Biological Trace Element Research

, Volume 152, Issue 2, pp 275–283 | Cite as

Silicon-Mediated Tomato Resistance Against Ralstonia solanacearum is Associated with Modification of Soil Microbial Community Structure and Activity

Article

Abstract

Bacterial wilt caused by Ralstonia solanacearum is a serious soil-borne disease of Solanaceae crops. In this study, the soil microbial effects of silicon-induced tomato resistance against R. solanacearum were investigated through pot experiment. The results showed that exogenous 2.0 mM Si treatment reduced the disease index of bacterial wilt by 19.18 % to 52.7 % compared with non-Si-treated plants. The uptake of Si was significantly increased in the Si-treated tomato plants, where the Si content was higher in the roots than that in the shoots. R. solanacearum inoculation resulted in a significant increase of soil urease activity and reduction of soil sucrase activity, but had no effects on soil acid phosphatase activity. Si supply significantly increased soil urease and soil acid phosphatase activity under pathogen-inoculated conditions. Compared with the non-inoculated treatment, R. solanacearum infection significantly reduced the amount of soil bacteria and actinomycetes by 52.5 % and 16.5 %, respectively, but increased the ratio of soil fungi/soil bacteria by 93.6 %. After R. solanacearum inoculation, Si amendments significantly increased the amount of soil bacteria and actinomycetes and reduced soil fungi/soil bacteria ratio by 53.6 %. The results suggested that Si amendment is an effective approach to control R. solanacearum. Moreover, Si-mediated resistance in tomato against R. solanacearum is associated with the changes of soil microorganism amount and soil enzyme activity.

