A Synthetic Community Approach Reveals Plant Genotypes Affecting the Phyllosphere Microbiota

PLoS Genetics

Volumn 10, Issue 4, 2014, Pages

  Bodenhausen, Natacha ^a   Bortfeld Miller, Miriam ^a   Ackermann, Martin ^a,b   Vorholt, Julia A ^a  

^a ETH ZURICH   (Switzerland)

^b Department of Environmental Sciences ETH Zurich ^*  (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ETHYLENE; RNA 16S;

ARABIDOPSIS THALIANA; ARTHROBACTER; ARTICLE; CONTROLLED STUDY; EIN2 GENE; ENVIRONMENTAL FACTOR; GENE; GENOTYPE; GNOTOBIOTICS; HOST; LACS2 GENE; MICROBIAL COMMUNITY; MICROFLORA; NONHUMAN; NUCLEOTIDE SEQUENCE; PEC1 GENE; PHYLOGENY; PLANT GENETICS; RHODOCOCCUS; SIGNAL TRANSDUCTION; VARIOVORAX; ALLELE; ARABIDOPSIS; CELL WALL; GENETICS; MICROBIOLOGY; MUTATION; PLANT LEAF;

ALLELES; ARABIDOPSIS; CELL WALL; GENOTYPE; MICROBIOTA; MUTATION; PHYLOGENY; PLANT LEAVES; RNA, RIBOSOMAL, 16S;

EID: 84901342373     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004283     Document Type: Article

References (79)

