Sniffing on microbes: Diverse roles of microbial volatile organic compounds in plant health

Molecular Plant-Microbe Interactions

Volumn 26, Issue 8, 2013, Pages 835-843

  Bitas, Vasileios ^a   Kim, Hye Seon ^b   Bennett, Joan W ^c   Kang, Seogchan ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VOLATILE ORGANIC COMPOUND;

BACTERIUM; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PLANT; REVIEW;

BACTERIA; MOLECULAR STRUCTURE; PLANTS; VOLATILE ORGANIC COMPOUNDS;

EID: 84880078845     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-10-12-0249-CR     Document Type: Review

References (94)

1. Bailly, A. l., and Weisskopf, L. 2012. The modulating effect of bacterial volatiles on plant growth: Current knowledge and future challenges. Plant Signal. Behav. 7: 79-85.
2. Baldwin, I. T. 2010. Plant volatiles. Curr. Biol. 20: 392-397.
3. Bednarek, P., Kwon, C., and Schulze-Lefert, P. 2010. Not a peripheral issue: Secretion in plant-microbe interactions. Curr. Opin. Plant Biol. 13: 378-387.
4. Beltran-Garcia, M. J., Estarron-Espinosa, M., and Ogura, T. 1997. Volatile compounds secreted by the oyster mushroom (Pleurotus ostreatus) and their antibacterial activities. J. Agric. Food. Chem. 45: 4049-4052.
5. Bennett, J. W., Hung, R., Lee, S., and Padhi, S. 2013. Fungal and bacterial volatile organic compounds: An overview and their role as ecological signaling agents. Pages 373-393 in: The Mycota IX Fungal Interactions. B. Hock, ed. Springer, Berlin
6. Berendsen, R. L., Pieterse, C. M. J., and Bakker, P. A. H. M. 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17: 478-486.
7. Bever, J. D., Dickie, I. A., Facelli, E., Facelli, J. M., Klironomos, J., Moora, M., Rillig, M. C., Stock, W. D., Tibbett, M., and Zobel, M. 2010. Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 25: 468-478.
8. Blom, D., Fabbri, C., Connor, E. C., Schiestl, F. P., Klauser, D. R., Boller, T., Eberl, L., and Weisskopf, L. 2011a. Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ. Microbiol. 13: 3047-3058.
9. Blom, D., Fabbri, C., Eberl, L., and Weisskopf, L. 2011b. Volatile-mediated killing of Arabidopsis thaliana by bacteria is mainly due to hydrogen cyanide. Appl. Environ. Microbiol. 77: 1000-1008.
10. Bonfante, P., and Anca, I. A. 2009. Plants, mycorrhizal fungi, and bacteria: A network of interactions. Annu. Rev. Microbiol. 63: 363-383.
11. Bruce, A., Stewart, D., Verrall, S., and Wheatley, R. E. 2003. Effect of volatiles from bacteria and yeast on the growth and pigmentation of sapstain fungi. Int. Biodeterior. Biodegrad. 51: 101-108.
12. Bruce, T. J. A., Wadhams, L. J., and Woodcock, C. M. 2005. Insect host location: A volatile situation. Trends Plant Sci. 10: 269-274.
13. Buée, M., De Boer, W., Martin, F., van Overbeek, L., and Jurkevitch, E. 2009. The rhizosphere zoo: An overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321: 189-212.
14. Cheng, S. S., Lin, H. Y., and Chang, S. T. 2005. Chemical composition and antifungal activity of essential oils from different tissues of Japanese cedar (Cryptomeria japonica). J. Agric. Food. Chem. 53: 614-619.
15. Chitarra, G. S., Abee, T., Rombouts, F. M., Posthumus, M. A., and Dijksterhuis, J. 2004. Germination of Penicillium paneum conidia is regulated by 1-octen-3-ol, a volatile self-inhibitor. Appl. Environ. Microbiol. 70: 2823-2829.
16. Chitarra, G. S., Abee, T., Rombouts, F. M., and Dijksterhuis, J. 2005. 1- octen-3-ol inhibits conidia germination of Penicillium paneum despite of mild effects on membrane permeability, respiration, intracellular pH, and changes the protein composition. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Ecol. 54: 67-75.