Keywords

Silicon Tomato Ralstonia solanacearum Soil enzyme activity Soil microorganism 

References

  1. 1.
    Bandick AK, Dick RP (1999) Field management effects on soil enzyme activities. Soil Biol Biochem 31:1471–1479CrossRefGoogle Scholar
  2. 2.
    Bao SD (2000) Soil agrochemical analysis. Third edition. China Agriculture Press, Beijing 234–235Google Scholar
  3. 3.
    Bélanger RR, Benhamou N, Menzies JG (2003) Cytological evidence of an active role of silicon in wheat resistance to powdery mildew (Blumeria graminis f. sp. tritici). J Phytopathol 93:402–12CrossRefGoogle Scholar
  4. 4.
    Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486PubMedCrossRefGoogle Scholar
  5. 5.
    Bowen P, Menzies J, Ehret D, Samuels L, Glass ADM (1992) Soluble silicon sprays inhibit powdery mildew development on grape leaves. J Am Soc Hortic Sci 117:906–912Google Scholar
  6. 6.
    Bulluck LR III, Ristaino JB (2002) Effect of synthetic and organic soil fertility amendments on southern blight, soil microbial communities and yield of processing tomatoes. Phytopathology 92:181–189PubMedCrossRefGoogle Scholar
  7. 7.
    Cai KZ, Gao D, Luo SM, Zeng RS, Yang JY, Zhu XY (2008) Physiological and cytological mechanisms of silicon-induced resistance in rice against blast disease. Physiol Plant 134:324–333PubMedCrossRefGoogle Scholar
  8. 8.
    Carver TLW, Zeyen RJ, Ahlstrand GG (1987) The relationship between insoluble silicon and success or failure of at tempted primary penetration by powdery mildew (Erysiphe graminis) germlings on barley. Physiol Mol Plant P 31:133–148CrossRefGoogle Scholar
  9. 9.
    Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fert Soils 48:489–499CrossRefGoogle Scholar
  10. 10.
    Chérif M, Asselin A, Bélanger RR (1994) Defense responses induced by soluble silicon in cucumber roots infected by Pythium spp. Mol Plant Pathol 84:236–242Google Scholar
  11. 11.
    Coventry E, Noble R, Mead A, Whipps JM (2005) Suppression of Allium white rot (Sclerotium cepivorum) in different soils using vegetable wastes. Eur J Plant Pathol 111:101–112CrossRefGoogle Scholar
  12. 12.
    Dannon EA, Wydra K (2004) Interaction between silicon amendment, bacterial wilt development and phenotype of Ralstonia solanacearum in tomato genotypes. Physiol Mol Plant P 64:233–243CrossRefGoogle Scholar
  13. 13.
    Datnoff LE, Deren CW, Snyder GH (1997) Silicon fertilization for disease management of rice in Florida. Crop Prot 16:525–31CrossRefGoogle Scholar
  14. 14.
    Deng SP, Tabatabai MA (1994) Cellulase activity of soils. Soil Biol Biochem 26:347–354Google Scholar
  15. 15.
    Diogo RVC, Wydra K (2007) Silicon-induced basal resistance in tomato against Ralstonia solanacearum is related to modification of pectic cell wall polysaccharide structure. Physiol Mol Plant P 70:120–129CrossRefGoogle Scholar
  16. 16.
    Eivazi F, Tabatabai MA (1977) Phosphatases in soils. Soil Biol Biochem 9:167–172CrossRefGoogle Scholar
  17. 17.
    Epstein E (1994) The anomaly of silicon in plant biology. Proc Natl Acad Sci USA 91:11–17PubMedCrossRefGoogle Scholar
  18. 18.
    Fang ZD (1998) Plant pathology research methods (third edition). China Agriculture Press, Beijing, 388Google Scholar
  19. 19.
    Fawe A, Abou-Zaid M, Menzies JG, Bélanger RR (1998) Silicon-mediated accumulation of flavonoid phytoalexins in cucumber. Phytopathology 88:396–401PubMedCrossRefGoogle Scholar
  20. 20.
    Fauteux F, Rémus-Borel W, Menzies JG, Bélanger RR (2005) Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiol Lett 249:1–6PubMedCrossRefGoogle Scholar
  21. 21.
    Fauteux F, Chain F, Belzile F, Menzies JG, Bélanger RR (2006) The protective role silicon in the Arabidopsis–powdery mildew pathosystem. Proc Natl Acad Sci USA 103:17554–17559PubMedCrossRefGoogle Scholar
  22. 22.
    Ghareeb H, Bozsó Z, Ott PG, Repenning C, Stahl F, Wydra K (2011) Transcriptome of silicon-induced resistance against Ralstonia solanacearum in the silicon non-accumulator tomato implicates priming effect. Physiol Mol Plant P 75:83–9CrossRefGoogle Scholar
  23. 23.
    Ghareeb H, Bozsób Z, Ottb PG, Wydra K (2011) Silicon and Ralstonia solanacearum modulate expression stability of housekeeping genes in tomato. Physiol Mol Plant P 75:176–179CrossRefGoogle Scholar
  24. 24.
    Gianfreda L, Rao MA, Piotrowska A, Palumbo G, Colombo C (2005) Soil enzyme activities as affected by anthropogenic alterations: intensive agricultural practices and organic pollution. Sci Total Environ 341:265–279PubMedCrossRefGoogle Scholar
  25. 25.
    Guan SY (1986) Soil enzymes and their research methods. Agriculture Press, BeijingGoogle Scholar
  26. 26.
    Guan SY, Zhang DS, Zhang ZM (1991) Methods of soil enzyme activities analysis. Agriculture Press, Beijing, pp. 263–271Google Scholar
  27. 27.
    Hayasaka T, Fujii H, Ishiguro K (2008) The role of silicon in preventing appressorial penetration by the rice blast fungus. Phytopathology 98:1038–1044PubMedCrossRefGoogle Scholar
  28. 28.
    Hayward AC (1991) Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu Rev Phytopathol 29:65–87PubMedCrossRefGoogle Scholar
  29. 29.
    Heath MC, Stumpf MA (1986) Ultrastructural observations of penetration sites of the cowpea rust fungus in untreated and silicon-depleted French bean cells. Physiol Mol Plant P 29:27–39CrossRefGoogle Scholar
  30. 30.
    Hoitink HAJ, Fahy PC (1986) Basis for the control of soilborne plant pathogens with composts. Annu Rev Phytopathol 24:93–114CrossRefGoogle Scholar
  31. 31.
    Janvier C, Villeneuve F, Alabouvette C, Edel-Hermannb V, Mateille T, Steinbergb C (2007) Soil health through soil disease suppression: which strategy from descriptors to indicators? Soil Biol Biochem 39:1–23CrossRefGoogle Scholar
  32. 32.