1. Vorholt JA, (2012) Microbial life in the phyllosphere. Nature Rev Microbiol 10: 828-840.
2. Berendsen RL, Pieterse CM, Bakker PA, (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17: 478-486.
3. Berg G, (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84: 11-18.
4. Conrath U, Beckers GJ, Flors V, Garcia-Agustin P, Jakab G, et al. (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19: 1062-1071.
5. Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC, (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28: 489-521.
6. Innerebner G, Knief C, Vorholt JA, (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. Cabrefiga J, Bonaterra A, Montesinos E, (2007) Mechanisms of antagonism of Pseudomonas fluorescens EPS62e against Erwinia amylovora, the causal agent of fire blight. Intern Microbiol 10: 123-132.
8. Weiher E, Freund D, Bunton T, Stefanski A, Lee T, 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. Lawton JH, (1999) Are there general laws in ecology? Oikos 84: 177-192.
10. Vellend M, (2010) Conceptual synthesis in community ecology. Quart Rev Biol 85: 183-206.
11. Nemergut DR, Schmidt SK, Fukami T, O'Neill SP, Bilinski TM, et al. (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77: 342-356.
12. Meyer KM, Leveau JHJ, (2012) Microbiology of the phyllosphere: a playground for testing ecological concepts. Oecologia 168: 621-629.
13. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, et al. (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci U S A 106: 16428-16433.
14. Lindow SE, Brandl MT, (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69: 1875-1883.
15. Beattie GA, (2011) Water relations in the interaction of foliar bacterial pathogens with plants. Annu Rev Phytopathol 49: 533-555.
16. Knief C, Ramette A, Frances L, Alonso-Blanco C, Vorholt JA, (2010) Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J 4: 719-728.
17. Ercolani GL, (1991) Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microbial Ecol 21: 35-48.
18. Yang CH, Crowley DE, Borneman J, Keen NT, (2001) Microbial phyllosphere populations are more complex than previously realized. Proc Natl Acad Sci U S A 98: 3889-3894.
19. Rasche F, Trondl R, Naglreiter C, Reichenauer T, Sessitsch A, (2006) Chilling and cultivar type affect the diversity of bacterial endophytes colonizing sweet pepper (Capsicum anuum L.). Can J Microbiol 52: 1036-1045.
20. Hunter PJ, Hand P, Pink D, Whipps JM, Bending GD, (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. Rastogi G, Sbodio A, Tech JJ, Suslow TV, Coaker GL, et al. (2012) Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J 6: 1812-1822.
22. Kinkel LL, Wilson M, Lindow SE, (2000) Plant species and plant incubation conditions influence variability in epiphytic bacterial population size. Microb Ecol 39: 1-11.
23. Balint-Kurti P, Simmons SJ, Blum JE, Ballare CL, Stapleton AE, (2010) Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection. Mol Plant Microbe Interact 23: 473-484.
24. Smith KP, Handelsman J, Goodman RM, (1999) Genetic basis in plants for interactions with disease-suppressive bacteria. Proc Natl Acad Sci U S A 96: 4786-4790.
25. Kniskern JM, Traw MB, Bergelson J, (2007) Salicylic acid and jasmonic acid signaling defense pathways reduce natural bacterial diversity on Arabidopsis thaliana. Mol Plant Microbe Interact 20: 1512-1522.
26. Reisberg EE, Hildebrandt U, Riederer M, Hentschel U, (2012) Phyllosphere bacterial communities of trichome-bearing and trichomeless Arabidopsis thaliana leaves. Ant Van Leeuwenhoek 101: 551-560.
27. Gomez-Gomez L, Boller T, (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003-1011.
28. Jones JD, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
29. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, et al. (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468: 527-532.
30. Grallath S, Weimar T, Meyer A, Gumy C, Suter-Grotemeyer M, et al. (2005) The AtProT family. Compatible solute transporters with similar substrate specificity but differential expression patterns. Plant Physiol 137: 117-126.
31. Buer CS, Muday GK, (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. Buer CS, Imin N, Djordjevic MA, (2010) Flavonoids: new roles for old molecules. J Integr Plant Biol 52: 98-111.
33. Sy A, Timmers AC, Knief C, Vorholt JA, (2005) Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions. Appl Environ Microbiol 71: 7245-7252.
34. Faith JJ, McNulty NP, Rey FE, Gordon JI, (2011) Predicting a human gut microbiota's response to diet in gnotobiotic mice. Science 333: 101-104.
35. McNulty NP, Yatsunenko T, Hsiao A, Faith JJ, Muegge BD, 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. Bodenhausen N, Horton MW, Bergelson J, (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. Plos One 8: e56329.
37. Knief C, Frances L, Vorholt JA, (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. Ramette A, (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75: 2495-2505.
39. Kembel SW, Wu M, Eisen JA, Green JL, (2012) Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLoS Comput Biol 8: e1002743.
40. Bessire M, Chassot C, Jacquat AC, Humphry M, Borel S, et al. (2007) A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J 26: 2158-2168.
41. Bessire M, Borel S, Fabre G, Carraca L, Efremova N, 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. Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR, (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284: 2148-2152.
43. Guzman P, Ecker JR, (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2: 513-523.
44. Zhao Q, Guo HW, (2011) Paradigms and paradox in the ethylene signaling pathway and interaction network. Mol Plant 4: 626-634.
45. Schnurr J, Shockey J, Browse J, (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. Schreiber L, Krimm U, Knoll D, Sayed M, Auling G, et al. (2005) Plant-microbe interactions: identification of epiphytic bacteria and their ability to alter leaf surface permeability. New Phytologist 166: 589-594.
50. Marcell LM, Beattie GA, (2002) Effect of leaf surface waxes on leaf colonization by Pantoea agglomerans and Clavibacter michiganensis. Mol Plant Microbe Interact 15: 1236-1244.
51. Reisberg EE, Hildebrandt U, Riederer M, Hentschel U, (2013) Distinct phyllosphere bacterial communities on Arabidopsis wax mutant leaves. Plos One 8: e78613.
52. Yadav RKP, Karamanoli K, Vokou D, (2005) Bacterial colonization of the phyllosphere of Mediterranean perennial species as influenced by leaf structural and chemical features. Microb Ecol 50: 185-196.
53. Tang DZ, Simonich MT, Innes RW, (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. Bleecker AB, Kende H, (2000) Ethylene: A gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16: 1-18.
55. Muday GK, Rahman A, Binder BM, (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17: 181-195.
56. van Loon LC, Geraats BPJ, Linthorst HJM, (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11: 184-191.
57. Fukuda H, Ogawa T, Tanase S, (1993) Ethylene production by microorganisms. Adv Microbial Physiol 35: 275-306.
58. Volksch B, Weingart H, (1998) Toxin production by pathovars of Pseudomonas syringae and their antagonistic activities against epiphytic microorganisms. J Basic Microbiol 38: 135-145.
59. Saleem M, Arshad M, Hussain S, Bhatti AS, (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Indust Microbiol Biotechnol 34: 635-648.
60. Doornbos RF, Geraats BPJ, Kuramae EE, Van Loon LC, Bakker PAHM, (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. Long HH, Sonntag DG, Schmidt DD, Baldwin IT, (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. Koornneef M, Alonso-Blanco C, Vreugdenhil D, (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55: 141-172.
63. Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, et al. (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465: 627-631.
64. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, et al. (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488: 86-90.
65. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, et al. (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488: 91-95.
66. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, 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. Peyraud R, Kiefer P, Christen P, Massou S, Portais JC, 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-Emsermann MN, Tecon R, Kowalchuk GA, Leveau JH, (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. Borneman J, Triplett EW, (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. Chelius MK, Triplett EW, (2001) The diversity of archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 41: 252-263.
72. Hodkinson BP, Lutzoni F, (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49: 163-180.
73. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR, (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17.
74. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, et al. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45.
75. Tornero P, Dangl JL, (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. Anderson MJ, (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
78. Ito H, Iizuka H, (1971) Taxonomic studies on a radio-resistant Pseudomonas. XII. Studies on microorganisms of cereal grain. Agricultural Biol Chem 35: 1566-1571.
79. Rivas R, Abril A, Trujillo ME, Velazquez E, (2004) Sphingomonas phyllosphaerae sp nov., from the phyllosphere of Acacia caven in Argentina. Int J System Evol Microbiol 54: 2147-2150.