[en] Phyllosphere microbial communities inhabit the aerial plant parts, such as leaves and flowers, where they form complex molecular interactions with the host plant. Contrary to the relatively well-studied rhizosphere microbiome, scientists are just starting to understand, and potentially utilize, the phyllosphere microbiome. In this article, we summarize the recent studies that have provided novel insights into the mechanism of the host genotype shaping the phyllosphere microbiome and the possibility to select a stable and well-adapted microbiome. We also discuss the most pressing gaps in our knowledge and identify the most promising research directions and tools for understanding the assembly and function of phyllosphere microbiomes - this understanding is necessary if we are to harness phyllosphere microbiomes for improving plant growth and health in managed systems.
Shakir, Sara ; Université de Liège - ULiège > Département GxABT > Plant Sciences
Zaidi, Syed Shan-E-Ali; Plant Genetics, TERRA Teaching and Research Center, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium
de Vries, Franciska T; Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands
Mansoor, Shahid; Agricultural Biotechnology Division, National Institute for Biotechnology and Genetic Engineering, Faisalabad, Pakistan. Electronic address: shahidmansoor7@gmail.com
F.R.S.-FNRS - Fonds de la Recherche Scientifique WBI - Wallonie-Bruxelles International
Funding text :
The authors acknowledge financial support from the Belgian FNRS (Fonds de la Recherché Scientifique) grant number 1.B456.20 to S.S.Z.; and WBI ( Wallonie-Bruxelles International ) Excellence Scholarship to S.S.The authors acknowledge financial support from the Belgian FNRS (Fonds de la Recherch? Scientifique) grant number 1.B456.20 to S.S.Z.; and WBI (Wallonie-Bruxelles International) Excellence Scholarship to S.S.
Vorholt, J.A., Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10 (2012), 828–840.
Andrews, J.H., Harris, R.F., The ecology and biogeography of microorganisms on plant surfaces. Annu. Rev. Phytopathol. 38 (2000), 145–180.
Delmotte, N., et al. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 16428–16433.
Knief, C., et al. Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J. 6 (2012), 1378–1390.
Grady, K.L., et al. Assembly and seasonality of core phyllosphere microbiota on perennial biofuel crops. Nat. Commun., 10, 2019, 4135.
Knief, C., et al. Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J. 4 (2010), 719–728.
Morris, C.E., et al. Movement of bioaerosols in the atmosphere and the consequences for climate and microbial evolution. Aerosol Science, 2013, Wiley, 393–415.
Lopez-Velasco, G., et al. Changes in spinach phylloepiphytic bacteria communities following minimal processing and refrigerated storage described using pyrosequencing of 16S rRNA amplicons. J. Appl. Microbiol. 110 (2011), 1203–1214.
Rastogi, G., et al. Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J. 6 (2012), 1812–1822.
Bulgarelli, D., et al. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64 (2013), 807–838.
Chung, S.H., et al. Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 15728–15733.
Humphrey, P.T., et al. Diversity and abundance of phyllosphere bacteria are linked to insect herbivory. Mol. Ecol. 23 (2014), 1497–1515.
Muller, D.B., et al. The plant microbiota: systems-level insights and perspectives. Annu. Rev. Genet. 50 (2016), 211–234.
Pieterse, C.M.J., et al. The soil-borne supremacy. Trends Plant Sci. 21 (2016), 171–173.
Wagner, M.R., et al. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat. Commun., 7, 2016, 12151.
Aydogan, E.L., et al. Long-term warming shifts the composition of bacterial communities in the phyllosphere of galium album in a permanent grassland field-experiment. Front. Microbiol., 9, 2018, 144.
Laforest-Lapointe, I., et al. Leaf bacterial diversity mediates plant diversity and ecosystem function relationships. Nature 546 (2017), 145–147.
Kim, M., et al. Distinctive phyllosphere bacterial communities in tropical trees. Microb. Ecol. 63 (2012), 674–681.
