1887

Abstract

Pseudomonads producing the antimicrobial metabolite 2,4-diacetylphloroglucinol (Phl) can control soil-borne phytopathogens, but their impact on other plant-beneficial bacteria remains poorly documented. Here, the effects of synthetic Phl and Phl F113 on phytostimulators were investigated. Most strains were moderately sensitive to Phl. , Phl induced accumulation of carotenoids and poly-β-hydroxybutyrate-like granules, cytoplasmic membrane damage and growth inhibition in Cd. Experiments with F113 and a Phl mutant indicated that Phl production ability contributed to growth inhibition of Cd and Sp245. Under gnotobiotic conditions, each of the three strains, F113 and Cd and Sp245, stimulated wheat growth. Co-inoculation of Sp245 and resulted in the same level of phytostimulation as in single inoculations, whereas it abolished phytostimulation when Cd was used. Phl production ability resulted in lower cell numbers per root system (based on colony counts) and restricted microscale root colonization of neighbouring cells (based on confocal microscopy), regardless of the strain used. Therefore, this work establishes that Phl pseudomonads have the potential to interfere with phytostimulators on roots and with their plant growth promotion capacity.

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2011-06-01
2019-10-15
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References

  1. Aßmus B. , Schloter M. , Kirchhof G. , Hutzler P. , Hartmann A. . ( 1997; ). Improved in situ tracking of rhizosphere bacteria using dual staining with fluorescence-labeled antibodies and rRNA targeted oligonucleotides. . Microb Ecol 33:, 32–40. [CrossRef].[PubMed].
    [Google Scholar]
  2. Bakker P. A. H. M. , Pieterse C. M. J. , van Loon L. C. . ( 2007; ). Induced systemic resistance by fluorescent Pseudomonas spp. . Phytopathology 97:, 239–243. [CrossRef].[PubMed].
    [Google Scholar]
  3. Bally R. , Elmerich C. . ( 2007; ). Biocontrol of plant diseases by associative and endophytic nitrogen-fixing bacteria. . In Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations, pp. 171–190. Edited by Elmerich C. , Newton W. E. . . Dordrecht, The Netherlands:: Kluwer Academic Publishers;. [CrossRef].
    [Google Scholar]
  4. Barea J. M. , Pozo M. J. , Azcón R. , Azcón-Aguilar C. . ( 2005; ). Microbial co-operation in the rhizosphere. . J Exp Bot 56:, 1761–1778. [CrossRef].[PubMed].
    [Google Scholar]
  5. Bashan Y. , Levanony H. , Whitmoyer R. E. . ( 1991; ). Root surface colonization of non-cereal crop plants by pleomorphic Azospirillum brasilense Cd. . J Gen Microbiol 137:, 187–196.[CrossRef]
    [Google Scholar]
  6. Blaha D. , Prigent-Combaret C. , Mirza M. S. , Moënne-Loccoz Y. . ( 2006; ). Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. . FEMS Microbiol Ecol 56:, 455–470. [CrossRef].[PubMed].
    [Google Scholar]
  7. Bloemberg G. V. , Wijfjes A. H. , Lamers G. E. , Stuurman N. , Lugtenberg B. J. . ( 2000; ). Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere: new perspectives for studying microbial communities. . Mol Plant Microbe Interact 13:, 1170–1176. [CrossRef].[PubMed].
    [Google Scholar]
  8. Brazelton J. N. , Pfeufer E. E. , Sweat T. A. , Gardener B. B. , Coenen C. . ( 2008; ). 2,4-diacetylphloroglucinol alters plant root development. . Mol Plant Microbe Interact 21:, 1349–1358. [CrossRef].[PubMed].
    [Google Scholar]
  9. Chilton M. D. , Currier T. C. , Farrand S. K. , Bendich A. J. , Gordon M. P. , Nester E. W. . ( 1974; ). Agrobacterium tumefaciens DNA and PS8 bacteriophage DNA not detected in crown gall tumors. . Proc Natl Acad Sci U S A 71:, 3672–3676. [CrossRef].[PubMed].
