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A Synthetic Community Approach Reveals Plant Genotypes Affecting the Phyllosphere Microbiota
The leaves of plants are inhabited by a diverse community of microorganisms. These leaf inhabitants influence their hosts with respect to growth and resistance to abiotic and biotic stresses. Recent studies revealed that the bacterial communities associated with leaves undergo selection, resulting in conserved microbial communities. However, the factors that are involved in structuring of bacterial communities are not well understood. In order to uncover host genetic factors that determine the community composition and to exclude confounding environmental effects, we inoculated Arabidopsis thaliana with a synthetic bacterial community under controlled conditions We screened a panel of Arabidopsis mutants defective in various traits for alterations in community structure and abundance and were able to show that cuticle synthesis and ethylene perception affect the bacterial community. In addition, we identified plant ecotypes with drastic differences in the community composition. Our system can thus be used to identify additional host genes and to broaden insights into plant microbe interactions, potentially providing a basis for applied plant protection through the identification of traits that enhance growth of plant probiotic bacteria.
Vyšlo v časopise: A Synthetic Community Approach Reveals Plant Genotypes Affecting the Phyllosphere Microbiota. PLoS Genet 10(4): e32767. doi:10.1371/journal.pgen.1004283
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004283Souhrn
The leaves of plants are inhabited by a diverse community of microorganisms. These leaf inhabitants influence their hosts with respect to growth and resistance to abiotic and biotic stresses. Recent studies revealed that the bacterial communities associated with leaves undergo selection, resulting in conserved microbial communities. However, the factors that are involved in structuring of bacterial communities are not well understood. In order to uncover host genetic factors that determine the community composition and to exclude confounding environmental effects, we inoculated Arabidopsis thaliana with a synthetic bacterial community under controlled conditions We screened a panel of Arabidopsis mutants defective in various traits for alterations in community structure and abundance and were able to show that cuticle synthesis and ethylene perception affect the bacterial community. In addition, we identified plant ecotypes with drastic differences in the community composition. Our system can thus be used to identify additional host genes and to broaden insights into plant microbe interactions, potentially providing a basis for applied plant protection through the identification of traits that enhance growth of plant probiotic bacteria.
Zdroje
1. VorholtJA (2012) Microbial life in the phyllosphere. Nature Rev Microbiol 10 : 828–840.
2. BerendsenRL, PieterseCM, BakkerPA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17 : 478–486.
3. BergG (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84 : 11–18.
4. ConrathU, BeckersGJ, FlorsV, Garcia-AgustinP, JakabG, et al. (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19 : 1062–1071.
5. PieterseCM, Van der DoesD, ZamioudisC, Leon-ReyesA, Van WeesSC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28 : 489–521.
6. InnerebnerG, KniefC, VorholtJA (2011) Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Appl Environ Microbiol 77 : 3202–3210.
7. CabrefigaJ, BonaterraA, MontesinosE (2007) Mechanisms of antagonism of Pseudomonas fluorescens EPS62e against Erwinia amylovora, the causal agent of fire blight. Intern Microbiol 10 : 123–132.
8. WeiherE, FreundD, BuntonT, StefanskiA, LeeT, et al. (2011) Advances, challenges and a developing synthesis of ecological community assembly theory. Philos Trans R Soc Lond B Biol Sci 366 : 2403–2413.
9. LawtonJH (1999) Are there general laws in ecology? Oikos 84 : 177–192.
10. VellendM (2010) Conceptual synthesis in community ecology. Quart Rev Biol 85 : 183–206.
11. NemergutDR, SchmidtSK, FukamiT, O'NeillSP, BilinskiTM, et al. (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77 : 342–356.
12. MeyerKM, LeveauJHJ (2012) Microbiology of the phyllosphere: a playground for testing ecological concepts. Oecologia 168 : 621–629.
13. DelmotteN, KniefC, ChaffronS, InnerebnerG, RoschitzkiB, et al. (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci U S A 106 : 16428–16433.
14. LindowSE, BrandlMT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69 : 1875–1883.
15. BeattieGA (2011) Water relations in the interaction of foliar bacterial pathogens with plants. Annu Rev Phytopathol 49 : 533–555.
16. KniefC, RametteA, FrancesL, Alonso-BlancoC, VorholtJA (2010) Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J 4 : 719–728.
17. ErcolaniGL (1991) Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microbial Ecol 21 : 35–48.
18. YangCH, CrowleyDE, BornemanJ, KeenNT (2001) Microbial phyllosphere populations are more complex than previously realized. Proc Natl Acad Sci U S A 98 : 3889–3894.
19. RascheF, TrondlR, NaglreiterC, ReichenauerT, SessitschA (2006) Chilling and cultivar type affect the diversity of bacterial endophytes colonizing sweet pepper (Capsicum anuum L.). Can J Microbiol 52 : 1036–1045.
