Effects of nitrogen nutrition on disease development caused by Acidovorax citrulli on melon foliage

Abstract

Bacterial fruit blotch (BFB) of cucurbits, caused by the seed-borne bacterium Acidovorax citrulli, is a destructive disease that threatens the melon and watermelon industries worldwide. The available means to manage the disease are very limited and there are no reliable sources of BFB resistance. Mineral nutrition has marked effects on plant diseases. To the best of our knowledge, no studies reporting effects of mineral nutrition on BFB severity have been reported to date. In the present study we assessed the influence of nitrogen nutrition on BFB severity and A. citrulli establishment in the foliage of melon plants under greenhouse conditions. Our results show that nitrogen fertilization, based on nitrate only, led to reduced disease severity and bacterial numbers in melon leaves, as compared with two combinations of nitrate and ammonium. No consistent effect of nitrogen nutrition on expression of several plant defense-associated transcripts was found, except for hydroperoxide lyase (HPL), which upon inoculation was repressed to a greater extent under the “nitrate-only” nitrogen regime compared with combined nitrate and ammonium. Reducing BFB severity and A. citrulli establishment in the plant foliage are of particular importance since establishment of the pathogen during the growing season is assumed to increase the incidence of fruit infection, leading to serious yield losses. Further research is needed to elucidate the mechanisms by which nitrogen nutrition influences BFB development, and to assess the effects of nitrogen as well as other minerals on the disease under field conditions.

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References

  1. Almagro, L., Ros, L. V. G., Belchi-Navarro, S., Bru, R., Barcelo, A. R., & Pedreno, M. A. (2009). Class III peroxidases in plant defence reactions. Journal of Experimental Botany, 60, 377–390.

    CAS  Article  PubMed  Google Scholar 

  2. Bahar, O., & Burdman, S. (2010). Bacterial fruit blotch: a threat to the cucurbit industry. Israel Journal of Plant Sciences, 58, 19–32.

    Article  Google Scholar 

  3. Bahar, O., Efrat, M., Hadar, E., Dutta, B., Walcott, R. R., & Burdman, S. (2008). New subspecies-specific polymerase chain reaction-based assay for the detection of Acidovorax avenae subsp. citrulli. Plant Pathology, 57, 754–763.

    CAS  Article  Google Scholar 

  4. Bahar, O., Kritzman, G., & Burdman, S. (2009). Bacterial fruit blotch of melon: screens for disease tolerance and role of seed transmission in pathogenicity. European Journal of Plant Pathology, 123, 71–83.

    Article  Google Scholar 

  5. Bahar, O., Levi, N., & Burdman, S. (2011). The cucurbit pathogenic bacterium Acidovorax citrulli requires a polar flagellum for full virulence before and after host-tissue penetration. Molecular Plant-Microbe Interactions, 24, 1040–1050.

    CAS  Article  PubMed  Google Scholar 

  6. Bar-Tal, A., Aloni, B., Karni, L., Oserovitz, J., Hazan, A., Itach, M., et al. (2001). Nitrogen nutrition of greenhouse pepper: II. Effects of nitrogen concentration and NO3:NH4 ratio on growth, transpiration, and nutrient uptake. Hortscience, 36, 1252–1259.

    CAS  Google Scholar 

  7. Bate, N. J., & Rothstein, S. J. (1998). C-6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. The Plant Journal, 16, 561–569.

    CAS  Article  PubMed  Google Scholar 

  8. Bindschedler, L. V., Dewdney, J., Blee, K. A., Stone, J. M., Asai, T., Plotnikov, J., et al. (2006). Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. The Plant Journal, 47, 851–863.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Burdman, S., & Walcott, R. (2012). Acidovorax citrulli: generating basic and applied knowledge to tackle a global threat to the cucurbit industry. Molecular Plant Pathology, 13, 805–815.

    Article  PubMed  Google Scholar 

  10. Burdman, S., Kots, N., Kritzman, G., & Kopelowitz, J. (2005). Molecular, physiological, and host-range characterization of Acidovorax avenae subsp. citrulli isolates from watermelon and melon in Israel. Plant Disease, 89, 1339–1347.

