Microbial genome-enabled insights into plant-microorganism interactions

Nature Reviews Genetics

Volumn 15, Issue 12, 2014, Pages 797-813

  Guttman, David S ^a   McHardy, Alice C ^b,c   Schulze Lefert, Paul ^c,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c Heinrich Heine Universität and Cluster of Excellence on Plant Sciences   (Germany)

^d MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; DNA SEQUENCE; FUNGAL COMMUNITY; GENETIC VARIABILITY; GENOME SIZE; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; HOST RANGE; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL GENOME; NEXT GENERATION SEQUENCING; NODULATION; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; PLANT DISEASE; PLANT IMMUNITY; PLANT MICROORGANISM INTERACTION; PRIORITY JOURNAL; REPRODUCTION; REVIEW; RHIZOSPHERE; SPECIES DIFFERENTIATION; TRANSPOSON; TYPE III SECRETION SYSTEM; TYPE VI SECRETION SYSTEM; BACTERIA; BACTERIAL PHENOMENA AND FUNCTIONS; CLASSIFICATION; CROP; FUNGUS; IMMUNOLOGY; MICROBIOLOGY; PHYSIOLOGY; PLANT;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; CROPS, AGRICULTURAL; FUNGI; GENOME, MICROBIAL; HOST SPECIFICITY; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; PLANTS;

EID: 84922335265     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg3748     Document Type: Review

References (171)

1. Jones, J. D. G., & Dangl, J. L. The plant immune system. Nature 444, 323-329 (2006
2. Dodds, P. N., & Rathjen, J. P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Rev. Genet. 11, 539-548 (2010
3. Thomma, B. P., Nurnberger, T., & Joosten, M. H. Of pamps and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23, 4-15 (2011
4. Boller, T., & Felix, G. A renaissance of elicitors: Perception of microbe-Associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379-406 (2009
5. Brunner, F. et al. Pep-13, a plant defense-inducing pathogen-Associated pattern from phytophthora transglutaminases. EMBO J. 21, 6681-6688 (2002
6. de Jonge, R. et al. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl Acad. Sci. USA 109, 5110-5115 (2012
7. Liebrand, T. W. H. et al. Receptor-like kinase SOBIR/EVR interacts with receptor-like proteins in plant immunity against fungal infection Proc. Natl Acad. Sci. USA 110, 10010-10015 (2013
8. Stergiopoulos, I. et al. Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. Proc. Natl Acad. Sci. USA 107, 7610-7615 (2010
9. Maekawa, T., Kufer, T. A., & Schulze-Lefert, P. NLR functions in plant and animal immune systems: so far and yet so close. Nature Immunol. 12, 818-826 (2011
10. Panstruga, R., & Dodds, P. N. Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science 324, 748-750 (2009
11. Kale, S. D. et al. External lipid Pi3p mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142, 284-295 (2010
12. Petre, B., & Kamoun, S. How do filamentous pathogens deliver effector proteins into plant cells PLoS Biol. 12, e1001801 (2014
13. Lewis, J. D., Guttman, D. S., & Desveaux, D. The targeting of plant cellular systems by injected type III effector proteins. Semin. Cell Dev. Biol. 20, 1055-1063 (2009
14. Vetter, M. M. et al. Flagellin perception varies quantitatively in Arabidopsis thaliana and its relatives. Mol. Biol. Evol. 29, 1655-1667 (2012
15. Bulgarelli, D., Schlaeppi, K., Spaepen, S., Ver Loren van Themaat, E., & Schulze-Lefert, P. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64, 807-838 (2013
16. Vorholt, J. A. Microbial life in the phyllosphere. Nature Rev. Microbiol. 10, 828-840 (2012
17. Flor, H. H. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275-296 (1971
18. Keen, N. T. Specific elicitors of plant phytoalexin production - determinants of race specificity in pathogens. Science 187, 74-75 (1975
19. Staskawicz, B. J., Sahlbeck, D., & Keen, N. T. Cloned avirulence gene of Pseudomonas syringae pathovar glycinea determines race-specific incompatiblity of Glycine max. Proc. Natl Acad. Sci. USA 81, 6024-6028 (1984
20. Napoli, C., & Staskawicz, B. Molecular characterization and nucleic-Acid sequence of an avirulence gene from race 6 of Pseudomonas syringae pv glycinea. J. Bacteriol. 169, 572-578 (1987
21. Lindgren, P. B., Peet, R. C., & Panopoulos, N. J. Gene cluster of Pseudomonas syringae pv.phaseolicola controls pathogenicity of bean plants and hypersensitivity of nonhost plants. J. Bacteriol. 168, 512-522 (1986
