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Populations of Xanthomonas citri pv. mangiferaeindicae from Asymptomatic Mango Leaves Are Primarily Endophytic

  • Plant Microbe Interactions
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Abstract

Epiphytic survival of several Xanthomonas pathovars has been reported, but most studies failed to determine whether such populations were resident epiphytes, resulting from latent infections, or casual epiphytes. This study aimed at understanding the nature of Xanthomonas citri pv. mangiferaeindicae populations associated with asymptomatic leaves. When spray-inoculated on mango leaves cv. Maison Rouge, the pathogen multiplied markedly in association with juvenile leaves, but was most often detected as low population sizes (<1 × 103 cfu g−1) in association with mature leaves. Our results suggest a very low biological significance of biofilm-associated populations of X. citri pv. mangiferaeindicae, while saprophytic microbiota associated with mango leaves survived frequently as biofilms. A chloroform vapor-based disinfestation assay which kills cells specifically located on the leaf surface and not those located within the leaf mesophyll was developed. When applied to spray-inoculated leaves maintained under controlled environmental conditions, 155 out of the 168 analyzed datasets collected over three assessment dates for seven bacterial strains representative of the genetic diversity of the pathogen failed to demonstrate a significant X. citri pv. mangiferaeindicae population decrease on chloroform treated leaves up to 13 days after inoculation. We conclude that an efficient survival of X. citri pv. mangiferaeindicae present on mango leaf surfaces following a limited dissemination event is largely dependent on the availability of juvenile plant tissues. The bacterium gains access to protected sites (e.g., mesophyll) through stomata where it becomes endophytic and eventually causes disease. Chloroform vapor-based disinfestation assays should be useful for further studies aiming at evaluating survival sites of bacteria associated with the phyllosphere.

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References

  1. Ah-You N, Gagnevin L, Chiroleu F, Jouen E, Neto JR, Pruvost O (2007) Pathological variations within Xanthomonas campestris pv. mangiferaeindicae support its separation into three distinct pathovars that can be distinguished by Amplified Fragment Length Polymorphism. Phytopathology 97:1568–1577

    Article  PubMed  CAS  Google Scholar 

  2. Ah-You N, Gagnevin L, Grimont PAD, Brisse S, Nesme X, Chiroleu F, Bui Thi Ngoc L, Jouen E, Lefeuvre P, Vernière C, Pruvost O (2009) Polyphasic characterization of xanthomonads pathogenic to Anacardiaceae and their relatedness to different Xanthomonas species. Int J Syst Evol Microbiol 59. doi:10.1099/ijs.0.65453-0

  3. Bashan Y, Sharon E, Okon Y, Henis Y (1981) Scanning electron and light microscopy of infection and symptom development in tomato leaves infected with Pseudomonas tomato. Physiol Plant Pathol 19:139–144

    Google Scholar 

  4. Beattie GA, Lindow SE (1999) Bacterial colonization of leaves: a spectrum of strategies. Phytopathology 89:353–359

    Article  PubMed  CAS  Google Scholar 

  5. Darsonval A, Darrasse A, Meyer D, Demarty M, Durand K, Bureau C, Manceau C, Jacques MA (2008) Type III secretion system of Xanthomonas fuscans subsp. fuscans is involved in phyllosphere colonization process and in transmission to seeds of susceptible bean. Appl Environ Microbiol 74:2669–2678

    Article  PubMed  CAS  Google Scholar 

  6. Dodd JC, Prusky D, Jeffries P (1997) Fruit diseases. In: Litz RE (ed) The mango: botany, production and uses. CAB International, Oxon, pp 257–291

    Google Scholar 

  7. Dunger G, Relling VM, Tondo ML, Barreras M, Ielpi L, Orellano EG, Ottado J (2007) Xanthan is not essential for pathogenicity in citrus canker but contributes to Xanthomonas epiphytic survival. Arch Microbiol 188:127–135