    CAS  Article  Google Scholar 

  11. Canaday, C. H., & Wyatt, J. E. (1992). Effects of nitrogen fertilization on bacterial soft rot in two broccoli cultivars, one resistant and one susceptible to the disease. Plant Disease, 76, 989–991.

  12. Chalupowicz, L., Dror, O., Reuven, M., Burdman, S., & Manulis-Sasson, S. (2015). Cotyledons are the main source of secondary spread of Acidovorax citrulli in melon nurseries. Plant Pathology, 64, 528–536.

    CAS  Article  Google Scholar 

  13. Chase, A. R. (1989). Effect of nitrogen and potassium fertilizer rates on severity of Xanthomonas blight of Syngonium podophyllum. Plant Disease, 73, 972–975.

  14. Chase, A. R. (1990). Effect of nitrogen, phosphorus and potassium rates on severity of Xanthomonas leaf spot of Schefflera. Journal of Environmental Horticulture, 8, 74–78.

  15. Datnoff, L. E., Elmer, W. H., & Huber, D. M. (2007). Mineral nutrition and plant disease. St. Paul: American Phytopathological Society Press.

    Google Scholar 

  16. Daudi, A., Cheng, Z., O'Brien, J. A., Mammarella, N., Khan, S., Ausubel, F. M., et al. (2012). The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. The Plant Cell, 24, 275–287.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Deng, W. L., Hamilton-Kemp, T. R., Nielsen, M. T., Andersen, R. A., Collins, G. B., & Hildebrand, D. F. (1993). Effects of 6-carbon aldehydes and alcohols on bacterial proliferation. Journal of Agricultural and Food Chemistry, 41, 506–510.

    CAS  Article  Google Scholar 

  18. Duffy, B. K., & Défago, G. (1999). Macro- and microelement fertilizers influence the severity of Fusarium crown and root rot of tomato in a soilless production system. Hostscience, 34, 287–291.

  19. Dutta, B., Sanders, H., Langston, D. B., Booth, C., Smith, S., & Gitaitis, R. D. (2014). Long-term survival of Acidovorax citrulli in citron melon (citrullus lanatus var. citroides) seeds. Plant Pathology, 63, 1130–1137.

    CAS  Article  Google Scholar 

  20. Eckshtain-Levi, N., Munitz, T., Zivanovic, M., Traore, S. M., Spröer, C., Zhao, B., et al. (2014). Comparative analysis of type III secreted effector genes reflects divergence of Acidovorax citrulli strains into three distinct lineages. Phytopathology, 104, 1152–1162.

    CAS  Article  PubMed  Google Scholar 

  21. Elad, Y., Yunis, H., & Volpin, H. (1993). Effect of nutrition on susceptibility of cucumber, eggplant, and pepper crops to Botrytis cinerea. Canadian Journal of Botany, 71, 602–608.

    Article  Google Scholar 

  22. Elmer, W. H. (1989). Effects of chloride and nitrogen form on growth of asparagus infected by Fusarium spp. Plant Disease, 73, 736–740.

  23. Elmer, W. H. (2000). Comparison of plastic mulch and nitrogen form on the incidence of Verticillium wilt of eggplant. Plant Disease, 84, 1231–1234.

  24. Elmer, W. H., & LaMondia, J. A. (1999). Influence of ammonium sulfate and rotation crops on strawberry black root rot. Plant Disease, 83, 119–123.

  25. Farmer, E. E., Almeras, E., & Krishnamurthy, V. (2003). Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Current Opinion in Plant Biology, 6, 372–378.

    CAS  Article  PubMed  Google Scholar 

  26. Garcia-Mas, J., Benjak, A., Sanseverino, W., Bourgeois, M., Mir, G., González, V. M., et al. (2012). The genome of melon (Cucumis melo L.). Proceedings of the National Academy of Sciences USA, 109, 11872–11877.

    CAS  Article  Google Scholar 

  27. Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology, 43, 205–227.

    CAS  Article  PubMed  Google Scholar 

  28. Gomi, K., Yamasaki, Y., Yamamoto, H., & Akimitsu, K. (2003). Characterization of a hydroperoxide lyase gene and effect of C6-volatiles on expression of genes of the oxylipin metabolism in citrus. Journal of Plant Physiology, 160, 1219–1231.

