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The above-ground parts of terrestrial plants are collectively known as the phyllosphere. The surface of the leaf blade is a unique and extensive habitat for microbial communities. Phyllosphere bacteria are the second most closely associated microbial group with plants after fungi and viruses, and are the most abundant, occupying a dominant position in the phyllosphere microbial community. Host species are a major factor influencing the community diversity and structure of phyllosphere microorganisms. In this study, six Populus spp. were selected for study under the same site conditions and their phyllosphere bacterial community DNA fragments were paired-end sequenced using 16S ribosomal RNA (rRNA) gene amplicon sequencing. Based on the distribution of the amplicon sequence variants (ASVs), we assessed the alpha-diversity level of each sample and further measured the differences in species abundance composition among the samples, and predicted the metabolic function of the community based on the gene sequencing results. The results revealed that different Populus spp. under the same stand conditions resulted in different phyllosphere bacterial communities. The bacterial community structure was mainly affected by the carbon and soluble sugar content of the leaves, and the leaf nitrogen, phosphorus and carbon/nitrogen were the main factors affecting the relative abundance of phyllosphere bacteria. Previous studies have shown that a large proportion of the variation in the composition of phyllosphere microbial communities was explained by the hosts themselves. In contrast, leaf-borne nutrients were an available resource for bacteria living on the leaf surface, thus influencing the community structure of phyllosphere bacteria. These were similar to the conclusions obtained in this study. This study provides theoretical support for the study of the composition and structure of phyllosphere bacterial communities in woody plants and the factors influencing them.

As an important habitat for microorganisms, the phyllosphere has a great impact on plant growth and health, and changes in phyllosphere microorganisms are closely related to the occurrence of leaf diseases. However, there remains a limited understanding regarding alterations to the microbial community in the phyllosphere resulting from pathogen infections. Here, we analyzed and compared the differences in phyllosphere microorganisms of powdery mildew cucumber from three disease severity levels (0% < L1 < 30%, 30% ≤ L2 < 50%, L3 ≥ 50%, the number represents the lesion coverage rate of powdery mildew on leaves). There were significant differences in α diversity and community structure of phyllosphere communities under different disease levels. Disease severity altered the community structure of phyllosphere microorganisms, Rosenbergiella, Rickettsia, and Cladosporium accounted for the largest proportion in the L1 disease grade, while Bacillus, Pantoea, Kocuria, and Podosphaera had the highest relative abundance in the L3 disease grade. The co-occurrence network analysis of the phyllosphere microbial community indicated that the phyllosphere bacterial community was most affected by the severity of disease. Our results suggested that with the development of cucumber powdery mildew, the symbiotic relationship between species was broken, and the entire bacterial community tended to compete.

The aboveground parts of terrestrial plants, collectively called the phyllosphere, have a key role in the global balance of atmospheric carbon dioxide and oxygen. The phyllosphere represents one of the most abundant habitats for microbiota colonization. Whether and how plants control phyllosphere microbiota to ensure plant health is not well understood. Here we show that the Arabidopsis quadruple mutant ( min7 fls2 efr cerk1 ; hereafter, mfec ) 1 , simultaneously defective in pattern-triggered immunity and the MIN7 vesicle-trafficking pathway, or a constitutively activated cell death1 ( cad1 ) mutant, carrying a S205F mutation in a membrane-attack-complex/perforin (MACPF)-domain protein, harbour altered endophytic phyllosphere microbiota and display leaf-tissue damage associated with dysbiosis. The Shannon diversity index and the relative abundance of Firmicutes were markedly reduced, whereas Proteobacteria were enriched in the mfec and cad1 S205F mutants, bearing cross-kingdom resemblance to some aspects of the dysbiosis that occurs in human inflammatory bowel disease. Bacterial community transplantation experiments demonstrated a causal role of a properly assembled leaf bacterial community in phyllosphere health. Pattern-triggered immune signalling, MIN7 and CAD1 are found in major land plant lineages and are probably key components of a genetic network through which terrestrial plants control the level and nurture the diversity of endophytic phyllosphere microbiota for survival and health in a microorganism-rich environment. Mutations in genes involved in immune signalling and vesicle trafficking cause defects in the leaf microbiome of Arabidopsis thaliana that result in damage to leaf tissues, suggesting mechanisms by which terrestrial plants control the level and diversity of endophytic phyllosphere microbiota.