    Article  PubMed  CAS  Google Scholar 

  8. Gagnevin L, Leach JE, Pruvost O (1997) Genomic variability of the Xanthomonas pathovar mangiferaeindicae, agent of mango bacterial black spot. Appl Environ Microbiol 63:246–253

    PubMed  CAS  Google Scholar 

  9. Gagnevin L, Pruvost O (2001) Epidemiology and control of mango bacterial black spot. Plant Dis 85:928–935

    Article  Google Scholar 

  10. Graham JH, Gottwald TR, Cubero J, Achor DS (2004) Xanthomonas axonopodis pv. citri: factors affecting successful eradication of citrus canker. Mol Plant Pathol 5:1–15

    Article  Google Scholar 

  11. Haefele DM, Lindow SE (1987) Flagellar motility confers epiphytic fitness advantages upon Pseudomonas syringae. Appl Environ Microbiol 53:2528–2533

    PubMed  Google Scholar 

  12. Hirano SS, Upper CD (2000) Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae—a pathogen, ice nucleus, and epiphyte. Microbiol Mol Biol Rev 64:624–653

    Article  PubMed  CAS  Google Scholar 

  13. Ishimaru C, Eskridge KM, Vidaver AK (1991) Distribution analyses of naturally occurring epiphytic populations of Xanthomonas campestris pv. phaseoli on dry beans. Phytopathology 81:262–268

    Article  Google Scholar 

  14. Jacques MA, Josi K, Darrasse A, Samson R (2005) Xanthomonas axonopodis pv. phaseoli var. fuscans is aggregated in stable biofilm population sizes in the phyllosphere of field-grown beans. Appl Environ Microbiol 71:2008–2015

    Article  PubMed  CAS  Google Scholar 

  15. Kishun R (1982) Loss in mango fruit due to bacterial canker Xanthomonas mangiferaeindicae. In: Lozano JC (ed) Plant pathogenic bacteria. C.I.A.T., Cali, pp 181–184

    Google Scholar 

  16. Leben C (1965) Epiphytic microorganisms in relation to plant disease. Annu Rev Phytopathol 3:209–230

    Article  Google Scholar 

  17. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883

    Article  PubMed  CAS  Google Scholar 

  18. Madden LV (2006) Botanical epidemiology: some key advances and its continuing role in disease management. Eur J Plant Pathol 115:3–23

    Article  Google Scholar 

  19. Manicom BQ (1986) Factors affecting bacterial black spot of mangoes caused by Xanthomonas campestris pv. mangiferaeindicae. Ann Appl Biol 109:129–135

    Article  Google Scholar 

  20. Monier JM, Lindow SE (2004) Frequency, size, and localization of bacterial aggregates on bean leaf surfaces. Appl Environ Microbiol 70:346–355

    Article  PubMed  CAS  Google Scholar 

  21. Morris CE, Monier JM, Jacques MA (1998) A technique to quantify the population size and composition of the biofilm component in communities of bacteria in the phyllosphere. Appl Environ Microbiol 64:4789–4795

    PubMed  CAS  Google Scholar 

  22. Ploetz RC, Prakash O (1997) Foliar, floral and soilborne diseases. In: Litz RE (ed) The mango: botany, production and uses. CAB International, Oxon, pp 281–327

    Google Scholar 

  23. Poplawsky AR, Chun W (1998) Xanthomonas campestris pv. campestris requires a functional pigB for epiphytic survival and host infection. Mol Plant-Microbe Interact 11:466–475

    Article  PubMed  CAS  Google Scholar 

  24. Poplawsky AR, Urban SC, Chun W (2000) Biological role of xanthomonadin pigments in Xanthomonas campestris pv. campestris. Appl Environ Microbiol 66:5123–5127

    Article  PubMed  CAS  Google Scholar 

  25. Prakash O, Misra AK (1992) Important diseases of mango and their effect on production. Biol Memoirs 18:39–55

    Google Scholar 

  26. Pruvost O, Roumagnac P, Gaube C, Chiroleu F, Gagnevin L (2005) New media for the semi-selective isolation and enumeration of Xanthomonas campestris pv. mangiferaeindicae, the causal agent of mango bacterial black spot. J Appl Microbiol 99:803–815