    Johnson NN, Lisa LBA, Kathy K, Carl G (2002) Soil microbial and chemical indicators of soil health response to agricultural intensification practices on black cracking clay soils. 17th WCSS, Thailand 14–21Google Scholar
  33. 33.
    Kelman A (1954) The relationship of pathogenicity in Pseudomonas solanacearum to colony appearance in a tetrazolium medium. Phytopathology 44:693–695Google Scholar
  34. 34.
    Larkin RP (2003) Characterization of soil microbial communities under different potato cropping systems by microbial population dynamics, substrate utilization, and fatty acid profiles. Soil Biol Biochem 35:1451–1466CrossRefGoogle Scholar
  35. 35.
    Leon MCC, Stone A, Dick RP (2006) Organic soil amendments: impacts on snap bean common root rot (Aphanomyces euteiches) and soil quality. Appl Soil Ecol 31:199–210CrossRefGoogle Scholar
  36. 36.
    Liang YC, Sun WC, Si J, Römheld V (2005) Effects of foliar- and root-applied silicon on the enhancement of induced resistance to powdery mildew in Cucumis sativus. Plant Pathol 54:678–685CrossRefGoogle Scholar
  37. 37.
    Lindow SE, Leveau JH (2002) Phyllosphere microbiology. Curr Opin Biotech 13:238–243PubMedCrossRefGoogle Scholar
  38. 38.
    Liu QG, Yang Y (2006) The relationship between tomato resistance and the quantity of Ralstonia solanacearum and rhizosphere microbes. J Zhongkai Univ Agr Tech 19:31–34Google Scholar
  39. 39.
    Ma JF, Yamaji NK (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397PubMedCrossRefGoogle Scholar
  40. 40.
    Makoi JHJR, Ndakidemi PA (2008) Selected soil enzymes: examples of their potential roles in the ecosystem. Afr J Biotechnol 7:181–191Google Scholar
  41. 41.
    Martin JP (1950) Use of acid, rose Bengal and streptomycin in the plate method for estimating soil fungi. Soil Sci 69:215–232CrossRefGoogle Scholar
  42. 42.
    Nelson EB, Craft CM (1992) Suppression of dollar spot on creeping bentgrass and annual bluegrass turf with compost-amended topdressings. Plant Dis 76:954–958CrossRefGoogle Scholar
  43. 43.
    Pavel R, Doyle J, Steinberger Y (2004) Seasonal pattern of cellulase concentration in desert soil. Soil Biol Biochem 36:549–554CrossRefGoogle Scholar
  44. 44.
    Rasmussen PH, Knudsen IMB, Elmholt S, Jensen DF (2002) Relationship between soil cellulolytic activity and suppression of seedling blight of barley in arable soils. Appl Soil Ecol 19:91–96CrossRefGoogle Scholar
  45. 45.
    Rémus-Borel W, Menzies JG, Bélanger RR (2005) Silicon induces antifungal compounds in powdery mildew-infected wheat. Physiol Mol Plant P 66:108–115CrossRefGoogle Scholar
  46. 46.
    Rodrigues FÁ, Benhamou N, Datnoff LE, Jones JB, Bélanger RR (2003) Ultrastructural and cytochemical aspects of silicon-mediated rice blast resistance. Phytopathology 93:535–546Google Scholar
  47. 47.
    Ros M, Hernandez MT, Garcia C, Bernal A, Pascual JA (2005) Biopesticide effect of green compost against fusarium wilt on melon plants. J Appl Microbiol 98:845–854PubMedCrossRefGoogle Scholar
  48. 48.
    Samuels AL, Glass ADM, Ehret DL, Menzies JG (1991) Distribution of silicon in cucumber leaves during infection by powdery mildew fungus (Sphaerotheca fuliginea). Can J Bot 69:140–146CrossRefGoogle Scholar
  49. 49.
    Shetty R, Jensen B, Shetty NP, Hansen M, Hansen CW, Starkey KR, Jørgensen HJL (2012) Silicon induced resistance against powdery mildew of roses caused by Podosphaera pannosa. Plant Pathol 61:120–131CrossRefGoogle Scholar
  50. 50.
    Sun XS, Feng HS, Wan SB, Zuo XQ (2001) Changes of main microbial strains and enzymes activities in peanut continuous cropping soil and their interactions. Acta Agron Sin 27:617–621Google Scholar
  51. 51.
    Tabatabai MA (1994) Soil enzymes. In: Weaver RW, Angel GS, Bottomley PS (eds.) Methods of soil analysis. Soil Science Society of America, Madison, pp. 775–833Google Scholar
  52. 52.
    Overbeek LSV, Cassidy M, Kozdroj J, Trevors JT, Elsas JDV (2002) A polyphasic approach for studying the interaction between Ralstonia solanacearum and potential and potential control agent in the tomato phytosphere. J Microbiol Meth 48:69–86CrossRefGoogle Scholar
  53. 53.
    Van der Vorm PDJ (1987) Dry ashing of plant material and dissolution of the ash in HF for the colorimetric determination of silicon. Commun Soil Sci Plant 18:1181–1189CrossRefGoogle Scholar
  54. 54.
    Visser S, Parkinson D (1992) Soil biological criteria as indicators of soil quality: soil microorganisms. AJAA 7:33–37CrossRefGoogle Scholar
  55. 55.
    Wang RH, Zhou BL, Zhang QF, Zhang FL, Fu YW (2005) Effects of grafting on rhizosphere microbial populations of eggplants. Acta Hortic Sin 32:124–126Google Scholar
  56. 56.
    Wiggins BE, Kinkel LL (2005) Green manures and crop sequences influence alfalfa root rot and pathogen inhibitory activity among soil-borne streptomycetes. Plant Soil 268:271–283CrossRefGoogle Scholar
  57. 57.
    Yao HY, Huang CY (2006) Microbial ecology and experimental techniques. Sciences Press, BeijingGoogle Scholar
  58. 58.
    Yogev A, Laor Y, Katan J, Hadar Y, Cohen R, Medina S, Raviv M (2011) Does organic farming increase soil suppression against Fusarium wilt of melon? Org Agr 1:203–216CrossRefGoogle Scholar
  59. 59.
    Zhao N, Cai KZ, Wang GP, Wang Y (2008) Induced resistance of tomato plants to bacterial wilt by livestock wastes compost and its physiological mechanisms. J Agro-Environ Sci 27:2058–2063Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Lei Wang
    • 1
  • Kunzheng Cai
    • 1
  • Yuting Chen
    • 1
  • Guoping Wang
    • 2
  1. 1.Key Laboratory of Tropical Agro-environment, Ministry of AgricultureSouth China Agricultural UniversityGuangzhouChina
  2. 2.College of HorticultureSouth China Agricultural UniversityGuangzhouChina

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