Table 1.
Summary of important studies associated with the leaf microbiome
| Host plant | Leaf microbiota/leaf microbe under study | Perturbation | Key findings | Reference |
|---|---|---|---|---|
| Microbial colonization | ||||
| Arabidopsis thaliana | Bacteria | – | Phyllosphere community profile of A. thaliana wild-type Landsberg erecta (Ler) and eceriferum (cer) mutants (cer1, cer6, cer9, and cer16) involved in cuticle biosynthesis. Plant cuticular wax composition affects the phyllosphere bacterial community. | Reisberg et al. (2013) |
| Faba bean (Vicia faba L.) and Arabidopsis thaliana | Pseudomonas syringae DC3118, a coronatine-deficient mutant of Pseudomonas syringae DC3000 | – | In a specific environmental setting, leaf surface colonization by bacteria correlated with stomatal aperture regulation. | Ou et al. (2014) |
| Bean (Phaseolus vulgaris L.) | P. syringae pv. syringae B728a | – | Biosurfactant, syringafactin, produced by P. syringae pv. syringae B728a on leaves adsorbed on waxy leaf cuticle surface. Provide benefit to bacteria by attracting moisture and aid in nutrient availability. | Burch et al. (2014) |
| Arabidopsis thaliana | Pseudomonas syringae DC3000 | – | Humidity-controlled, pathogen-guided establishment of an aqueous intercellular space (apoplast) as an important step in leaf bacterial infection. | Xin et al. (2016) |
| Microbial composition and diversity | ||||
| Sugar beet (Beta vulgaris) | Bacteria, yeasts, and filamentous fungi | – | Seasonal dynamics over a growing season. Fungi: Cladosporium and Alternaria sp. | Thompson et al. (1993) |
| Yeast: Cryptococcus and Sporobolomyces Bacteria: Pseudomonas sp. and Erwinia herbicola |
||||
| Cacao (Theobroma cacao) | Fungi (endophytes) | Phytophthora sp. | High diversity, spatial structure, and host affinity among foliar endophytes.
Endophyte-mediated protection against foliar pathogen. |
Arnold et al. (2003) |
| Common wood sorrel (Oxalis acetosella L.) | Yeast (epiphytes) | – | Seasonal dynamics of yeasts. Species diversity—maximum in autumn; minimum in spring. |
Glushakova and Chernov (2004) |
| Rhodotorula glutinis and Sporobolomyces roseus species abundant throughout the year. | ||||
| Loblolly pine (Pinus taeda) | Fungi (endophytes) | – | High diversity of foliar fungal endophytes. | Arnold et al. (2007) |
| Arabidopsis thaliana, Trifolium repens, and Glycine max | Bacteria | – | Metaproteogenomic analysis found consistency in three plant species. | Delmotte et al. (2009) |
| High abundance of Sphingomonas sp. and Methylobacterium sp. | ||||
| Important role of the one-carbon metabolism and transport processes in the microbiota. | ||||
| Tree species | Bacteria (epiphytes) | – | In trees, interspecies variation is more than intraspecies variation in bacterial communities. | Redford et al. (2010) |
| Correlation between tree phylogeny and bacterial community composition. | ||||
| Maize | Bacteria (epiphytes) | Southern leaf blight (SLB) | A specific set of epiphytic bacteria can restrict phyllosphere bacterial diversity and increase resistance to Southern leaf blight (SLB) fungal infection. | Balint-Kurti et al. (2010) |
| Eucalyptus citriodora Hook | Fungi (epiphytes and edophytes) | – | Total 33 fungal species assigned to 33 taxa (endophytes, 20; epiphytes, 22). | Kharwar et al. (2010) |
| Difference in frequency of colonization. Antagonism against human and plant pathogen. | ||||
| Lettuce | Bacteria | – | Bacterial community composition by pyrosequencing. Proteobacteria, Firmicutes, Bacteroidetes, and Actinobacteria—most abundant phyla. Insights on variability in bacterial community profile with respect to time, space, and environment. | Rastogi et al. (2012) |
| Common bean (Phaseolus vulgaris) | Bacteria (endophytes) | – | 158 culturable endophytic bacteria. Phyla distribution 36.7% Proteobacteria, 32.9% Firmicutes, 29.7% Actinobacteria, and 0.6% Bacteroidetes | de Oliveira Costa et al. (2012) |
| Arabidopsis thaliana | Bacteria (epiphytes and endophytes) | – | Proteobacteria, Actinobacteria, and Bacteroidetes were found most abundant. Massilia and Flavobacterium are prevalent genera | Bodenhausen et al. (2013) |