17. Cho, S. M., Kang, B. R., Han, S. H., Anderson, A. J., Park, J. Y., Lee, Y. H., Cho, B. H., Yang, K. Y., Ryu, C. M., and Kirn, Y. C. 2008. 2R,3Rbutanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 21: 1067-1075.
18. Cho, S. M., Kang, B. R., Kim, J. J., and Kim, Y. C. 2012. Induced systemic drought and salt tolerance by Pseudomonas chlororaphis O6 root colonization is mediated by ABA-independent stomatal closure. Plant Pathol. J. 28: 202-206.
19. Clavijo-McCormick, A., Unsicker, S. B., and Gershenzon, J. 2012. The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci. 17: 303-310.
20. Dubey, S. C., Suresh, M., and Singh, B. 2007. Evaluation of Trichoderma species against Fusarium oxysporum f. sp. ciceris for integrated management of chickpea wilt. Biol. Control 40: 118-127.
21. Dudareva, N., Negre, F., Nagegowda, D. A., and Orlova, I. 2006. Plant volatiles: Recent advances and future perspectives. Crit. Rev. Plant Sci. 25: 417-440.
22. Effmert, U., Kalderás, J., Warnke, R., and Piechulla, B. 2012. Volatile mediated interactions between bacteria and fungi in the soil. J. Chem. Ecol. 38: 665-703.
23. Ezenwa, V. O., Gerardo, N. M., Inouye, D. W., Medina, M. N., and Xavier, J. B. 2012. Animal behavior and the microbiome. Science 338: 198-199.
24. Ezquer, I., Li, J., Ovecka, M., Baroja-Fernandez, E., Munoz, F. J., Montero, M., de Cerio, J. D., Hidalgo, M., Sesma, M. T., Bahaji, A., Etxeberria, E., and Pozueta-Romero, J. 2010. Microbial volatile emissions promote accumulation of exceptionally high levels of starch in leaves in monoand dicotyledonous plants. Plant Cell Physiol. 51: 1674-1693.
25. Faldt, J., Jonsell, M., Nordlander, G., and Borg-Karlson, A. K. 1999. Volatiles of bracket fungi Fomitopsis pinicola and Fomes fomentarius and their functions as insect attractants. J. Chem. Ecol. 25: 567-590.
26. Farag, M. A., Ryu, C.-M., Sumner, L. W., and Pare, P. W. 2006. GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67: 2262-2268.
27. Fernando, W. G. D., Ramarathnam, R., Krishnamoorthy, A. S., and Savchuk, S. C. 2005. Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol. Biochem. 37: 955-964.
28. Gutierrez-Luna, F. M., Lopez-Bucio, J., Altamirano-Hernandez, J., Valencia-Cantero, E., de la Cruz, H. R., and Macias-Rodriguez, L. 2010. Plant growth-promoting rhizobacteria modulate root system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51: 75-83.
29. Han, S. H., Lee, S. J., Moon, J. H., Park, K. H., Yang, K. Y., Cho, B. H., Kim, K. Y., Kim, Y. W., Lee, M. C., Anderson, A. J., and Kim, Y. C. 2006. GacS-dependent production of 2R,3R-butanediol by Pseudomonas chlororaphis O6 is a major determinant for eliciting systemic resistance against Erwinia carotovora but not against Pseudomonas syringae pv. tabaci in tobacco. Mol. Plant-Microbe Interact. 19: 924-930.
30. Harman, G. 2011. Trichoderma - not just for biocontrol anymore. Phytoparasitica 39: 103-108.
31. Heil, M., and Karban, R. 2010. Explaining evolution of plant communication by airborne signals. Trends Ecol. Evol. 25: 137-144.
32. Herrmann, A., ed. 2010. The Chemistry and Biology of Volatiles. John Wiley & Sons, Chichester, U.K.
33. Humphris, S. N., Bruce, A., Buultjens, E., and Wheatley, R. E. 2002. The effects of volatile microbial secondary metabolites on protein synthesis in Serpula lacrymans. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 210: 215-219.
34. Hung, R., Lee, S., and Bennett, J. W. 2013. Arabidopsis thaliana as a model system for testing the effect of Trichoderma volatile organic compounds. Fungal Ecol. 6: 19-26.