We have explored the importance of the phyllosphere microbiome in plant resistance in the cuticle mutants bdg (BODYGUARD) or lacs2.3 (LONG CHAIN FATTY ACID SYNTHASE 2) that are strongly resistant to the fungal pathogen Botrytis cinerea. The study includes infection of plants under sterile conditions, 16S ribosomal DNA sequencing of the phyllosphere microbiome, and isolation and high coverage sequencing of bacteria from the phyllosphere. When inoculated under sterile conditions bdg became as susceptible as wild-type (WT) plants whereas lacs2.3 mutants retained the resistance. Adding washes of its phyllosphere microbiome could restore the resistance of bdg mutants, whereas the resistance of lacs2.3 results from endogenous mechanisms. The phyllosphere microbiome showed distinct populations in WT plants compared to cuticle mutants. One species identified as Pseudomonas sp isolated from the microbiome of bdg provided resistance to B. cinerea on Arabidopsis thaliana as well as on apple fruits. No direct activity was observed against B. cinerea and the action of the bacterium required the plant. Thus, microbes present on the plant surface contribute to the resistance to B. cinerea. These results open new perspectives on the function of the leaf microbiome in the protection of plants.

Background Plants can recruit beneficial microbes to enhance their ability to defend against pathogens. However, in contrast to the intensively studied roles of the rhizosphere microbiome in suppressing plant pathogens, the collective community-level change and effect of the phyllosphere microbiome in response to pathogen invasion remains largely elusive. Results Here, we integrated 16S metabarcoding, shotgun metagenomics and culture-dependent methods to systematically investigate the changes in phyllosphere microbiome between infected and uninfected citrus leaves by Diaporthe citri , a fungal pathogen causing melanose disease worldwide. Multiple microbiome features suggested a shift in phyllosphere microbiome upon D . citri infection, highlighted by the marked reduction of community evenness, the emergence of large numbers of new microbes, and the intense microbial network. We also identified the microbiome features from functional perspectives in infected leaves, such as enriched microbial functions for iron competition and potential antifungal traits, and enriched microbes with beneficial genomic characteristics. Glasshouse experiments demonstrated that several bacteria associated with the microbiome shift could positively affect plant performance under D . citri challenge, with reductions in disease index ranging from 65.7 to 88.4%. Among them, Pantoea asv90 and Methylobacterium asv41 identified as “recruited new microbes” in the infected leaves, exhibited antagonistic activities to D . citri  both in vitro and in vivo, including inhibition of spore germination and/or mycelium growth. Sphingomonas spp. presented beneficial genomic characteristics and were found to be the main contributor for the functional enrichment of iron complex outer membrane receptor protein in the infected leaves. Moreover, Sphingomonas asv20 showed a stronger suppression ability against D . citri in iron-deficient conditions than iron-sufficient conditions, suggesting a role of iron competition during their antagonistic action. Conclusions Overall, our study revealed how phyllosphere microbiomes differed between infected and uninfected citrus leaves by melanose pathogen, and identified potential mechanisms for how the observed microbiome shift might have helped plants cope with pathogen pressure. Our findings provide novel insights into understanding the roles of phyllosphere microbiome responses during pathogen challenge. BXFXiVHRdF5-go6BavLYay Video abstract

Pine wood nematode, Bursaphelenchus xylophilus, as one of the greatest threats to pine trees, is spreading all over the world. Plant microorganisms play an important role in the pathogenesis of nematodes. The phyllosphere and rhizosphere bacterial and fungal communities associated with healthy Pinus koraiensis (PKa) and P. koraiensis infected by B. xylophilus at the early (PKb) and last (PKc) stages were analyzed. Our results demonstrated that pine wood nematode (PWD) could increase the phyllosphere bacterial Pielou_e, Shannon, and Simpson index; phyllosphere fungal Chao 1 index, as well as rhizosphere bacterial Pielou_e, Shannon, and Simpson index; and rhizosphere fungal Pielou_e, Shannon, and Simpson index. What’s more, slight shifts of the microbial diversity were observed at the early stage of infection, and the microbial diversity increased significantly as the symptoms of infection worsened. With the infection of B. xylophilus in P. koraiensis, Bradyrhizobium (rhizosphere bacteria), Massilia (phyllosphere bacteria), and Phaeosphaeriaceae (phyllosphere fungi) were the major contributors to the differences in community compositions among different treatments. With the infection of PWD, most of the bacterial groups tended to be co-excluding rather than co-occurring. These changes would correlate with microbial ability to suppress plant pathogen, enhancing the understanding of disease development and providing guidelines to pave the way for its possible management.

