, 231:397 | Cite as

Inoculation of tomato plants (Solanum lycopersicum) with growth-promoting Bacillus subtilis retards whitefly Bemisia tabaci development

  • José Humberto Valenzuela-Soto
  • María Gloria Estrada-Hernández
  • Enrique Ibarra-Laclette
  • John Paul Délano-Frier
Original Article


Root inoculation of tomato (Solanum lycopersicum) plants with a Bacillus subtilis strain BEB-DN (BsDN) isolated from the rhizosphere of cultivated potato plants was able to promote growth and to generate an induced systemic resistance (ISR) response against virus-free Bemisia tabaci. Growth promotion was evident 3 weeks after inoculation. No changes in oviposition density, preference and nymphal number in the early stages of B. tabaci development were observed between BsDN-treated plants and control plants inoculated with a non-growth promoting Bs strain (PY-79), growth medium or water. However, a long-term ISR response was manifested by a significantly reduced number of B. tabaci  pupae developing into adults in BsDN-treated plants. The observed resistance response appeared to be a combination of jasmonic acid (JA) dependent and JA-independent responses, since the BsDN-related retardation effect on B. tabaci development was still effective in the highly susceptible spr2 tomato mutants with an impaired capacity for JA biosynthesis. A screening of 244 genes, 169 of which were previously obtained from subtractive-suppressive-hybridization libraries generated from B. tabaci-infested plants suggested that the BsDN JA-dependent ISR depended on an anti-nutritive effect produced by the simultaneous expression of genes coding principally for proteases and proteinase inhibitors, whereas the JA-independent ISR observed in the spr2 background curiously involved the up-regulation of several photosynthetic genes, key components of the phenyl-propanoid and terpenoid biosynthetic pathways and of the Hsp90 chaperonin, which probably mediated pest resistance response(s), in addition to the down-regulation of pathogenesis and hypersensitive response genes.


Bacillus subtilis Bemisia tabaci Growth promoting rhizobacteria Induced systemic response Jasmonic acid Phenyl propanoids Salicylic acid 



Colony forming units


Jasmonic acid


Methyl salicylate


Salicylic acid


Systemic acquired resistance


Induced systemic response


Suppressor of prosystemin-mediated responses2



This work was supported by two postgraduate scholarships (165105, to MGEH and 182416, to JHVS) granted by The National Council for Science and Technology (CONACyT, México). We are grateful to Dr. Víctor Olalde Portugal for the provision of the BsDN PGPR.

Supplementary material

425_2009_1061_MOESM1_ESM.doc (265 kb)
Supplementary material 1 (DOC 265 kb)