22. Fenselau, S., Balbo, I., & Bonas, U. Determinants of pathogenicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in secretion in bacterial pathogens of animals. Mol. Plant Microbe Interact. 5, 390-396 (1992
23. Gough, C. L., Genin, S., Zischek, C., & Boucher, C. A. hrp genes of Pseudomonas solanacearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria. Mol. Plant Microbe Interact. 5, 384-389 (1992
24. Guttman, D. S., Vinatzer, B. A., Sarkar, S. F., Ranall, M., & Greenberg, J. T. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295, 1722-1726 (2002
25. Chang, J. H. et al. A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proc. Natl Acad. Sci. USA 102, 2549-2554 (2005
26. Roden, J. A. et al. A genetic screen to isolate type III effectors translocated into pepper cells during Xanthomonas infection. Proc. Natl Acad. Sci. USA 101, 16624-16629 (2004
27. Fouts, D. E. et al. Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the hrpl alternative sigma factor. Proc. Natl Acad. Sci. USA 99, 2275-2280 (2002
28. Schechter, L. M., Roberts, K. A., Jamir, Y., Alfano, J. R., & Collmer, A. Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a cya translocation reporter. J. Bacteriol. 186, 543-555 (2004
29. Ferreira, A. O. et al. Whole-genome expression profiling defines the hrpl regulon of Pseudomonas syringae pv. tomato DC3000, allows de novo reconstruction of the Hrp cis clement, and identifies novel coregulated genes. Mol. Plant-Microbe Interact. 19, 1167-1179 (2006
30. Petnicki-Ocwieja, T. et al. Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. Proc. Natl Acad. Sci. USA 99, 7652-7657 (2002
31. Vencato, M. et al. Bioinformatics-enabled inventory of the hrp regulon and type III secretion system effector proteins of Pseudomonas syringae pv. phaseolicola 1448a. Mol. Plant-Microbe Interact. 19, 1193-1206 (2006
32. Arnold, R. et al. Sequence-based prediction of type III secreted proteins. PLoS Pathog. 5, e1000376 (2009
33. Yang, Y., Zhao, J., Morgan, R. L., Ma, W., & Jiang, T. Computational prediction of type III secreted proteins from Gram-negative bacteria. BMC Bioinformatics 11 (Suppl. 1), S47 (2010
34. Lower, M., & Schneider, G. Prediction of type III secretion signals in genomes of gram-negative bacteria. PLoS ONE 4, e5917 (2009
35. Buell, C. R. et al. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl Acad. Sci. USA 100, 10181-10186 (2003
36. Feil, H. et al. Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae b728a and pv. tomato DC3000. Proc. Natl Acad. Sci. USA 102, 11064-11069 (2005
37. Joardar, V. et al. Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448a reveals divergence among pathovars in genes involved in virulence and transposition. J. Bacteriol. 187, 6488-6498 (2005
38. Lindeberg, M. et al. Closing the circle on the discovery of genes encoding Hrp regulon members and type III secretion system effectors in the genomes of three model Pseudomonas syringae strains. Mol. Plant-Microbe Interact. 19, 1151-1158 (2006
39. Baltrus, D. A. et al. Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Path. 7, 22 (2011
40. Bart, R. et al. High-throughput genomic sequencing of cassava bacterial blight strains identifies conserved effectors to target for durable resistance. Proc. Natl Acad. Sci. USA 109, E1972-E1979 (2012
41. Boch, J., & Bonas, U. Xanthomonas avrbs3 family-type III effectors: discovery and function. Annu. Rev. Phytopathol. 48, 419-436 (2010
42. O'Brien, H. E. et al. Extensive remodeling of the Pseudomonas syringae pv. avellanae type III secretome associated with two independent host shifts onto hazelnut. BMC Microbiol. 12, 141 (2012
43. Wang, P. W., Morgan, R. L., Scortichini, M., & Guttman, D. S. Convergent evolution of phytopathogenic pseudomonads onto hazelnut. Microbiology 153, 2067-2073 (2007
44. Hogenhout, S. A. et al. Phytoplasmas: bacteria that manipulate plants and insects. Mol. Plant Pathol. 9, 403-423 (2008
45. Bai, X. D. et al. AY-WB phytoplasma secretes a protein that targets plant cell nuclei. Mol. Plant-Microbe Interact. 22, 18-30 (2009
46. Oshima, K. et al. Dramatic transcriptional changes in an intracellular parasite enable host switching between plant and insect. PLoS ONE 6, e23242 (2011
