Shaping the leaf microbiota: plant–microbe–microbe interactions

Journal of Experimental Botany - Tập 72 Số 1 - Trang 36-56 - 2021
Vasvi Chaudhry1, Paul Runge1,2, Priyamedha Sengupta3, Gunther Doehlemann3, Jane E. Parker3, Eric Kemen1
1Department of Microbial Interactions, IMIT/ZMBP, University of Tübingen, Tübingen, Germany
2Max Planck Institute for Plant Breeding Research, Köln, Germany
3Institute for Plant Sciences and Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, Center for Molecular Biosciences, Cologne, Germany

Tóm tắt

AbstractThe aerial portion of a plant, namely the leaf, is inhabited by pathogenic and non-pathogenic microbes. The leaf’s physical and chemical properties, combined with fluctuating and often challenging environmental factors, create surfaces that require a high degree of adaptation for microbial colonization. As a consequence, specific interactive processes have evolved to establish a plant leaf niche. Little is known about the impact of the host immune system on phyllosphere colonization by non-pathogenic microbes. These organisms can trigger plant basal defenses and benefit the host by priming for enhanced resistance to pathogens. In most disease resistance responses, microbial signals are recognized by extra- or intracellular receptors. The interactions tend to be species specific and it is unclear how they shape leaf microbial communities. In natural habitats, microbe–microbe interactions are also important for shaping leaf communities. To protect resources, plant colonizers have developed direct antagonistic or host manipulation strategies to fight competitors. Phyllosphere-colonizing microbes respond to abiotic and biotic fluctuations and are therefore an important resource for adaptive and protective traits. Understanding the complex regulatory host–microbe–microbe networks is needed to transfer current knowledge to biotechnological applications such as plant-protective probiotics.

Từ khóa


Tài liệu tham khảo

Adame-Álvarez, 2014, Order of arrival shifts endophyte–pathogen interactions in bean from resistance induction to disease facilitation, FEMS Microbiology Letters, 355, 100, 10.1111/1574-6968.12454

Agler, 2016, Microbial hub taxa link host and abiotic factors to plant microbiome variation, PLoS Biology, 14, e1002352, 10.1371/journal.pbio.1002352

Aragón, 2017, The intimate talk between plants and microorganisms at the leaf surface, Journal of Experimental Botany, 68, 5339, 10.1093/jxb/erx327

Arnaud, 2015, A sophisticated network of signaling pathways regulates stomatal defenses to bacterial pathogens, Molecular Plant, 8, 566, 10.1016/j.molp.2014.10.012

Arnold, 2007, Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR, Mycologia, 99, 185, 10.1080/15572536.2007.11832578

Arnold, 2003, Fungal endophytes limit pathogen damage in a tropical tree, Proceedings of the National Academy of Sciences, USA, 100, 15649, 10.1073/pnas.2533483100

Astudillo-García, 2017, Evaluating the core microbiota in complex communities: a systematic investigation, Environmental Microbiology, 19, 1450, 10.1111/1462-2920.13647

Aung, 2018, The role of water in plant–microbe interactions, The Plant Journal, 93, 771, 10.1111/tpj.13795

Bai, 2015, Functional overlap of the Arabidopsis leaf and root microbiota, Nature, 528, 364, 10.1038/nature16192

Bailly, 2017, Mining the volatilomes of plant-associated microbiota for new biocontrol solutions, Frontiers in Microbiology, 8, 1638, 10.3389/fmicb.2017.01638

Bakker, 2013, Induced systemic resistance and the rhizosphere microbiome, The Plant Pathology Journal, 29, 136, 10.5423/PPJ.SI.07.2012.0111

Baldotto, 2008, Phylloepiphytic interaction between bacteria and different plant species in a tropical agricultural system, Canadian Journal of Microbiology, 54, 918, 10.1139/W08-087

Balint-Kurti, 2010, Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection, Molecular Plant-Microbe Interactions, 23, 473, 10.1094/MPMI-23-4-0473

Balogh, 2018, Relative level of bacteriophage multiplication in vitro or in phyllosphere may not predict in planta efficacy for controlling bacterial leaf spot on tomato caused by Xanthomonas perforans, Frontiers in Microbiology, 9, 2176, 10.3389/fmicb.2018.02176

Bao, 2020, Seasonal variation of epiphytic bacteria in the phyllosphere of Gingko biloba, Pinus bungeana and Sabina chinensis, FEMS Microbiology Ecology, 96, fiaa017, 10.1093/femsec/fiaa017

Barda, 2015, Pseudozyma aphidis induces salicylic-acid-independent resistance to Clavibacter michiganensis in tomato plants, Plant Disease, 99, 621, 10.1094/PDIS-04-14-0377-RE

Beattie, 1999, Bacterial colonization of leaves: a spectrum of strategies, Phytopathology, 89, 353, 10.1094/PHYTO.1999.89.5.353

Belhaj, 2017, Arabidopsis late blight: infection of a nonhost plant by Albugo laibachii enables full colonization by Phytophthora infestans, Cellular Microbiology, 19, e12628, 10.1111/cmi.12628

Beuchat, 2002, Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables, Microbes and Infection, 4, 413, 10.1016/S1286-4579(02)01555-1

Bi, 2017, MAP kinase signaling pathways: a hub of plant–microbe interactions, Cell Host & Microbe, 21, 270, 10.1016/j.chom.2017.02.004

Bigeard, 2015, Signaling mechanisms in pattern-triggered immunity (PTI), Molecular Plant, 8, 521, 10.1016/j.molp.2014.12.022

Bodenhausen, 2014, A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota, PLoS Genetics, 10, e1004283, 10.1371/journal.pgen.1004283

Bodenhausen, 2013, Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana, PLoS One, 8, e56329, 10.1371/journal.pone.0056329

