A Volatile Relationship: Profiling an Inter-Kingdom Dialogue Between two Plant Pathogens, Ralstonia Solanacearum and Aspergillus Flavus

Journal of Chemical Ecology

Volumn 40, Issue 5, 2014, Pages 502-513

  Spraker, Joseph E ^a   Jewell, Kelsea ^a   Roze, Ludmila V ^b   Scherf, Jacob ^a   Ndagano, Dora ^c   Beaudry, Randolph ^b   Linz, John E ^d   Allen, Caitilyn ^a   Keller, Nancy P ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d Michigan State University   (United States)

Author keywords

Aflatoxin; Aspergillus flavus; Conidiation; Extracellular polysaccharides; Inter kingdom; Ralstonia solanacearum; Volatile organic compounds

Indexed keywords

BACTERIUM; FUNGUS; GROUNDNUT; INTERSPECIFIC INTERACTION; PATHOGEN; POLYSACCHARIDE; TOXIN; VIRULENCE; VOLATILE ORGANIC COMPOUND;

ARACHIS HYPOGAEA; ASPERGILLUS FLAVUS; BACTERIA (MICROORGANISMS); FUNGI; RALSTONIA SOLANACEARUM;

AFLATOXIN; BACTERIAL POLYSACCHARIDE; VOLATILE ORGANIC COMPOUND;

ASPERGILLUS FLAVUS; METABOLISM; MICROBIOLOGY; ORGANISMAL INTERACTION; PEANUT; PHYSIOLOGY; PLANT DISEASE; RALSTONIA SOLANACEARUM;

AFLATOXINS; ARACHIS HYPOGAEA; ASPERGILLUS FLAVUS; MICROBIAL INTERACTIONS; PLANT DISEASES; POLYSACCHARIDES, BACTERIAL; RALSTONIA SOLANACEARUM; VOLATILE ORGANIC COMPOUNDS;

EID: 84902145334     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-014-0432-2     Document Type: Article

References (69)

