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Acta Biologica Hungarica

, Volume 69, Issue 2, pp 170–181 | Cite as

Mycorrhiza-Induced Alleviation of Plant Disease Caused by Clavibacter michiganensis Subsp. Michiganensis and Role of Ethylene in Mycorrhiza-Induced Resistance in Tomato

  • Nguyen Hong Duc
  • Katalin PostaEmail author
Article

Abstract

The protective role of arbuscular mycorrhizal fungi (AMF) against the phytopathogen Clavibacter michiganensis subsp. michiganensis (Cmm) was examined in tomato plants. Seven different AMF isolates were used to determine which ones were able to induce effectively resistance against Cmm. Stems of seven-week tomato plants were infected with Cmm, then a disease severity index (DSI) was determined during the next three weeks. In addition to different responses to mycorrhizal inoculation, three levels of responses to the bacterial disease were recognized in treatments. Plants inoculated with Rhizophagus irregularis (Ri) showed both the highest colonization and the highest induced resistance to Cmm while the effect of Funneliformis mosseae, Gigaspora margarita and Claroideoglomus claroideum on mycorrhizal colonization and on the induced resistance were intermediate and high, respectively. Subsequently, Ri was chosen to inoculate ethylene-insensitive tomato mutant line Never ripe (Nr) and its background (Pearson) to investigate the possible role of ethylene (ET) in the mycorrhiza-induced resistance (MIR). The results showed that Ri could induce systemic resistance against Cmm in the Pearson background, whereas ET-insensitivity in Nr plants impaired MIR. These results suggest that ET is required for Ri-induced resistance against Cmm. To our knowledge, this is the first study to examine the effect of different AMF isolates on the response of tomato plants to Cmm and involvement of ET in MIR against Cmm.

Keywords

Clavibacter michiganensis subsp. michiganensis arbuscular mycorrhizal fungi mycorrhiza-induced resistance tomato ethylene 

Abbreviations

AM

arbuscular mycorrhizal

AMF

arbuscular mycorrhizal fungi

Cmm

Clavibacter michiganensis subsp. michiganensis

Cc

Claroideoglomus claroideum

DSI

disease severity index

ET

ethylene

Fg

Funneliformis geosporum

Fm

Funneliformis mosseae

Gm

Gigaspora margarita

MIR

mycorrhiza-induced resistance

Sc

Septoglomus constrictum

Ri

Rhizophagus irregularis

Rs

Rhizophagus sp.

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Notes

Acknowledgements

The study was funded by Stipendium Hungaricum and Research Centre of Excellence 1476-4/2016/FEKUT. The authors thank Dr. Turoczi Gyorgy, Institute of Plant Protection, Szent István University, for useful advices during the study. We also would like to thank Tomato Genetics Resource Center (University of California, UC) for kindly providing tomato seeds of Never ripe mutant and its background Pearson.