| Tomato (Solanum lycopersicum L.) | Bacteria (epiphytes) | – | Members of endophytic bacterial communities of tomato leaves exert multiple effects on growth and health of tomato plants. | Romero et al. (2014) |
| Neotropical forest | Bacteria | – | Dominated bacterial communities: Actinobacteria, Alpha-, Beta-, Gammaproteobacteria, and Sphingobacteria. Correlation of bacterial community with host growth, mortality, and function. | Kembel et al. (2014) |
| Arabidopsis thaliana | Bacteria | – | Taxonomic and functional overlap of leaf and root bacterial communities. Soil as main driver for bacterial members.. | Bai et al. (2015) |
| Rice (Oryza sativa L.) | Actinomycetes | Pyricularia oryzae (syn. Magnaporthe oryzae) | Rice phyllosphere-associated actinomycetes produce bioactive compounds and control leaf blast disease caused by Pyricularia oryzae. | Harsonowati et al. (2017) |
| Sugar maple (Acer saccharum) | Bacteria and fungi (epiphytes and endophytes) | – | Microbial communities at the edge of the species’ elevational range differ from those within the natural range. | Wallace et al. (2018) |
| Poplar tree | Bacteria and fungi (epiphytes and endophytes) | Mercury | Methylobacterium, Kineococcus, Sphingomonas, and Hymenobacter on the leaf surface. | Durand et al. (2018) |
| Mussaenda pubescens var. alba | Fungi | – | Dothideomycetes and Eurotiomycetes are dominant members. Intraspecific host genetic identity, primary driver in shaping regional phyllosphere fungal communities. | Qian et al. (2018) |
| Arabidopsis thaliana | Bacteria | – | Determined biosynthetic potential of 224 bacterial strains from Arabidopsis leaf microbiome. Phyllosphere as a valuable resource for the identification and characterization of antibiotics and natural products. | Helfrich et al. (2018) |
| Tomato (Solanum lycopersicum L.) | Bacteria (epiphytes) | – | Comprehensive view of the tomato-associated bacterial community. | Dong et al. (2019) |
| Isolation of beneficial bacterial for future functional studies. | ||||
| Mangrove | Fungi (epiphytes and endophytes) | – | Dothideomycetes and Tremellomycetes are dominant members. Plant identity significantly affects endophytic but not epiphytic fungi. | Yao et al. (2019) |
| Catharanthus roseus | Fungi (Endophytes) | – | Colletotrichum, Alternaria, and Chaetomium are common genera. | Dhayanithy et al. (2019) |
| Biofilm | ||||
| Common bean (Phaseolus vulgaris) | P. syringae pv. syringae | – | Cause of brown spot disease of bean leaves was the result of biofilm formation of P. syringae. | Monier and Lindow (2004) |
| Citrus limon ‘Eureka’ | Xanthomonas axonopodis pv. citri | – | Motility and role of flagellum is required for mature biofilm and canker development. | Malamud et al. (2011) |
| Tomato (Solanum lycopersicum L.) | Xanthomonas vesicatoria | – | Aggressiveness of Xv strains correlated with their ability to move by flagella or type IV pili, adherence to leaves and form well-developed biofilms, help in improved phyllosphere colonization. | Felipe et al. (2018) |
| Tomato (Solanum lycopersicum L.) | Bacillus amyloliquefaciens | Botrytis cinerea | Reduction of biocontrol of BBC 023 on leaves due to its limited ability to generate robust biofilms and colonization in the phylloplane. | Salvatierra-Martinez et al. (2018) |
| Quorum sensing | ||||
| Tomato (Solanum lycopersicum L.) | Bacteria | – | Culturable leaf-associated bacteria community with BCA activity against tomato disease have the ability to produce AHL and IAA. | Enya et al. (2007) |
| Tobacco (Nicotiana tobacum) | Epiphytes | – | AHLs induced variation in the bacterial community composition. Pseudomonas and other AHL-producing Gammaproteobacteria use QS signals for their survival and protection. | Lv et al. (2012) |
| Tobacco (Nicotiana tobacum), common bean (Phaseolus vulgaris) | Pseudomonas syringae | – | QS-mediated control of motility and exopolysaccharide synthesis was observed for their role in biofilm formation and colonization of bacteria on leaf. | Quiñones et al. (2005) |
| Microbe–microbe–host interactions | ||||