Background Plants can retain atmospheric particulate matter (PM) through their unique foliar microstructures, which has a profound impact on the phyllosphere microbial communities. Yet, the underlying mechanisms linking atmospheric particulate matter (PM) retention by foliar microstructures to variations in the phyllosphere microbial communities remain a mystery. In this study, we conducted a field experiment with ten Ulmus lines. A series of analytical techniques, including scanning electron microscopy, atomic force microscopy, and high-throughput amplicon sequencing, were applied to examine the relationship between foliar surface microstructures, PM retention, and phyllosphere microbial diversity of Ulmus L. Results We characterized the leaf microstructures across the ten Ulmus lines. Chun exhibited a highly undulated abaxial surface and dense stomatal distribution. Langya and Xingshan possessed dense abaxial trichomes, while Lieye, Zuiweng, and Daguo had sparsely distributed, short abaxial trichomes. Duomai, Qingyun, and Lang were characterized by sparse stomata and flat abaxial surfaces, whereas Jinye had sparsely distributed but extensive stomata. The mean leaf retention values for total suspended particulate (TSP), PM 2.5 , PM 2.5-10 , PM 10-100 , and PM > 100 were 135.76, 6.60, 20.10, 90.98, and 13.08 µg·cm − 2 , respectively. Trichomes substantially contributed to PM 2.5 retention, while larger undulations enhanced PM 2.5-10 retention, as evidenced by positive correlations between PM 2.5 and abaxial trichome density and between PM 2.5-10 and the adaxial raw microroughness values. Phyllosphere microbial diversity patterns varied among lines, with bacteria dominated by Sediminibacterium and fungi by Mycosphaerella , Alternaria , and Cladosporium . Redundancy analysis confirmed that dense leaf trichomes facilitated the capture of PM 2.5 -associated fungi, while bacteria were less impacted by PM and struggled to adhere to leaf microstructures. Long and dense trichomes provided ideal microhabitats for retaining PM-borne microbes, as evidenced by positive feedback loops between PM 2.5 , trichome characteristics, and the relative abundances of microorganisms like Trichoderma and Aspergillus . Conclusions Based on our findings, a three-factor network profile was constructed, which provides a foundation for further exploration into how different plants retain PM through foliar microstructures, thereby impacting phyllosphere microbial communities.

Multicellular organisms, including plants, are colonized by microorganisms, some of which are beneficial to growth and health. The assembly rules for establishing plant microbiota are not well understood, and neither is the extent to which their members interact. We conducted drop-out and late introduction experiments by inoculating Arabidopsis thaliana with synthetic communities from a resource of 62 native bacterial strains to test how arrival order shapes community structure. As a read-out we tracked the relative abundance of all strains in the phyllosphere of individual plants. Our results showed that community assembly is historically contingent and subject to priority effects. Missing strains could, to various degrees, invade an already established microbiota, which was itself resistant and remained largely unaffected by latecomers. Additionally, our results indicate that individual strains of Proteobacteria ( Sphingomonas , Rhizobium ) and Actinobacteria ( Microbacterium , Rhodococcus ) have the greatest potential to affect community structure as keystone species. Conducting a series of removal experiments using synthetic leaf-inhabiting bacterial communities, the authors identify several keystone strains and show that priority effects drive phyllosphere community assembly.

AimsForest ecosystems provide a large area inhabited by functional microbial communities and thus have an important influence on nitrogen (N) cycling in terrestrial ecosystems. However, little is known about how tree species alter the functional microorganisms involved in the leaf phyllosphere and soil N cycling.MethodsThe impacts of seven common subtropical tree species across different mycorrhizal types and leaf phenology on the abundance of N cycling-related functional genes were evaluated in phyllosphere and soil.ResultsWe found that deciduous trees harbored significantly higher functional gene abundance of nifH, narK, and nrfA by 26.2–46.4% compared to evergreen trees in soils. Ectomycorrhizal trees harbored significantly higher gene abundance of nifH, AOA amoA, AOB amoA, nxrA, nxrB, comammox amoA, narG, narK, nirS, and nrfA by 22.1–131% in comparison to arbuscular mycorrhizal trees in soils. Leaf dry matter content, leaf C and N contents, and litter C and N contents were important drivers of soil N cycling-related functional genes. Nonetheless, there was no significant association between the N cycling-related functional genes in the phyllosphere and soil. Leaf phenology and mycorrhizal type had little effect on N cycling-related functional genes in the phyllosphere. Root density was the best predictor for leaf phyllosphere N cycling-related functional genes.ConclusionsOur results demonstrated that tree functional traits have a crucial role in driving leaf phyllosphere and soil functional microorganisms, and emphasized the potential of manipulating tree mycorrhizal type and taxonomic identity to increase ecosystem N retention in subtropical forests.