DOI QR코드

DOI QR Code

Differential Control Efficacies of Vitamin Treatments against Bacterial Wilt and Grey Mould Diseases in Tomato Plants

  • Hong, Jeum Kyu (Department of Horticultural Science, Gyeongnam National University of Science and Technology (GNTech)) ;
  • Kim, Hyeon Ji (Department of Horticultural Science, Gyeongnam National University of Science and Technology (GNTech)) ;
  • Jung, Heesoo (Department of Horticultural Science, Gyeongnam National University of Science and Technology (GNTech)) ;
  • Yang, Hye Ji (Department of Horticultural Science, Gyeongnam National University of Science and Technology (GNTech)) ;
  • Kim, Do Hoon (Department of Horticultural Science, Gyeongnam National University of Science and Technology (GNTech)) ;
  • Sung, Chang Hyun (Turfgrass Science Institute, Hanul Inc.) ;
  • Park, Chang-Jin (Department of Bioresources Engineering and PERI, Sejong University) ;
  • Chang, Seog Won (Department of Golf Course Management, Korea Golf University)
  • Received : 2016.03.28
  • Accepted : 2016.05.16
  • Published : 2016.10.01

Abstract

Bacterial wilt and grey mould in tomato plants are economically destructive bacterial and fungal diseases caused by Ralstonia solanacearum and Botrytis cinerea, respectively. Various approaches including chemical and biological controls have been attempted to arrest the tomato diseases so far. In this study, in vitro growths of bacterial R. solanacearum and fungal B. cinerea were evaluated using four different vitamins including thiamine (vitamin B1), niacin (vitamin B3), pyridoxine (vitamin B6), and menadione (vitamin K3). In planta efficacies of the four vitamin treatments on tomato protection against both diseases were also demonstrated. All four vitamins showed different in vitro antibacterial activities against R. solanacearum in dose-dependent manners. However, treatment with 2 mM thiamine was only effective in reducing bacterial wilt of detached tomato leaves without phytotoxicity under lower disease pressure ($10^6$ colony-forming unit [cfu]/ml). Treatment with the vitamins also differentially reduced in vitro conidial germination and mycelial growth of B. cinerea . The four vitamins slightly reduced the conidial germination, and thiamine, pyridoxine and menadione inhibited the mycelial growth of B. cinerea. Menadione began to drastically suppress the conidial germination and mycelial growth by 5 and 0.5 mM, respectively. Grey mould symptoms on the inoculated tomato leaves were significantly reduced by pyridoxine and menadione pretreatments one day prior to the fungal challenge inoculation. These findings suggest that disease-specific vitamin treatment will be integrated for eco-friendly management of tomato bacterial wilt and grey mould.