47. Sugio, A., Kingdom, H. N., MacLean, A. M., Grieve, V. M., & Hogenhout, S. A. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proc. Natl Acad. Sci. USA 108, E1254-E1263 (2011
48. Sawada, H., Kuykendall, L. D., & Young, J. M. Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J. Gen. Appl. Microbiol. 49, 155-179 (2003
49. Amadou, C. et al. Genome sequence of the ?-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res. 18, 1472-1483 (2008
50. Masson-Boivin, C., Giraud, E., Perret, X., & Batut, J. Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes Trends Microbiol. 17, 458-466 (2009
51. Giraud, E. et al. Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316, 1307-1312 (2007
52. Fauvart, M., & Michiels, J. Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiol. Lett. 285, 1-9 (2008
53. Okazaki, S. et al. Identification and functional analysis of type III effector proteins in Mesorhizobium loti. Mol. Plant-Microbe Interact. 23, 223-234 (2010
54. Okazaki, S., Kaneko, T., Sato, S., & Saeki, K. Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. Proc. Natl Acad. Sci. USA 110, 17131-17136 (2013
55. Bozkurt, T. O., Schornack, S., Banfield, M. J., & Kamoun, S. Oomycetes, effectors, and all that jazz. Curr. Opin. Plant Biol. 15, 483-492 (2012
56. de Jonge, R. et al. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 23, 1271-1282 (2013
57. Duplessis, S. et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc. Natl Acad. Sci. USA 108, 9166-9171 (2011
58. Hacquard, S. et al. Mosaic genome structure of the barley powdery mildew pathogen and conservation of transcriptional programs in divergent hosts. Proc. Natl Acad. Sci. USA 110, E2219-E2228 (2013
59. Kemen, E. et al. Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biol. 9, e1001094 (2011
60. Nemri, A. et al. The genome sequence and effector complement of the flax rust pathogen Melampsora lini. Front. Plant Sci. 5, 98 (2014
61. O'Connell, R. J. et al. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nature Genet. 44, 1060-1065 (2012
62. Raffaele, S. et al. Genome evolution following host jumps in the irish potato famine pathogen lineage. Science 330, 1540-1543 (2010
63. Schirawski, J. et al. Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330, 1546-1548 (2010
64. Spanu, P. D. et al. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330, 1543-1546 (2010
65. Wicker, T. et al. The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nature Genet. 45, 1092-1096 (2013
66. Pedersen, C. et al. Structure and evolution of barley powdery mildew effector candidates. BMC Genomics 13, 694 (2012
67. Coleman, J. J. et al. The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet. 5, e1000618 (2009
68. Croll, D., & McDonald, B. A. The accessory genome as a cradle for adaptive evolution in pathogens. PLoS Pathog. 8, e1002608 (2012
69. Ma, L. J. et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464, 367-373 (2010
70. Rouxel, T. et al. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nature Commun. 2, 202 (2011
71. Van de Wouw, A. P. et al. Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog. 6, e1001180 (2010
72. Raffaele, S., & Kamoun, S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nature Rev. Microbiol. 10, 417-430 (2012
73. Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431-437 (2013
74. Win, J. et al. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 19, 2349-2369 (2007
75. Kryazhimskiy, S., & Plotkin, J. B. The population genetics of dN/dS. PLoS Genet. 4, e1000304 (2008
76. Stukenbrock, E. H. et al. The making of a new pathogen: insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Res. 21, 2157-2166 (2011
77. Giraldo, M. C. et al. Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nature Commun. 4, 1996 (2013
78. Martin, F. et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452, 88-92 (2008
79. Martin, F. et al. Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464, 1033-1038 (2010
80. Tisserant, E. et al. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis Proc. Natl Acad. Sci. USA 111, 20117-20122 (2013
81. Zuccaro, A. et al. Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7, e1002290 (2011
82. Kloppholz, S., Kuhn, H., & Requena, N. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21, 1204-1209 (2011