20. HunterPJ, HandP, PinkD, WhippsJM, BendingGD (2010) Both leaf properties and microbe-microbe interactions influence within-species variation in bacterial population diversity and structure in the Lettuce (Lactuca species) phyllosphere. Appl Environ Microbiol 76 : 8117–8125.
21. RastogiG, SbodioA, TechJJ, SuslowTV, CoakerGL, et al. (2012) Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J 6 : 1812–1822.
22. KinkelLL, WilsonM, LindowSE (2000) Plant species and plant incubation conditions influence variability in epiphytic bacterial population size. Microb Ecol 39 : 1–11.
23. Balint-KurtiP, SimmonsSJ, BlumJE, BallareCL, StapletonAE (2010) Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection. Mol Plant Microbe Interact 23 : 473–484.
24. SmithKP, HandelsmanJ, GoodmanRM (1999) Genetic basis in plants for interactions with disease-suppressive bacteria. Proc Natl Acad Sci U S A 96 : 4786–4790.
25. KniskernJM, TrawMB, BergelsonJ (2007) Salicylic acid and jasmonic acid signaling defense pathways reduce natural bacterial diversity on Arabidopsis thaliana. Mol Plant Microbe Interact 20 : 1512–1522.
26. ReisbergEE, HildebrandtU, RiedererM, HentschelU (2012) Phyllosphere bacterial communities of trichome-bearing and trichomeless Arabidopsis thaliana leaves. Ant Van Leeuwenhoek 101 : 551–560.
27. Gomez-GomezL, BollerT (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5 : 1003–1011.
28. JonesJD, DanglJL (2006) The plant immune system. Nature 444 : 323–329.
29. ChenLQ, HouBH, LalondeS, TakanagaH, HartungML, et al. (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468 : 527–532.
30. GrallathS, WeimarT, MeyerA, GumyC, Suter-GrotemeyerM, et al. (2005) The AtProT family. Compatible solute transporters with similar substrate specificity but differential expression patterns. Plant Physiol 137 : 117–126.
31. BuerCS, MudayGK (2005) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 17 : 2614–2614.
32. BuerCS, IminN, DjordjevicMA (2010) Flavonoids: new roles for old molecules. J Integr Plant Biol 52 : 98–111.
33. SyA, TimmersAC, KniefC, VorholtJA (2005) Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions. Appl Environ Microbiol 71 : 7245–7252.
34. FaithJJ, McNultyNP, ReyFE, GordonJI (2011) Predicting a human gut microbiota's response to diet in gnotobiotic mice. Science 333 : 101–104.
35. McNultyNP, YatsunenkoT, HsiaoA, FaithJJ, MueggeBD, et al. (2011) The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci Transl Med 3 : 106ra106.
36. BodenhausenN, HortonMW, BergelsonJ (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. Plos One 8: e56329.
37. KniefC, FrancesL, VorholtJA (2010) Competitiveness of diverse Methylobacterium strains in the phyllosphere of Arabidopsis thaliana and identification of representative models, including M. extorquens PA1. Microb Ecol 60 : 440–452.
38. RametteA (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75 : 2495–2505.
39. KembelSW, WuM, EisenJA, GreenJL (2012) Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLoS Comput Biol 8: e1002743.
40. BessireM, ChassotC, JacquatAC, HumphryM, BorelS, et al. (2007) A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J 26 : 2158–2168.
41. BessireM, BorelS, FabreG, CarracaL, EfremovaN, et al. (2011) A member of the PLEIOTROPIC DRUG RESISTANCE family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis. Plant Cell 23 : 1958–1970.
42. AlonsoJM, HirayamaT, RomanG, NourizadehS, EckerJR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284 : 2148–2152.
43. GuzmanP, EckerJR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2 : 513–523.
44. ZhaoQ, GuoHW (2011) Paradigms and paradox in the ethylene signaling pathway and interaction network. Mol Plant 4 : 626–634.
45. SchnurrJ, ShockeyJ, BrowseJ (2004) The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16 : 629–642.
46. Jeffree CE (2006) Biology of the Plant Cuticle. In: Riederer M, Muller C, editors. Annu Plant Rev. Oxford: Blackwell Publishing.
47. Riederer M (2006) Introduction: biology of the plant cuticle. In: Riederer M, Muller C, editors. Annual Plant Reviews Volume 23: Biology of the Plant Cuticle. Oxford: Blackwell Publishing.
48. Beattie GA (2002) Leaf surface waxes and the process of leaf colonization by microorganisms. In: Lindow SE, Hecht-Poinar EI, Elliott VJ, editors. Phyllosphere microbiology. St. Paul, Minnesota: The American Phytopathological Society. pp. 3–26.
49. SchreiberL, KrimmU, KnollD, SayedM, AulingG, et al. (2005) Plant-microbe interactions: identification of epiphytic bacteria and their ability to alter leaf surface permeability. New Phytologist 166 : 589–594.
