Plant-associated Microorganisms Research Articles

Plant Growth Stimulation by Microbial Consortia

Plant-associated microorganisms play an important role in agricultural production. Although various studies have shown that single microorganisms can exert beneficial effects on plants, it is increasingly evident that when a microbial consortium—two or more interacting microorganisms—is involved, additive or synergistic results can be expected. This occurs, in part, due to the fact that multiple species can perform a variety of tasks in an ecosystem like the rhizosphere. Therefore, the beneficial mechanisms of plant growth stimulation (i.e., enhanced nutrient availability, phytohormone modulation, biocontrol, biotic and abiotic stress tolerance) exerted by different microbial players within the rhizosphere, such as plant-growth-promoting bacteria (PGPB) and fungi (such as Trichoderma and Mycorrhizae), are reviewed. In addition, their interaction and beneficial activity are highlighted when they act as part of a consortium, mainly as mixtures of different species of PGPB, PGPB–Mycorrhizae, and PGPB–Trichoderma, under normal and diverse stress conditions. Finally, we propose the expansion of the use of different microbial consortia, as well as an increase in research on different mixtures of microorganisms that facilitate the best and most consistent results in the field.

Arsenate-reducing bacteria affect As accumulation and tolerance in Salix atrocinerea

Arsenic (As)-reducing bacteria are able to influence As-speciation and, in this way, change As bio-availability. In consequence, this has an impact on As uptake by plants growing on polluted soil and on the effectiveness of the phytoremediation process. To be able to efficiently utilize these bacteria for As-phytoremediation in the field, a better understanding of the plant-bacterial interactions involved in As-tolerance or toxicity is needed. In this work, seedlings of a clone of Salix atrocinerea derived from a specimen naturally growing on an As-polluted brownfield were grown under gnotobiotic conditions exposed to As, and in the presence or absence of two of its field-associated and in vitro characterized plant growth-promoting (PGP) bacteria. The inoculation with Pantoea sp., induced a moderate reduction of AsV to AsIII in the exposure medium that, together with a coordinated plant response of As uptake, chelation and sequestration, increased As accumulation in roots; which is reflected into a higher phytostabilization. However, inoculation with Rhodococcus erythropolis due to a higher disproportionate reduction of AsV to AsIII in the medium caused less As accumulation in roots that non-bioaugmented plants and despite the lower As content, the concentrations of AsIII present in the medium and the damage suffered in roots and leaves, indicated that As tolerance mechanisms (such as prevention of AsIII uptake and efflux) did not occur in time to avoid physical disturbance and plants growth reduction. Interestingly, by two different metabolic pathways -coordinated by different key transporters mediating As uptake, tolerance, distribution and vacuolar accumulation at the roots- both bacteria limited As accumulation in Salix shoots. Our results provide for the first time a detailed insight in the plant-bacterial responses and physiological changes contributing to As tolerance in S. atrocinerea, that will facilitate the design of effective strategies for exploitation of plant-associated microorganisms for phytoremediation.

Microbial communities in the rhizosphere of different willow genotypes affect phytoremediation potential in Cd contaminated soil

Plant-associated microorganisms play an important role in controlling heavy metal uptake and accumulation in aerial parts. The microbial community and its interaction with Cd accumulation by willow were assessed to explore the association of phytoextraction efficiency and rhizospheric microbial populations.Therefore, the rhizosphere microbial compositions of three willow genotypes grown in two Cd polluted sites were investigated, focusing on their interactions with phytoremediation potential. Principal coordinate analysis revealed a significant effect of genotype on the rhizosphere microbial communities. Distinct beneficial microorganisms, such as plant growth promoting bacteria (PGPB) and mycorrhizal fungi, were assembled in the rhizosphere of different willow genotypes. Linear mixed models showed that the relative abundance of PGPB was positively associated (p < 0.01) with Cd accumulation, since these microbes significantly increased willow growth. The higher abundance of arbuscular mycorrhizal fungi in the rhizosphere of Salix × aureo-pendula CL ‘J1011’ at the Kejing site, showed a negative correlation with the Cd content, but a positive correlation with biomass. Conversely, mycorrhizal fungi, were more abundant in the rhizosphere of S. × jiangsuensis CL. ‘J2345’ and positively correlated with the Cd content in willow tissues. This study provides new insights into the distinctive microbial communities in rhizosphere of different willow genotypes, which may be consistent with the phytoremediation potential.