Keywords

References

  1. Abba, S., Khouja, H. R., Martino, E., Archer, D. B. and Perotto, S. 2009. SOD1-targeted gene disruption in the ericoid mycorrhizal fungus Oidiodendron maius reduces conidiation and the capacity for mycorrhization. Mol. Plant-Microbe Interact. 22:1412-1421. https://doi.org/10.1094/MPMI-22-11-1412
  2. Ahn, I. P., Kim, S. and Lee, Y. H. 2005. Vitamin B1 functions as an activator of plant disease resistance. Plant Physiol. 138:1505-1515. https://doi.org/10.1104/pp.104.058693
  3. Anith, K. N., Momol, M. T., Kloepper, J. W., Marios, J. J., Olson, S. M. and Jones, J. B. 2004. Efficacy of plant growthpromoting rhizocbacteria, acibenzolar-S-methyl, and soil amendment for integrated management of bacterial wilt on tomato. Plant Dis. 88:669-673. https://doi.org/10.1094/PDIS.2004.88.6.669
  4. Arenas, F. A., Diaz, W. A., Leal, C. A., Perez-Donoso, J. M., Imlay, J. A. and Vasquez, C. C. 2010. The Escherichia coli btuE gene, encodes a glutathione peroxidase that is induced under oxidative stress conditions. Biochem. Biophys. Res. Commun. 398:690-694. https://doi.org/10.1016/j.bbrc.2010.07.002
  5. Bahuguna, R. N., Joshi, R., Shukla, A., Pandey, M. and Kumar, J. 2012. Thiamine primed defense provides reliable alternative to systemic fungicide carbendazim against sheath blight disease in rice (Oryza sativa L.). Plant Physiol. Biochem. 57:159-167. https://doi.org/10.1016/j.plaphy.2012.05.003
  6. Ben-Jabeur, M., Ghabri, E., Myriam, M. and Hamada, W. 2015. Thyme essential oil as a defense inducer of tomato against gray mold and Fusarium wilt. Plant Physiol. Biochem. 94:35-40. https://doi.org/10.1016/j.plaphy.2015.05.006
  7. Borges, A. A., Borges-Perez, A. and Fernandez-Falcon, M. 2003a. Effect of menadione sodium bisulfite, an inducer of plant defenses, on the dynamic of banana phytoalexin accumulation during pathogenesis. J. Agric. Food Chem. 51: 5326-5328. https://doi.org/10.1021/jf0300689
  8. Borges, A. A., Cools, H. J. and Lucas, J. A. 2003b. Menadione sodium bisulfite: a novel plant defence activator which enhances local and systemic resistance to infection by Leptosphaeria maculans in oilseed rape. Plant Pathol. 52:429-436. https://doi.org/10.1046/j.1365-3059.2003.00877.x
  9. Borges, A. A., Dobon, A., Exposito-Rodriguez, M., Jimenez-Arias, D., Borges-Perez, A., Casanas-Sanchez, V., Perez, J. A., Luis, J. C. and Tornero, P. 2009. Molecular analysis of menadione-induced resistance against biotic stress in Arabidopsis. Plant Biotechnol. J. 7:744-762. https://doi.org/10.1111/j.1467-7652.2009.00439.x
  10. Boubakri, H., Wahab, M. A., Chong, J., Bertsch, C., Mliki, A. and Soustre-Gacougnolle, I. 2012. Thiamine induced resistance to Plasmopara viticola in grapevine and elicited host-defense responses, including HR like-cell death. Plant Physiol. Biochem. 57:120-133. https://doi.org/10.1016/j.plaphy.2012.05.016
  11. Carmeille, A., Prior, P., Kodja, H., Chiroleu, F., Luisetti, J. and Besse, P. 2006. Evaluation of resistance to race 3, biovar 2 of Ralstonia solanacearum in tomato germplasm. J. Phytopathol. 154:398-402. https://doi.org/10.1111/j.1439-0434.2006.01112.x
  12. Cristescu, S. M., De Martinis, D., Te Lintel Hekkert, S., Parker, D. H. and Harren, F. J. 2002. Ethylene production by Botrytis cinerea in vitro and in tomatoes. Appl. Environ. Microbiol. 68:5342-5350. https://doi.org/10.1128/AEM.68.11.5342-5350.2002
  13. Denslow, S. A., Walls, A. A. and Daub, M. E. 2005. Regulation of biosynthetic genes and antioxidant properties of vitamin B6 vitamers during plant defense responses. Physiol. Mol. Plant Pathol. 66:244-255. https://doi.org/10.1016/j.pmpp.2005.09.004
  14. Egashira, H., Kuwashima, A., Ishiguro, H., Fukushima, K., Kaya, T. and Imanishi, S. 2000. Screening of wild accessions resistant to gray mold (Botrytis cinerea Pers.) in Lycopersicon. Acta Physiol. Plant. 22:324-326. https://doi.org/10.1007/s11738-000-0046-x