83. Richards, T. A. et al. Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc. Natl Acad. Sci. USA 108, 15258-15263 (2011
84. Friesen, T. L. et al. Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genet. 38, 953-956 (2006
85. Loper, J. E. et al. Comparative genomics of plant-Associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet. 8, e1002784 (2012
86. Yoshida, K. et al. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 21, 1573-1591 (2009
87. Wittenberg, A. H. J. et al. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS ONE 4, e5863 (2009
88. Tzeng, T. H., Lyngholm, L. K., Ford, C. F., & Bronson, C. R. A restriction-fragment-length-polymorphism map and electrophoretic karyotype of the fungal maize pathogen Cochliobolus heterostrophus. Genetics 130, 81-96 (1992
89. Leclair, S., AnsanMelayah, D., Rouxel, T., & Balesdent, M. H. Meiotic behaviour of the minichromosome in the phytopathogenic ascomycete Leptosphaeria maculans. Curr. Genet. 30, 541-548 (1996
90. Hatta, R. et al. A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161, 59-70 (2002
91. Chuma, I., Tosa, Y., Taga, M., Nakayashiki, H., & Mayama, S. Meiotic behavior of a supernumerary chromosome in Magnaporthe oryzae. Curr. Genet. 43, 191-198 (2003
92. Gale, L. R., Katan, T., & Kistler, H. C. The probable center of origin of Fusarium oxysporum f. sp lycopersici vcg 0033. Plant Dis. 87, 1433-1438 (2003
93. Heitman, J., Kronstad, J. W., Taylor, J. W., & Casselton, L. A. (ed.) Sex in Fungi: Molecular Determination and Evolutionary Implications (ASM Press, 2007
94. Chen, R. S., & McDonald, B. A. Sexual reproduction plays a major role in the genetic structure of populations of the fungus Mycosphaerella graminicola. Genetics 142, 1119-1127 (1996
95. Stukenbrock, E. H., Christiansen, F. B., Hansen, T. T., Dutheil, J. Y., & Schierup, M. H. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. Proc. Natl Acad. Sci. USA 109, 10954-10959 (2012
96. Knief, C., Delmotte, N., & Vorholt, J. A. Bacterial adaptation to life in association with plants - a proteomic perspective from culture to in situ conditions. Proteomics 11, 3086-3105 (2011
97. Hugenholtz, P. Exploring prokaryotic diversity in the genomic era. Genome Biol. 3, REVIEWS0003 (2002
98. Riesenfeld, C. S., Schloss, P. D., & Handelsman, J. Metagenomics: genomic analysis of microbial communities. Annu. Rev. Genet. 38, 525-552 (2004
99. Xu, L., Ravnskov, S., Larsen, J., & Nicolaisen, M. Linking fungal communities in roots, rhizosphere, and soil to the health status of Pisum sativum. FEMS Microbiol. Ecol. 82, 736-745 (2012
100. Turner, T. R. et al. Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J. 7, 2248-2258 (2013
101. Berg, G., & Smalla, K. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68, 1-13 (2009
102. Hirsch, P. R., & Mauchline, T. H. Who's who in the plant root microbiome? Nature Biotech. 30, 961-962 (2012
103. Dennis, P. G., Miller, A. J., & Hirsch, P. R. Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities FEMS Microbiol. Ecol. 72, 313-327 (2010
104. Uroz, S., Buee, M., Murat, C., Frey-Klett, P., & Martin, F. Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ. Microbiol. Rep. 2, 281-288 (2010
105. Badri, D. V. et al. An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol. 151, 2006-2017 (2009
106. Badri, D. V., Zolla, G., Bakker, M. G., Manter, D. K., & Vivanco, J. M. Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. New Phytol. 198, 264-273 (2013
107. Berendsen, R. L., Pieterse, C. M., & Bakker, P. A. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478-486 (2012
108. Mendes, R., Garbeva, P., & Raaijmakers, J. M. The rhizosphere microbiome: significance of plant-beneficial, plant-pathogenic and human-pathogenic microorganisms. FEMS Microbiol. Rev. 37, 634-663 (2013
109. Mendes, R. et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097-1100 (2011
110. Peiffer, J. A. et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl Acad. Sci. USA 110, 6548-6553 (2013
111. Lundberg, D. S. et al. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86-90 (2012
112. Bulgarelli, D. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91-95 (2012