    Article  PubMed  CAS  Google Scholar 

  27. Rai R, Vatsala P (1985) Epidermal morphology and stomatal development in Anacardiaceae. Acta Hort 108:237–246

    Google Scholar 

  28. Rigano LA, Siciliano F, Enrique R, Sendin L, Filippone P, Torres PS, Questa J, Dow JM, Castagnaro AP, Vojnov AA, Marano MR (2007) Biofilm formation, epiphytic fitness, and canker development in Xanthomonas axonopodis pv. citri. Mol Plant-Microbe Interact 20:1222–1230

    Article  PubMed  CAS  Google Scholar 

  29. Rudolph K (1993) Infection of the plant by Xanthomonas. In: Swings JG, Civerolo EL (eds) Xanthomonas. Chapman & Hall, London, pp 193–264

    Google Scholar 

  30. Schneider RW, Grogan RG (1977) Tomato leaf trichomes, a habitat for resident populations of Pseudomonas tomato. Phytopathology 67:898–902

    Article  Google Scholar 

  31. Sokal RR, Rohlf FJ (1969) Biometry. The principles and practice of statistics in biological research. Freeman, W. H. & Co., San Francisco

    Google Scholar 

  32. Spurr HWJ (1979) Ethanol treatment. Available technique for foliage biocontrol studies of plant disease. Phytopathology 69:773–776

    Article  CAS  Google Scholar 

  33. Stall RE, Gottwald TR, Koizumi M, Schaad NC (1993) Ecology of plant pathogenic xanthomonads. In: Swings JG, Civerolo EL (eds) Xanthomonas. Chapman & Hall, London, pp 265–299

    Google Scholar 

  34. Timmer LW, Zitko SE, Gottwald TR (1996) Population dynamics of Xanthomonas campestris pv. citri on symptomatic and asymptomatic citrus leaves under various environmental conditions. , Vol. In: Manicom B, Robinson J, Du Plessis SF, Joubert P, Van Zyl JL, Du Preez S (eds) Proceedings of the International Society of Citriculture. vol. 1. International Society of Citriculture, Sun City, pp 448–451

    Google Scholar 

  35. Vernière C, Devaux M, Pruvost O, Couteau A, Luisetti J (1991) Studies on the biochemical and physiological variations among strains of Xanthomonas campestris pv. citri, the causal agent of citrus bacterial canker disease. Fruits 46:162–170

    Google Scholar 

  36. Wichmann G, Bergelson J (2004) Effector genes of Xanthomonas axonopodis pv. vesicatoria promote transmission and enhance other fitness traits in the field. Genetics 166:693–706

    Article  PubMed  CAS  Google Scholar 

  37. Wilson M, Hirano SS, Lindow SE (1999) Location and survival of leaf-associated bacteria in relation to pathogenicity and potential for growth within the leaf. Appl Environ Microbiol 65:1435–1443

    PubMed  CAS  Google Scholar 

  38. Xu KD, McFeters GA, Stewart PS (2000) Biofilm resistance to antimicrobial agents. Microbiology-UK 146:547–549

    CAS  Google Scholar 

Download references

Acknowledgments

We wish to express our appreciation to V. Glories and M. Payet for technical assistance and E. L. Civerolo and T. Boureau for reviewing the manuscript and proofreading in English. This work was funded by CIRAD, fonds communs INRA-CIRAD, Région Réunion and the European Union (FEOGA).

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Correspondence to Olivier Pruvost.

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Pruvost, O., Savelon, C., Boyer, C. et al. Populations of Xanthomonas citri pv. mangiferaeindicae from Asymptomatic Mango Leaves Are Primarily Endophytic. Microb Ecol 58, 170–178 (2009). https://doi.org/10.1007/s00248-008-9480-x

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