Bogino, 2013, The role of bacterial biofilms and surface components in plant–bacterial associations, International Journal of Molecular Sciences, 14, 15838, 10.3390/ijms140815838

Boutrot, 2017, Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance, Annual Review of Phytopathology, 55, 257, 10.1146/annurev-phyto-080614-120106

Braga, 2016, Microbial interactions: ecology in a molecular perspective, Brazilian Journal of Microbiology, 47, 86, 10.1016/j.bjm.2016.10.005

Brandl, 2002, Fitness of Salmonella enterica serovar Thompson in the Cilantro phyllosphere, Applied and Environmental Microbiology, 68, 3614, 10.1128/AEM.68.7.3614-3621.2002

Branine, 2019, Biology and applications of endophytic insect-pathogenic fungi, PLoS Pathogens, 15, e1007831, 10.1371/journal.ppat.1007831

Bringel, 2015, Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics, Frontiers in Microbiology, 6, 486, 10.3389/fmicb.2015.00486

Bruisson, 2019, Endophytes and epiphytes from the grapevine leaf microbiome as potential biocontrol agents against phytopathogens, Frontiers in Microbiology, 10, 2726, 10.3389/fmicb.2019.02726

Brunings, 2003, Xanthomonas citri: breaking the surface, Molecular Plant Pathology, 4, 141, 10.1046/j.1364-3703.2003.00163.x

Bunster, 1989, Effect of surface-active Pseudomonas spp. on leaf wettability, Applied and Environmental Microbiology, 55, 1340, 10.1128/AEM.55.6.1340-1345.1989

Burch, 2011, Comparison of biosurfactant detection methods reveals hydrophobic surfactants and contact-regulated production, Environmental Microbiology, 13, 2681, 10.1111/j.1462-2920.2011.02534.x

Burch, 2012, Pseudomonas syringae coordinates production of a motility-enabling surfactant with flagellar assembly, Journal of Bacteriology, 194, 1287, 10.1128/JB.06058-11

Burch, 2014, The hygroscopic biosurfactant syringafactin produced by Pseudomonas syringae enhances fitness on leaf surfaces during fluctuating humidity, Environmental Microbiology, 16, 2086, 10.1111/1462-2920.12437

Burdett, 2019, The plant ‘resistosome’: structural insights into immune signaling, Cell Host & Microbe, 26, 193, 10.1016/j.chom.2019.07.020

Busby, 2015, Genetics-based interactions among plants, pathogens, and herbivores define arthropod community structure, Ecology, 96, 1974, 10.1890/13-2031.1

Busby, 2016, Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity, New Phytologist, 209, 1681, 10.1111/nph.13742

Buswell, 2018, Chemical priming of immunity without costs to plant growth, New Phytologist, 218, 1205, 10.1111/nph.15062

Caballo-Ponce, 2018, Quorum sensing in Pseudomonas savastanoi pv. savastanoi and Erwinia toletana: role in virulence and interspecies interactions in the olive knot, Applied and Environmental Microbiology, 84, 10.1128/AEM.00950-18

Cawoy, 2014, Plant defense stimulation by natural isolates of Bacillus depends on efficient surfactin production, Molecular Plant-Microbe Interactions, 27, 87, 10.1094/MPMI-09-13-0262-R

Chen, 2020, A plant genetic network for preventing dysbiosis in the phyllosphere, Nature, 580, 653, 10.1038/s41586-020-2185-0

Cheng, 2019, Plant–microbe interactions facing environmental challenge, Cell Host & Microbe, 26, 183, 10.1016/j.chom.2019.07.009

Cooper, 2008, Basic compatibility of Albugo candida in Arabidopsis thaliana and Brassica juncea causes broad-spectrum suppression of innate immunity, Molecular Plant-Microbe Interactions, 21, 745, 10.1094/MPMI-21-6-0745

Cooper, 2002, Albugo candida (white rust) suppresses resistance to downy mildew pathogens in Arabidopsis thaliana, Plant Protection Sciences, 38, 474, 10.17221/10527-PPS

Copeland, 2015, Seasonal community succession of the phyllosphere microbiome, Molecular Plant-Microbe Interactions, 28, 274, 10.1094/MPMI-10-14-0331-FI

Crombie, 2018, Poplar phyllosphere harbors disparate isoprene-degrading bacteria, Proceedings of the National Academy of Sciences, USA, 115, 13081, 10.1073/pnas.1812668115

Danhorn, 2007, Biofilm formation by plant-associated bacteria, Annual Review of Microbiology, 61, 401, 10.1146/annurev.micro.61.080706.093316

Davey, 2000, Microbial biofilms: from ecology to molecular genetics, Microbiology and Molecular Biology Reviews, 64, 847, 10.1128/MMBR.64.4.847-867.2000

de Lamo, 2020, Biocontrol by Fusarium oxysporum using endophyte-mediated resistance, Frontiers in Plant Science, 11, 37, 10.3389/fpls.2020.00037

Delmotte, 2009, Community proteogenomics reveals insights into the physiology of phyllosphere bacteria, Proceedings of the National Academy of Sciences, USA, 106, 16428, 10.1073/pnas.0905240106

de Oliveira Costa, 2012, Isolation and characterization of endophytic bacteria isolated from the leaves of the common bean (Phaseolus vulgaris), Brazilian Journal of Microbiology, 43, 1562, 10.1590/S1517-83822012000400041

De Vrieze, 2018, Combining different potato-associated Pseudomonas strains for improved biocontrol of Phytophthora infestans, Frontiers in Microbiology, 9, 2573, 10.3389/fmicb.2018.02573

de Weyer, 2019, A species-wide inventory of NLR genes and alleles in Arabidopsis thaliana, Cell, 178, 1260, 10.1016/j.cell.2019.07.038