    CAS  Article  PubMed  Google Scholar 

  29. Gupta, K. J., Brotman, Y., Segu, S., Zeier, T., Zeier, J., Presijn, S. T., et al. (2013). The form of nitrogen nutrition affects resistance against Pseudomonas syringae pv. phaseolicola in tobacco. Journal of Experimental Botany, 64, 553–568.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Harrison, U. J., & Shew, H. D. (2001). Effects of soil pH and nitrogen fertility on the population dynamics of Thielaviopsis basicola. Plant and Soil, 228, 147–155.

  31. Hildebrand, D. F., Brown, G. C., Jackson, D. M., & Hamilton-Kemp, T. R. (1993). Effects of some leaf-emitted volatile compounds on aphid population increase. Journal of Chemical Ecology, 19, 1875–1887.

    CAS  Article  PubMed  Google Scholar 

  32. Holeva, M. C., Karafla, C. D., Glynos, P. E., & Alivizatos, A. S. (2009). First report of natural infection of watermelon plants and fruits by the phytopathogenic bacterium Acidovorax avenae subsp. citrulli in Greece. Phytopathologia Mediterranea, 48, 316.

    Google Scholar 

  33. Hopkins, D. L., & Thompson, C. M. (2002). Seed transmission of Acidovorax avenae subsp. citrulli in cucurbits. Hortscience, 37, 924–926.

    Google Scholar 

  34. Hopkins, D. L., Thompson, C. M., & Elmstrom, G. W. (1993). Resistance of watermelon seedling and fruit to the fruit blotch bacterium. Hortscience, 28, 122–123.

    Google Scholar 

  35. Hopkins, D. L., Cucuzza, J. D., & Watterson, J. C. (1996). Wet seed treatments for the control of bacterial fruit blotch of watermelon. Plant Disease, 80, 529–532.

    Article  Google Scholar 

  36. Howe, G. A., & Schilmiller, A. L. (2002). Oxylipin metabolism in response to stress. Current Opinion in Plant Biology, 5, 230–236.

    CAS  Article  PubMed  Google Scholar 

  37. Huber, D. M., & Haneklaus, S. (2007). Managing nutrition to control plant disease. Landbauforschung Volkenrode, 57, 313–322.

    CAS  Google Scholar 

  38. Huber, D. M., & Thompson, A. (2007). Nitrogen and plant disease. In L. E. Datnoff, W. H. Elmer, & D. M. Huber (Eds.), Mineral nutrition and plant disease (pp. 31–44). St. Paul: American Phytopathological Society Press.

    Google Scholar 

  39. Jones, J. J. B., & Case, V. W. (1990). Sampling, handling, and analyzing plant tissue samples. In R. L. Westman (Ed.), Soil testing and plant analysis (3rd ed., pp. 389–427). Madison: Soil Science Society of America, Inc.

    Google Scholar 

  40. Kao, C. W., & Ko, W. H. (1986). The role of calcium and microorganisms in suppression of cucumber damping-off caused by Pythium splendens in Hawaiian soil. Phytopathology, 76, 221–225.

    CAS  Article  Google Scholar 

  41. Kirkby, E. A. (1968). Influence of ammonium and nitrate nutrition on the cation-anion balance and nitrogen and carbohydrate metabolism of white mustard plants grown in dilute nutrient solutions. Soil Science, 105, 133–141.

    CAS  Article  Google Scholar 

  42. Kishimoto, K., Matsui, K., Ozawa, R., & Takabayashi, J. (2005). Volatile C6-aldehydes and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant and Cell Physiology, 46, 1093–1102.

    CAS  Article  PubMed  Google Scholar 

  43. Kishimoto, K., Matsui, K., Ozawa, R., & Takabayashi, J. (2006). ETR1-, JAR1- and PAD2-dependent signaling pathways are involved in C6-aldehyde-induced defense responses of Arabidopsis. Plant Science, 171, 415–423.

    CAS  Article  PubMed  Google Scholar 

  44. Latin, R. C., & Hopkins, D. L. (1995). Bacterial fruit blotch of watermelon: the hypothetical exam question becomes reality. Plant Disease, 79, 761–765.