    [Google Scholar]
  10. Combes-Meynet E. , Pothier J. F. , Moënne-Loccoz Y. , Prigent-Combaret C. . ( 2011; ). The Pseudomonas secondary metabolite 2,4-diacetylphloroglucinol is a signal inducing rhizoplane expression of Azospirillum genes involved in plant-growth promotion. . Mol Plant Microbe Interact 24:, 271–284. [CrossRef].[PubMed].
    [Google Scholar]
  11. Costacurta A. , Vanderleyden J. . ( 1995; ). Synthesis of phytohormones by plant-associated bacteria. . Crit Rev Microbiol 21:, 1–18. [CrossRef].[PubMed].
    [Google Scholar]
  12. Couillerot O. , Prigent-Combaret C. , Caballero-Mellado J. , Moënne-Loccoz Y. . ( 2009; ). Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens. . Lett Appl Microbiol 48:, 505–512. [CrossRef].[PubMed].
    [Google Scholar]
  13. Creus C. M. , Graziano M. , Casanovas E. M. , Pereyra M. A. , Simontacchi M. , Puntarulo S. , Barassi C. A. , Lamattina L. . ( 2005; ). Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. . Planta 221:, 297–303. [CrossRef].[PubMed].
    [Google Scholar]
  14. Cronin D. , Moënne-Loccoz Y. , Fenton A. , Dunne C. , Dowling D. N. , O’Gara F. . ( 1997; a). Ecological interaction of a biocontrol Pseudomonas fluorescens strain producing 2,4-diacetylphloroglucinol with the soft rot potato pathogen Erwinia carotovora subsp. atroseptica . . FEMS Microbiol Ecol 23:, 95–106. [CrossRef]
    [Google Scholar]
  15. Cronin D. , Moënne-Loccoz Y. , Fenton A. , Dunne C. , Dowling D. N. , O’Gara F. . ( 1997; b). Role of 2,4-diacetylphloroglucinol in the interactions of the biocontrol pseudomonad strain F113 with the potato cyst nematode Globodera rostochiensis . . Appl Environ Microbiol 63:, 1357–1361.[PubMed].
    [Google Scholar]
  16. de Souza J. T. , Arnould C. , Deulvot C. , Lemanceau P. , Gianinazzi-Pearson V. , Raaijmakers J. M. . ( 2003; ). Effect of 2,4-diacetylphloroglucinol on Pythium: cellular responses and variation in sensitivity among propagules and species. . Phytopathology 93:, 966–975. [CrossRef].[PubMed].
    [Google Scholar]
  17. Dobbelaere S. , Croonenborghs A. , Thys A. , Vande Broek A. , Vanderleyden J. . ( 1999; ). Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. . Plant Soil 212:, 153–164. [CrossRef]
    [Google Scholar]
  18. Dobbelaere S. , Croonenborghs A. , Thys A. , Ptacek D. , Vanderleyden J. , Dutto P. , Labandera-Gonzalez C. , Caballero-Mellado J. , Aguirre J. F. et al. ( 2001; ). Responses of agronomically important crops to inoculation with Azospirillum . . Aust J Plant Physiol 28:, 871–879.
    [Google Scholar]
  19. Dobbelaere S. , Vanderleyden J. , Okon Y. . ( 2003; ). Plant growth-promoting effects of diazotrophs in the rhizosphere. . Crit Rev Plant Sci 22:, 107–149. [CrossRef]
    [Google Scholar]
  20. Duffy B. K. , Défago G. . ( 1999; ). Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. . Appl Environ Microbiol 65:, 2429–2438.[PubMed].
    [Google Scholar]
  21. Elbeltagy A. , Nishioka K. , Sato T. , Suzuki H. , Ye B. , Hamada T. , Isawa T. , Mitsui H. , Minamisawa K. . ( 2001; ). Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. . Appl Environ Microbiol 67:, 5285–5293. [CrossRef].[PubMed].