Dhayanithy, 2019, Diversity and biological activities of endophytic fungi associated with Catharanthus roseus, BMC Microbiology, 19, 22, 10.1186/s12866-019-1386-x

Dong, 2019, Bacterial communities in the rhizosphere, phyllosphere and endosphere of tomato plants, PLoS One, 14, e0223847, 10.1371/journal.pone.0223847

Dong, 2001, Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase, Nature, 411, 813, 10.1038/35081101

Dong, 2000, AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora, Proceedings of the National Academy of Sciences, USA, 97, 3526, 10.1073/pnas.97.7.3526

Dudler, 2006, Interactions between bacteria and eukaryotes via small molecules, Current Opinion in Biotechnology, 17, 268, 10.1016/j.copbio.2006.04.004

Dulla, 2008, Quorum size of Pseudomonas syringae is small and dictated by water availability on the leaf surface, Proceedings of the National Academy of Sciences, USA, 105, 3082, 10.1073/pnas.0711723105

Durand, 2018, Bacterial diversity associated with poplar trees grown on a Hg-contaminated site: community characterization and isolation of Hg-resistant plant growth-promoting bacteria, The Science of the total environment, 622–623, 1165, 10.1016/j.scitotenv.2017.12.069

Eitas, 2010, NB-LRR proteins: pairs, pieces, perception, partners, and pathways, Current Opinion in Plant Biology, 13, 472, 10.1016/j.pbi.2010.04.007

Eitzen, 2020, An antagonistic driver of the microbial phyllosphere suppresses infection of Arabidopsis thaliana by the oomycete pathogen Albugo laibachii via a secreted hydrolase, bioRxiv

Elias, 2012, Multi-species biofilms: living with friendly neighbors, FEMS Microbiology Reviews, 36, 990, 10.1111/j.1574-6976.2012.00325.x

Enya, 2007, Culturable leaf-associated bacteria on tomato plants and their potential as biological control agents, Microbial Ecology, 53, 524, 10.1007/s00248-006-9085-1

Fall, 1996, Leaf methanol—the simplest natural product from plants, Trends in Plant Science, 1, 296, 10.1016/S1360-1385(96)88175-0

Federle, 2009, Autoinducer-2-based chemical communication in bacteria: complexities of interspecies signaling, Contributions to Microbiology, 16, 18, 10.1159/000219371

Feehan, 2020, Plant NLRs get by with a little help from their friends, Current Opinion in Plant Biology, 56, 99, 10.1016/j.pbi.2020.04.006

Felipe, 2018, Xanthomonas vesicatoria virulence factors involved in early stages of bacterial spot development in tomato, Plant Pathology, 67, 1936, 10.1111/ppa.12905

Ference, 2018, Recent advances in the understanding of Xanthomonas citri ssp. citri pathogenesis and citrus canker disease management, Molecular Plant Pathology, 19, 1302, 10.1111/mpp.12638

Flemming, 2019, Bacteria and archaea on Earth and their abundance in biofilms, Nature Reviews. Microbiology, 17, 247, 10.1038/s41579-019-0158-9

Flores-Núñez, 2020, Functional signatures of the epiphytic prokaryotic microbiome of agaves and cacti, Frontiers in Microbiology, 10, 3044, 10.3389/fmicb.2019.03044

Frank, 2019, Molecular host mimicry and manipulation in bacterial symbionts., FEMS Microbiology Letters, 10.1093/femsle/fnz038

Frank, 2017, Transmission of bacterial endophytes, Microorganisms, 5, 70, 10.3390/microorganisms5040070

Gafni, 2015, Biological control of the cucurbit powdery mildew pathogen Podosphaera xanthii by means of the epiphytic fungus Pseudozyma aphidis and parasitism as a mode of action, Frontiers in Plant Science, 6, 132, 10.3389/fpls.2015.00132

Gantner, 2006, In situ quantitation of the spatial scale of calling distances and population density-independent N-acylhomoserine lactone-mediated communication by rhizobacteria colonized on plant roots, FEMS Microbiology Ecology, 56, 188, 10.1111/j.1574-6941.2005.00037.x

Glushakova, 2004, Seasonal dynamics in a yeast population on leaves of the common wood sorrel Oxalis acetosella L, Microbiology, 73, 184, 10.1023/B:MICI.0000023987.40253.2d

Gniwotta, 2005, What do microbes encounter at the plant surface? Chemical composition of pea leaf cuticular waxes, Plant Physiology, 139, 519, 10.1104/pp.104.053579

Griffiths, 2020, Complex associations between cross-kingdom microbial endophytes and host genotype in ash dieback disease dynamics, Journal of Ecology, 108, 291, 10.1111/1365-2745.13302

Grinberg, 2019, Bacterial surface colonization, preferential attachment and fitness under periodic stress, PLoS Computational Biology, 15, e1006815, 10.1371/journal.pcbi.1006815

Guan, 2015, Multilayered regulation of ethylene induction plays a positive role in Arabidopsis resistance against Pseudomonas syringae, Plant Physiology, 169, 299, 10.1104/pp.15.00659

Hall, 2017, The evolutionary consequences of stepwise infection processes, Trends in Ecology & Evolution, 32, 612, 10.1016/j.tree.2017.05.009

Haney, 2018, Rhizosphere-associated Pseudomonas induce systemic resistance to herbivores at the cost of susceptibility to bacterial pathogens, Molecular Ecology, 27, 1833, 10.1111/mec.14400

Hardoim, 2015, The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes, Microbiology and Molecular Biology Reviews, 79, 293, 10.1128/MMBR.00050-14

Harsonowati, 2017, Leaf blast disease reduction by rice-phyllosphere Actinomycetes producing bioactive compounds, Journal of General Plant Pathology, 83, 98, 10.1007/s10327-017-0700-4