Redford, A.J., et al. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ. Microbiol. 12 (2010), 2885–2893.
Bodenhausen, N., et al. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genet., 10, 2014, e1004283.
Chen, T., et al. A plant genetic network for preventing dysbiosis in the phyllosphere. Nature 580 (2020), 653–657.
Farré-Armengol, G., et al. Bidirectional interaction between phyllospheric microbiotas and plant volatile emissions. Trends Plant Sci. 21 (2016), 854–860.
Horton, M.W., et al. Genome-wide association study of Arabidopsis thaliana leaf microbial community. Nat. Commun., 5, 2014, 5320.
Xin, X.F., et al. Bacteria establish an aqueous living space in plants crucial for virulence. Nature 539 (2016), 524–529.
Aragón, W., et al. The intimate talk between plants and microorganisms at the leaf surface. J. Exp. Bot. 68 (2017), 5339–5350.
Mang, H.G., et al. The arabidopsis resurrection1 gene regulates a novel antagonistic interaction in plant defense to biotrophs and necrotrophs. Plant Physiol. 151 (2009), 290–305.
Reisberg, E.E., et al. Distinct phyllosphere bacterial communities on Arabidopsis wax mutant leaves. PLoS One, 8, 2013, e78613.
Ritpitakphong, U., et al. The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. New Phytol. 210 (2016), 1033–1043.
Fuchs, G., et al. Microbial degradation of aromatic compounds – from one strategy to four. Nat. Rev. Microbiol. 9 (2011), 803–816.
Kolton, M., et al. Comparative genomic analysis indicates that niche adaptation of terrestrial flavobacteria is strongly linked to plant glycan metabolism. PLoS One, 8, 2013, e76704.
Leveau, J.H.J., Lindow, S.E., Appetite of an epiphyte: quantitative monitoring of bacterial sugar consumption in the phyllosphere. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 3446–3453.
Ryffel, F., et al. Metabolic footprint of epiphytic bacteria on Arabidopsis thaliana leaves. ISME J. 10 (2016), 632–643.
Gao, Y., et al. Volatile organic compounds and their roles in bacteriostasis in five conifer species. J. Integr. Plant Biol. 47 (2005), 499–507.
Utama, I.M., et al. In vitro efficacy of plant volatiles for inhibiting the growth of fruit and vegetable decay microorganisms. J. Agric. Food Chem. 50 (2002), 6371–6377.
Kawaguchi, K., et al. Yeast methylotrophy and autophagy in a methanol-oscillating environment on growing Arabidopsis thaliana leaves. PLoS One, 6, 2011, e25257.
Fall, R., Benson, A.A., Leaf methanol – the simplest natural product from plants. Trends Plant Sci. 1 (1996), 296–301.
Nagatoshi, Y., Nakamura, T., Arabidopsis HARMLESS TO OZONE LAYER protein methylates a glucosinolate breakdown product and functions in resistance to Pseudomonas syringae pv. maculicola. J. Biol. 284 (2009), 19301–19309.
Carvalhais, L.C., et al. Linking plant nutritional status to plant-microbe interactions. PLoS One, 8, 2013, e68555.
Pant, B.D., et al. Identification of primary and secondary metabolites with phosphorus status-dependent abundance in Arabidopsis, and of the transcription factor PHR1 as a major regulator of metabolic changes during phosphorus limitation. Plant Cell Environ. 38 (2015), 172–187.
Weibull, J., et al. Free amino acid composition of leaf exudates and phloem sap: a comparative study in oats and barley. Plant Physiol. 92 (1990), 222–226.
Hiruma, K., et al. Root endophyte colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165 (2016), 464–474.
Karamanoli, K., et al. Bacterial colonization of the phyllosphere of nineteen plant species and antimicrobial activity of their leaf secondary metabolites against leaf associated bacteria. Chemoecology 15 (2005), 59–67.
Vacher, C., et al. The phyllosphere: microbial jungle at the plant–climate interface. Annu. Rev. Ecol. Evol. Syst. 47 (2016), 1–24.