    [Google Scholar]
  22. Eskew D. L. , Focht D. D. , Ting I. P. . ( 1977; ). Nitrogen fixation, denitrification, and pleomorphic growth in a highly pigmented Spirillum lipoferum . . Appl Environ Microbiol 34:, 582–585.[PubMed].
    [Google Scholar]
  23. Fenton A. M. , Stephens P. M. , Crowley J. , O’Callaghan M. , O’Gara F. . ( 1992; ). Exploitation of gene(s) involved in 2,4-diacetylphloroglucinol biosynthesis to confer a new biocontrol capability to a Pseudomonas strain. . Appl Environ Microbiol 58:, 3873–3878.[PubMed].
    [Google Scholar]
  24. Fuentes-Ramirez L. , Caballero-Mellado J. . ( 2006; ). Bacterial biofertilizers. . In PGPR: Biocontrol and Biofertilization, pp. 143–172. Edited by Siddiqui Z. A. . . Heidelberg, Germany:: Springer;. [CrossRef].
    [Google Scholar]
  25. Girlanda M. , Perotto S. , Moënne-Loccoz Y. , Bergero R. , Lazzari A. , Défago G. , Bonfante P. , Luppi A. M. . ( 2001; ). Impact of biocontrol Pseudomonas fluorescens CHA0 and a genetically modified derivative on the diversity of culturable fungi in the cucumber rhizosphere. . Appl Environ Microbiol 67:, 1851–1864. [CrossRef].[PubMed].
    [Google Scholar]
  26. Gleeson O. , O’Gara F. , Morrissey J. P. . ( 2010; ). The Pseudomonas fluorescens secondary metabolite 2,4 diacetylphloroglucinol impairs mitochondrial function in Saccharomyces cerevisiae . . Antonie van Leeuwenhoek 97:, 261–273. [CrossRef].[PubMed].
    [Google Scholar]
  27. Haas D. , Défago G. . ( 2005; ). Biological control of soil-borne pathogens by fluorescent pseudomonads. . Nat Rev Microbiol 3:, 307–319. [CrossRef].[PubMed].
    [Google Scholar]
  28. Haas D. , Keel C. . ( 2003; ). Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. . Annu Rev Phytopathol 41:, 117–153. [CrossRef].[PubMed].
    [Google Scholar]
  29. Hartmann A. , Hurek T. . ( 1988; ). Effect of carotenoid overproduction on oxygen tolerance of nitrogen fixation in Azospirillum brasilense Sp7. . J Gen Microbiol 134:, 2449–2455.
    [Google Scholar]
  30. Hontzeas N. , Zoidakis J. , Glick B. R. , Abu-Omar M. M. . ( 2004; ). Expression and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the rhizobacterium Pseudomonas putida UW4: a key enzyme in bacterial plant growth promotion. . Biochim Biophys Acta 1703:, 11–19.[PubMed].[CrossRef]
    [Google Scholar]
  31. Howell C. R. , Stipanovic R. D. . ( 1979; ). Control of Rhizoctonia solani on cotton seedlings with Pseudomonas fluorescens and with an antibiotic produced by the bacterium. . Phytopathology 69:, 480–482. [CrossRef]
    [Google Scholar]
  32. Iavicoli A. , Boutet E. , Buchala A. , Métraux J.-P. . ( 2003; ). Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. . Mol Plant Microbe Interact 16:, 851–858. [CrossRef].[PubMed].
    [Google Scholar]
  33. Johansen J. E. , Binnerup S. J. , Lejbølle K. B. , Mascher F. , Sørensen J. , Keel C. . ( 2002; ). Impact of biocontrol strain Pseudomonas fluorescens CHA0 on rhizosphere bacteria isolated from barley (Hordeum vulgare L.) with special reference to Cytophaga-like bacteria. . J Appl Microbiol 93:, 1065–1074. [CrossRef].[PubMed].
    [Google Scholar]
  34. Kabir M. , Faure D. , Heulin T. , Achouak W. , Bally R. . ( 1996; ). Azospirillum populations in soils infested by a parasitic weed (Striga) under Sorghum cultivation in Mali, West Africa. . Eur J Soil Biol 32:, 157–163.