Hassani, 2018, Microbial interactions within the plant holobiont, Microbiome, 6, 58, 10.1186/s40168-018-0445-0

Helfrich, 2018, Bipartite interactions, antibiotic production and biosynthetic potential of the Arabidopsis leaf microbiome, Nature Microbiology, 3, 909, 10.1038/s41564-018-0200-0

Helliwell, 2016, Ethylene biosynthesis and signaling is required for rice immune response and basal resistance against Magnaporthe oryzae infection, Molecular Plant-Microbe Interactions, 29, 831, 10.1094/MPMI-06-16-0121-R

Herrera, 2008, Pantoea stewartii subsp. stewartii exhibits surface motility, which is a critical aspect of Stewart’s wilt disease development on maize, Molecular Plant-Microbe Interactions, 21, 1359, 10.1094/MPMI-21-10-1359

Hopkins, 1989, Xylella fastidiosa: xylem-limited bacterial pathogen of plants, Annual Review of Phytopathology, 27, 271, 10.1146/annurev.py.27.090189.001415

Hutchison, 1993, Evidence for the involvement of the surface active properties of the extracellular toxin tolaasin in the manifestation of brown blotch disease symptoms by Pseudomonas tolaasii on Agaricus bisporus, Physiological and Molecular Plant Pathology, 42, 373, 10.1016/S0885-5765(05)80013-X

Innerebner, 2011, Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system, Applied and Environmental Microbiology, 77, 3202, 10.1128/AEM.00133-11

Into, 2020, Yeast diversity associated with the phylloplane of corn plants cultivated in Thailand, Microorganisms, 8, 80, 10.3390/microorganisms8010080

Irie, 2008, Quorum sensing and microbial biofilms, Current Topics in Microbiology and Immunology, 322, 67

Islam, 2004, Persistence of enterohemorrhagic Escherichia coli O157:H7 in soil and on leaf lettuce and parsley grown in fields treated with contaminated manure composts or irrigation water, Journal of Food Protection, 67, 1365, 10.4315/0362-028X-67.7.1365

Ives, 2000, Stability and species richness in complex communities, Ecology Letters, 3, 399, 10.1046/j.1461-0248.2000.00144.x

Jacob, 2019, Human pathogen colonization of lettuce dependent upon plant genotype and defense response activation, Frontiers in Plant Science, 10, 1769, 10.3389/fpls.2019.01769

Jahn, 2008, The flagellar sigma factor fliA is required for Dickeya dadantii virulence, Molecular Plant-Microbe Interactions, 21, 1431, 10.1094/MPMI-21-11-1431

Jakuschkin, 2016, Deciphering the pathobiome: intra- and interkingdom interactions involving the pathogen Erysiphe alphitoides, Microbial Ecology, 72, 870, 10.1007/s00248-016-0777-x

Jones, 2016, Intracellular innate immune surveillance devices in plants and animals, Science, 354, aaf6395, 10.1126/science.aaf6395

Kamo, 2018, Methylobamine, a UVA-absorbing compound from the plant-associated bacteria Methylobacterium sp, Natural Product Communications, 13, 141, 10.1177/1934578X1801300208

Karasov, 2019, The relationship between microbial biomass and disease in the Arabidopsis thaliana phyllosphere, bioRxiv, 828814

Kaur, 2011, Pre-inoculation with Hyaloperonospora parasitica reduces incubation period and increases severity of disease caused by Albugo candida in a Brassica juncea variety resistant to downy mildew, Journal of General Plant Pathology, 77, 101, 10.1007/s10327-011-0293-2

Kembel, 2014, Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest, Proceedings of the National Academy of Sciences, USA, 111, 13715, 10.1073/pnas.1216057111

Kerdraon, 2019, Differential dynamics of microbial community networks help identify microorganisms interacting with residue-borne pathogens: the case of Zymoseptoria tritici in wheat, Microbiome, 7, 125, 10.1186/s40168-019-0736-0

Kharwar, 2010, A comparative study of endophytic and epiphytic fungal association with leaf of Eucalyptus citriodora Hook., and their antimicrobial activity, World Journal of Microbiology and Biotechnology, 26, 1941, 10.1007/s11274-010-0374-y

Knief, 2010, Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere, The ISME Journal, 4, 719, 10.1038/ismej.2010.9

Kong, 2010, Zoospore interspecific signaling promotes plant infection by Phytophthora, BMC Microbiology, 10, 313, 10.1186/1471-2180-10-313

Kruse, 2017, Asexual and sexual morphs of Moesziomyces revisited, IMA Fungus, 8, 117, 10.5598/imafungus.2017.08.01.09

Kumar, 2018, Does plant–microbe interaction confer stress tolerance in plants: a review?, Microbiological Research, 207, 41, 10.1016/j.micres.2017.11.004

Kyrkou, 2018, Pierce’s disease of grapevines: a review of control strategies and an outline of an epidemiological model, Frontiers in Microbiology, 9, 2141, 10.3389/fmicb.2018.02141

Laforest-Lapointe, 2016, Host species identity, site and time drive temperate tree phyllosphere bacterial community structure, Microbiome, 4, 27, 10.1186/s40168-016-0174-1

Laforest-Lapointe, 2019, Decrypting the phyllosphere microbiota: progress and challenges, American Journal of Botany, 106, 171, 10.1002/ajb2.1229

Lai, 2018, Transcript-level expression control of plant NLR genes, Molecular Plant Pathology, 19, 1267, 10.1111/mpp.12607

Lapin, 2020, Origins and immunity networking functions of EDS1 family proteins, Annual Review of Phytopathology, 58, 253, 10.1146/annurev-phyto-010820-012840

Lebeis, 2015, Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa, Science, 349, 860, 10.1126/science.aaa8764

