Bacillus thuringiensis suppresses bacterial wilt disease caused by Ralstonia solanacearum with systemic induction of defense-related gene expression in tomato

Microbes and Environments

Volumn 28, Issue 1, 2013, Pages 128-134

  Hyakumachi, Mitsuro ^a   Nishimura, Mitsuyoshi ^a   Arakawa, Tatsuyuki ^a   Asano, Shinichiro ^b   Yoshida, Shigenobu ^c   Tsushima, Seiya ^c   Takahashi, Hideki ^d  

^a GIFU UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE FOR AGRO ENVIRONMENTAL SCIENCES   (Japan)

^d TOHOKU UNIVERSITY   (Japan)

Author keywords

Bacillus thuringiensis; Induced resistance; Ralstonia solanacearum; Tomato

Indexed keywords

CHITINASE; GLUCAN 1,3 BETA GLUCOSIDASE; VEGETABLE PROTEIN;

ARTICLE; BACILLUS THURINGIENSIS; BIOLOGICAL PEST CONTROL; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT ROOT; PLANT STEM; RALSTONIA SOLANACEARUM; TOMATO;

BACILLUS THURINGIENSIS; CHITINASE; GENE EXPRESSION REGULATION, PLANT; GLUCAN 1,3-BETA-GLUCOSIDASE; LYCOPERSICON ESCULENTUM; PEST CONTROL, BIOLOGICAL; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANT STEMS; RALSTONIA SOLANACEARUM;

EID: 84875200208     PISSN: 13426311     EISSN: 13474405     Source Type: Journal    
DOI: 10.1264/jsme2.ME12162     Document Type: Article

References (54)