1. Affeldt KJ, Brodhagen M, Keller NP (2012) Aspergillus oxylipin signaling and quorum sensing pathways depend on G protein-coupled receptors. Toxins (Basel) 4: 695-717.
2. Amaike S, Keller NP (2011) Aspergillus flavus. Annu Rev Phytopathol 49: 107-133.
3. Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotechnol 20: 642-650.
4. Berendsen RL, Pieterse CMJ, Bakker PHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17: 478-486.
5. Bitas V, Kim HS, Bennett JW, Kang S (2013) Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. Mol Plant Microbe Interact 26: 835-843.
6. Boucher C, van Gijsegem F, Barberis P, Arlat M, Zischek C (1987) Pseudomonas solanacearum genes controlling both pathogenicity on tomato and hypersensitivity on tobacco are clustered. J Bacteriol 169: 5626-5632.
7. Brodhagen M, Keller NP (2006) Signalling pathways connecting mycotoxin production and sporulation. Mol Plant Pathol 7: 285-301.
8. Brodhagen M, Tsitsigiannis DI, Hornung E, Goebel C, Feussner I, Keller NP (2008) Reciprocal oxylipin-mediated cross-talk in the Aspergillus-seed pathosystem. Mol Microbiol 67: 378-391.
9. Brown SH, Scott JB, Bhaheetharan J, Sharpee WC, Milde L, Wilson R, Keller NP (2009) Oxygenase coordination is required for morphological transition and the host-fungus interaction of Aspergillus flavus. Mol Plant Microbe Interact 22: 882-894.
10. Bruins M, Rahim Z, Bos A, van de Sande WWJ, Endtz HP, van Belkum A (2013) Diagnosis of active tuberculosis by e-nose analysis of exhaled air. Tuberculosis (Edinb) 93: 232-238, Elsevier Ltd.
11. Brumbley SM, Carney BF, Denny TP (1993) Phenotype conversion in pseudomonas solanacearum due to spontaneous inactivation of PhcA, a putative LysR transcriptional regulator. J Bacteriol 175: 5477-5487.
12. Campagnoli A, Cheli F, Savoini G, Crotti A, Pastori GM, Dell'Orto V (2009) Application of an electronic nose to detection of aflatoxins in corn. Vet Res Commun 33(1): 273-275.
13. Chakrabarti A, Singh R (2011) The emerging epidemiology of mould infections in developing countries. Curr Opin Infect Dis 24: 521-526.
14. Chambers ST, Scott-Thomas A, Epton M (2012) Developments in novel breath tests for bacterial and fungal pulmonary infection. Curr Opin Pulm Med 18: 228-232.
15. Chaurasia B, Pandey A, Palni LMS, Trivedi P, Kumar B, Colvin N (2005) Diffusible and volatile compounds produced by an antagonistic bacillus subtilis strain cause structural deformations in pathogenic fungi in vitro. Microbiol Res 160: 75-81.
16. Clough SJ, Flavier B, Schell M, Denny TP (1997) Differential expression of virulence genes and motility in ralstonia (Pseudomonas) solanacearum during exponential growth. Appl Environ Microbiol 63: 844-850.
17. Cugini C, Calfee MW, Farrow JM, Morales DK, Pesci EC, Hogan D (2007) Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol Microbiol 65: 896-906.
18. De Lucca J, Carter-Wientjes CH, Boué S, Bhatnagar D (2011) Volatile trans-2-hexenal, a soybean aldehyde, inhibits Aspergillus flavus growth and aflatoxin production in corn. J Food Sci 76: M381-M386.
19. De Lucca AJ, Boue SM, Carter-Wientjes C, Bhatnagar D (2012) Volatile profiles and aflatoxin production by toxigenic and non-toxigenic isolates of Aspergillus flavus grown on sterile and non-sterile cracked corn. Ann Agric Environ Med 19: 91-98.
20. Denny TP (2006) Plant pathogenic ralstonia species. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer Publishing, Dordrecht, pp 573-644.
21. Duran RM, Cary JW, Calvo AM (2009) The role of veA in Aspergillus flavus infection of peanut. Corn and Cotton Open Mycol J 3: 27-36.
22. Effmert U, Kalderás J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38: 665-703.
23. Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37: 955-964.
24. Flavier AB, Clough SJ, Schell MA, Denny TP (1997) Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in ralstonia solanacearum. Mol Microbiol 26: 251-259.
25. Forseth RR, Amaike S, Schwenk D, Affeldt KJ, Hoffmeister D, Schroeder FC, Keller NP (2013) Homologous NRPS-like gene clusters mediate redundant small-molecule biosynthesis in Aspergillus flavus. Angew Chem Int Ed Engl 52: 1590-1594.
26. Gandomi H, Misaghi A, Basti AA, Bokaei S, Khosravi A, Abbasifar A, Javan AJ (2009) Effect of zataria multiflora boiss. essential oil on growth and aflatoxin formation by Aspergillus flavus in culture media and cheese. Food Chem Toxicol 47: 2397-2400.
27. Gao X, Brodhagen M, Isakeit T, Brown SH, Göbel C, Betran J, Feussner I, Keller NP, Kolomiets MV (2009) Inactivation of the lipoxygenase ZmLOX3 increases susceptibility of maize to Aspergillus spp. Mol Plant Microbe Interact 22: 222-231.
28. Genin S, Denny TP (2012) Pathogenomics of the ralstonia solanacearum species complex. Annu Rev Phytopathol 50: 67-89.
29. Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3: 307-319.
30. Hanahan D (1985) DNA cloning. In: Glover DM (ed) A practical approach. IRL Press, McLean, p 109.
31. Hayward A (1991) Biology and epidemiology of bacterial wilt caused by pseudomonas solanacearum. Annu Rev Phytopathol 29: 65-87.
32. He Z-M, Price MS, Obrian GR, Georgianna DR, Payne GA (2007) Improved protocols for functional analysis in the pathogenic fungus Aspergillus flavus. BMC Microbiol 7: 104-114.
33. Hendrick CA, Sequeira L (1984) Lipopolysaccharide-defective mutants of the wilt pathogen Pseudomonas solanacearum. Appl Environ Microbiol 48: 94-101.
34. Hernández-Romero D, Solano F, Herna D, Sanchez-Amat A (2005) Polyphenol oxidase activity expression in ralstonia solanacearum. Appl Environ Microbiol 71: 6808-6815.
35. Hogan D, Vik A, Kolter R (2004) A Pseudomonas aeruginosa quorum-sensing molecule influences candida albicans morphology. Mol Microbiol 54: 1212-1223.
36. Horowitz Brown S, Zarnowski R, Sharpee WC, Keller NP (2008) Morphological transitions governed by density dependence and lipoxygenase activity in Aspergillus flavus. Appl Environ Microbiol 74: 5674-5685.