Lee, 2009, Endophytic Fusarium verticillioides reduces disease severity caused by Ustilago maydis on maize, FEMS Microbiology Letters, 299, 31, 10.1111/j.1574-6968.2009.01719.x

Lee, 2002, Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis, Applied and Environmental Microbiology, 68, 3919, 10.1128/AEM.68.8.3919-3924.2002

Lemanceau, 2017, Plant communication with associated microbiota in the spermosphere, rhizosphere and phyllosphere, How plants communicate with their biotic environment. Advances in Botanical Research, 101, 10.1016/bs.abr.2016.10.007

Leopold, 2020, Host genotype and colonist arrival order jointly govern plant microbiome composition and function, bioRxiv

Leveau, 2019, A brief from the leaf: latest research to inform our understanding of the phyllosphere microbiome, Current Opinion in Microbiology, 49, 41, 10.1016/j.mib.2019.10.002

Levy, 2018, Genomic features of bacterial adaptation to plants, Nature Genetics, 50, 138, 10.1038/s41588-017-0012-9

Li, 2019, Diffusible signal factor (DSF)-mediated quorum sensing modulates expression of diverse traits in Xanthomonas citri and responses of citrus plants to promote disease, BMC Genomics, 20, 55, 10.1186/s12864-018-5384-4

Lindow, 2003, Microbiology of the phyllosphere, Applied and Environmental Microbiology, 69, 1875, 10.1128/AEM.69.4.1875-1883.2003

Ludlow, 2019, Analysis of the indole diterpene gene cluster for biosynthesis of the epoxy-janthitrems in Epichloë endophytes, Microorganisms, 7, 560, 10.3390/microorganisms7110560

Luo, 2019, Variations in phyllosphere microbial community along with the development of angular leaf-spot of cucumber, AMB Express, 9, 76, 10.1186/s13568-019-0800-y

Lv, 2012, Response of leaf-associated bacterial communities to primary acyl-homoserine lactone in the tobacco phyllosphere, Research in Microbiology, 163, 119, 10.1016/j.resmic.2011.11.001

Ma, 2013, Quorum quenching in culturable phyllosphere bacteria from tobacco, International Journal of Molecular Sciences, 14, 14607, 10.3390/ijms140714607

Maignien, 2014, Ecological succession and stochastic variation in the assembly of Arabidopsis thaliana phyllosphere communities, mBio, 5, e00682, 10.1128/mBio.00682-13

Malamud, 2011, The Xanthomonas axonopodis pv. citri flagellum is required for mature biofilm and canker development, Microbiology, 157, 819, 10.1099/mic.0.044255-0

Manching, 2014, Southern leaf blight disease severity is correlated with decreased maize leaf epiphytic bacterial species richness and the phyllosphere bacterial diversity decline is enhanced by nitrogen fertilization, Frontiers in Plant Science, 5, 403, 10.3389/fpls.2014.00403

Marques, 2002, Characterization of biofilm formation by Xylella fastidiosa in vitro, Plant Disease, 86, 633, 10.1094/PDIS.2002.86.6.633

Martinez-Medina, 2016, Recognizing plant defense priming, Trends in Plant Science, 21, 818, 10.1016/j.tplants.2016.07.009

Martins, 2018, Persistence in phytopathogenic bacteria: do we know enough?, Frontiers in Microbiology, 9, 1099, 10.3389/fmicb.2018.01099

Melotto, 2006, Plant stomata function in innate immunity against bacterial invasion, Cell, 126, 969, 10.1016/j.cell.2006.06.054

Melotto, 2017, Stomatal defense a decade later, Plant Physiology, 174, 561, 10.1104/pp.16.01853

Mersmann, 2010, Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity, Plant Physiology, 154, 391, 10.1104/pp.110.154567

Miller, 2012, Investigation of the biosynthetic potential of endophytes in traditional Chinese anticancer herbs, PLoS One, 7, e35953, 10.1371/journal.pone.0035953

Mittelviefhaus, 2019, A modular atomic force microscopy approach reveals a large range of hydrophobic adhesion forces among bacterial members of the leaf microbiota, The ISME Journal, 13, 1878, 10.1038/s41396-019-0404-1

Monier, 2003, Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces, Proceedings of the National Academy of Sciences, USA, 100, 15977, 10.1073/pnas.2436560100

Monier, 2004, Frequency, size, and localization of bacterial aggregates on bean leaf surfaces, Applied and Environmental Microbiology, 70, 346, 10.1128/AEM.70.1.346-355.2004

Monier, 2005, Aggregates of resident bacteria facilitate survival of immigrant bacteria on leaf surfaces, Microbial Ecology, 49, 343, 10.1007/s00248-004-0007-9

Monteiro, 2018, Structural, functional, and genomic diversity of plant NLR proteins: an evolved resource for rational engineering of plant immunity, Annual Review of Phytopathology, 56, 243, 10.1146/annurev-phyto-080417-045817

Morella, 2020, Successive passaging of a plant-associated microbiome reveals robust habitat and host genotype-dependent selection, Proceedings of the National Academy of Sciences, USA, 117, 1148, 10.1073/pnas.1908600116

Morris, 2002, Fifty years of phyllosphere microbiology: significant contributions to research in related fields, Phyllosphere microbiology, 365

Mougi, 2012, Diversity of interaction types and ecological community stability, Science, 337, 349, 10.1126/science.1220529

Müller, 2005, Plant surface properties in chemical ecology, Journal of Chemical Ecology, 31, 2621, 10.1007/s10886-005-7617-7

Munch, 2018, The Brassicaceae family displays divergent, shoot-skewed NLR resistance gene expression, Plant Physiology, 176, 1598, 10.1104/pp.17.01606