  1. Achuo EA, Prinsen E, Höfte M (2006) Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinerea and Oidium neolycopersici. Plant Pathol 55:178–186CrossRefGoogle Scholar
  2. Ahn IP, Lee SW, Suh SC (2007) Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPR1. Mol Plant Microbe Interact 20:759–768CrossRefPubMedGoogle Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  4. Attaran E, Zeier TE, Griebel T, Zeier J (2009) Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21:954–971CrossRefPubMedGoogle Scholar
  5. Bellés JM, López-Gresa MP, Fayos J, Pallás V, Rodrigo I, Conejero V (2008) Induction of cinnamate 4-hydroxylase and phenylpropanoids in virus-infected cucumber and melon plants. Plant Sci 174:524–533Google Scholar
  6. Bhattarai KK, Li Q, Liu Y, Dinesh-Kumar SP, Kaloshian I (2007) The Mi-1-mediated pest resistance requires Hsp90 and Sgt11. Plant Physiol 144:312–323CrossRefPubMedGoogle Scholar
  7. Brown JK, Czosnek H (2002) Whitefly transmission of plant viruses. Adv Bot Res 36:65–92CrossRefGoogle Scholar
  8. Cartieaux F, Contesto C, Gallou A, Desbrosses G, Kopka J, Taconnat L, Renou JP, Touraine B (2008) Simultaneous interaction of Arabidopsis thaliana with Bradyrhizobium Sp. Strain ORS278 and Pseudomonas syringae pv. tomato DC3000 leads to complex transcriptome changes. Mol Plant Microbe Interact 21:244–259CrossRefPubMedGoogle Scholar
  9. Chacón O, Hernández I, Portieles R, López Y, Pujol M, Borrás-Hidalgo O (2009) Identification of defense-related genes in tobacco responding to black shank disease. Plant Sci 177:175–180CrossRefGoogle Scholar
  10. Chen M-S (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15:101–114CrossRefGoogle Scholar
  11. Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci USA 102:18771–18772CrossRefGoogle Scholar
  12. Cock MJN (1986) Bemisia tabaci—a literature survey on the cotton whitefly with an annotated bibliography. FAO/CAB International Institute of Biological Control, Ascot, UK, pp 21Google Scholar
  13. Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant–pathogen interactions. Trends Plant Sci 7:210–216CrossRefPubMedGoogle Scholar
  14. Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman M-A, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne W, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071CrossRefPubMedGoogle Scholar
  15. Czosnek H, Laterrot H (1997) A worldwide survey of tomato yellow leaf curl viruses. Arch Virol 142:1391–1406CrossRefPubMedGoogle Scholar
  16. de la Fuente van Bentem S, Vossen JH, de Vries KJ, van Wees S, Tameling WIL, Dekker HL, de Koster CG, Haring MA, Takken FLW, Cornelissen BJC (2005) Heat shock protein 90 and its co-chaperone protein phosphatase 5 interact with distinct regions of the tomato I-2 disease resistance protein. Plant J 43:284–298CrossRefPubMedGoogle Scholar
  17. Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD (2002) The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J Biol Chem 277:33105–33114CrossRefPubMedGoogle Scholar
  18. Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57:747–754CrossRefPubMedGoogle Scholar
  19. Duijff BJ, Gianinazzi-Pearson V, Lemanceau P (1997) Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol 135:325–334CrossRefGoogle Scholar
  20. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209CrossRefPubMedGoogle Scholar
  21. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868CrossRefPubMedGoogle Scholar
  22. Estrada-Hernández MG, Valenzuela-Soto JH, Ibarra-Laclette E, Délano-Frier JP (2009) Differential gene expression in whitefly Bemisia tabaci-infested tomato (Solanum lycopersicum) plants at progressing developmental stages of the insect’s life cycle. Physiol Plant 137:44–60CrossRefGoogle Scholar
  23. Felton GW (2005) Indigestion is a plant’s best defense. Proc Natl Acad Sci USA 102:18771–18772CrossRefPubMedGoogle Scholar
  24. Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824CrossRefPubMedGoogle Scholar
  25. Germain H, Chevalier E, Caron S, Matton DP (2005) Characterization of five RALF-like genes from Solanum chacoense provides support for a developmental role in plants. Planta 220:447–454CrossRefPubMedGoogle Scholar
  26. Gopalan S, Wei W, He SY (1996) hrp gene-dependent induction of hin 1: a plant gene activated rapidly by both harpins and the avrPto gene-mediated signal. Plant J 10:591–600CrossRefPubMedGoogle Scholar