50. MarcellLM, BeattieGA (2002) Effect of leaf surface waxes on leaf colonization by Pantoea agglomerans and Clavibacter michiganensis. Mol Plant Microbe Interact 15 : 1236–1244.
51. ReisbergEE, HildebrandtU, RiedererM, HentschelU (2013) Distinct phyllosphere bacterial communities on Arabidopsis wax mutant leaves. Plos One 8: e78613.
52. YadavRKP, KaramanoliK, VokouD (2005) Bacterial colonization of the phyllosphere of Mediterranean perennial species as influenced by leaf structural and chemical features. Microb Ecol 50 : 185–196.
53. TangDZ, SimonichMT, InnesRW (2007) Mutations in LACS2, a long-chain acyl-coenzyme a synthetase, enhance susceptibility to avirulent Pseudomonas syringae but confer resistance to Botrytis cinerea in Arabidopsis. Plant Physiology 144 : 1093–1103.
54. BleeckerAB, KendeH (2000) Ethylene: A gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16 : 1–18.
55. MudayGK, RahmanA, BinderBM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17 : 181–195.
56. van LoonLC, GeraatsBPJ, LinthorstHJM (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11 : 184–191.
57. FukudaH, OgawaT, TanaseS (1993) Ethylene production by microorganisms. Adv Microbial Physiol 35 : 275–306.
58. VolkschB, WeingartH (1998) Toxin production by pathovars of Pseudomonas syringae and their antagonistic activities against epiphytic microorganisms. J Basic Microbiol 38 : 135–145.
59. SaleemM, ArshadM, HussainS, BhattiAS (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Indust Microbiol Biotechnol 34 : 635–648.
60. DoornbosRF, GeraatsBPJ, KuramaeEE, Van LoonLC, BakkerPAHM (2011) Effects of jasmonic acid, ethylene, and salicylic acid signaling on the rhizosphere bacterial community of Arabidopsis thaliana. Mol Plant Microbe Interact 24 : 395–407.
61. LongHH, SonntagDG, SchmidtDD, BaldwinIT (2010) The structure of the culturable root bacterial endophyte community of Nicotiana attenuata is organized by soil composition and host plant ethylene production and perception. New Phytologist 185 : 554–567.
62. KoornneefM, Alonso-BlancoC, VreugdenhilD (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55 : 141–172.
63. AtwellS, HuangYS, VilhjalmssonBJ, WillemsG, HortonM, et al. (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465 : 627–631.
64. LundbergDS, LebeisSL, ParedesSH, YourstoneS, GehringJ, et al. (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488 : 86–90.
65. BulgarelliD, RottM, SchlaeppiK, Ver Loren van ThemaatE, AhmadinejadN, et al. (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488 : 91–95.
66. PeifferJA, SporA, KorenO, JinZ, TringeSG, et al. (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci U S A 110 : 6548–6553.
67. PeyraudR, KieferP, ChristenP, MassouS, PortaisJC, et al. (2009) Demonstration of the ethylmalonyl-CoA pathway by using 13C metabolomics. Proc Natl Acad Sci U S A 106 : 4846–4851.
68. Remus-EmsermannMN, TeconR, KowalchukGA, LeveauJH (2012) Variation in local carrying capacity and the individual fate of bacterial colonizers in the phyllosphere. ISME J 6 : 756–765.
69. Lane DS (1990) 16S and 23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. New York: John Wiley and Sons. pp. 115–148.
70. BornemanJ, TriplettEW (1997) Molecular microbial diversity in soils from eastern Amazonia: Evidence for unusual microorganisms and microbial population shifts associated with deforestation. Appl Environ Microbiol 63 : 2647–2653.
71. CheliusMK, TriplettEW (2001) The diversity of archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 41 : 252–263.
72. HodkinsonBP, LutzoniF (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49 : 163–180.
73. CzechowskiT, StittM, AltmannT, UdvardiMK, ScheibleWR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139 : 5–17.
74. RuijterJM, RamakersC, HoogaarsWM, KarlenY, BakkerO, et al. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45.
75. TorneroP, DanglJL (2001) A high-throughput method for quantifying growth of phytopathogenic bacteria in Arabidopsis thaliana. Plant J 28 : 475–481.
76. Oksanen J, Blanchet FG, Kindt R, Legendre P, O'Hara RB, et al. (2011) Vegan: Community Ecology Package. R package version 1.17–10.
77. AndersonMJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26 : 32–46.
78. ItoH, IizukaH (1971) Taxonomic studies on a radio-resistant Pseudomonas. XII. Studies on microorganisms of cereal grain. Agricultural Biol Chem 35 : 1566–1571.
79. RivasR, AbrilA, TrujilloME, VelazquezE (2004) Sphingomonas phyllosphaerae sp nov., from the phyllosphere of Acacia caven in Argentina. Int J System Evol Microbiol 54 : 2147–2150.
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