Munther, 2020, Formation of Escherichia coli O157:H7 persister cells in the lettuce phyllosphere and application of differential equation models to predict their prevalence on lettuce plants in the field, Applied and Environmental Microbiology, 86, 10.1128/AEM.01602-19

Nadakuduti, 2012, Pleiotropic phenotypes of the sticky peel mutant provide new insight into the role of CUTIN DEFICIENT2 in epidermal cell function in tomato, Plant Physiology, 159, 945, 10.1104/pp.112.198374

Naimi, 2003, Concurrent outbreaks of Shigella sonnei and enterotoxigenic Escherichia coli infections associated with parsley: implications for surveillance and control of foodborne illness, Journal of Food Protection, 66, 535, 10.4315/0362-028X-66.4.535

Nascimento, 2018, Ethylene and 1-aminocyclopropane-1-carboxylate (ACC) in plant–bacterial interactions, Frontiers in Plant Science, 9, 114, 10.3389/fpls.2018.00114

Nawrath, 2013, Apoplastic diffusion barriers in Arabidopsis, The Arabidopsis Book, 11, e0167, 10.1199/tab.0167

Nelson, 2018, The seed microbiome: origins, interactions, and impacts, Plant and Soil, 422, 7, 10.1007/s11104-017-3289-7

Neu, 1990, Surface active properties of viscosin: a peptidolipid antibiotic, Applied Microbiology and Biotechnology, 32, 518, 10.1007/BF00173720

Newcombe, 2018, A hypothetical bottleneck in the plant microbiome, Frontiers in Microbiology, 9, 1645, 10.3389/fmicb.2018.01645

Ng, 2009, Bacterial quorum-sensing network architectures, Annual Review of Genetics, 43, 197, 10.1146/annurev-genet-102108-134304

Noman, 2019, PRRs and NB-LRRs: from signal perception to activation of plant innate immunity, International Journal of Molecular Sciences, 20, 1882, 10.3390/ijms20081882

Okamoto, 2009, High humidity induces abscisic acid 8'-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis, Plant Physiology, 149, 825, 10.1104/pp.108.130823

Oso, 2019, Utilisation of hydrocarbons and production of surfactants by bacteria isolated from plant leaf surfaces, FEMS Microbiology Letters, 366, fnz061, 10.1093/femsle/fnz061

Ou, 2014, Stomata prioritize their responses to multiple biotic and abiotic signal inputs, PLoS One, 9, e101587, 10.1371/journal.pone.0101587

Pan, 2008, Effects of host plant environment and Ustilago maydis infection on the fungal endophyte community of maize (Zea mays), New Phytologist, 178, 147, 10.1111/j.1469-8137.2007.02350.x

Pańka, 2013, Production of phenolics and the emission of volatile organic compounds by perennial ryegrass (Lolium perenne L.)/Neotyphodium lolii association as a response to infection by Fusarium poae, Journal of Plant Physiology, 170, 1010, 10.1016/j.jplph.2013.02.009

Peredo, 2018, Leaf-FISH: microscale imaging of bacterial taxa on phyllosphere, Frontiers in Microbiology, 8, 2669, 10.3389/fmicb.2017.02669

Peng, 2018, Convergent and divergent signaling in PAMP-triggered immunity and effector-triggered immunity, Molecular Plant-Microbe Interactions, 31, 403, 10.1094/MPMI-06-17-0145-CR

Peyraud, 2019, Intercellular cooperation in a fungal plant pathogen facilitates host colonization, Proceedings of the National Academy of Sciences, USA, 116, 3193, 10.1073/pnas.1811267116

Porras-Alfaro, 2011, Hidden fungi, emergent properties: endophytes and microbiomes, Annual Review of Phytopathology, 49, 291, 10.1146/annurev-phyto-080508-081831

Poudel, 2016, Microbiome networks: a systems framework for identifying candidate microbial assemblages for disease management, Phytopathology, 106, 1083, 10.1094/PHYTO-02-16-0058-FI

Purahong, 2018, Plant microbiome and its link to plant health: host species, organs and Pseudomonas syringae pv. actinidiae infection shaping bacterial phyllosphere communities of Kiwifruit plants, Frontiers in Plant Science, 9, 1563, 10.3389/fpls.2018.01563

Qian, 2018, Host genotype strongly influences phyllosphere fungal communities associated with Mussaenda pubescens var. alba (Rubiaceae), Fungal Ecology, 36, 141, 10.1016/j.funeco.2018.10.001

Qin, 2019, Responses of phyllosphere microbiota and plant health to application of two different biocontrol agents, AMB Express, 9, 42, 10.1186/s13568-019-0765-x

Quiñones, 2005, Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae, Molecular Plant-Microbe Interactions, 18, 682, 10.1094/MPMI-18-0682

Raghavendra, 2013, The contribution of foliar endophytes to quantitative resistance to Melampsora rust, New Phytologist, 197, 909, 10.1111/nph.12066

Rajesh, 2014, Quorum quenching activity in cell-free lysate of endophytic bacteria isolated from Pterocarpus santalinus Linn., and its effect on quorum sensing regulated biofilm in Pseudomonas aeruginosa PAO1, Microbiological Research, 169, 561, 10.1016/j.micres.2013.10.005

Rastogi, 2013, New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches, FEMS Microbiology Letters, 348, 1, 10.1111/1574-6968.12225

Rastogi, 2012, Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce, The ISME Journal, 6, 1812, 10.1038/ismej.2012.32

Redford, 2010, The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves, Environmental Microbiology, 12, 2885, 10.1111/j.1462-2920.2010.02258.x

Reisberg, 2013, Distinct phyllosphere bacterial communities on Arabidopsis wax mutant leaves, PLoS One, 8, e78613, 10.1371/journal.pone.0078613

Remus-Emsermann, 2018, Phyllosphere microbiology: at the interface between microbial individuals and the plant host, New Phytologist, 218, 1327, 10.1111/nph.15054