| Arabidopsis thaliana | Hyaloperonospora parasitica subsp., Arabidopsis thaliana, H. parasitica subsp. Brassica oleracea, Bremia lactucae, and Albugo candida | – | Albugo candida suppressed defense signaling pathways in the host, facilitating sporulation by the incompatible downy mildews | Cooper et al., (2002) |
| Quercus robur L. | Foliar fungi and bacteria | Erysiphe alphitoides | Direct interaction between E. alphitoides and 13 fungal and bacterial operational taxonomic units (OTUs). Fungal endophytes Mycosphaerella punctiformis and Monochaetia kansensis could be possible antagonists of E. alphitoides. | Jakuschkin et al. (2016) |
| Arabidopsis thaliana | - | Phytophthora infestans: Albugo laibachii | Prior colonization of host by A. laibachii, helps P. infestans to infect an essentially non-host plant. | Belhaj et al., (2017) |
| Phaseolus lunatus | Endophytic fungi for e.g. Rhizopus, Fusarium, Penicillium, Cochliobolus, and Artomyces spp. | Pseudomonas syringae pv. syringae, Enterobacter sp. strain FCB1, and the fungus Colletotrichum lindemuthianum | Order of arrival of fungal endophytes and pathogens on the plant surface can determine disease resistance or facilitation. | Adame-Alvarez et al. (2014) |
| Zea mays | Endophyte Fusarium verticillioides | Ustilago maydis | F. verticillioides can inhibit U. maydis disease progression by direct interaction. | Lee et al. (2009) |
| Olive plants (Olea europaea) | Pseudomonas savastanoi pv. savastanoi (olive knot pathogen) and Erwinia toletana (olive knot cooperator). | The bacteria stabilize the community, exchange QS signals, and this cooperation results in disease aggression. | Caballo-Ponce et al. (2018) | |
| Arabidopsis thaliana | Basidiomycete yeast, Dioszegia sp. | Albugo laibachii | Construction of an extensive phyllosphere microbial network encompassing bacterial, fungal, and oomycetal communities. Presence of Dioszegia sp. is positively correlated with that of A. laibachii. | Agler et al. (2016) |
| Arabidopsis thaliana | Basidiomycete yeast, Moesziomyces albugensis | Albugo laibachii | Moesziomyces albugensis antagonizes A. laibachii on the host leaf surface. | Eitzen et al. (2020) |
| Innate immunity interaction | ||||
| Arabidopsis thaliana | Bacteria | – | The author showed evidence of ethylene signaling (ein2) affecting the abundance of Variovorax. | Bodenhausen et al, (2014) |
| Arabidopsis thaliana | Bacteria | – | Affected diversity of Firmicutes sp. and Proteobacteria sp. in min7 fls2 efr cerk1 (mfec) and constitutively activated cell death1 (cat1) mutants (involving PTI, MIN7 vesicle trafficking, or cell death pathways). | Chen et al. (2020) |
| Arabidopsis thaliana | Streptomyces AgN23. | Alternaria brassicicola | The bacteria Streptomyces induces defense responses, which prevents Alternaria infection. | Vergnes et al. (2020) |
| Tomato (Solanum lycopersicum, Solanum pimpinellifolium) | Bacteria | – | Host resistance shapes leaf microbiota under environmental fluctuations and is time dependent. | Morella et al. (2020) |
| Cucumber Cucumis sativus (Suyan 10) | Bacteria and fungi | Pseudomonas syringae pv. Lachrymans | Plant-specific microbes such as Sphingomonas, Methylobacterium, Pseudomonas, and Alternaria are significantly affected by the causal agent of angular leaf-spot of cucumber at different infection stages. | Luo et al. (2019) |
| Pepper (Capsicum annuum L.) | Bacillus thuringiensis | – | Significant changes of phyllosphere microbiota in Firmicutes and Gammaproteobacteria. | Zhang et al. (2008) |
| Grapevine (Vitis vinifera) | Bacteria | Botrytis cinerea, Phytophthora infestans | Potential biocontrol agents (Bacillus, Variovorax, Pantoea, Staphylococcus, Herbaspirillum, Sphingomonas) from leaf microbiome acting against phytopathogens. | Bruisson et al. (2019) |
| Wheat (Triticum aestivum) | Bacteria and fungi | Zymoseptoria tritici | Microbial dynamics upon infection | Kerdraon et al. (2019 |
| Tobacco (Nicotiana sp.) | Bacteria | Pseudomonas syringae pv. tabaci | The application of two BCAs changed the bacterial phyllosphere community and decreased bacterial wildfire outbreak. | Qin et al. (2019) |