1. Bargabus, R.L., N.K. Zidack, J.W. Sherwood, and B.J. Jacobsen. 2002. Characterization of systemic resistance in sugar beet elicited by a non-pathogenic, phyllosphere-colonizing Bacillus mycoides, biological control agent. Physiol. Mol. Plant Pathol. 61:289-298.
2. Bennett, A.E., J. Alers-Garcia, and J.D. Bever. 2006. Three way interactions among mutualistic mycorrhizal fungi, plants and plant enemies: hypothesis and synthesis. American Natural. 167:141-152.
3. Cherif, A., S. Chehimi, F. Limem, B.M. Hansen, N.B. Hendriksen, D. Daffonchio, and A. Boudabous. 2003. Purification and characterization of the novel bacteriocin entomocine 9, and safety evaluation of its producer, Bacillus thuringiensis subsp. entomocidus HD9. J. Appl. Microbiol. 95:990-1000.
4. Cherif, A., W. Rezgui, N. Raddadi, D. Daffonchio, and A. Boudabous. 2008. Characterization and partial purification of entomocin 110, a newly identified bacteriocin from Bacillus thuringiensis subsp. entomocidus HD110. Microbiol. Res. 163:684-692.
5. Dong, Y.H., A.R. Gusti, Q. Zhang, J.L. Xu, and L.H. Zhang. 2002. Identification of quorum-quenching N-acylhomoserine lactonases from Bacillus species. Appl. Environ. Microbiol. 68:1754-1759.
6. Fravel, D. 2005. Commercialization and implementation of biocontrol. Annu. Rev. Phytopathol. 43:337-359.
7. Glazebrook, J. 2001. Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr. Opin. Plant Biol. 4:301-308.
8. Haas, D., and G. Défago. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3:307-319.
9. Handelsman, J., S. Raffel, E.H. Mester, L. Wunderlich, and C.R. Grau. 1990. Biological control of damping-off of alfalfa seedlings with Bacillus cereus UW85. Appl. Environ. Microbiol. 56:713-718.
10. Hara, H., and K. Ono. 1983. Ecological studies on the bacterial wilt of tobacco, caused by Pseudomonas solanacearum E. F. Smith. I. A selective medium for isolation and detection of P. solanacearum. Bull. Okayama Tob. Exp. Sta. 42:127-138.
11. Hoster, F., J.E. Schmitz, and R. Daniel. 2005. Enrichment of chitinolytic microorganisms: isolation and characterization of a chitinase exhibiting antifungal activity against phytopathogenic fungi from a novel Streptomyces strain. Appl. Microbiol. Biotech. 66:434-442.
12. Jetiyanon, K., W.D. Fowler, and J.W. Kloepper. 2003. Broadspectrum protection against several pathogens by PGPR mixtures under field conditions in Thailand. Plant Dis. 87:1390-1394.
13. Kloepper, J.W., D.J. Hume, F.M. Scher, et al. 1988. Plant growthpromoting Rhizobacteria on canola (rapeseed). Plant Dis. 72:42-46.
14. Kloepper, J.W., C.M. Ryu, and S. Zhang. 2004. Induce systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259-1266.
15. Liu, Y., A. Kanda, K. Yano, et al. 2009. Molecular typing of Japanese strains of Ralstonia solanacearum in relation to the ability to induce a hypersensitive reaction in tobacco. J. Gen. Plant Pathol. 75:369-380.
16. Manjula, K., and A.R. Podile. 2005. Production of fungal cell wall degrading enzymes by a biocontrol strain of Bacillus subtilis AF1. Indian J. Exp. Biol. 43:892-896.
17. Murphy, J.F., M.S. Reddy, C.-M. Ryu, J.W. Kloepper, and R. Li. 2003. Rhizobacteria-mediated growth promotion of tomato leads to protection against Cucumber mosaic virus. Phytopathology 93:1301-1307.
18. Nakaho, K. 1997. Distribution and multiplication of Ralstonia solanacearum (synonym Pseudomonas solanacearum) in tomato plants of resistant rootstock cultivar LS-89 and susceptible ponderosa. Ann. Phytopathol. Soc. Jpn. 63:83-88.
19. Nakaho, K. 1997. Distribution and multiplication of Ralstonia solanacearum in stem-inoculated tomato rootstock cultivar LS-89 resistant to bacterial wilt. Ann. Phytopathol. Soc. Jpn. 63:341-344.
20. Nakaho, K., H. Inoue, T. Takayama, and H. Miyagawa. 2004. Distribution and multiplication of Ralstonia solanacearum in tomato plants with resistance derived from different origins. J. Gen. Plant Pathol. 70:115-119.
21. Niki, T., I. Mitsuhara, S. Seo, N. Ohtsubo, and Y. Ohashi. 1998. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol. 39:500-507.
22. Pal, K.K., and B.M. Gardener. 2006. Biological control of plant pathogens. The Plant Health Instructor DOI: 10.1094/PHI-A-2006-1117-02
23. Pieterse, C.M.J., S.C.M. van Wees, J. Ton, J.A. van Pelt, and L.C. van Loon. 2002. Signalling in rhizobacteria-induced systemic resistance in Arabidopsis thaliana. Plant Biol. 4:535-544.
24. Pieterse, C.M.J., S.C.M. van Wees, J.A. van Pelt, M. Knoester, R. Laan, H. Gerrits, P.J. Weisbeek, and L.C. van Loon. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571-1580.
25. Ramamoorthy, V., R. Viswanathan, T. Raguchander, V. Prakasam, and R. Samiyappan. 2001. Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Protect. 20:1-11.
26. Raddadi, N., A. Belaouis, I. Tamagnini, B.M. Hansen, N.B. Hendriksen, A. Boudabous, A. Cherif, and D. Daffonchio. 2009. Characterization of polyvalent and safe Bacillus thuringiensis strains with potential use for biocontrol. J. Basic Microbiol. 49:293-303.
27. Reyes-Ramirez, A., B.I. Escudero-Abarca, G. Aguilar-Uscanga, P.M. Hayward-Jones, and J. Eleazar-Barbozacorona. 2004. Antifungal activity of Bacillus thuringiensis chitinase and its potential for the biocontrol of phytopathogenic fungi in soybean seeds. Food Microbiol. Safety 69:M131-M134.