  15. Elad, Y. and Volpin, H. 1993. Reduced development of grey mould (Botrytis cinerea) in bean and tomato plants by calcium nutrition. J. Phytopathol. 139:146-156. https://doi.org/10.1111/j.1439-0434.1993.tb01410.x
  16. Han, Y. K., Min, J. S., Park, J. H., Han, K. S., Kim, D. H., Lee, J. S. and Kim, H. H. 2009. Screening of tomato cultivars resistant to bacterial wilts. Res. Plant Dis. 15:198-201 (in Korean). https://doi.org/10.5423/RPD.2009.15.3.198
  17. Harel, Y. M., Mehari, Z. H., Rav-David, D. and Elad, Y. 2014. Systemic resistance to gray mold induced in tomato by benzothiadiazole and Trichoderma harzianum T39. Phytopathology 104:150-157. https://doi.org/10.1094/PHYTO-02-13-0043-R
  18. Hong, J. C., Momol, M. T., Ji, P., Olson, S. M., Colee, J. and Jones, J. B. 2011. Management of bacterial wilt in tomatoes with thymol and acibenzolar-S-methyl. Crop Protect. 30:1340-1345. https://doi.org/10.1016/j.cropro.2011.05.019
  19. Hong, J. K., Kang, S. R., Kim, Y. H., Yoon, D. J., Kim, D. H., Kim, H. J., Sung, C. H., Kang, H. S., Choi, C. W., Kim, S. H. and Kim, Y. S. 2013. Hydrogen peroxide- and nitric oxidemediated disease control of bacterial wilt in tomato plants. Plant Pathol. J. 29:386-396. https://doi.org/10.5423/PPJ.OA.04.2013.0043
  20. Hong, J. K., Yang, H. J., Jung, H., Yoon, D. J., Sang, M. K. and Jeun, Y. C. 2015. Application of volatile antifungal plant essential oils for controlling pepper fruit anthracnose by Colletotrichum gloeosporioides. Plant Pathol. J. 31:269-277. https://doi.org/10.5423/PPJ.OA.03.2015.0027
  21. Huang, Q. and Lakshman, D. K. 2010. Effect of clove oil on plant pathogenic bacteria and bacterial wilt of tomato and geranium. J. Plant Pathol. 92:701-707.
  22. Igbaria, A., Lev, S., Rose, M. S., Lee, B. N., Hadar, R., Degani, O. and Horwitz, B. A. 2008. Distinct and combined roles of the MAP kinases of Cochliobolus heterostrophus in virulence and stress responses. Mol. Plant-Microbe Interact. 21:769-780. https://doi.org/10.1094/MPMI-21-6-0769
  23. Imada, K., Tanaka, S., Ibaraki, Y., Yoshimura, K. and Ito, S. 2014. Antifungal effect of 405-nm light on Botrytis cinerea. Lett. Appl. Microbiol. 59:670-676. https://doi.org/10.1111/lam.12330
  24. Ji, P., Momol, M. T., Olson, S. M., Pradhanang, P. M. and Jones, J. B. 2005. Evaluation of thymol as biofumigant for control of bacterial wilt of tomato under field conditions. Plant Dis. 89:497-500. https://doi.org/10.1094/PD-89-0497
  25. Jiang, J., Lu, Y., Li, J., Li, L., He, X., Shao, H. and Dong, Y. 2014. Effect of seed treatment by cold plasma on the resistance of tomato to Ralstonia solanacearum (bacterial wilt). PLoS One 9:e97753. https://doi.org/10.1371/journal.pone.0097753
  26. Jimenez-Arias, D., Borges, A. A., Luis, J. C., Valdes, F., Sandalio, L. M. and Perez, J. A. 2015. Priming effect of menadione sodium bisulphite against salinity stress in Arabidopsis involves epigenetic changes in genes controlling proline metabolism. Environ. Exper. Bot. 120:23-30. https://doi.org/10.1016/j.envexpbot.2015.07.003
  27. Jyothi, H. K., Santhosha, H. M. and Basamma. 2012. Recent advances in breeding for bacterial wilt (Ralstonia solanacearum) resistance in tomato: review. Curr. Biotica 6:370-398.
  28. Kim, H. S., Cho, K. W. and Lee, D. K. 2005. A study on the antimicrobial activity and preservative effect of thiamine dilauryl sulfate in cosmetics. J. Korean Oil Chemist's Soc. 22:212-218.
  29. Kim, Y. C., Kim, Y. H., Lee, Y. H., Lee, S. W., Chae, Y. S., Kang, H. K., Yun, B. W. and Hong, J. K. 2013. ${\beta}$-Amino-n-butyric acid regulates seedling growth and disease resistance of kimchi cabbage. Plant Pathol. J. 29:305-316. https://doi.org/10.5423/PPJ.OA.12.2012.0191
  30. Lai, T., Wang, Y., Li, B., Qin, G. and Tian, S. 2011. Defense responses of tomato fruit to exogenous nitric oxide during postharvest storage. Postharvest Biol. Technol. 62:127-132. https://doi.org/10.1016/j.postharvbio.2011.05.011