    [Google Scholar]
  35. Kadouri D. , Burdman S. , Jurkevitch E. , Okon Y. . ( 2002; ). Identification and isolation of genes involved in poly(β-hydroxybutyrate) biosynthesis in Azospirillum brasilense and characterization of a phbC mutant. . Appl Environ Microbiol 68:, 2943–2949. [CrossRef].[PubMed].
    [Google Scholar]
  36. Kadouri D. , Jurkevitch E. , Okon Y. . ( 2003; ). Involvement of the reserve material poly-β-hydroxybutyrate in Azospirillum brasilense stress endurance and root colonization. . Appl Environ Microbiol 69:, 3244–3250. [CrossRef].[PubMed].
    [Google Scholar]
  37. Keel C. , Schnider U. , Maurhofer M. , Voisard C. , Laville J. , Burger U. , Wirthner P. , Haas D. , Défago G. . ( 1992; ). Suppression of root diseases by Pseudomonas fluorescens CHA0: Importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. . Mol Plant Microbe Interact 5:, 4–13. [CrossRef]
    [Google Scholar]
  38. King E. O. , Ward M. K. , Raney D. E. . ( 1954; ). Two simple media for the demonstration of pyocyanin and fluorescin. . J Lab Clin Med 44:, 301–307.[PubMed].
    [Google Scholar]
  39. Kyselková M. , Kopecký J. , Frapolli M. , Défago G. , Ságová-Marecková M. , Grundmann G. L. , Moënne-Loccoz Y. . ( 2009; ). Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black root rot disease. . ISME J 3:, 1127–1138. [CrossRef].[PubMed].
    [Google Scholar]
  40. Lemanceau P. , Bakker P. A. H. M. , De Kogel W. J. , Alabouvette C. , Schippers B. . ( 1992; ). Effect of pseudobactin 358 production by Pseudomonas putida WCS358 on suppression of fusarium wilt of carnations by nonpathogenic Fusarium oxysporum Fo47. . Appl Environ Microbiol 58:, 2978–2982.[PubMed].
    [Google Scholar]
  41. Maurhofer M. , Baehler E. , Notz R. , Martinez V. , Keel C. . ( 2004; ). Cross talk between 2,4-diacetylphloroglucinol-producing biocontrol pseudomonads on wheat roots. . Appl Environ Microbiol 70:, 1990–1998. [CrossRef].[PubMed].
    [Google Scholar]
  42. Michiels K. , Vanderleyden J. , Van Gool A. . ( 1989; ). Azospirillum-plant root associations: a review. . Biol Fertil Soils 8:, 356–368. [CrossRef]
    [Google Scholar]
  43. Mirza M. S. , Mehnaz S. , Normand P. , Prigent-Combaret C. , Moënne-Loccoz Y. , Bally R. , Malik K. A. . ( 2006; ). Molecular characterization and PCR detection of a nitrogen-fixing Pseudomonas strain promoting rice growth. . Biol Fertil Soils 43:, 163–170. [CrossRef]
    [Google Scholar]
  44. Moënne-Loccoz Y. , Tichy H. V. , O’Donnell A. , Simon R. , O’Gara F. . ( 2001; ). Impact of 2,4-diacetylphloroglucinol-producing biocontrol strain Pseudomonas fluorescens F113 on intraspecific diversity of resident culturable fluorescent pseudomonads associated with the roots of field-grown sugar beet seedlings. . Appl Environ Microbiol 67:, 3418–3425. [CrossRef].[PubMed].
    [Google Scholar]
  45. Natsch A. , Keel C. , Hebecker N. , Laasik E. , Défago G. . ( 1998; ). Impact of Pseudomonas fluorescens strain CHA0 and a derivative with improved biocontrol activity on the culturable resident bacterial community on cucumber roots. . FEMS Microbiol Ecol 27:, 365–380. [CrossRef]
    [Google Scholar]
  46. Nelson L. M. , Knowles R. . ( 1978; ). Effect of oxygen and nitrate on nitrogen fixation and denitrification by Azospirillum brasilense grown in continuous culture. . Can J Microbiol 24:, 1395–1403. [CrossRef].[PubMed].