Pillitteri, L.J., Dong, J., Stomatal development in Arabidopsis. Arabidopsis book. 11, 2013, e0162.
Zhao, Q., Chen, X.-Y., Development: a new function of plant trichomes. Nat. Plants, 2, 2016, 16096.
Guo, W.J., et al. SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol. 164 (2014), 777–789.
Sharma, T., et al. The ALMT family of organic acid transporters in plants and their involvement in detoxification and nutrient security. Front. Plant Sci., 7, 2016, 1488.
Dündar, E., Bush, D.R., BAT1, a bidirectional amino acid transporter in Arabidopsis. Planta 229 (2009), 1047–1056.
Hirner, A., et al. Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18 (2006), 1931–1946.
Ladwig, F., et al. Siliques are Red1 from Arabidopsis acts as a bidirectional amino acid transporter that is crucial for the amino acid homeostasis of siliques. Plant Physiol. 158 (2012), 1643–1655.
Liu, H., et al. Microbiome-mediated stress resistance in plants. Trends Plant Sci. 25 (2020), 733–743.
Levy, A., et al. Genomic features of bacterial adaptation to plants. Nat. Genet. 50 (2017), 138–150.
Macho, A.P., Zipfel, C., Plant PRRs and the activation of innate immune signaling. Mol. Cell 54 (2014), 263–272.
Vogel, C., et al. The Arabidopsis leaf transcriptome reveals distinct but also overlapping responses to colonization by phyllosphere commensals and pathogen infection with impact on plant health. New Phytol. 212 (2016), 192–207.
Hall, A.B., et al. Human genetic variation and the gut microbiome in disease. Nat. Rev. Genet. 18 (2017), 690–699.
Levy, M., et al. Dysbiosis and the immune system. Nat. Rev. Immunol. 17 (2017), 219–232.
Carvalhais, L.C., et al. Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Mol. Plant-Microbe Interact. 28 (2015), 1049–1058.
Lebeis, S.L., et al. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349 (2015), 860–864.
Pieterse, C.M., et al. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5 (2009), 308–316.
Pieterse, C.M., et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52 (2014), 347–375.
Kniskern, J.M., et al. Salicylic acid and jasmonic acid signaling defense pathways reduce natural bacterial diversity on Arabidopsis thaliana. Mol. Plant-Microbe Interact. 20 (2007), 1512–1522.
Miche, L., et al. Upregulation of jasmonate-inducible defense proteins and differential colonization of roots of Oryza sativa cultivars with the endophyte Azoarcus sp. Mol. Plant-Microbe Interact. 19 (2006), 502–511.
Nakagawa, T., Kawaguchi, M., Shoot-applied MeJA suppresses root nodulation in Lotus japonicus. Plant Cell Physiol. 47 (2006), 176–180.
Carvalhais, L.C., et al. Activation of the jasmonic acid plant defence pathway alters the composition of rhizosphere bacterial communities. PLoS One, 8, 2013, e56457.
Iniguez, A.L., et al. Regulation of enteric endophytic bacterial colonization by plant defenses. Mol. Plant-Microbe Interact. 18 (2005), 169–178.
Janda, M., et al. Temporary heat stress suppresses PAMP-triggered immunity and resistance to bacteria in Arabidopsis thaliana. Mol. Plant Pathol. 20 (2019), 1005–1012.
MacQueen, A., Bergelson, J., Modulation of R-gene expression across environments. J. Exp. Bot. 67 (2016), 2093–2105.
Singh, P., et al. Environmental history modulates arabidopsis pattern-triggered immunity in a histone acetyltransferase1-dependent manner. Plant Cell 26 (2014), 2676–2688.
Liu, Y., et al. Arbuscular mycorrhiza fungi increased the susceptibility of Astragalus adsurgens to powdery mildew caused by Erysiphe pisi. Mycology 9 (2018), 223–232.
Robert-Seilaniantz, A., et al. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49 (2011), 317–343.