113. Burke, C., Steinberg, P., Rusch, D., Kjelleberg, S., & Thomas, T. Bacterial community assembly based on functional genes rather than species. Proc. Natl Acad. Sci. USA 108, 14288-14293 (2011
114. Wang, H. B. et al. Characterization of metaproteomics in crop rhizospheric soil. J. Proteome Res. 10, 932-940 (2011
115. Wu, L., Wang, H., Zhang, Z., Lin, R., & Lin, W. Comparative metaproteomic analysis on consecutively Rehmannia glutinosa-monocultured rhizosphere soil. PLoS ONE 6, e20611 (2011
116. Knief, C. et al. Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J. 6, 1378-1390 (2012
117. Gottel, N. R. et al. Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl. Environ. Microbiol. 77, 5934-5944 (2011
118. Schlaeppi, K., Dombrowski, N., Oter, R. G., Ver Loren van Themaat, E., & Schulze-Lefert, P. Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc. Natl Acad. Sci. USA 111, 585-592 (2014
119. Lopez-Velasco, G., Welbaum, G. E., Boyer, R. R., Mane, S. P., & Ponder, M. A. Changes in spinach phylloepiphytic bacteria communities following minimal processing and refrigerated storage described using pyrosequencing of 16s rRNA amplicons. J. Appl. Microbiol. 110, 1203-1214 (2011
120. Balint, M. et al. Host genotype shapes the foliar fungal microbiome of balsam poplar (Populus balsamifera). PLoS ONE 8, e53987 (2013
121. Finkel, O. M., Burch, A. Y., Lindow, S. E., Post, A. F., & Belkin, S. Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl. Environ. Microbiol. 77, 7647-7655 (2011
122. Jumpponen, A., & Jones, K. L. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate quercus Macrocarpa phyllosphere. New Phytol. 184, 438-448 (2009
123. Kim, M. et al. Distinctive phyllosphere bacterial communities in tropical trees. Microb. Ecol. 63, 674-681 (2012
124. Knief, C., Ramette, A., Frances, L., Alonso-Blanco, C., & Vorholt, J. A. Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J. 4, 719-728 (2010
125. Koopman, M. M., & Carstens, B. C. The microbial phyllogeography of the carnivorous plant Sarracenia alata. Microb. Ecol. 61, 750-758 (2011
126. Koopman, M. M., Fuselier, D. M., Hird, S., & Carstens, B. C. The carnivorous pale pitcher plant harbors diverse, distinct, and time-dependent bacterial communities. Appl. Environ. Microbiol. 76, 1851-1860 (2010
127. Ottesen, A. R., White, J. R., Skaltsas, D. N., Newell, M. J., & Walsh, C. S. Impact of organic and conventional management on the phyllosphere microbial ecology of an apple crop. J. Food Prot. 72, 2321-2325 (2009
128. Redford, A. J., Bowers, R. M., Knight, R., Linhart, Y., & Fierer, N. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ. Microbiol. 12, 2885-2893 (2010
129. Redford, A. J., & Fierer, N. Bacterial succession on the leaf surface: a novel system for studying successional dynamics. Microb. Ecol. 58, 189-198 (2009
130. Rastogi, G. et al. Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J. 6, 1812-1822 (2012
131. Whipps, J. M., Hand, P., Pink, D., & Bending, G. D. Phyllosphere microbiology with special reference to diversity and plant genotype. J. Appl. Microbiol. 105, 1744-1755 (2008
132. Delmotte, N. et al. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl Acad. Sci. USA 106, 16428-16433 (2009
133. Altshuler, D., Daly, M. J., & Lander, E. S. Genetic mapping in human disease. Science 322, 881-888 (2008
134. Hirschhorn, J. N., & Daly, M. J. Genome-wide association studies for common diseases and complex traits. Nature Rev. Genet. 6, 95-108 (2005
135. Yoshida, K. et al. The rise and fall of the Phytophthora infestans lineage that triggered the irish potato famine. eLife 2, e00731 (2013
136. Eaton, C. J., Cox, M. P., & Scott, B. What triggers grass endophytes to switch from mutualism to pathogenism? Plant Sci. 180, 190-195 (2011
137. Bodenhausen, N., Bortfeld-Miller, M., Ackermann, M., & Vorholt, J. A. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genet. 10, 12 (2014
138. Lebeis, S. L., Rott, M., Dangl, J. L., & Schulze-Lefert, P. Culturing a plant microbiome community at the cross-rhodes. New Phytol. 196, 341-344 (2012
139. Mardis, E. R. Next-generation DNA sequencing methods. Annu. Rev. Genom. Hum. Genet. 9, 387-402 (2008
140. Schmidt, S. M., & Panstruga, R. Pathogenomics of fungal plant parasites: What have we learnt about pathogenesis Curr. Opin. Plant Biol. 14, 392-399 (2011