References

  1. 1.
    Abeles, F. B., Morgan, P. W., Saltveit, M. E. (1992) Ethylene in Plant Biology. Ed. 2. Academic Press, New York.Google Scholar
  2. 2.
    Adie, B., Chico, J. M., Rubio-Somoza, I., Solano, R. (2007) Modulation of plant defenses by ethylene. J. Plant Growth Regul. 26, 160–177.Google Scholar
  3. 3.
    Arshad, M., Frankenberger, W. T. (2002) Ethylene, Agricultural Sources and Applications. New York, Kluwer/Plenum.Google Scholar
  4. 4.
    Balaji, V., Mayrose, M., Sherf, O., Jacob-Hirsch, J., Eichenlaub, R., Iraki, N., Manulis-Sasson, S., Rechavi, G., Barash, I., Sessa, G. (2008) Tomato transcriptional changes in response to Clavibacter michiganensis subsp. michiganensis reveal a role for ethylene in disease development. Plant Physiol. 146, 1797–1809.PubMedGoogle Scholar
  5. 5.
    Ballhorn, D. J., Younginger, B. S., Kautz, S. (2014) An aboveground pathogen inhibits belowground rhizobia and arbuscular mycorrhizal fungi in Phaseolus vulgaris. BMC Plant Biol. 14, 321.PubMedGoogle Scholar
  6. 6.
    Broekaert, W. F., Delaure, S. L., De Bolle, M. F. C., Cammuel, B. P. A. (2006) The role of ethylene in host-pathogen interactions. Annu. Rev. Phytopathol. 44, 393–416.PubMedGoogle Scholar
  7. 7.
    Davis, M. J., Gillespie, J. A., Vidaver, A. K., Harris, R. W. (1984) Clavibacter: a new genus containing some phytopathogenic coryneform bacteria, including Clavibacter xyli subsp. xyli sp. nov., subsp. nov. and Clavibacter xyli subsp. cynodontis subsp. nov., pathogens that cause ratoon stunting disease of sugarcane and bermudagrass stunting disease. Int. J. Syst. Bacteriol. 34, 107–117.Google Scholar
  8. 8.
    Ellis, C., Turner, J. G. (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13, 1025–1033.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Filion, M., ST-Arnaud, M., Fortin, J. A. (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol. 141, 525–533.Google Scholar
  10. 10.
    Fiorilli, V., Catoni, M., Francia, D., Cardinale, F., Lanfranco, L. (2011). The arbuscular mycorrhizal symbiosis reduces disease severity in tomato plants infected by Botrytis cinerea. J. Plant Pathol. 93, 237–242.Google Scholar
  11. 11.
    Fracetto, G. G. M., Peres, L. E. P., Lambais, M. R. (2017) Gene expression analyses in tomato near isogenic lines provide evidence for ethylene and abscisic acid biosynthesis fne-tuning during arbuscular mycorrhiza development. Arch. Microbiol. 199), 787–798.PubMedGoogle Scholar
  12. 12.
    Fritz, M., Jakobsen, I., Langkjaer, M. F., Thordal-Christensen, H., Pons-Kühnemann, J. (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16, 413–419.Google Scholar
  13. 13.
    Giovannetti, M., Mosse, B. (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol. 84, 489–500.Google Scholar
  14. 14.
    Hewitt, E. J. (1966) Sand and Water Culture Methods Used in the Study of Plant Nutrition. 2nd edn. London: Commonwealth Agricultural Bureau.Google Scholar
  15. 15.
    Hossain, M. M., Sultana, F., Kubota, M., Hyakumachi, M. (2008) Differential inducible defense mechanisms against bacterial speck pathogen in Arabidopsis thaliana by plant-growth-promoting-fungus Penicillium sp. GP16-2 and its cell free fltrate. Plant Soil 304, 227–239.Google Scholar
  16. 16.
    Iavicoli, A., Boutet, E., Buchala, A., Métraux, J. P. (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fuorescens CHA0. Mol. Plant-Microbe Interact. 16, 851–858.Google Scholar
  17. 17.
    Jung, S. C., Martinez-Medina, A., Lopez-Raez, J. A., Pozo, M. J. (2012) Mycorrhiza-induced resistance and priming of plant defenses. J. Chem. Ecol. 38, 651–664.PubMedGoogle Scholar
  18. 18.
    Khatabi, B., Schäfer, P. (2012) Ethylene in mutualistic symbioses. Plant Signal. Behav. 7, 1634–1638.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Korolev, N., David, D. R., Elad, Y. (2008) The role of phytohormones in basal resistance and Trichoderma induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana. Biocontrol 53, 667–683.Google Scholar
  20. 20.
    Lanahan, M. B., Yen, H. C., Giovannoni, J. J., Klee, H. J. (1994) The never ripe mutation blocks ethylene perception in tomato. Plant Cell 6, 521–530.PubMedPubMedCentralGoogle Scholar
  21. 21.
    Liu, J., Maldonado-Mendoza, I., Lopez-Meyer, M., Cheung, F., Town, C. D., Harrison, M. J. (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J. 50, 529–544.PubMedPubMedCentralGoogle Scholar
  22. 22.
    López-Ráez, J. A., Verhage, A., Fernández, I., García, J. M., Azcón-Aguilar, C., Flors, V., Pozo, M. J. (2010) Hormonal and transcriptional profles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J. Exp. Bot. 61, 2589–2601.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Maffei, G., Miozzi, L., Fiorilli, V., Novero, M., Lanfranco, L., Accotto, G. P. (2014) The arbuscular mycorrhizal symbiosis attenuates symptom severity and reduces virus concentration in tomato infected by Tomato yellow leaf curl Sardinia virus (TYLCSV). Mycorrhiza 24, 179–186.PubMedGoogle Scholar
  24. 24.
    Møller, K., Kristensen, K., Yohalem, D., Larsen, J. (2009) Biological management of gray mold in pot roses by coinoculation of the biocontrol agent Ulocladium atrum and the mycorrhizal fungus Glomus mosseae. Biol. Control 49, 120–125.Google Scholar