    [Google Scholar]
  47. Nur I. , Steinitz Y. L. , Okon Y. , Henis Y. . ( 1981; ). Carotenoid composition and function in nitrogen-fixing bacteria of the genus Azospirillum . . J Gen Microbiol 122:, 27–32.
    [Google Scholar]
  48. Penot I. , Bergès N. , Guinguené C. , Fages J. . ( 1992; ). Characterization of Azospirillum associated with maize (Zea mays) in France using biochemical tests and plasmid profiles. . Can J Microbiol 38:, 798–803. [CrossRef]
    [Google Scholar]
  49. Phillips D. A. , Fox T. C. , King M. D. , Bhuvaneswari T. V. , Teuber L. R. . ( 2004; ). Microbial products trigger amino acid exudation from plant roots. . Plant Physiol 136:, 2887–2894. [CrossRef].[PubMed].
    [Google Scholar]
  50. Picard C. , Bosco M. . ( 2005; ). Maize heterosis affects the structure and dynamics of indigenous rhizospheric auxins-producing Pseudomonas populations. . FEMS Microbiol Ecol 53:, 349–357. [CrossRef].[PubMed].
    [Google Scholar]
  51. Pothier J. F. , Wisniewski-Dyé F. , Weiss-Gayet M. , Moënne-Loccoz Y. , Prigent-Combaret C. . ( 2007; ). Promoter-trap identification of wheat seed extract-induced genes in the plant-growth-promoting rhizobacterium Azospirillum brasilense Sp245. . Microbiology 153:, 3608–3622. [CrossRef].[PubMed].
    [Google Scholar]
  52. Raaijmakers J. M. , Vlami M. , de Souza J. T. . ( 2002; ). Antibiotic production by bacterial biocontrol agents. . Antonie van Leeuwenhoek 81:, 537–547. [CrossRef].[PubMed].
    [Google Scholar]
  53. Raaijmakers J. M. , Paulitz T. C. , Steinberg C. , Alabouvette C. , Moënne-Loccoz Y. . ( 2009; ). The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. . Plant Soil 321:, 341–361. [CrossRef]
    [Google Scholar]
  54. Reid J. B. , Renquist A. R. . ( 1997; ). Enhanced root production as a feed-forward response to soil water deficit in field-grown tomatoes. . Aust J Plant Physiol 24:, 685–692. [CrossRef]
    [Google Scholar]
  55. Rezzonico F. , Zala M. , Keel C. , Duffy B. , Moënne-Loccoz Y. , Défago G. . ( 2007; ). Is the ability of biocontrol fluorescent pseudomonads to produce the antifungal metabolite 2,4-diacetylphloroglucinol really synonymous with higher plant protection?. New Phytol 173:, 861–872. [CrossRef].[PubMed].
    [Google Scholar]
  56. Richardson A. E. , Barea J.-M. , McNeill A. M. , Prigent-Combaret C. . ( 2009; ). Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. . Plant Soil 321:, 305–339. [CrossRef]
    [Google Scholar]
  57. Rinaudo G. . ( 1982; ). Fixation hétérotrophe de l'azote dans la rhizosphère du riz. . PhD thesis, Université Paris-Sud, Orsay, France.
  58. Sambrook J. , Fritsch E. F. , Maniatis T. . ( 1989; ). Molecular Cloning: a Laboratory Manual, , 2nd edn.. Cold Spring Harbor, NY, USA:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  59. Sanguin H. , Sarniguet A. , Gazengel K. , Moënne-Loccoz Y. , Grundmann G. L. . ( 2009; ). Rhizosphere bacterial communities associated with disease suppressiveness stages of take-all decline in wheat monoculture. . New Phytol 184:, 694–707. [CrossRef].[PubMed].