  27. Hanafi A, Traoré M, Schnitzler WH, Woitke M (2007) Induced resistance of tomato to whiteflies and Phytium with the PGPR Bacillus subtilis in a soilless crop grown under greenhouse conditions. In: Hanafi A, Schnitzler WH (eds) Proceedings of VIIIth IS on protected cultivation in mild winter climates. Acta horticulturae, vol 747, pp 315–322Google Scholar
  28. Herbette S, Lenne C, Leblanc N, Julien J-L, Drevet JR, Roeckel-Drevet P (2002) Two GPX-like proteins from Lycopersicon esculentum and Helianthus annuus are antioxidant enzymes with phospholipid hydroperoxide glutathione peroxidase and thioredoxin peroxidase activities. Eur J Biochem 269:2414–2420CrossRefPubMedGoogle Scholar
  29. Hermosa MR, Turra D, Foglianoc V, Montea E, Lorito M (2006) Identification and characterization of potato protease inhibitors able to inhibit pathogenicity and growth of Botrytis cinerea. Physiol Mol Plant Pathol 68:138–148CrossRefGoogle Scholar
  30. Hoelmer KA, Osborne LS, Yokomi RK (1991) Foliage disorders in Florida associated with feeding by sweetpotato whitefly, Bemisia tabaci. Florida Entomol 74:162–166CrossRefGoogle Scholar
  31. Howe GA (2004) Jasmonates as signals in the wound response. J Plant Growth Regul 23:223–237Google Scholar
  32. Howe GA, Ryan CA (1999) Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 153:1411–1421PubMedGoogle Scholar
  33. Jiménez-Delgadillo MR (1999) Evaluación y caracterización fisiológica de rizobacterias empleadas como posibles agentes de biocontrol. MSc Dissertation. Cinvestav I.P.N. Unidad Irapuato, MéxicoGoogle Scholar
  34. Jones DR (2003) Plant viruses transmitted by whiteflies. Eur J Plant Pathol 109:195–219CrossRefGoogle Scholar
  35. Jordá L, Conejero V, Vera P (2000) Characterization of two differentially regulated genes (P69E and P69F) encoding new members of the subtilisin-like protease clan from tomato plants. Plant Physiol 122:67–74CrossRefPubMedGoogle Scholar
  36. Kazan K, Manners JM (2008) Jasmonate signaling: toward an integrated view. Plant Physiol 146:1459–1468CrossRefPubMedGoogle Scholar
  37. Kempema LA, Cui X, Holzer FM, Walling LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Plant Physiol 143:849–865CrossRefPubMedGoogle Scholar
  38. Kloepper JW, Tuzun S, Ku J (1992) Proposed definitions related to induced disease resistance. Biocontrol Sci Technol 2:349–351CrossRefGoogle Scholar
  39. Kloepper JW, Ryu CM, Zhang SA (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266CrossRefPubMedGoogle Scholar
  40. Koornneef A, Pieterse CMJ (2008) Cross-talk in defense signaling. Plant Physiol 146:839–844CrossRefPubMedGoogle Scholar
  41. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CMJ (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147:1358–1368CrossRefPubMedGoogle Scholar
  42. Leeman M, Van Pelt JA, Hendrickx MJ, Scheffer RJ, Bakker PAHM, Schippers B (1995) Biocontrol of fusarium wilt of radish in commercial greenhouse trials by seed treatment with Pseudomonas fluorescens WCS374. Phytopathology 85:1301–1305CrossRefGoogle Scholar
  43. Li C, Liu G, Xu C, Lee GI, Bauer P, Ling H-Q, Ganal MW, Howe GA (2003) The tomato suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell 15:1646–1661CrossRefPubMedGoogle Scholar
  44. Liu Y, Burch-Smith T, Schiff M, Feng S, Dinesh-Kumar SP (2004) Molecular chaperone Hsp90 associates with resistance protein n and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J Biol Chem 279:2101–2108CrossRefPubMedGoogle Scholar
  45. Mayer RT, McCollum TG, McDonald RE, Polston JE, Doostdar H (1995) Bemisia feeding induces pathogenesis-related proteins in tomato. In: Gerling D, Mayer RT (eds) Bemisia: 1995. Taxonomy, biology, damage, control and management, Andover Intercept Ltd., pp 179–188Google Scholar
  46. Maynard DN, Cantliffe DJ (1989) Squash silverleaf and irregular ripening: new vegetable disorders in Florida. Fla Coop Ext Ser IFAS VC-37, pp 4Google Scholar
  47. McAuslane HJ, Cheng J, Carle RB, Schmalstig J (2004) Influence of Bemisia argentifolii (Homoptera: Aleyrodidae) infestation and squash silver leaf disorder on zucchini seedling growth. J Econ Entomol 97:1096–1105CrossRefPubMedGoogle Scholar
  48. McKenzie CL, Sisisterra XH, Powell CA, Bausher M, Albano JP, Shatters RG Jr (2005) Deciphering changes in plant physiological response to whitefly feeding using microarray technology. In: Momol MT, Ji P, Jones JB (eds) Proceedings of the first international symposium on tomato diseases. Acta Horticulturae vol 695, pp 347–351Google Scholar
