Metabolic footprint of epiphytic bacteria on Arabidopsis thaliana leaves

ISME Journal

Volumn 10, Issue 3, 2016, Pages 632-643

  Ryffel, Florian ^a   Helfrich, Eric J N ^a   Kiefer, Patrick ^a   Peyriga, Lindsay ^b,c,d   Portais, Jean Charles ^b,c,d   Piel, Jörn ^a   Vorholt, Julia A ^a  

^a ETH ZURICH   (Switzerland)

^b INSA   (France)

^c UMR792 INGÉNIERIE DES SYSTÈMES BIOLOGIQUES ET DES PROCÉDÉS   (France)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANNUAL PLANT; BACTERIUM; CARBOHYDRATE; COLONIZATION; EPIPHYTE; FOOTPRINT; GENOMICS; HETEROTROPHY; LEAF; METABOLISM; MICROBIAL ACTIVITY; ORGANIC MATTER; PATHOGEN; PHYLLOSPHERE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); METHYLOBACTERIUM EXTORQUENS; PSEUDOMONAS SYRINGAE PV. TOMATO; SPHINGOMONAS MELONIS;

ARABIDOPSIS; CARBOHYDRATE METABOLISM; ECOSYSTEM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PLANT LEAF; PSEUDOMONAS SYRINGAE; SPHINGOMONAS;

ARABIDOPSIS; CARBOHYDRATE METABOLISM; ECOSYSTEM; PLANT LEAVES; PSEUDOMONAS SYRINGAE; SPHINGOMONAS;

EID: 84940093005     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.141     Document Type: Article

References (65)