Beneficial Plant-Associated Microorganisms From Semiarid Regions and Seasonally Dry Environments: A Review.

Semiarid regions are apparently low biodiversity environments; however, these environments may host a phylogenetically diverse microbial community associated with plants. Their microbial inhabitants are often recruited to withstand stressful settings and improve plant growth under harsh conditions. Thus, plant-associated microorganisms isolated from semiarid and seasonally dry environments will be detailed in the present review, focusing on plant growth promotion potential and the microbial ability to alleviate plant abiotic stress. Initially, we explored the role of microbes from dry environments around the world, and then, we focused on seasonally dry Brazilian biomes, the Caatinga and the Cerrado. Cultivable bacteria from semiarid and seasonally dry environments have demonstrated great plant growth promotion traits such as plant hormone production, mobilization of insoluble nutrients, and mechanisms related to plant abiotic stress alleviation. Several of these isolates were able to improve plant growth under stressful conditions commonly present in typical semiarid regions, such as high salinity and drought. Additionally, we highlight the potential of plants highly adapted to seasonal climates from the Caatinga and Cerrado biomes as a suitable pool of microbial inoculants to maintain plant growth under abiotic stress conditions. In general, we point out the potential for the exploitation of new microbial inoculants from plants growing in dry environments to ensure a sustainable increase in agricultural productivity in a future climate change scenario.

Formation, characterization and modeling of emergent synthetic microbial communities

Microbial communities colonize plant tissues and contribute to host function. How these communities form and how individual members contribute to shaping the microbial community are not well understood. Synthetic microbial communities, where defined individual isolates are combined, can serve as valuable model systems for uncovering the organizational principles of communities. Using genome-defined organisms, systematic analysis by computationally-based network reconstruction can lead to mechanistic insights and the metabolic interactions between species. In this study, 10 bacterial strains isolated from the Populus deltoides rhizosphere were combined and passaged in two different media environments to form stable microbial communities. The membership and relative abundances of the strains stabilized after around 5 growth cycles and resulted in just a few dominant strains that depended on the medium. To unravel the underlying metabolic interactions, flux balance analysis was used to model microbial growth and identify potential metabolic exchanges involved in shaping the microbial communities. These analyses were complemented by growth curves of the individual isolates, pairwise interaction screens, and metaproteomics of the community. A fast growth rate is identified as one factor that can provide an advantage for maintaining presence in the community. Final community selection can also depend on selective antagonistic relationships and metabolic exchanges. Revealing the mechanisms of interaction among plant-associated microorganisms provides insights into strategies for engineering microbial communities that can potentially increase plant growth and disease resistance. Further, deciphering the membership and metabolic potentials of a bacterial community will enable the design of synthetic communities with desired biological functions.

Endophytic microorganisms of apple fruit (Malus domestica)

The plant-associated microorganisms are of key importance in ensuring the quality and safety of plant products. This paper focuses on the study and composition of endophytic microorganisms inautumn apple varieties from domestic selection intended for long-term storage: Bessemyanka Barantseva, Orlovsky Pioner, Alesya and Verbnoe.It was discovered that the internal tissues of fruits are richly populated with microorganisms, the number of which depends on the plant variety and the stage of fruit development. The dominant group is yeast (up to 107 CFU/g). The most common speciesis Hanseniaspora uvarum (26,0%). The number of bacteria averages 102-104 CFU/g, the dominant species–Lactobacillus sp. (52,0%) and Pantoea agglomerans(34,2%). The soft tissue of the fruits of all studied apple varieties contains mycelial fungi, the number of which, as a rule, does not exceed 102 CFU/g. The dominant species is Cladosporium aggregatocicatricatum (33,3%). The microorganisms - producers of biologically active compounds, promising for agrobiotechnologies, have been identified.

The plant endosphere world - bacterial life within plants.

The plant endosphere is colonized by complex microbial communities and microorganisms, which colonize the plant interior at least part of their lifetime and are termed endophytes. Their functions range from mutualism to pathogenicity. All plant organs and tissues are generally colonized by bacterial endophytes and their diversity and composition depend on the plant, the plant organ and its physiological conditions, the plant growth stage as well as on the environment. Plant-associated microorganisms, and in particular endophytes, have lately received high attention, because of the increasing awareness of the importance of host-associated microbiota for the functioning and performance of their host. Some endophyte functions are known from mostly lab assays, genome prediction and few metagenome analyses; however, we have limited understanding on in planta activities, particularly considering the diversity of micro-environments and the dynamics of conditions. In our review, we present recent findings on endosphere environments, their physiological conditions and endophyte colonization. Furthermore, we discuss microbial functions, the interaction between endophytes and plants as well as methodological limitations of endophyte research. We also provide an outlook on needs of future research to improve our understanding on the role of microbiota colonizing the endosphere on plant traits and ecosystem functioning.