35. Hynes, J., Müller, C., Jones, T., and Boddy, L. 2007. Changes in volatile production during the course of fungal mycelial interactions between Hypholoma fasciculare and Resinicium bicolor. J. Chem. Ecol. 33: 43-57.
36. Inderjit, and van der Putten, W. H. 2010. Impacts of soil microbial communities on exotic plant invasions. Trends Ecol. Evol. 25: 512-519.
37. Insam, H., and Seewald, M. S. A. 2010. Volatile organic compounds (VOC) in soils. Biol. Fertil. Soils 46: 199-213.
38. Kai, M., and Piechulla, B. 2009. Plant growth promotion due to rhizobacterial volatiles - An effect of CO2? FEBS (Fed. Eur. Biochem. Soc.) Lett. 583: 3473-3477.
39. Kai, M., Haustein, M., Molina, F., Petri, A., Scholz, B., and Piechulla, B. 2009. Bacterial volatiles and their action potential. Appl. Microbiol. Biotechnol. 81: 1001-1012.
40. Kaiser, R. 2006. Flowers and fungi use scents to mimic each other. Science 311: 806-807.
41. Kant, M. R., Bleeker, P. M., Van Wijk, M., Schuurink, R. C., and Haring, M. A. 2009. Plant volatiles in defence. Pages 613-666 in: Plant Innate Immunity, Academic Press, London.
42. Khan, M. S., Zaidi, A., Wani, P. A., Ahemad, M., and Oves, M. 2009. Functional diversity among plant growth-promoting rhizobacteria: Current status microbial strategies for crop improvement. Pages 105-132 in: Microbial Strategies for Crop Improvement. M. S. Khan, A. Zaidi, and J. Musarrat, eds. Springer, Berlin.
43. Kishimoto, K., Matsui, K., Ozawa, R., and Takabayashi, J. 2007. Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J. Gen. Plant Pathol. 73: 35-37.
44. Konopka, A. 2009. What is microbial community ecology? ISME J. 3: 1223-1230.
45. Kordali, S., Kotan, R., Mavi, A., Cakir, A., Ala, A., and Yildirim, A. 2005. Determination of the chemical composition and antioxidant activity of the essential oil of Artemisia dracunculus and of the antifungal and antibacterial activities of Turkish Artemisia absinthium, A. dracunculus, Artemisia santonicum, and Artemisia spicigera essential oils. J. Agric. Food Chem. 53: 9452-9458.
46. Kramer, R., and Abraham, W.-R. 2012. Volatile sesquiterpenes from fungi: What are they good for? Phytochem. Rev. 11: 15-37.
47. Kwon, Y. S., Ryu, C. M., Lee, S., Park, H. B., Han, K. S., Lee, J. H., Lee, K., Chung, W. S., Jeong, M. J., Kim, H. K., and Bae, D. W. 2010. Proteome analysis of Arabidopsis seedlings exposed to bacterial volatiles. Planta 232: 1355-1370.
48. Leeder, A. C., Palma-Guerrero, J., and Glass, N. L. 2011. The social network: Deciphering fungal language. Nat. Rev. Microbiol. 9: 440-451.
49. Lewis, W. J., vanLenteren, J. C., Phatak, S. C., and Tumlinson, J. H. 1997. A total system approach to sustainable pest management. Proc. Natl. Acad. Sci. U.S.A. 94: 12243-12248.
50. Lorito, M., Woo, S. L., Harman, G. E., and Monte, E. 2010. Translational research on Trichoderma: From 'omics to the field. Annu. Rev. Phytopathol. 48: 395-417.
51. Lundberg, D. S., Lebeis, S. L., Paredes, S. H., Yourstone, S., Gehring, J., Malfatti, S., Tremblay, J., Engelbrektson, A., Kunin, V., del Rio, T. G., Edgar, R. C., Eickhorst, T., Ley, R. E., Hugenholtz, P., Tringe, S. G., and Dangl, J. L. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488: 86-90.