1. Abanda-Nkpwatt D, Müsch M, Tschiersch J, Boettner M, Schwab W. (2006). Molecular interaction between Methylobacterium extorquens and seedlings: growth promotion, methanol consumption, and localization of the methanol emission site. J Exp Bot. 57: 4025-4032.
2. Adio AM, Casteel CL, DeVos M, Kim JH, Joshi V, Li BH, et al. (2011). Biosynthesis and Defensive function of N-d-Acetylornithine, a jasmonateinduced Arabidopsis metabolite. Plant Cell. 23: 3303-3318.
3. Atamna-Ismaeel N, Finkel O, Glaser F, von Mering C, Vorholt JA, Koblížek M, et al. (2012). Bacterial anoxygenic photosynthesis on plant leaf surfaces. Env Microbiol Rep. 4: 209-216.
4. Beattie GA, Lindow SE. (1999). Bacterial colonization of leaves: a spectrum of strategies. Phytopathology. 89: 353-359.
5. BoDenhausen N, Horton MW, Bergelson J. (2013). Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. Plos ONE. 8: e56329.
6. Burch AY, Browne PJ, Dunlap CA, Price NP, Lindow SE. (2011). Comparison of biosurfactant Detection methods reveals hydrophobic surfactants and contact-regulated production. Environ Microbiol. 13: 2681-2691.
7. Chassot C, Buchala A, Schoonbeek HJ, Metraux JP, Lamotte O. (2008). Wounding of Arabidopsis leaves causes a powerful but transient protection against Botrytis infection. Plant J. 55: 555-567.
8. Choi YJ, Bourque D, Morel L, Groleau D, Míguez CB. (2006). Multicopy integration and expression of heterologous genes in Methylobacterium extorquens ATCC 55366. Appl Environ Microb. 72: 753-759.
9. Cuppels DA. (1986). Generation and characterization of Tn5 insertion mutations in Pseudomonas syringae pv. tomato. Appl Environ Microbiol. 51: 323-327.
10. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, et al. (2009). Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci USA. 106: 16428-16433.
11. Ebert B, Zöller D, Erban A, Fehrle I, Hartmann J, Niehl A, et al. (2010). Metabolic profiling of Arabidopsis thaliana epiDermal cells. J Exp Bot. 61: 1321-1335.
12. Effantin G, Rivasseau C, Gromova M, Bligny R, Hugouvieux-Cotte-Pattat N. (2011). Massive production of butanediol during plant infection by phytopathogenic bacteria of the genera Dickeya and Pectobacterium. Mol Microbiol. 82: 988-997.
13. Fiala V, Glad C, Martin M, Jolivet E, Derridj S. (1990). Occurrence of soluble carbohydrates on the phylloplane of maize (Zea mays L.): variations in relation to leaf heterogeneity and position on the plant. New Phytol. 115: 609-615.
14. Folkers A, Hüve K, Ammann C, Dindorf T, Kesselmeier J, Kleist E, et al. (2008). Methanol emissions from Deciduous tree species: DepenDence on temperature and light intensity. Plant Biology. 10: 65-75.
15. Gibon Y, UsaDel B, Blaesing OE, Kamlage B, Hoehne M, Trethewey R, et al. (2006). Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol. 7: R76.
16. Glawischnig E. (2007). Camalexin. Phytochemistry. 68: 401-406.
17. GouDeau DM, Parker CT, Zhou YG, Sela S, Kroupitski Y, Brandl MT. (2013). The Salmonella transcriptome in lettuce and cilantro soft rot reveals a niche overlap with the animal host intestine. Appl Environ Microb. 79: 250-262.
18. Gourion B, Francez-Charlot A, Vorholt JA. (2008). PhyR is involved in the general stress response of Methylobacterium extorquens AM1. J Bacteriol. 190: 1027-1035.
19. Grivet JP, Delort AM, Portais JC. (2003). NMR and microbiology: from physiology to metabolomics. Biochimie. 85: 823-840.
20. Horai H, Arita M, Kanaya S, Nihei Y, Ikeda T, Suwa K, et al. (2010). MassBank: A public repository for sharing mass spectral data for life sciences. J Mass Spectrom. 45: 703-714.
21. 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.
22. Joyner DC, Lindow SE. (2000). Heterogeneity of iron bioavailability on plants assessed with a whole-cell GFP-based bacterial biosensor. Microbiology. 146: 2435-2445.
23. Kaczmarczyk A, Hochstrasser R, Vorholt JA, Francez-Charlot A. (2014). Complex two-component signaling regulates the general stress response in Alphaproteobacteria. Proc Natl Acad Sci USA. 111: E5196-E5204.
24. Kawaguchi K, Yurimoto H, Oku M, Sakai Y. (2011). Yeast methylotrophy and autophagy in a methanoloscillating environment on growing Arabidopsis thaliana leaves. Plos ONE. 6: e25257.
25. Kiefer P, Buchhaupt M, Christen P, Kaup B, SchraDer J, Vorholt JA. (2009). Metabolite profiling uncovers plasmid-induced cobalt limitation unDer methylotrophic growth conditions. Plos ONE. 4: e7831.
26. Kiefer P, Schmitt U, Vorholt JA. (2013). eMZed: An open source framework in python for rapid and interactive Development of LC/MS data analysis workflows. Bioinformatics. 29: 963-964.
27. 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.
28. 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.
29. Knief C. (2014). Analysis of plant microbe interactions in the era of next generation sequencing technologies. Front Plant Sci. 5: 216.
30. Lambin EF, Meyfroidt P. (2011). Global land use change, economic globalization, and the looming land scarcity. Proc Natl Acad Sci USA. 108: 3465-3472.
31. Leveau JH, Lindow SE. (2001). Appetite of an epiphyte: Quantitative monitoring of bacterial sugar consumption in the phyllosphere. Proc Natl Acad Sci USA. 98: 3446-3453.
32. LinDeberg M, Cunnac S, Collmer A. (2012). Pseudomonas syringae type III effector repertoires: last words in endless arguments. Trends Microbiol. 20: 199-208.
33. Lindow SE, Leveau JH. (2002). Phyllosphere microbiology. Curr Opin Biotech. 13: 238-243.