28. Roh, J.Y., J. Choi, M.S. Li, B.R. Jin, and Y.H. Je. 2007. Bacillus thuringiensis as a specific, safe, and effective tool for insert pest control. J. Microbiol. Biotech. 17:547-559.
29. Ryu, C.M., C.H. Hu, M.S. Reddy, and J.W. Kloepper. 2003. Different signaling pathways of induced resistance by rhizobacteria in Arabidopsis thaliana against two pathovars of Pseudomonas syringae. New Phytol. 160:413-420.
30. Ryu, C.M., J.F. Murphy, K.S. Mysore, and J.W. Kloepper. 2004. Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. Plant J. 39:381-392.
31. Saile, E., J.A. McGarvey, M.A. Schell, and T.P. Denny. 1997. Role of extracellular polysaccharide and endoglucanase in root invasion and colonization of tomato plants by Ralstonia solanacearum. Phytopathology 87:1264-1271.
32. Sambrook, J., and D.W. Russell. 2001. Molecular Cloning. A Laboratory Manual. 3rd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
33. Schardl, C.L., A. Leutchmann, and M.J. Spiering. 2004. Symbioses of grasses with seedborne fungal endophytes. Annu. Rev. Plant Biol. 55:315-340.
34. Schnepf, E., N. Crickmore, D. van Rie Lereclus, J. Baum, J. Feitelson, D.R. Zeigler, and D.H. Dean. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62:775-806.
35. Silo-Suh, L.A., B.J. Lethbridge, S.J. Raffel, H. He, J. Clardy, and J. Handelsman. 1994. Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85. Appl. Environ. Microbiol. 60:2023-2030.
36. Stabb, E.V., L.M. Jacobson, and J. Handelsman. 1994. Zwittermycin A producing strains of Bacillus cereus from diverse soils. Appl. Environ. Microbiol. 60:4404-4412.
37. Stein, T. 2005. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Microbiol. 56:845-857.
38. Takahashi, H., and Y. Ehara. 1993. Severe chlorotic spot symptoms in cucumber mosaic virus strain Y-infected tobaccos are induced by a combination of the virus coat protein gene and two host recessive genes. Mol. Plant-Microbe Interact. 6:182-189.
39. Takahashi, H., Y. Kanayama, M.S. Zheng, T. Kusano, S. Hase, M. Ikegami, and J. Shah. 2004. Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to Cucumber mosaic virus. Plant Cell Physiol. 45:803-809.
40. Thomma, B.P.H.J., K. Eggermont, I.A.M.A. Penninckx, B. Mauch-Mani, R. Vogelsang, B.P.A. Cammue, and W.F. Broekaert. 1998. Separate jasmonate-dependent and salicylate-dependent defenseresponse pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. U.S.A. 95:15107-15111.
41. Ton, J., J.A. van Pelt, L.C. van Loon, and C.M.J. Pieterse. 2002. Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol. Plant- Microbe Interact. 15:27-34.
42. van Kan, J.A.L., M.H.A.J. Joosten, C.A.M. Wagemakers, G.C.M. van den Berg-Velthuis, and P.J.G.M. De Wit. 1992. Differential accumulation of mRNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladosporium fulvum. Plant Mol. Biol. 20:513-527.
43. van Loon, L.C., P.A.H.M. Bakker, and C.M.J. Pieterse. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453-485.
44. van Peer, R., G.J. Niemann, and B. Schippers. 1991. Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81:728-734.
45. Vasse, J., P. Frey, and A. Trigalet. 1995. Microscopic studies of intercellular infection and protoxylem invasion of tomato roots by Pseudomonas solanacearum. Mol. Plant Microbe Interact. 8:241-251.
46. Waller, F., B. Achatz, H. Baltruschat, et al. 2005. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. U.S.A. 102:13386-13391.
47. Walters, D., and T. Daniell. 2007. Microbial induction of resistance to pathogens, p. 143-156. In D. Walters, A. Newton and G. Lyon (ed.), Induced Resistance for Plant Defence. Blackwell Publishing, Oxford, UK.
48. Wei, G., J.W. Kloepper, and S. Tuzun. 1991. Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth-promoting rhizobacteria. Phytopathology 81:1508-1512.
49. Xu, Y., P.L.C. Chang, D. Liu, M.L. Narasimhan, G.R. Kashchandra, P.M. Hasegawa, and R.A. Bressan. 1994. Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6:1077-1085.
50. Zehnder, G.W., C. Yao, J.F. Murphy, E.J. Sikora, and J.W. Kloepper. 2000. Induction of resistance in tomato against cucumber mosaic cucumovirus by plant growth-promoting rhizobacteria. Biocontrol 45:127-137.
51. Zhang, S., M.S. Reddy, and J.W. Kloepper. 2002. Development of assays for assessing induced systemic resistance by plant growthpromoting rhizobacteria against blue mold of tobacco. Biol. Control 23:79-86.
52. Zhang, S., A.-L. Moyne, M.S. Reddy, and J.W. Kloepper. 2002. The role of salicylic acid in induced systemic resistance elicited by plant growth-promoting rhizobacteria against blue mold of tobacco. Biol. Control 25:288-296.
53. Zhang, S., M.S. Reddy, and J.W. Kloepper. 2004. Tobacco growth enhancement and blue mold disease protection by rhizobacteria: relationship between plant growth promotion and systemic disease protection by PGPR strain 90-166. Plant Soil 262:277-288.
54. Zhou, Y., Y.L. Choi, M. Sun, and Z. Yu. 2008. Novel roles of Bacillus thuringiensis to control plant diseases. Appl. Microbiol. Biotechnol. 80:563-572.