52. Martin, F., and Kamoun, S., eds. 2012. Effectors in Plant-Microbe Interactions. Wiley-Blackwell, Oxford.
53. McCain, A. H. 1966. A volatile antibiotic produced by Streptomyces griseus. (Abstr.) Phytopathology 56: 150.
54. McNeal, K. S., and Herbert, B. E. 2009. Volatile organic metabolites as indicators of soil microbial activity and community composition shifts. Soil Sci. Soc. Am. J. 73: 579-588.
55. Mercier, J., and Smilanick, J. L. 2005. Control of green mold and sour rot of stored lemon by biofumigation with Muscodor albus. Biol. Control 32: 401-407.
56. Minerdi, D., Bossi, S., Gullino, M. L., and Garibaldi, A. 2009. Volatile organic compounds: A potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ. Microbiol. 11: 844-854.
57. Minerdi, D., Bossi, S., Maffei, M. E., Gullino, M. L., and Garibaldi, A. 2011. Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansin A5 gene expression through microbial volatile organic compound (MVOC) emission. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Ecol. 76: 342-351.
58. Morath, S., Hung, R., and Bennett, J. W. 2012. Fungal volatile organic compounds: A review with emphasis on their biotechnological potential. Fungal Biol. Rev. 30: 1-11.
59. Nemcovic, M., Jakubikova, L., Viden, I., and Farkas, V. 2008. Induction of conidiation by endogenous volatile compounds in Trichoderma spp. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 284: 231-236.
60. Pal, K. K., and McSpadden Gardener, B. 2007. Biological control of plant pathogens. The Plant Health Instructor. doi: 10.1094/PHI-A-2006-1117-02. Published online.
61. Porras-Alfaro, A., and Bayman, P. 2011. Hidden fungi, emergent properties: Endophytes and microbiomes. Annu. Rev. Phytopathol. 49: 291-315.
62. Ramin, A. A., Braun, P. G., Prange, R. K., and DeLong, J. M. 2005. In vitro effects of Muscodor albus and three volatile components on growth of selected postharvest microorganisms. HortScience 40: 2109-2114.
63. Reaves, M.-L., and Rabinowitz, J. D. 2011. Metabolomics in systems microbiology. Curr. Opin. Biotechnol. 22: 17-25.
64. Robert-Seilaniantz, A., Grant, M., and Jones, J. D. G. 2011. Hormone crosstalk in plant disease and defense: More than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49: 317-343.
65. Roy, B. A. 1993. Floral mimicry by a plant pathogen. Nature 362: 56-58.
66. Ryu, C.-M., Farag, M. A., Hu, C.-H., Reddy, M. S., Wei, H.-X., Pare, P. W., and Kloepper, J. W. 2003. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 100: 4927-4932.
67. Ryu, C.-M., Farag, M. A., Hu, C.-H., Reddy, M. S., Kloepper, J. W., and Pare, P. W. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134: 1017-1026.
68. Sardans, J., Penuelas, J., and Rivas-Ubach, A. 2011. Ecological metabolomics: Overview of current developments and future challenges. Chemoecology 21: 191-225.
69. Saunders, M., Glenn, A. E., and Kohn, L. M. 2010. Exploring the evolutionary ecology of fungal endophytes in agricultural systems: Using functional traits to reveal mechanisms in community processes. Evol. Appl. 3: 525-537.
70. Schiestl, F. P., Steinebrunner, F., Schulz, C., von Reuss, S., Francke, W., Weymuth, C., and Leuchtmann, A. 2006. Evolution of 'pollinator'- attracting signals in fungi. Biol. Lett. 2: 401-404.
71. Schulz, S., and Dickschat, J. S. 2007. Bacterial volatiles: The smell of small organisms. Nat. Prod. Rep. 24: 814-842.
72. Soylu, S., Yigitbas, H., Soylu, E. M., and Kurt, S. 2007. Antifungal effects of essential oils from oregano and fennel on Sclerotinia sclerotiorum. J. Appl. Microbiol. 103: 1021-1030.
73. Splivallo, R., Novero, M., Bertea, C. M., Bossi, S., and Bonfante, P. 2007. Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytol. 175: 417-424.
74. Steinebrunner, F., Schiestl, F. P., and Leuchtmann, A. 2008a. Ecological role of volatiles produced by Epichloë: Differences in antifungal toxicity. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Ecol. 64: 307-316.