  25. 25.
    Mora-Romero, G. A., Gonzalez-Ortiz, M. A., Quiroz-Figueroa, F., Calderon-Vazquez, C. L., Medina-Godoy, S., Maldonado-Mendoza, I., Arroyo-Becerra, A., Perez-Torres, A., Alatorre-Cobos, F., Sanchez, F., Lopez-Meyer, M. (2015) PvLOX2 silencing in common bean roots impairs arbuscular mycorrhiza-induced resistance without affecting symbiosis establishment. Funct. Plant Biol. 42, 18–30.Google Scholar
  26. 26.
    Nair, A., Kolet, S. P., Thulasiram, H. V., Bhargava, S. (2015) Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata. Plant Biol. 17, 625–631.PubMedGoogle Scholar
  27. 27.
    Nair, A., Kolet, S. P., Thulasiram, H. V., Bhargava, S. (2015) Role of methyl jasmonate in the expression of mycorrhizal induced resistance against Fusarium oxysporum in tomato plants. Physiol. Mol. Plant Pathol. 92, 139–145.Google Scholar
  28. 28.
    Plenchette, C., Fortin, J. A., Furlan, V. (1983) Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility: I. Mycorrhizal dependency under feld conditions. Plant Soil 70, 199–209.Google Scholar
  29. 29.
    Pieterse, C. M., Van Loon, L. C. (1999) Salicylic-acid-independent plant defence pathways. Trends Plant Sci. 4, 52–58.PubMedGoogle Scholar
  30. 30.
    Pozo, M. J., Jung, S. C., López-Ráez, J. A., Azcón-Aguilar, C. (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: The role of plant defence mechanisms. In: Koltai, H., Kapulnik, Y. (eds), Arbuscular Mycorrhizas: Physiology and Function. Springer Netherlands, Dordrecht, pp. 193–207.Google Scholar
  31. 31.
    de la Providencia, I. E., de Souza, F. A., Fernández, F., Delmas, N. S., Declerck, S. (2005) Arbuscular mycorrhizal fungi reveal distinct patterns of anastomosis formation and hyphal healing mechanisms between different phylogenic groups. New Phytol. 165, 261–271.PubMedGoogle Scholar
  32. 32.
    Raupach, G. S., Liu, L., Murphy, J. F., Tuzun, S. T., Kloepper, J. W. (1996) Induced systemic resistance in cucumber and tomato against cucumber mosaic cucumovirus using plant growth-promoting rhizobacteria (PGPR). Plant Dis. 80, 891–894.Google Scholar
  33. 33.
    Santos, R. T. D. L., Rosales, N. M., Ocampo, J. A., García-Garrido, J. M. (2016) Ethylene alleviates the suppressive effect of phosphate on arbuscular mycorrhiza formation. J. Plant Growth Regul. 35, 611–617.Google Scholar
  34. 34.
    Savidor, A., Teper, D., Gartemann, K. H., Eichenlaub, R., Chalupowicz, L., Manulis-Sasson, S., Barash, I., Tews, H., Mayer, K., Giannone, R. J., Hettich, R. L., Sessa, G. (2012) The Clavibacter michiganensis subsp. michiganensis-Tomato interactome reveals the perception of pathogen by the host and suggests mechanisms of infection. J. Proteome Res. 11, 736–750.PubMedGoogle Scholar
  35. 35.
    Savidor, A., Chalupowicz, L., Teper, D., Gartemann, K. H., Eichenlaub, R., Manulis-Sasson, S., Barash, I., Sessa, G. (2014) Clavibacter michiganensis subsp. michiganensis Vatr1 and Vatr2 transcriptional regulators are required for virulence in tomato. Mol. Plant Microbe Interact. 27, 1035–1047.PubMedGoogle Scholar
  36. 36.
    Schenk, P. M., Kazan, K., Wilson, L., Anderson, J. P., Richmond, T., Somerville, S. C., Manners, J. M. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl Acad. Sci. USA 97, 11655–11660.PubMedGoogle Scholar
  37. 37.
    Silvani, V. A., Bidondo, L. F., Bompadre, M. J., Colombo, R. P., Pérgola, M., Bompadre, A., Fracchia, S., Godeas, A. (2014) Growth dynamics of geographically different arbuscular mycorrhizal fungal isolates belonging to the ‘Rhizophagus clade’ under monoxenic conditions. Mycologia 106, 963–975.PubMedGoogle Scholar
  38. 38.
    Song, Y., Chen, D., Lu, K., Sun, Z., Zeng, R. (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Frontiers in Plant Science 6, 1–13.Google Scholar
  39. 39.
    Song, Y. Y., Zeng, R., Sen, Xu, J. F., Li, J., Shen, X., Yihdego, W. G. (2010) Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS ONE 5.Google Scholar
  40. 40.
    Van Loon, L. C., Geraats, B. P. J., Linthorst, H. J. M. (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci. 11, 184–191.PubMedGoogle Scholar
  41. 41.
    Vierheilig, H., Coughlan, A. P., Wyss, U., Piché, Y. (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl. Environ. Microbiol. 64, 5004–5007.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Weller, D. M., Mavrodi, D. V., Van Pelt, J. A., Pieterse, C. M. J., Van Loon, L. C., Bakker, P. A. H. M. (2012) Induced systemic resistance (ISR) in Arabidopsis thaliana against Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol-producing Pseudomonas fuorescens. Phytopathology 102, 403–412.Google Scholar
  43. 43.
    Yan, Z., Reddy, M. S., Ryu, C.-M., McInroy, J. A., Wilson, M., Kloepper, J. W. (2002) Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 92, 1329–1333.PubMedGoogle Scholar

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© Akadémiai Kiadó Zrt. 2018

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Institute of Genetics, Microbiology and BiotechnologySzent István UniversityGödöllőHungary

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