PGPR-mediated induction of systemic resistance and physiochemical alterations in plants against the pathogens: Current perspectives.

Plant growth-promoting rhizobacteria (PGPR) are diverse groups of plant-associated microorganisms, which can reduce the severity or incidence of disease during antagonism among bacteria and soil-borne pathogens, as well as by influencing a systemic resistance to elicit defense response in host plants. An amalgamation of various strains of PGPR has improved the efficacy by enhancing the systemic resistance opposed to various pathogens affecting the crop. Many PGPR used with seed treatment causes structural improvement of the cell wall and physiological/biochemical changes leading to the synthesis of proteins, peptides, and chemicals occupied in plant defense mechanisms. The major determinants of PGPR-mediated induced systemic resistance (ISR) are lipopolysaccharides, lipopeptides, siderophores, pyocyanin, antibiotics 2,4-diacetylphoroglucinol, the volatile 2,3-butanediol, N-alkylated benzylamine, and iron-regulated compounds. Many PGPR inoculants have been commercialized and these inoculants consequently aid in the improvement of crop growth yield and provide effective reinforcement to the crop from disease, whereas other inoculants are used as biofertilizers for native as well as crops growing at diverse extreme habitat and exhibit multifunctional plant growth-promoting attributes. A number of applications of PGPR formulation are needed to maintain the resistance levels in crop plants. Several microarray-based studies have been done to identify the genes, which are associated with PGPR-induced systemic resistance. Identification of these genes associated with ISR-mediating disease suppression and biochemical changes in the crop plant is one of the essential steps in understanding the disease resistance mechanisms in crops. Therefore, in this review, we discuss the PGPR-mediated innovative methods, focusing on the mode of action of compounds authorized that may be significant in the development contributing to enhance plant growth, disease resistance, and serve as an efficient bioinoculants for sustainable agriculture. The review also highlights current research progress in this field with a special emphasis on challenges, limitations, and their environmental and economic advantages.

Symbiosis and stress: how plant microbiomes affect host evolution.

Existing paradigms for plant microevolution rarely acknowledge the potential impacts of diverse microbiomes on evolutionary processes. Many plant-associated microorganisms benefit the host via access to resources, protection from pathogens, or amelioration of abiotic stress. In doing so, they alter the plant's perception of the environment, potentially reducing the strength of selection acting on plant stress tolerance or defence traits or altering the traits that are the target of selection. We posit that the microbiome can affect plant microevolution via (1) manipulation of plant phenotypes in ways that increase plant fitness under stress and (2) direct microbial responses to the environment that benefit the plant. Both mechanisms might favour plant genotypes that attract or stimulate growth of the most responsive microbial populations or communities. We provide support for these scenarios using infectious disease and quantitative genetics models. Finally, we discuss how beneficial plant-microbiome associations can evolve if traditional mechanisms maintaining cooperation in pairwise symbioses, namely partner fidelity, partner choice and fitness alignment, also apply to the interactions between plants and diverse foliar and soil microbiomes. To understand the role of the plant microbiome in host evolution will require a broad ecological understanding of plant-microbe interactions across both space and time. This article is part of the theme issue 'The role of the microbiome in host evolution'.

Harnessing the genetic potential of the plant microbiome

Plant-associated microorganisms, such as bacteria and fungi, can grow on and survive in healthy plant tissues, making up the plant microbiome. Members of the plant microbiome can provide benefits to their host, and emerging research suggests that plants can reshape the composition of their microbiomes in response to environmental cues. The plant microbiome collectively acts as a reservoir for genes that may improve plant growth and survival in response to challenges, therefore contributing to the total genetic potential of the plant. Understanding the impact of the plant microbiome has unlocked new strategies for improving crop production, especially as climate change threatens to increase the prevalence of pathogens and stressful growth conditions. Applying microbiome engineering strategies, such as inoculation with plant growth-promoting rhizobacteria (PGPR), and incorporating the microbiome into the breeding process show promise for improving future agricultural crop production.

Two New Putative Plant Viruses from Wood Metagenomics Analysis of an Esca Diseased Vineyard.