75. Steinebrunner, F., Twele, R., Francke, W., Leuchtmann, A., and Schiestl, F.P. 2008b. Role of odour compounds in the attraction of gamete vectors in endophytic Epichloë fungi. New Phytol. 178: 401-411.
76. Strobel, G. 2006a. Harnessing endophytes for industrial microbiology. Curr. Opin. Microbiol. 9: 240-244.
77. Strobel, G. 2006b. Muscodor albus and its biological promise. J. Ind. Microbiol. Biotechnol. 33: 514-522.
78. Strobel, G. A., Dirkse, E., Sears, J., and Markworth, C. 2001. Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 147: 2943-2950.
79. Thacker, J. R. M., and Train, M. R. 2010. Use of volatiles in pest control. Pages 151-172 in: The Chemistry and Biology of Volatiles. John Wiley & Sons, Hoboken, NJ, U.S.A.
80. Thomma, B. P. H. J., Nurnberger, T., and Joosten, M. H. A. J. 2011. Of PAMPs and effectors: The blurred PTI-ETI dichotomy. Plant Cell 23: 4-15.
81. Verhulst, N. O., Mukabana, W. R., Takken, W., and Smallegange, R. C. 2011. Human skin microbiota and their volatiles as odour baits for the malaria mosquito Anopheles gambiae s.s. Entomol. Exp. Appl. 139: 170-179.
82. Vespermann, A., Kai, M., and Piechulla, B. 2007. Rhizobacterial volatiles affect the growth of 18 fungi and Arabidopsis thaliana. Appl. Environ. Microbiol. 73: 5639-5641.
83. Vickers, C. E., Gershenzon, J., Lerdau, M. T., and Loreto, F. 2009. A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat. Chem. Biol. 5: 283-291.
84. Wenke, K., Kai, M., and Piechulla, B. 2010. Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231: 499-506.
85. Wenke, K., Wanke, D., Kilian, J., Berendzen, K., Harter, K., and Piechulla, B. 2012a. Volatiles of two growth-inhibiting rhizobacteria commonly engage AtWRKY18 function. Plant J. 70: 445-459.
86. Wenke, K., Weise, T., Warnke, R., Valverde, C., Wanke, D., Kai, M., and Piechulla, B. 2012b. Bacterial volatiles mediating information between bacteria and plants. Pages 327-347 in: Biocommunication of Plants. G. Witzany and F. Baluska, eds. Springer-Verlag, Berlin.
87. Yi, H.-S., Ryu, C.-M., and Heil, M. 2010. Sweet smells prepare plants for future stress: Airborne induction of plant disease immunity. Plant Signal. Behav. 5: 528-531.
88. Zhang, C.-L., Wang, G.-P., Mao, L.-J., Komon-Zelazowska, M., Yuan, Z.-L., Lin, F.-C., Druzhinina, I. S., and Kubicek, C. P. 2010. Muscodor fengyangensis sp. nov. from southeast China: Morphology, physiology and production of volatile compounds. Fungal Biol. 114: 797-808.
89. Zhang, H., Kim, M.-S., Krishnamachari, V., Payton, P., Sun, Y., Grimson, M., Farag, M. A., Ryu, C.-M., Allen, R., Melo, I. S., and Pare, P. W. 2007. Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226: 839-851.
90. Zhang, H., Kim, M.-S., Sun, Y., Dowd, S. E., Shi, H. Z., and Pare, P. W. 2008a. Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol. Plant-Microbe Interact. 21: 737-744.
91. Zhang, H., Xie, X., Kim, M.-S., Kornyeyev, D. A., Holaday, S., and Pare, P. W. 2008b. Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J. 56: 264-273.
92. Zhang, P., and Chen, K. 2009. Age-dependent variations of volatile emissions and inhibitory activity toward Botrytis cinerea and Fusarium oxysporum in tomato leaves treated with chitosan oligosaccharide. J. Plant Biol. 52: 332-339.
93. Zhang, Z., and Li, G. 2010. A review of advances and new developments in the analysis of biological volatile organic compounds. Microchem. J. 95: 127-139.
94. Zou, C.-S., Mo, M.-H., Gu, Y.-Q., Zhou, J.-P., and Zhang, K.-Q. 2007. Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol. Biochem. 39: 2371-2379.