Castrillo, G., et al. Root microbiota drive direct integration of phosphate stress and immunity. Nature 543 (2017), 513–518.
Stringlis, I.A., et al. MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc. Natl. Acad. Sci. U. S. A. 115 (2018), 5213–5222.
Cheng, C., et al. Plant immune response to pathogens differs with changing temperatures. Nat. Commun., 4, 2013, 2530.
Hacquard, S., et al. Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. Nat. Commun., 7, 2016, 11362.
Wang, W., et al. Timing of plant immune responses by a central circadian regulator. Nature 470 (2011), 110–114.
Shin, J., et al. TIME FOR COFFEE represses accumulation of the MYC2 transcription factor to provide time-of-day regulation of jasmonate signaling in Arabidopsis. Plant Cell 24 (2012), 2470–2482.
Zhang, C., et al. Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog., 9, 2013, e1003370.
Berendsen, R.L., et al. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J. 12 (2018), 1496–1507.
Duran, P., et al. Microbial interkingdom interactions in roots promote arabidopsis survival. Cell 175 (2018), 973–983.e14.
Kwak, M.J., et al. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat. Biotechnol. 36 (2018), 1100–1109.
Vorholt, J.A., et al. Establishing causality: opportunities of synthetic communities for plant microbiome research. Cell Host Microbe 22 (2017), 142–155.
Gargallo-Garriga, A., et al. Shifts in plant foliar and floral metabolomes in response to the suppression of the associated microbiota. BMC Plant Biol., 16, 2016, 78.
Müller, D.B., et al. Systems-level proteomics of two ubiquitous leaf commensals reveals complementary adaptive traits for phyllosphere colonization. Mol. Cell. Proteomics 15 (2016), 3256–3269.
Lambais, M.R., et al. Phyllosphere metaproteomes of trees from the Brazilian Atlantic Forest show high levels of functional redundancy. Microb. Ecol. 73 (2017), 123–134.
Liu, H., et al. Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front. Microbiol., 8, 2017, 2552.
Finkel, O.M., et al. Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl. Environ. Microbiol. 77 (2011), 7647–7655.
Smets, W., et al. Impact of urban land use on the bacterial phyllosphere of ivy (Hedera sp.). Atmospheric 147 (2016), 376–383.
Castaneda, L.E., et al. Effects of agricultural management on phyllosphere fungal diversity in vineyards and the association with adjacent native forests. Peer J., 6, 2018, e5715.
Bowers, R.M., et al. Spatial variability in airborne bacterial communities across land-use types and their relationship to the bacterial communities of potential source environments. ISME J. 5 (2011), 601–612.
Eschen, R., et al. The foliar endophytic fungal community composition in Cirsium arvense is affected by mycorrhizal colonization and soil nutrient content. Fungal Biol. 114 (2010), 991–998.
Poosakkannu, A., et al. Native arbuscular mycorrhizal symbiosis alters foliar bacterial community composition. Mycorrhiza 27 (2017), 801–810.
Koskella, B., Brockhurst, M.A., Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38 (2014), 916–931.
Weinbauer, M.G., Rassoulzadegan, F., Are viruses driving microbial diversification and diversity?. Environ. Microbiol. 6 (2004), 1–11.
Mueller, U.G., Sachs, J.L., Engineering microbiomes to improve plant and animal health. Trends Microbiol. 23 (2015), 606–617.
Wu, J., et al. Purple phototrophic bacterium enhances stevioside yield by Stevia rebaudiana Bertoni via foliar spray and rhizosphere irrigation. PLoS One, 8, 2013, e67644.
Morella, N.M., et al. Successive passaging of a plant-associated microbiome reveals robust habitat and host genotype-dependent selection. Proc. Natl. Acad. Sci. U. S. A. 117 (2020), 1148–1159.
Ferreira, J.L., et al. Gamma-proteobacteria eject their polar flagella under nutrient depletion, retaining flagellar motor relic structures. PLoS Biol., 17, 2019, e3000165.