Rigano, 2007, Biofilm formation, epiphytic fitness, and canker development in Xanthomonas axonopodis pv. citri, Molecular Plant-Microbe Interactions, 20, 1222, 10.1094/MPMI-20-10-1222

Ritpitakphong, 2016, The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen, New Phytologist, 210, 1033, 10.1111/nph.13808

Romero, 2014, The communities of tomato (Solanum lycopersicum L.) leaf endophytic bacteria, analyzed by 16S-ribosomal RNA gene pyrosequencing, FEMS Microbiology Letters, 351, 187, 10.1111/1574-6968.12377

Roy, 2013, Escherichia coli O157:H7 induces stronger plant immunity than Salmonella enterica Typhimurium SL1344, Phytopathology, 103, 326, 10.1094/PHYTO-09-12-0230-FI

Rudrappa, 2008, Causes and consequences of plant-associated biofilms, FEMS Microbiology Ecology, 64, 153, 10.1111/j.1574-6941.2008.00465.x

Ruhe, 2016, Obligate biotroph pathogens of the genus Albugo are better adapted to active host defense compared to niche competitors, Frontiers in Plant Science, 7, 820, 10.3389/fpls.2016.00820

Saijo, 2018, Pattern recognition receptors and signaling in plant–microbe interactions, The Plant Journal, 93, 592, 10.1111/tpj.13808

Saldaña, 2011, Surface structures involved in plant stomata and leaf colonization by shiga-toxigenic Escherichia coli O157:H7, Frontiers in Microbiology, 2, 119, 10.3389/fmicb.2011.00119

Salvatierra-Martinez, 2018, Colonization ability as an indicator of enhanced biocontrol capacity—an example using two Bacillus amyloliquefaciens strains and Botrytis cinerea infection of tomatoes, Journal of Phytopathology, 166, 601, 10.1111/jph.12718

Sanjenbam, 2020, Phenotypic diversity of Methylobacterium associated with rice landraces in North-East India, PLoS One, 15, e0228550, 10.1371/journal.pone.0228550

Sapp, 2018, Protists are an integral part of the Arabidopsis thaliana microbiome, Environmental Microbiology, 20, 30, 10.1111/1462-2920.13941

Schönherr, 2006, Characterization of aqueous pores in plant cuticles and permeation of ionic solutes, Journal of Experimental Botany, 57, 2471, 10.1093/jxb/erj217

Schreiber, 2005, Plant–microbe interactions: identification of epiphytic bacteria and their ability to alter leaf surface permeability, New Phytologist, 166, 589, 10.1111/j.1469-8137.2005.01343.x

Scott, 2017, Escherichia coli O157:H7 converts plant-derived choline to glycine betaine for osmoprotection during pre- and post-harvest colonization of injured lettuce leaves, Frontiers in Microbiology, 8, 2436, 10.3389/fmicb.2017.02436

Seong, 2020, Evolution of NLR resistance genes with noncanonical N-terminal domains in wild tomato species, New Phytologist, 227, 1530, 10.1111/nph.16628

Sharma, 2019, Saprotrophic yeasts formerly classified as Pseudozyma have retained a large effector arsenal, including functional Pep1 orthologs, Mycological Progress, 18, 763, 10.1007/s11557-019-01486-2

Shivas, 1984, Identification and enumeration of yeasts on Banksia collina and Callistemon viminalis leaves, Transactions of the British Mycological Society, 83, 687, 10.1016/S0007-1536(84)80188-6

Singh, 2018, Genotype–environment interaction shapes the microbial assemblage in grapevine’s phyllosphere and carposphere: an NGS approach, Microorganisms, 6, 96, 10.3390/microorganisms6040096

Stone, 2018, The role of the phyllosphere microbiome in plant health and function, Annual Plant Reviews, 1, 1

Streletskii, 2019, Yeasts producing zeatin, PeerJ, 7, e6474, 10.7717/peerj.6474

Sun, 2014, Indole-3-acetic acid-producing yeasts in the phyllosphere of the carnivorous plant Drosera indica L, PLoS One, 9, e114196, 10.1371/journal.pone.0114196

Sy, 2005, Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions, Applied and Environmental Microbiology, 71, 7245, 10.1128/AEM.71.11.7245-7252.2005

Taga, 2003, Chemical communication among bacteria, Proceedings of the National Academy of Sciences, USA, 100, 14549, 10.1073/pnas.1934514100

Tans-Kersten, 2001, Ralstonia solanacearum needs motility for invasive virulence on tomato, Journal of Bacteriology, 183, 3597, 10.1128/JB.183.12.3597-3605.2001

Tecon, 2012, The mechanics of bacterial cluster formation on plant leaf surfaces as revealed by bioreporter technology, Environmental Microbiology, 14, 1325, 10.1111/j.1462-2920.2012.02715.x

Teixeira, 2019, Beyond pathogens: microbiota interactions with the plant immune system, Current Opinion in Microbiology, 49, 7, 10.1016/j.mib.2019.08.003

Teplitski, 2011, Untangling metabolic and communication networks: interactions of enterics with phytobacteria and their implications in produce safety., Trends in Microbiology, 19, 121, 10.1016/j.tim.2010.11.007

Thébault, 2010, Stability of ecological communities and the architecture of mutualistic and trophic networks, Science, 329, 853, 10.1126/science.1188321

Thevenet, 2017, The priming molecule β-aminobutyric acid is naturally present in plants and is induced by stress, New Phytologist, 213, 552, 10.1111/nph.14298

Thines, 2014, Phylogeny and evolution of plant pathogenic oomycetes—a global overview, European Journal of Plant Pathology, 138, 431, 10.1007/s10658-013-0366-5