    Article  Google Scholar 

  45. Lima, G. S., Assunção, I. P., & de Oliveira, M. A. (1998). Effect of treatment of melon fruits (cucumis melo L.) with different calcium sources on rot caused by Myrothecium roridum. Summa Phytopathologica, 24, 276–279.

    Google Scholar 

  46. Liu, J., Luo, S. Z., Zhang, Q., Wang, Q. H., Chen, J. F., Guo, A. G., et al. (2012a). Tn5 transposon mutagenesis in Acidovorax citrulli for identification of genes required for pathogenicity on cucumber. Plant Pathology, 61, 364–374.

    CAS  Article  Google Scholar 

  47. Liu, X., Li, F., Tang, J., Wang, W., Zhang, F., Wang, G., et al. (2012b). Activation of the jasmonic acid pathway by depletion of the hydroperoxide lyase OsHPL3 reveals crosstalk between the HPL and AOS branches of the oxylipin pathway in rice. PloS One, 7, e50089.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Mirik, M., Aysan, Y., & Sahin, F. (2006). Occurrence of bacterial fruit blotch of watermelon caused by Acidovorax avenae subsp. citrulli in the Eastern Mediterranean region of Turkey. Plant Disease, 90, 829.

    Article  Google Scholar 

  49. Munitz, T. (2012). Characterization of type III-secreted effectors of Acidovorax citrulli, the causal agent of bacterial fruit blotch disease of cucurbits. Rehovot: The Hebrew University of Jerusalem, M.Sc thesis.

    Google Scholar 

  50. Palkovics, L., Petroczy, M., Kertesz, B., Nemeth, J., Barsony, C., Mike, Z., et al. (2008). First report of bacterial fruit blotch of watermelon caused by Acidovorax avenae subsp. citrulli in Hungary. Plant Disease, 92, 834–835.

    Article  Google Scholar 

  51. Penninckx, I., Thomma, B., Buchala, A., Metraux, J. P., & Broekaert, W. F. (1998). Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. The Plant Cell, 10, 2103–2113.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Popović, T., & Ivanović, Ž. (2015). Occurrence of Acidovorax citrulli causing bacterial fruit blotch of watermelon in Serbia. Plant Disease, 99, 886.

    Article  Google Scholar 

  53. Prabhu, A. S., Fageira, N. K., Berni, R. F., & Rodrigues, F. A. (2007). Phosphorous and plant disease. In L. E. Datnoff, W. H. Elmer, & D. M. Huber (Eds.), Mineral nutrition and plant disease (pp. 45–55). St. Paul: American Phytopathological Society Press.

    Google Scholar 

  54. Rahman, M., & Punja, Z. K. (2007). Calcium and plant disease. In L. E. Datnoff, W. H. Elmer, & D. M. Huber (Eds.), Mineral nutrition and plant disease (pp. 79–93). St. Paul: American Phytopathological Society Press.

    Google Scholar 

  55. Rane, K. K., & Latin, R. X. (1992). Bacterial fruit blotch of watermelon: association of the pathogen with seed. Plant Disease, 76, 509–512.

    Article  Google Scholar 

  56. Reuter, D. J., & Robinson, J. B. (1997). Plant analysis - an interpretation manual (2nd ed., ). Collingwood: CSIRO Publishing.

    Google Scholar 

  57. Sagar, V., & Sugha, S. K. (1998). Effect of soil type and available nutrients on fusarial population and severity of pea root rot. Journal of Mycology and Plant Pathology, 28, 294–299.

  58. Schaad, N. W., Sowell, G., Goth, R. W., Colwell, R. R., & Webb, R. E. (1978). Pseudomonas pseudoalcaligenes subsp. citrulli subsp-nov. International Journal of Systematic Bacteriology, 28, 117–125.