  31. Lee, J. P., Lee, S. W., Kim, C. S., Son, J. H., Song, J. H., Lee, K. Y., Kim, H. J., Jung, S. J. and Moon, B. J. 2006. Evaluation of formulations of Bacillus licheniformis for the biological control of tomato gray mold caused by Botrytis cinerea. Biol. Contr. 37:329-337. https://doi.org/10.1016/j.biocontrol.2006.01.001
  32. Lee, M. J. and Ha, S. D. 2008. Synergistic effect of vitamins B1 on sanitizer and disinfectant treatments for reduction of coliforms in rice. Food Cont. 19:113-118. https://doi.org/10.1016/j.foodcont.2007.02.009
  33. Lee, Y. H., Choi, C. W., Kim, S. H., Yun, J. G., Chang, S. W., Kim, Y. S. and Hong, J. K. 2012. Chemical pesticides and plant essential oils for disease control of tomato bacterial wilt. Plant Pathol. J. 28:32-39. https://doi.org/10.5423/PPJ.OA.10.2011.0200
  34. Lehmann, S., Serrano, M., L'Haridon, F., Tjamos, S. E. and Metraux, J. P. 2015. Reactive oxygen species and plant resistance to fungal pathogens. Phytochemistry 112:54-62. https://doi.org/10.1016/j.phytochem.2014.08.027
  35. Liu, L., Sun, C., Liu, S., Chai, R., Huang, W., Liu, X., Tang, C. and Zhang, Y. 2015. Bioorganic fertilizer enhances soil suppressive capacity against bacterial wilt of tomato. PLoS One 10:e0121304. https://doi.org/10.1371/journal.pone.0121304
  36. McFeeters, H. and McFeeters, R. L. 2012. Emerging approaches to inhibit Botrytis cinerea. Int. J. Mod. Bot. 2:127-144.
  37. Molan, Y. Y. and El-Komy, M. H. 2010. Expression of Sl-WRKY1 transcription factor during B. cinerea tomato interaction in resistant and susceptible cultivars. Int. J. Plant Breed. Genet. 4:1-12. https://doi.org/10.3923/ijpbg.2010.1.12
  38. Mongkolsuk, S., Loprasert, S., Vattanaviboon, P., Chanvanichayachai, C., Chamnongpol, S. and Supsamran, N. 1996. Heterologous growth phase- and temperature-dependent expression and $H_2O_2$ toxicity protection of a superoxideinducible monofunctional catalase gene from Xanthomonas oryzae pv. oryzae. J. Bacteriol. 178:3578-3584. https://doi.org/10.1128/jb.178.12.3578-3584.1996
  39. Nguyen, M. T. and Ranamukhaarachichi, S. L. 2010. Soil-borne antagonists for biological control of bacterial wilt disease caused by Ralstonia solanacearum in tomato and pepper. J. Plant Pathol. 92:395-406.
  40. Nikolaou, E., Agrafioti, I., Stumpf, M., Quinn, J., Stansfield, I. and Brown, A. J. 2009. Phylogenetic diversity of stress signalling pathway in fungi. BMC Evol. Biol. 9:44. https://doi.org/10.1186/1471-2148-9-44
  41. Pradhanang, P. M., Ji, P., Momol, M. T., Olson, S. M., Mayfield, J. L. and Jones, J. B. 2005. Application of acibenzolar-Smethyl enhances host resistance in tomato against Ralstonia solanacearum. Plant Dis. 89:989-993. https://doi.org/10.1094/PD-89-0989
  42. Pushpalatha, H. G., Mythrashree, S. R., Shetty, R., Geetha, N. P., Sharathchandra, R. G., Amruthesh, K. N. and Shetty, H. S. 2007. Ability of vitamins to induce downy mildew disease resistance and growth promotion in pearl millet. Crop Protect. 26:1674-1681. https://doi.org/10.1016/j.cropro.2007.02.012
  43. Rapala-Kozik, M., Kowalska, E. and Ostrowska, K. 2008. Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress. J. Exp. Bot. 59:4133-4143. https://doi.org/10.1093/jxb/ern253
  44. Rapala-Kozik, M., Wolak, N., Kujda, M. and Banas, A. K. 2012. The upregulation of thiamine (vitamin B1) biosynthesis in Arabidopsis thaliana seedlings under salt and osmotic stress conditions is mediated by abscisic acid at the early stages of this stress response. BMC Plant Biol. 12:2. https://doi.org/10.1186/1471-2229-12-2
  45. Rivard, C. L., O'Connell, S., Peet, M. M., Welker, R. M. and Louws, F. J. 2012. Grafting tomato to manage bacterial wilt caused by Ralstonia solanacearum in the southeastern United States. Plant Dis. 96:973-978. https://doi.org/10.1094/PDIS-12-10-0877
  46. Schaad, N. W., Jones, J. B. and Chun, W. 2001. Laboratory guide for identification of plant pathogenic bacteria. 3rd ed. APS Press, St. Paul, MN, USA.