The concept of plant as a holobiont is now spreading among the scientific community and the importance to study plant-associated microorganisms is becoming more and more necessary. Along with bacteria and fungi, also viruses can play important roles during the holobiont-environment interactions. In grapevine, viruses are studied mainly as pathological agents, and many species (more than 80) are known to be able to replicate inside its tissues. In this study two new viral species associated with grape wood tissues are presented, one belongs to the Potyviridae family and one to the Bunyavirales order. Due to the ability of potyviruses to enhance heterologous virus replication, it will be important to assess the presence of such a virus in the grapevine population to understand its ecological role. Furthermore, the association of the cogu-like virus with esca symptomatic samples opens new questions and the necessity of a more detailed characterization of this virus.

Soil fungal communities differ between shaded and sun-intensive coffee plantations in El Salvador.

Coffea arabica is a highly traded commodity worldwide, and its plantations are habitat to a wide range of organisms. Coffee farmers are shifting away from traditional shade coffee farms in favor of sun-intensive, higher yield farms, which can impact local biodiversity. Using plant-associated microorganisms in biofertilizers, particularly fungi collected from local forests, to increase crop yields has gained traction among coffee producers. However, the taxonomic and spatial distribution of many fungi in coffee soil, nearby forests and biofertilizers is unknown. We collected soil samples from a sun coffee system, shade coffee system, and nearby forest from Izalco, Sonsonate, El Salvador. At each coffee system, we collected soil from the surface (upper) and 10 cm below the surface (lower), and from the coffee plant drip line (drip line) and the walkway between two plants (walkway). Forest soils were collected from the surface only. We used ITS metabarcoding to characterize fungal communities in soil and in the biofertilizer (applied in both coffee systems), and assigned fungal taxa to functional guilds using FUNGuild. In the sun and shade coffee systems, we found that drip line soil had higher richness in pathotrophs, symbiotrophs, and saprotrophs than walkway soil, suggesting that fungi select for microhabitats closer to coffee plants. Upper and lower soil depths did not differ in fungal richness or composition, which may reflect the shallow root system of Coffea arabica. Soil from shade, sun, and forest had similar numbers of fungal taxa, but differed dramatically in community composition, indicating that local habitat differences drive fungal species sorting among systems. Yet, some fungal taxa were shared among systems, including seven fungal taxa present in the biofertilizer. Understanding the distribution of coffee soil mycobiomes can be used to inform sustainable, ecologically friendly farming practices and identify candidate plant-growth promoting fungi for future studies.

An α/β-Hydrolase Fold Subfamily Comprising Pseudomonas Quinolone Signal-Cleaving Dioxygenases.

The quinolone ring is a common core structure of natural products exhibiting antimicrobial, cytotoxic, and signaling activities. A prominent example is the Pseudomonas quinolone signal (PQS), a quorum-sensing signal molecule involved in the regulation of virulence of Pseudomonas aeruginosa The key reaction to quinolone inactivation and biodegradation is the cleavage of the 3-hydroxy-4(1H)-quinolone ring, catalyzed by dioxygenases (HQDs), which are members of the α/β-hydrolase fold superfamily. The α/β-hydrolase fold core domain consists of a β-sheet surrounded by α-helices, with an active site usually containing a catalytic triad comprising a nucleophilic residue, an acidic residue, and a histidine. The nucleophile is located at the tip of a sharp turn, called the "nucleophilic elbow." In this work, we developed a search workflow for the identification of HQD proteins from databases. Search and validation criteria include an [H-x(2)-W] motif at the nucleophilic elbow, an [HFP-x(4)-P] motif comprising the catalytic histidine, the presence of a helical cap domain, the positioning of the triad's acidic residue at the end of β-strand 6, and a set of conserved hydrophobic residues contributing to the substrate cavity. The 161 candidate proteins identified from the UniProtKB database originate from environmental and plant-associated microorganisms from all domains of life. Verification and characterization of HQD activity of 9 new candidate proteins confirmed the reliability of the search strategy and suggested residues correlating with distinct substrate preferences. Among the new HQDs, PQS dioxygenases from Nocardia farcinica, N. cyriacigeorgica, and Streptomyces bingchenggensis likely are part of a catabolic pathway for alkylquinolone utilization.IMPORTANCE Functional annotation of protein sequences is a major requirement for the investigation of metabolic pathways and the identification of sought-after biocatalysts. To identify heterocyclic ring-cleaving dioxygenases within the huge superfamily of α/β-hydrolase fold proteins, we defined search and validation criteria for the primarily motif-based identification of 3-hydroxy-4(1H)-quinolone 2,4-dioxygenases (HQD). HQDs are key enzymes for the inactivation of metabolites, which can have signaling, antimicrobial, or cytotoxic functions. The HQD candidates detected in this study occur particularly in environmental and plant-associated microorganisms. Because HQDs active toward the Pseudomonas quinolone signal (PQS) likely contribute to interactions within microbial communities and modulate the virulence of Pseudomonas aeruginosa, we analyzed the catalytic properties of a PQS-cleaving subset of HQDs and specified characteristics to identify PQS-cleaving dioxygenases within the HQD family.