37. Huang J, Carney BF, Denny TP, Weissinger AK, Schell MA (1995) A complex network regulates expression of eps and other virulence genes of pseudomonas solanacearum. J Bacteriol 177: 1259-1267.
38. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329.
39. Khare E, Arora NK (2011) Dual activity of pyocyanin from pseudomonas aeruginosa - antibiotic against phytopathogen and signal molecule for biofilm development by rhizobia. Can J Microbio 57: 708-713.
40. Klich MA (2007) Aspergillus flavus: the major producer of aflatoxin. Mol Plant Pathol 8: 713-722.
41. Le CN, Kruijt M, Raaijmakers JM (2012) Involvement of phenazines and lipopeptides in interactions between pseudomonas species and sclerotium rolfsii, causal agent of stem rot disease on groundnut. J Appl Microbiol 112: 390-403.
42. Mackie AE, Wheatley RE (1999) Effects and incidence of volatile organic compound interactions between soil bacterial and fungal isolates. Soil Biol Biochem 31: 375-385.
43. McCluskey K, Wiest A, Plamann M (2010) The fungal genetics stock center: a repository for 50 years of fungal genetics research. J Biosci 35: 119-126.
44. Middleton, K. J., and Hayward, A. C. (1990) Bacterial wilt of groundnuts. collaborative res. plan. meet., Genting Highlands, Malaysia, 18-19 March. Proc. ACIAR/ICRISAT 31: 1-58.
45. Nawrath T, Mgode GF, Weetjens B, Kaufmann SHE, Schulz S (2012) The volatiles of pathogenic and nonpathogenic mycobacteria and related bacteria. Beilstein J Org Chem 8: 290-299.
46. Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Denning DW (2005) Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438: 1151-1156.
47. Nosanchuk JD, Casadevall A (2003) Microreview: the contribution of melanin to microbial pathogenesis. Cell Microbiol 5: 203-223.
48. Partida-Martínez LP, Heil M (2011) The microbe-free plant: fact or artifact? Front Plant Sci 2: 1-16.
49. Peckham GD (2011) Mouse MAb 3. H7 recognizes ralstonia solanacearum race 3 biovar 2 strains. Hybridoma 30: 571-573.
50. Pel HJ, De Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Stam H (2007) Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513. 88. Nat Biotechnol 25: 221-231.
51. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11: 789-799.
52. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG, Ausubel FM (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899-1902.
53. Roze LV, Beaudry RM, Arthur AE, Calvo AM, Linz JE (2007) Aspergillus volatiles regulate aflatoxin synthesis and asexual sporulation in Aspergillus parasiticus. Appl Environ Microbiol 73: 7268-7276.
54. Roze LV, Chanda A, Laivenieks M, Beaudry RM, Artymovich K a, Koptina AV, Awad DW, Valeeva D, Jones AD, Linz JE (2010) Volatile profiling reveals intracellular metabolic changes in Aspergillus parasiticus: veA regulates branched chain amino acid and ethanol metabolism. BMC Biochem 11: 33-47.
55. Roze LV, Koptina AV, Laivenieks M, Beaudry RM, Jones DA, Kanarsky AV, Linz JE (2011) Willow volatiles influence growth, development, and secondary metabolism in Aspergillus parasiticus. Appl Microbiol Biotechnol 92: 359-370.
56. Saile E, Mcgarvey JA, Schell MA, Denny TP (1997) Role of extracellular polysaccharide and endoglucanase in root invasion and colonization of tomato plants by ralstonia solanacearum. Phytopathology 87: 1264-1271.
57. Schell, M. A. (2000) Control of virulence and pathogenicity genes of Ralstonia solanacearum by an elaborate sensory network. Annu. Rev. Phytopathol.: 263-292.
58. Schneider P, Jacobs JM, Neres J, Aldrich CC, Allen C, Nett M, Hoffmeister D (2009) The global virulence regulators VsrAD and PhcA control secondary metabolism in the plant pathogen Ralstonia solanacearum. ChemBioChem 10: 2730-2732.
59. Shimizu K, Keller NP (2001) Genetic involvement of a cAMP-dependent protein kinase in a G protein signaling pathway regulating morphological and chemical transitions in Aspergillus nidulans. Genetics 157: 591-600.
60. Song J, Fan L, Beaudry RM (1998) Application of solid phase microextraction and gas chromatography/time-of-flight mass spectrometry for rapid analysis of flavor volatiles in tomato and strawberry fruits. J Agric Food Chem 46: 3721-3726.
61. Theis KR, Venkataraman A, Dycus JA, Koonter KD, Schmitt-Matzen EN, Wagner AP, Holekamp KE, Schmidt TM (2013) Symbiotic bacteria appear to mediate hyena social odors. Proc Natl Acad Sci U S A 110: 19832-19837.
62. Tognon G, Campagnoli a, Pinotti L, Dell'Orto V, Cheli F (2005) Implementation of the electronic nose for the identification of mycotoxins in durum wheat (Triticum durum). Vet Res Commun 29(2): 391-393.
63. van Elsas JD, Kastelein P, De Vries PM, van Overbeek LS (2001) Effects of ecological factors on the survival and physiology of Ralstonia solanacearum bv. 2 in irrigation water. Can J Microbiol 47: 842-854.
64. van Overbeek LS, Bergervoet JHW, Jacobs FHH, van Elsas JD (2004) The low-temperature-induced viable-but-nonculturable state affects the virulence of Ralstonia solanacearum Biovar 2. Phytopathology 94: 463-469.
65. Wang C, Wang Z, Qiao X, Li Z, Li F, Chen M, Wang Y, Huang Y, Cui H (2013a) Antifungal activity of volatile organic compounds from Streptomyces alboflavus TD-1. FEMS Microbiol Lett 341: 45-51.
66. Wang K, PS Y, QL D, QX W, ZB W, Peng J (2013b) Diversity of culturable root-associated/endophytic bacteria and their chitinolytic and aflatoxin inhibition activity of peanut plant in China. World J Microbiol Biotechnol 29: 1-10.
67. Wenke K, Kai M, Piechulla B (2010) Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231: 499-506.
68. Wheatley RE (2002) The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie van Leeuwenhoek 81: 357-364.
69. Zhou Z, Meng Q, Yu Z (2011) Effects of methanogenic inhibitors on methane production and abundances of methanogens and cellulolytic bacteria in in vitro ruminal cultures. Appl Environ Microbiol 77: 2634-2639.