    [Google Scholar]
  60. Scher F. M. , Baker R. . ( 1982; ). Effect of Pseudomonas putida and a synthetic iron chelator on induction of soil suppressiveness to Fusarium wilt pathogens. . Phytopathology 72:, 1567–1573. [CrossRef]
    [Google Scholar]
  61. Schloter M. , Hartmann A. . ( 1998; ). Endophytic and surface colonization of wheat roots (Triticum aestivum) by different Azospirillum brasilense strains studied with strain-specific monoclonal antibodies. . Symbiosis 25:, 159–179.
    [Google Scholar]
  62. Schouten A. , Van den Berg G. , Edel-Hermann V. , Steinberg C. , Gautheron N. , Alabouvette C. , De Vos C. H. , Lemanceau P. , Raaijmakers J. M. . ( 2004; ). Defense responses of Fusarium oxysporum to 2,4-diacetylphloroglucinol, a broad-spectrum antibiotic produced by Pseudomonas fluorescens . . Mol Plant Microbe Interact 17:, 1201–1211. [CrossRef].[PubMed].
    [Google Scholar]
  63. Schouten A. , Maksimova O. , Cuesta-Arenas Y. , van den Berg G. , Raaijmakers J. M. . ( 2008; ). Involvement of the ABC transporter BcAtrB and the laccase BcLCC2 in defence of Botrytis cinerea against the broad-spectrum antibiotic 2,4-diacetylphloroglucinol. . Environ Microbiol 10:, 1145–1157. [CrossRef].[PubMed].
    [Google Scholar]
  64. Shanahan P. , O’sullivan D. J. , Simpson P. , Glennon J. D. , O’Gara F. . ( 1992; ). Isolation of 2,4-diacetylphloroglucinol from a fluorescent pseudomonad and investigation of physiological parameters influencing its production. . Appl Environ Microbiol 58:, 353–358.[PubMed].
    [Google Scholar]
  65. Tal S. , Okon Y. . ( 1985; ). Production of the reserve material poly-β-hydroxybutyrate and its function in Azospirillum brasilense Cd. . Can J Microbiol 31:, 608–613. [CrossRef]
    [Google Scholar]
  66. Tarrand J. J. , Krieg N. R. , Döbereiner J. . ( 1978; ). A taxonomic study of the Spirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. nov. and two species, Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov. . Can J Microbiol 24:, 967–980. [CrossRef].[PubMed].
    [Google Scholar]
  67. Thirunavukkarasu N. , Mishra M. N. , Spaepen S. , Vanderleyden J. , Gross C. A. , Tripathi A. K. . ( 2008; ). An extra-cytoplasmic function sigma factor and anti-sigma factor control carotenoid biosynthesis in Azospirillum brasilense . . Microbiology 154:, 2096–2105. [CrossRef].[PubMed].
    [Google Scholar]
  68. Vincent M. N. , Harrison L. A. , Brackin J. M. , Kovacevich P. A. , Mukerji P. , Weller D. M. , Pierson E. A. . ( 1991; ). Genetic analysis of the antifungal activity of a soilborne Pseudomonas aureofaciens strain. . Appl Environ Microbiol 57:, 2928–2934.[PubMed].
    [Google Scholar]
  69. Walsh U. F. , Moënne-Loccoz Y. , Tichy H.-V. , Gardner A. , Corkery D. M. , Lorkhe S. , O’Gara F. . ( 2003; ). Residual impact of the biocontrol inoculant Pseudomonas fluorescens F113 on the resident population of rhizobia nodulating a red clover rotation crop. . Microb Ecol 45:, 145–155. [CrossRef].[PubMed].
    [Google Scholar]
  70. Weller D. M. , Raaijmakers J. M. , Gardener B. B. M. , Thomashow L. S. . ( 2002; ). Microbial populations responsible for specific soil suppressiveness to plant pathogens. . Annu Rev Phytopathol 40:, 309–348. [CrossRef].[PubMed].
    [Google Scholar]
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