Host-adapted lactobacilli in food fermentations: impact of metabolic traits of host adapted lactobacilli on food quality and human health

Back-slopping of fermentation cultures in food fermentations can ensure stability of fermentation microbiota at the species or even at the strain level over extended periods of time. In contrast to the fermentation organisms in spontaneous food fermentations, which are derived from plant-associated or environmental micro-organisms, dominant micro-organisms in back-slopped fermentations are often recruited from lactic acid bacteria that are associated with insect or vertebrate hosts. Lifestyle-associated metabolic traits that relate to the ecological fitness of lactic acid bacteria in the host environment include biofilm formation through production of exopolysaccharides, acid resistance mediated by urease, glutaminase or glutamate decarboxylase, and polysaccharide hydrolysis mediated by extracellular glucosyl hydrolases. This review will discuss the ecological fitness of these organisms in food fermentations, and relate their specific metabolic properties to the safety, quality, and nutritional properties of food.

The Role of Plant-Associated Microbes in Mediating Host-Plant Selection by Insect Herbivores.

There is increasing evidence that plant-associated microorganisms play important roles in shaping interactions between plants and insect herbivores. Studies of both pathogenic and beneficial plant microbes have documented wide-ranging effects on herbivore behavior and performance. Some studies, for example, have reported enhanced insect-repellent traits or reduced performance of herbivores on microbe-associated plants, while others have documented increased herbivore attraction or performance. Insect herbivores frequently rely on plant cues during foraging and oviposition, suggesting that plant-associated microbes affecting these cues can indirectly influence herbivore preference. We review and synthesize recent literature to provide new insights into the ways pathogenic and beneficial plant-associated microbes alter visual, olfactory, and gustatory cues of plants that affect host-plant selection by insect herbivores. We discuss the underlying mechanisms, ecological implications, and future directions for studies of plant-microbial symbionts that indirectly influence herbivore behavior by altering plant traits.

Ecological impact of a rare sugar on grapevine phyllosphere microbial communities

Plants host a complex microbiota inside or outside their tissues, and phyllosphere microorganisms can be influenced by environmental, nutritional and agronomic factors. Rare sugars are defined as monosaccharides with limited availability in nature and they are metabolised by only few certain microbial taxa. Among rare sugars, tagatose (TAG) is a low-calories sweetener that stimulates and inhibits beneficial and pathogenic bacteria in the human gut microbiota, respectively. Based on this differential effect on human-associated microorganisms, we investigated the effect of TAG treatments on the grapevine phyllosphere microorganisms to evaluate whether it can engineer the microbiota and modify the ratio between beneficial and pathogenic plant-associated microorganisms. TAG treatments changed the structure of the leaf microbiota and they successfully reduced leaf infections of downy mildew (caused by Plasmopara viticola) and powdery mildew (caused by Erysiphe necator) under field conditions. TAG increased the relative abundance of indigenous beneficial microorganisms, such as some potential biocontrol agents, which could partially contribute to disease control. The taxonomic composition of fungal and bacterial leaf populations differed according to grapevine locations, therefore TAG effects on the microbial structure were influenced by the composition of the originally residing microbiota. TAG is a promising biopesticide that could shift the balance of pathogenic and beneficial plant-associated microorganisms, suggesting selective nutritional/anti-nutritional properties for some specific taxa. More specifically, TAG displayed possible plant prebiotic effects on the phyllosphere microbiota and this mechanism of action could represent a novel strategy that can be further developed for sustainable plant protection.

Root-associated microorganisms reprogram plant life history along the growth-stress resistance tradeoff.