    Article  Google Scholar 

  59. Schaad, N. W., Postnikova, E., & Randhawa, P. (2003). Emergence of Acidovorax avenae subsp. citrulli as a crop threatening disease of watermelon and melon. In N. S. Iacobellis, A. Collmer, S. W. Hutcheson, J. Mansfield, C. E. Morris, J. Murillo, N. W. Schaad, D. E. Stead, G. Surico, & M. S. Ullrich (Eds.), Pseudomonas syringae and related pathogens (pp. 573–581). Dordrecht: Kluwer Academic Publishers.

    Google Scholar 

  60. Schaad, N. W., Postnikova, E., Sechler, A., Claflin, L. E., Vidaver, A. K., Jones, J. B., et al. (2008). Reclassification of subspecies of Acidovorax avenae as A. avenae (Manns 1905) emend., A. cattleyae (Pavarino, 1911) comb. nov., A. citrulli (Schaad et al., 1978) comb. nov., and proposal of A. oryzae sp. nov. Systematic and Applied Microbiology, 31, 434–446.

    CAS  Article  PubMed  Google Scholar 

  61. Shoresh, M., Yedidia, I., & Chet, I. (2005). Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology, 95, 76–84.

    CAS  Article  PubMed  Google Scholar 

  62. Somodi, G. C., Jones, J. B., Hopkins, D. L., Stall, R. E., Kucharek, T. A., Hodge, N. C., et al. (1991). Occurrence of a bacterial watermelon fruit blotch in Florida. Plant Disease, 75, 1053–1056.

    Article  Google Scholar 

  63. Tesfaye, M., Silverstein, K. A. T., Nallu, S., Wang, L., Botanga, C. J., Gomez, S. K., et al. (2013). Spatio-temporal expression patterns of Arabidopsis thaliana and Medicago truncatula defensin-like genes. PloS One, 8, e58992.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Walcott, R. R., Castro, A. C., Fessehaie, A., & Ling, K. (2006). Progress towards a commercial PCR-based assay for Acidovorax avenae subsp. citrulli. Seed Science and Technology, 34, 101–116.

    Article  Google Scholar 

  65. Wall, G. C., & Santos, V. M. (1988). A new bacterial disease on watermelon in the Mariana Islands. Phytopathology, 78, 1605.

    Google Scholar 

  66. Willems, A., Goor, M., Thielemans, S., Gillis, M., Kersters, K., & De Ley, J. (1992). Transfer of several phytopathogenic Pseudomonas species to Acidovorax as Acidovorax avenae subsp. avenae subsp. nov., comb. nov., Acidovorax avenae subsp. citrulli, Acidovorax avenae subsp. cattleyae, and Acidovorax konjaci. International Journal of Systematic Bacteriology, 42, 107–119.

    CAS  Article  PubMed  Google Scholar 

  67. Yedidia, I., Shoresh, M., Kerem, Z., Benhamou, N., Kapulnik, Y., & Chet, I. (2003). Concomitant induction of systemic resistance to Pseudomonas spingae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Applied and Environmental Microbiology, 69, 7343–7353.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  68. Zhao, B., Ardales, E. Y., Raymundo, A., Bai, J., Trick, H. N., Leach, J. E., et al. (2004). The avrRxo1 gene from the rice pathogen Xanthomonas oryzae pv. oryzicola confers a nonhost defense reaction on maize with resistance gene Rxo1. Molecular Plant-Microbe Interactions, 17, 771–779.

    CAS  Article  PubMed  Google Scholar 

  69. Zvirin, T., Herman, R., Brotman, Y., Denisov, Y., Belausov, E., & Freeman, S. (2010). Differential colonization and defence responses of resistant and susceptible melon lines infected by Fusarium oxysporum race 1.2. Plant Pathology, 59, 576–585.

    CAS  Article  Google Scholar 

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Acknowledgments

This work was funded by the Agriculture, Environment and Natural Resources Center of the Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem.

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Correspondence to Saul Burdman.

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Zimerman-Lax, N., Shenker, M., Tamir-Ariel, D. et al. Effects of nitrogen nutrition on disease development caused by Acidovorax citrulli on melon foliage. Eur J Plant Pathol 145, 125–137 (2016). https://doi.org/10.1007/s10658-015-0822-5

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Keywords

  • Acidovorax citrulli
  • Cucumis melo
  • Bacterial fruit blotch
  • Nutrition
  • Nitrogen