  47. Smirnova, G. V., Muzyka, N. G., Glukhovchenko, M. N. and Oktyabrsky, O. N. 2000. Effects of menadione and hydrogen peroxide on glutathione status in growing Escherichia coli. Free Rad. Biol. Med. 28:1009-1016. https://doi.org/10.1016/S0891-5849(99)00256-7
  48. Soylu, E. M., Kurt, S. and Soylu, S. 2010. In vitro and in vivo antifungal activities of the essential oils of various plants against tomato grey mould disease agent Botrytis cinerea. Int. J. Food Microbiol. 143:183-189. https://doi.org/10.1016/j.ijfoodmicro.2010.08.015
  49. Tamarit, J., Cabisol, E. and Ros, J. 1998. Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J. Biol. Chem. 273:3027-3032. https://doi.org/10.1074/jbc.273.5.3027
  50. Tunc-Ozdemir, M., Miller, G., Song, L., Kim, J., Sodek, A., Koussevitzky, S., Misra, A. N., Mittler, R. and Shintani, D. 2009. Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiol. 151:421-432. https://doi.org/10.1104/pp.109.140046
  51. Vattanaviboon, P., Whangsuk, W. and Mongkolsuk, S. 2003. A suppressor of the menadione-hypersensitive phenotype of a Xanthomonas campestris pv. phaseoli oxyR mutant reveals a novel mechanism of toxicity and the protective role of alkyl hydroperoxides reductase. J. Bacteriol. 185:1734-1738. https://doi.org/10.1128/JB.185.5.1734-1738.2003
  52. Wang, L., Cai, K., Chen, Y. and Wang, G. 2013. Siliconmediated tomato resistance against Ralstonia solanacearum is associated with modification of soil microbial community structure and activity. Biol. Trace Elem. Res. 152:275-283. https://doi.org/10.1007/s12011-013-9611-1
  53. Wei, Z., Huang, J. F., Hu, J., Gu, Y. A., Yang, C. L., Mei, X. L., Shen, Q. R., Xu, Y. C. and Friman, V. P. 2015. Altering transplantation time to avoid periods of high temperature can efficiently reduce bacterial wilt disease incidence with tomato. PLoS One 10:e0139313. https://doi.org/10.1371/journal.pone.0139313
  54. Wu, Z., Yin, X., Banuelos, G. S., Lin, Z. Q., Zhu, Z., Liu, Y., Yuan, L. and Li, M. 2016. Effect of selenium on control of postharvest gray mold of tomato fruit and possible mechanisms involved. Front. Microbiol. 6:1441.
  55. Yamazaki, H. and Hoshina, T. 1995. Calcium nutrition affects resistance of tomato seedlings to bacterial wilt. HotScience 30:91-93.
  56. Yamazaki, H., Kikuchi, S., Hoshina, T. and Kimura, T. 1999. Effect of calcium concentration in nutrient solution before and after inoculation with Ralstonia solanacearum on resistance of tomato seedlings to bacterial wilt. Soil Sci. Plant Nutr. 45:1009-1014. https://doi.org/10.1080/00380768.1999.10414352
  57. Yan, L., Yang, Q., Jiang, J., Michailides, T. J. and Ma, Z. 2011. Involvement of a putative response regulator Brrg-1 in the regulation of sporulation, sensitivity to fungicides, and osmotic stress in Botrytis cinerea. Appl. Microbiol. Biotechnol. 90:215-226. https://doi.org/10.1007/s00253-010-3027-z
  58. Yuliar, Nion, Y. A. and Toyota, K. 2015. Recent trends in control methods for bacterial wilt diseases caused by Ralstonia solanacearum. Microbes Environ. 30:1-11. https://doi.org/10.1264/jsme2.ME14144
  59. Zhang, Y., Jin, X., Ouyang, Z., Li, X., Liu, B., Huang, L., Hong, Y., Zhang, H., Song, F. and Li, D. 2015. Vitamin B6 contributes to disease resistance against Pseudomonas syringae pv. tomato DC3000 and Botrytis cinerea in Arabidopsis thaliana. J. Plant Physiol. 175:21-25. https://doi.org/10.1016/j.jplph.2014.06.023
  60. Zhang, Y., Liu, B., Li, X., Ouyang, Z., Huang, L., Hong, Y., Zhang, H., Li, D. and Song, F. 2014. The de novo biosynthesis of vitamin B6 is required for disease resistance against Botrytis cinerea in tomato. Mol. Plant-Microbe Interact. 27:688-699. https://doi.org/10.1094/MPMI-01-14-0020-R

Cited by

  1. Identification and Characterization of Menadione and Benzethonium Chloride as Potential Treatments of Pierce’s Disease of Grapevines vol.109, pp.2, 2019, https://doi.org/10.1094/PHYTO-07-18-0244-FI