141. Proctor, L. M. The human microbiome project in 2011 and beyond. Cell Host Microbe 10, 287-291 (2011
142. Chin, C. S. et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nature Methods 10, 563-569 (2013
143. Baxter, L. et al. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330, 1549-1551 (2010
144. Nocker, A., Burr, M., & Camper, A. K. Genotypic microbial community profiling: a critical technical review. Microb. Ecol. 54, 276-289 (2007
145. Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541 (2009
146. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335-336 (2010
147. Quince, C., Lanzen, A., Davenport, R. J., & Turnbaugh, P. J. Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12, 38 (2011
148. Peng, Y., Leung, H. C., Yiu, S. M., & Chin, F. Y. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420-1428 (2012
149. Namiki, T., Hachiya, T., Tanaka, H., & Sakakibara, Y. Metavelvet: an extension of velvet assembler to de novo metagenome assembly from short sequence reads. Nucleic Acids Res. 40, e155 (2012
150. Boisvert, S., Raymond, F., Godzaridis, E., Laviolette, F., & Corbeil, J. Ray meta: scalable de novo metagenome assembly and profiling. Genome Biol. 13, R122 (2012
151. Stark, M., Berger, S. A., Stamatakis, A., & von Mering, C. MLTreeMap - accurate maximum likelihood placement of environmental DNA sequences into taxonomic and functional reference phylogenies. BMC Genomics 11, 461 (2010
152. Wu, M., & Scott, A. J. Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinformatics 28, 1033-1034 (2012
153. Wu, M., & Eisen, J. A. A simple, fast, and accurate method of phylogenomic inference. Genome Biol. 9, R151 (2008
154. Sunagawa, S. et al. Metagenomic species profiling using universal phylogenetic marker genes. Nature Methods 10, 1196-1199 (2013
155. Segata, N. et al. Metagenomic microbial community profiling using unique clade-specific marker genes. Nature Methods 9, 811-814 (2012
156. Patil, K. R. et al. Taxonomic metagenome sequence assignment with structured output models. Nature Methods 8, 191-192 (2011
157. Brady, A., & Salzberg, S. L. PHYMM and PHYMMBL: metagenomic phylogenetic classification with interpolated Markov models. Nature Methods 6, 673-676 (2009
158. Huson, D. H., Mitra, S., Ruscheweyh, H. J., Weber, N., & Schuster, S. C. Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21, 1552-1560 (2011
159. Glass, E. M., Wilkening, J., Wilke, A., Antonopoulos, D., & Meyer, F. Using the metagenomics RAST server (MG-RAST) for analyzing shotgun metagenomes. Cold Spring Harb. Protoc. 2010, pdb prot5368 (2010
160. Markowitz, V. M. et al. IMG/M: the integrated metagenome data management and comparative analysis system. Nucleic Acids Res. 40, D123-D129 (2012
161. Sun, S. et al. Community cyberinfrastructure for advanced microbial ecology research and analysis: the CAMERA resource. Nucleic Acids Res. 39, D546-D551 (2011
162. Leung, H. C., Yiu, S. M., Parkinson, J., & Chin, F. Y. IDBA-MT: de novo assembler for metatranscriptomic data generated from next-generation sequencing technology. J. Computat. Biol. 20, 540-550 (2013
163. Langmead, B., & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357-359 (2012
164. Li, H., & Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595 (2010
165. Schlotterer, C. Hitchhiking mapping - functional genomics from the population genetics perspective. Trends Genet. 19, 32-38 (2003
166. Pavlidis, P., Hutter, S., & Stephan, W. A population genomic approach to map recent positive selection in model species. Mol. Ecol. 17, 3585-3598 (2008
167. McCann, H. C., Nahal, H., Thakur, S., & Guttman, D. S. Identification of innate immunity elicitors using molecular signatures of natural selection. Proc. Natl Acad. Sci. USA 109, 4215-4220 (2012
168. Tibayrenc, M. Toward an integrated genetic epidemiology of parasitic protozoa and other pathogens. Annu. Rev. Genet. 33, 449-477 (1999
169. Chapman, N. H., & Thompson, E. A. Linkage disequilibrium mapping: The role of population history, size, and structure. Adv. Genet. 42, 413-437 (2001
170. Koonin, E. V. Orthologs, paralogs, and evolutionary genomics. Annu. Rev. Genet. 39, 309-338 (2005
171. Shade, A., McManus, P. S., & Handelsman, J. Unexpected diversity during community succession in the apple flower microbiome. MBio 4, e00602-e00612 (2013).