune outputs impose ecological selection pressures on phyllosphere microbial communities (Entila et al., 2024b). Some pathogen-derived flg22 variants are strongly immunogenic and amplify PTI outputs such as ROS and defense metabolite accumulation, potentially reshaping phyllosphere community composition (Stevens et al., 2024). By contrast, Xanthomonas flg22 variants are often weakly perceived or evade recognition, indicating their limited suitability as models for enhanced PTI (Lü et al., 2022b). Thus, by “reading” the density and identity of surface MAMPs, plants continuously recalibrate immunity, suppressing pathogens while tolerating, or even fostering, beneficial epiphytes. 5.Conclusion and Future Perspectives Chemical communication in the phyllosphere microenvironment is a decisive factor for plant health and ecosystem function. （Figure.3） In agriculture, deciphering and harnessing this chemical dialogue offers a promising route to achieving sustainable crop management. If crops can be encouraged to recruit beneficial microbes by pre-treating seeds or foliage with tailored metabolites or probiotics, and if the production of microbially derived compounds that deter pests and pathogens can be enhanced, reliance on synthetic pesticides could be reduced. Practical applications already exist. Foliar sprays containing beneficial microbes have been applied for disease management in vineyards and orchards, and several commercial biocontrol products based on such approaches are now available on the market (Alimzhanova et al., 2025; Altieri et al., 2023). Similarly, breeding or engineering plants with specific leaf traits (such as optimal cuticle permeability or exudate composition) may promote the formation of a healthy phyllosphere microbiome as a selectable trait (Clouse and Wagner, 2021). Although still in its infancy, manipulating the leaf chemical environment via plant traits is an exciting frontier. Despite recent advances, substantial knowledge gaps and challenges remain. From an applied perspective, a key challenge is ensuring that introduced beneficial microbes or elicitor compounds persist and remain effective under field conditions. The effectiveness of phyllosphere biocontrol may be unstable, partly because environmental stresses such as ultraviolet radiation and rainfall can reduce microbial survival on leaves or wash away secreted metabolites. Therefore, formulation technologies (protective coatings for microbes or slow-release matrices for signaling molecules) will be needed to stabilize interventions. Another factor to consider is that specific chemical cues intended to stimulate a beneficial microbe must not inadvertently favor a latent pathogen. A deeper mechanistic understanding will help improve precision. For example, by identifying a volatile that attracts Bacillus species but not Pseudomonas syringae, or a carbohydrate analogue usable only by non-pathogenic yeasts. The chemical complexity of the leaf surface poses an additional challenge: countless plant- and microbe-derived compounds interact simultaneously, forming a biochemical jigsaw. Untangling these signals requires advanced analytical tools. Traditional metabolite analyses, such as 16S/ITS metagenomics, can only profile ”who is present” and often struggle to easily distinguish whether a specific compound on leaves originates from plants or microbes. To disentangle ”who produces what,” emerging technologies such as single - cell metabolomics, fluorescence in situ hybridization (FISH) techniques combined with mass spectrometry imaging tools are required to precisely map metabolites to different microecological niches. This process should be combined with synthetic communities and CRISPR to validate causal relationships. Additionally, our understanding of community-level signaling remains rudimentary. Most of our current knowledge about chemical signals is derived from studies of single plant-microbe pairs or simple synthetic communities. However, in nature, dozens of microbial species coexist simultaneously on a single leaf. How are multiple signals integrated? A plant may simultaneously perceive microbial-associated molecular patterns (MAMPs) from bacteria and fungi, along with fluctuations in its own hormones. What combined impact does this have on its immunity or growth? Similarly, a microbe on the leaf surface responds not only to plant chemicals but also to metabolites from neighboring microbes, including competitors or mutualists. Network interactions may be critically important. Decoding these networked communications will require integrated experimentation and modeling. Figure 3 | From chemical ecology to practice: a roadmap for phyllosphere research and deployment The figure summarizes how chemical cues at the leaf surface can be translated into applications while highlighting key bottlenecks and enabling methods. (A) Application prospects and practices. Foliar delivery of probiotics or metabolite-based biostimulants aims to steer phyllosphere consortia, suppress disease, and enhance stress tolerance. (B) Challenges faced. UV, heat, desiccation and rainfall reduce on-leaf survival and wash off inputs; spatial heterogeneity and non-target effects complicate field robustness, calling for protective formulations and dosing strategies. (C) Technical requirements and analytical tools. Multi-omics and spatial metabolomics (metagenomics/amplicons, MSI-based metabolite mapping), together with genetics and synthetic communities, are needed to attribute “who makes what” and to validate causal interactions. (D) Future research directions. Decipher integration of multi-signal inputs, extend to multi-kingdom networks, and test microbiome/chemistry engineering for plant health in realistic environments. Icons indicate microbes, metabolites and interaction types. Acknowledge The research described here was supported by the Funding of National Natural Science Foundation of China (Grant No. 32470090); Project from Guangdong Basic Research Center of Excellence for Precise Breeding of Future Crops (Grant No. FCBRCE-202506); Guangdong Provincial Construction Project For Modern Agriculture Industry Technology System Innovation Teams (Oil Crop Industry Technology System) (Grant No. 2024CXTD06); Science and Technology Plan Project of Guangzhou (Grant No. 2024A04J5487)；Double First-class Discipline Promotion Project (Grant No.2021B10564001); Science and Technology Plan Project of Shanwei (Grant No. 2024E005); South China Agricultural University-La Domei Group Industry College Joint Open Research Project (Grant No. KLERUECSCMARAC202303). Author contributions Conceptualization: T.X.L., H.N., S.Z. Visualization: L.L., X.X.M. Writing-original draft: T.X.L, X.X.M,W.B. Writing-review and editing: T.X.L.,S.B., X.X.M., H.N., Q.B.M. Competing interests The authors declare no competing interests

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Authors Metrics & Citations Metrics Article Usage 679views 262downloads Citations Download citation Xuanxuan Ma, Li Ling, Bo Wang, et al. Chemical communication between plant and microbe in the phyllosphere. Authorea. 09 September 2025. DOI: https://doi.org/10.22541/au.175739964.49015293/v1 DOI: https://doi.org/10.22541/au.175739964.49015293/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download. For more information or tips please see 'Downloading to a citation manager' in the Help menu. Cited by - Do stomatal traits modulate leaf microbiome assembly?, New Phytologist, 250, 1, (41-50), (2026).https://doi.org/10.1111/nph.70914 Loading...