Thompson, 1993, Quantitative and qualitative seasonal changes in the microbial community from the phyllosphere of sugar beet (Beta vulgaris), Plant and Soil, 150, 177, 10.1007/BF00013015

Thorne, 2006, Pierce’s disease symptoms: comparison with symptoms of water deficit and the impact of water deficits, American Journal of Enology and Viticulture, 57, 1, 10.5344/ajev.2006.57.1.1

Ueda, 2018, Disease severity enhancement by an esterase from non-phytopathogenic yeast Pseudozyma Antarctica and its potential as adjuvant for biocontrol agents, Scientific Reports, 8, 16455, 10.1038/s41598-018-34705-z

Ulrich, 2020, A comparative analysis of ash leaf-colonizing bacterial communities identifies putative antagonists of Hymenoscyphus fraxineus, Frontiers in Microbiology, 11, 966, 10.3389/fmicb.2020.00966

Ulrich, 2004, Quorum quenching: enzymatic disruption of N-acylhomoserine lactone-mediated bacterial communication in Burkholderia thailandensis, Applied and Environmental Microbiology, 70, 6173, 10.1128/AEM.70.10.6173-6180.2004

Underwood, 2007, Role of plant stomata in bacterial invasion, Cellular Microbiology, 9, 1621, 10.1111/j.1462-5822.2007.00938.x

Vacher, 2016, The phyllosphere: microbial jungle at the plant–climate interface, Annual Review of Ecology, Evolution, and Systematics, 47, 1, 10.1146/annurev-ecolsys-121415-032238

van Dam, 2016, Effector profiles distinguish formae speciales of Fusarium oxysporum, Environmental Microbiology, 18, 4087, 10.1111/1462-2920.13445

Vandenkoornhuyse, 2015, The importance of the microbiome of the plant holobiont, New Phytologist, 206, 1196, 10.1111/nph.13312

Vannier, 2019, Microbiota-mediated disease resistance in plants, PLoS Pathogens, 15, e1007740, 10.1371/journal.ppat.1007740

Vergnes, 2020, Phyllosphere colonization by a soil Streptomyces sp. promotes plant defense responses against fungal infection, Molecular Plant-Microbe Interactions, 33, 223, 10.1094/MPMI-05-19-0142-R

Vogel, 2016, The Arabidopsis leaf transcriptome reveals distinct but also overlapping responses to colonization by phyllosphere commensals and pathogen infection with impact on plant health, New Phytologist, 212, 192, 10.1111/nph.14036

Vorholt, 2012, Microbial life in the phyllosphere, Nature Reviews. Microbiology, 10, 828, 10.1038/nrmicro2910

Vorholt, 2017, Establishing causality: opportunities of synthetic communities for plant microbiome research, Cell Host & Microbe, 22, 142, 10.1016/j.chom.2017.07.004

Wagner, 2014, Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative, Ecology Letters, 17, 717, 10.1111/ele.12276

Wagner, 2016, Host genotype and age shape the leaf and root microbiomes of a wild perennial plant, Nature Communications, 7, 12151, 10.1038/ncomms12151

Wallace, 2018, Variation in the leaf and root microbiome of sugar maple (Acer saccharum) at an elevational range limit, PeerJ, 6, e5293, 10.7717/peerj.5293

Wang, 2016, The isolation and characterization of resident yeasts from the phylloplane of Arabidopsis thaliana, Scientific Reports, 6, 39403, 10.1038/srep39403

Wang, 2015, Multigene phylogeny and taxonomic revision of yeasts and related fungi in the Ustilagino mycotina, Studies in Mycology, 81, 55, 10.1016/j.simyco.2015.10.004

Wei, 2016, Membrane glycerolipidome of soybean root hairs and its response to nitrogen and phosphate availability, Scientific Reports, 6, 36172, 10.1038/srep36172

Wu, 2017, NLR network mediates immunity to diverse plant pathogens, Proceedings of the National Academy of Sciences, USA, 114, 8113, 10.1073/pnas.1702041114

Xin, 2018, Pseudomonas syringae: what it takes to be a pathogen, Nature Reviews. Microbiology, 16, 316, 10.1038/nrmicro.2018.17

Xin, 2016, Bacteria establish an aqueous living space in plants crucial for virulence, Nature, 539, 524, 10.1038/nature20166

Yang, 2017, Activation of ethylene signaling pathways enhances disease resistance by regulating ROS and phytoalexin production in rice, The Plant Journal, 89, 338, 10.1111/tpj.13388

Yao, 2019, Phyllosphere epiphytic and endophytic fungal community and network structures differ in a tropical mangrove ecosystem, Microbiome, 7, 57, 10.1186/s40168-019-0671-0

Yoshida, 2019, Pantothenate auxotrophy of Methylobacterium spp. isolated from living plants, Bioscience, Biotechnology, and Biochemistry, 83, 569, 10.1080/09168451.2018.1549935

Yu, 2018, Brassinosteroid signaling in plant–microbe interactions, International Journal of Molecular Sciences, 19, 4091, 10.3390/ijms19124091

Zeng, 2010, Plant stomata: a checkpoint of host immunity and pathogen virulence, Current Opinion in Biotechnology, 21, 599, 10.1016/j.copbio.2010.05.006

Zhang, 2008, Assessing the impact of the biological control agent Bacillus thuringiensis on the indigenous microbial community within the pepper plant phyllosphere, FEMS Microbiology Letters, 284, 102, 10.1111/j.1574-6968.2008.01178.x

Zhao, 2019, Transcriptome profiling reveals the response process of tomato carrying Cf-19 and Cladosporium fulvum interaction, BMC Plant Biology, 19, 572, 10.1186/s12870-019-2150-y

Zheng, 2012, Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation, Cell Host & Microbe, 11, 587, 10.1016/j.chom.2012.04.014