34. Lindow SE, Brandl MT. (2003). Microbiology of the phyllosphere. Appl Environ Microb. 69: 1875-1883.
35. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, et al. (2012). Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol. 13: 614-629.
36. Mercier J, Lindow SE. (2000). Role of leaf surface sugars in colonization of plants by bacterial epiphytes. Appl Environ Microbiol. 66: 369-374.
37. Monier JM, Lindow SE. (2003). Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. Proc Natl Acad Sci USA. 100: 15977-15982.
38. Park DH, Mirabella R, Bronstein PA, Preston GM, Haring MA, Lim CK, et al. (2010). Mutations in ?-Aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. Plant J. 64: 318-330.
39. Peyraud R, Kiefer P, Christen P, Massou S, Portais JC, Vorholt JA. (2009). Demonstration of the ethylmalonyl-CoA pathway by using 13C metabolomics. Proc Natl Acad Sci USA. 106: 4846-4851.
40. Phelan VV, Liu WT, Pogliano K, Dorrestein PC. (2012). Microbial metabolic exchange-The chemotype-Tophenotype link. Nat Chem Biol. 8: 26-35.
41. Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA. (2014). Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol. 52: 347-375.
42. Reisberg EE, HilDebrandt U, RieDerer M, Hentschel U. (2013). Distinct phyllosphere bacterial communities on Arabidopsis wax mutant leaves. Plos ONE. 8: e78613.
43. Remus-Emsermann MN, Tecon R, Kowalchuk GA, Leveau JHJ. (2012). Variation in local carrying capacity and the individual fate of bacterial colonizers in the phyllosphere. ISME J. 6: 756-765.
44. Remus-Emsermann MN, Lücker S, Müller DB, Potthoff E, Daims H, Vorholt JA. (2014). Spatial distribution analyses of natural phyllospherecolonizing bacteria on Arabidopsis thaliana revealed by fluorescence in situ hybridization. Environ Microbiol. 16: 2329-2340.
45. Rico A, Preston GM. (2008). Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplastinduced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol Plant Microbe Interact. 21: 269-282.
46. Rico A, McCraw SL, Preston GM. (2011). The metabolic interface between Pseudomonas syringae and plant cells. Curr Opin Microbiol. 14: 31-38.
47. Rogers EE, Glazebrook J, Ausubel FN. (1996). MoDeof action of the Arabidopsis thaliana phytoalexin camalexin and its role in Arabidopsis-pathogen interactions. Mol Plant Microbe Interact. 9: 748-757.
48. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW. (2004). Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134: 1017-1026.
49. Schramm T, Hester A, Klinkert I, Both JP, Heeren RM, Brunelle A, et al. (2012). imzML - A common data format for the flexible exchange and processing of mass spectrometry imaging data. J Proteomics. 75: 5106-5110.
50. Schreiber L, Schönherr J. (2009). Water and Solute Permeability of Plant Cuticles: Measurement and Data Analysis. Springer: Berlin, New York
51. Schuhegger R, Nafisi M, Mansourova M, Petersen BL, Olsen CE, Svatoš A, et al. (2006). CYP71B15 (PAD3) catalyzes the final step in camalexin biosynthesis. Plant Physiol. 141: 1248-1254.
52. Sonnewald U, Brauer M, Vonschaewen A, Stitt M, Willmitzer L. (1991). Transgenic tobacco plants expressing yeast-Derived invertase in either the cytosol, vacuole or apoplast: a powerful tool for studying sucrose metabolism and sink/source interactions. Plant J. 1: 95-106.
53. Steeghs M, Bais HP, DeGouw J, Goldan P, Kuster W, Northway M, et al. (2004). Proton-Transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis. Plant Physiol. 135: 47-58.
54. 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 Microb. 71: 7245-7252.
55. Tukey HB. (1970). Leaching of Substances from Plants. Ann Rev Plant Physio. 21: 305.
56. van DeMortel JE, DeVos RC, Dekkers E, Pineda A, Guillod L, Bouwmeester K, et al. (2012). Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol. 160: 2173-2188.
57. van Der Wal A, Leveau JH. (2011). MoDelling sugar diffusion across plant leaf cuticles: the effect of free water on substrate availability to phyllosphere bacteria. Environ Microbiol. 13: 792-797.
58. Vogel C, Innerebner G, Zingg J, Guder J, Vorholt JA. (2012). Forward genetic in planta screen for iDentification of plant-protective traits of Sphingomonas sp strain Fr1 against Pseudomonas syringae DC3000. Appl Environ Microb. 78: 5529-5535.
59. Vorholt JA. (2012). Microbial life in the phyllosphere. Nat Rev Microbiol. 10: 828-840.
60. Ward JL, Forcat S, Beckmann M, Bennett M, Miller SJ, Baker JM, et al. (2010). The metabolic transition during disease following infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Plant J. 63: 443-457.
61. Wessling R, Epple P, Altmann S, He YJ, Yang L, Henz SR, et al. (2014). Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe. 16: 364-375.
62. Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters EC, et al. (2009). Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci USA. 106: 3698-3703.
63. Wilson M, Lindow SE. (1994). Coexistence among epiphytic bacterial-populations mediated through nutritional resource partitioning. Appl Environ Microb. 60: 4468-4477.
64. Zhang XL, Szydlowski N, Delvallé D, D'Hulst C, James MG, Myers AM. (2008). Overlapping functions of the starch synthases SSII and SSIII in amylopectin biosynthesis in Arabidopsis. BMC Plant Biol. 8: 96.
65. Zimmermann P, Laule O, Schmitz J, Hruz T, Bleuler S, Gruissem W. (2008). Genevestigator transcriptome meta-Analysis and biomarker search using rice and barley gene expression databases. Mol Plant. 1: 1088-1088.