Growth-defense tradeoffs are a major constraint on plant evolution. While the genetics of resource allocation is well established, the regulatory role of plant-associated microorganisms is still unclear. Here, we demonstrate that plant-associated microorganisms can reposition the plant phenotype along the same growth-defense tradeoff that determines phenotypic effects of plant mutations. We grew plants with microorganisms altering ethylene balance, a key hormone regulating plant investment into growth and stress tolerance. Microbial ethylene reduction had a similar effect to mutations disrupting ethylene signaling: both increased plant growth but at the cost of a strong stress hypersensitivity. We conclude that microbial impact on phenotype can offset the effects of mutations and that apparent plant growth promotion has strong pleiotropic effects. This study confirms that plant life history should be addressed as a joint product of plant genotype and its associated microbiota.

Deciphering the Symbiotic Plant Microbiome: Translating the Most Recent Discoveries on Rhizobia for the Improvement of Agricultural Practices in Metal-Contaminated and High Saline Lands

Rhizosphere and plant-associated microorganisms have been intensely studied for their beneficial effects on plant growth and health. These mainly include nitrogen-fixing bacteria (NFB) and plant-growth promoting rhizobacteria (PGPR). This beneficial fraction is involved in major functions such as plant nutrition and plant resistance to biotic and abiotic stresses, which include water deficiency and heavy-metal contamination. Consequently, crop yield emerges as the net result of the interactions between the plant genome and its associated microbiome. Here, we provide a review covering recent studies on PGP rhizobia as effective inoculants for agricultural practices in harsh soil, and we propose models for inoculant combinations and genomic manipulation strategies to improve crop yield.

Environmental pollution effects on plant microbiota: the case study of poplar bacterial-fungal response to silver nanoparticles.

Pollution affects most of the urban and forest environments at different levels causing well-known effects on human and plant health. The influence that pollutants exert on plant-associated microbiota might direct plant health and, in some cases, also the removal of pollutants by plants. With the advent of nanotechnologies, an increasing amount of engineered nanoparticles are being introduced into the environment, and consequently, their impact on plant-associated microorganisms needs to be investigated. In this context, silver nanoparticles (Ag-NPs) were experimentally supplied at leaf and root level of poplar plants to assess Ag-NPs effects on plant microbiota. Leaf Ag-NP treatment increased bacteria and fungi evenness and determined a significant reduction in both microbial groups, while root Ag-NP treatment reduced the bacterial and fungal biodiversity. Bioinformatics functional analysis showed that Ag-NP treatment reduced the aerobic and stimulated facultative anaerobic and oxidative stress-tolerant bacteria. Our study offers new insights into the effects of Ag-NPs on both phyllosphere and rhizosphere poplar-associated microbiota and may represent a first attempt to understand the behavior of microbial communities of a tree species growing in a polluted environment.

Revealing Cues for Fungal Interplay in the Plant-Air Interface in Vineyards.

Plant-associated microorganisms play a crucial role in plant health and productivity. Belowground microbial diversity is widely reported as a major factor in determining the composition of the plant microbiome. In contrast, much less is known about the role of the atmosphere in relation to the plant microbiome. The current study examined the hypothesis that the atmospheric microbiome influences the composition of fungal communities of the aboveground organs (flowers, fruit, and leaves) of table grape and vice versa. The atmosphere surrounding grape plantings exhibited a significantly higher level of fungal diversity relative to the nearby plant organs and shared a higher number of phylotypes (5,536 OTUs, 40.3%) with the plant than between organs of the same plant. Using a Bayesian source tracking approach, plant organs were determined to be the major source of the atmospheric fungal community (92%). In contrast, airborne microbiota had only a minor contribution to the grape microbiome, representing the source of 15, 4, and 35% of the fungal communities of leaves, flowers, and fruits, respectively. Moreover, data indicate that plant organs and the surrounding atmosphere shared a fraction of each other’s fungal communities, and this shared pool of fungal taxa serves as a two-way reservoir of microorganisms. Microbial association analysis highlighted more positive than negative interactions between fungal phylotypes. Positive interactions were more common within the same environment, while negative interactions appeared to occur more frequently between different environments, i.e., atmosphere, leaf, flower, and fruit. The current study revealed the interplay between the fungal communities of the grape phyllosphere with the surrounding air. Plants were identified as a major source of recruitment for the atmospheric microbiome, while the surrounding atmosphere contributed only a small fraction of the plant fungal community. The results of the study suggested that the plant–air interface modulates the plant recruitment of atmospheric fungi, taking a step forward in understanding the plant holobiont assembly and how the atmosphere surrounding plants plays a role in this process. The impact of plants on the atmospheric microbiota has several biological and epidemiological implications for plants and humans.