  49. Merkouropoulos G, Barnett DC, Shirsat AH (1999) The Arabidopsis extensin gene is developmentally regulated, is induced by wounding, methyl jasmonate abscisic and salicylic acid, and codes for a protein with unusual motifs. Planta 208:212–219CrossRefPubMedGoogle Scholar
  50. Murphy JF, Zehnder GW, Shuster DJ, Sikora EJ, Polston EJ, Kloepper JW (2000) Plant growth-promoting rhizobacterial mediated protection in tomato against tomato mottle virus. Plant Dis 84:779–784CrossRefGoogle Scholar
  51. Nabity PD, Zavala JA, DeLucia EH (2008) Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Ann Bot 103:655–663CrossRefPubMedGoogle Scholar
  52. Ng JCK, Tian T, Falk BW (2004) Quantitative parameters determining whitefly (Bemisia tabaci) transmission of lettuce infectious yellows virus and an engineered defective RNA. J Gen Virol 86:2697–2707CrossRefGoogle Scholar
  53. Oliveira MRV, Henneberry TJ, Anderson P (2001) History, current status and collaborative research projects for Bemisia tabaci. Crop Prot 20:709–723CrossRefGoogle Scholar
  54. Park KS, Kloepper JW (2000) Activation of PR-1a promoter by rhizobacteria that induce systemic resistance in tobacco against Pseudomonas syringae pv. tabaci. Biol Control 18:2–9CrossRefGoogle Scholar
  55. Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116CrossRefPubMedGoogle Scholar
  56. Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: From molecular mechanisms to ecology. Trends Plant Sci 12:564–569CrossRefPubMedGoogle Scholar
  57. Pieterse CMJ, Van Wees SCM, Hoffland E, Van Pelt JA, Van Loon LC (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225–1237CrossRefPubMedGoogle Scholar
  58. Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, Van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580CrossRefPubMedGoogle Scholar
  59. Pieterse CMJ, Van Wees SCM, Ton J, Van Pelt JA, Van Loon LC (2002) Signalling in rhizobacteria-induced systemic resistance in Arabidopsis thaliana. Plant Biol 4:535–544CrossRefGoogle Scholar
  60. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New YorkGoogle Scholar
  61. Pontier D, Tronchet M, Rogowsky P, Lam E, Roby D (1998) Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death. Mol Plant Microbe Interact 11:544–554CrossRefPubMedGoogle Scholar
  62. Raudenbush SW, Bryk AS (2002) Hierarchical linear models: applications and data analysis methods, 2nd edn. Sage, Thousand OaksGoogle Scholar
  63. Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404–411CrossRefPubMedGoogle Scholar
  64. Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R (2004) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell 16:616–628CrossRefPubMedGoogle Scholar
  65. Sánchez-Hernández C, López MG, Délano-Frier JP (2006) Reduced levels of volatile emissions in jasmonate-deficient spr2 tomato mutants favour oviposition by insect herbivores. Plant Cell Environ 29:546–557CrossRefPubMedGoogle Scholar
  66. Sato M, Mitra RM, Coller J, Wang D, Spivey NW, Dewdney J, Denoux C, Glazebrook J, Katagiri F (2007) A high-performance, small-scale microarray for expression profiling of many samples in Arabidopsis-pathogen studies. Plant J 49:565–577CrossRefPubMedGoogle Scholar
  67. Schoch GA, Nikov GN, Alworth WL, Werck-Reichhart D (2002) Chemical inactivation of the cinnamate 4-hydroxylase allows for the accumulation of salicylic acid in elicited cells. Plant Physiol 130:1022–1031CrossRefPubMedGoogle Scholar
  68. Shi L, Jones WD, Jensen RV, Harris SC, Perkins RG, Goodsaid FM, Guo L, Croner LJ, Boysen C, Fang H, Qian F, Amur S, Bao W, Barbacioru CC, Bertholet V, Cao XM, Chu T-M, Collins PJ, Fan X-H, Frueh FW, Fuscoe JC, Guo X, Han J, Herman D, Hong H, Kawasaki ES, Li Q-Z, Luo Y, Ma Y, Mei N, Peterson RL, Puri RK, Shippy R, Su Z, Sun YA, Sun H, Thorn B, Turpaz Y, Wang C, Wang SJ, Warrington JA, Willey JC, Wu J, Xie Q, Zhang L, Zhang L, Zhong S, Wolfinger RD, Tong W (2008) The balance of reproducibility, sensitivity, and specificity of lists of differentially expressed genes in microarray studies. BMC Bioinformatics 9(Suppl 9):S10CrossRefPubMedGoogle Scholar
  69. Summers CG, Estrada D (1996) Chlorotic streak of bell pepper: a new toxicogenic disorder induced by feeding of the silverleaf whitefly, Bemisia argentifolii. Plant Dis 80:822Google Scholar
  70. Teixeira J, Pereira S, Cánovas F, Salema R (2005) Glutamine synthetase of potato (Solanum tuberosum L. cv. Désirée) plants: cell- and organ-specific expression and differential developmental regulation reveal specific roles in nitrogen assimilation and mobilization. J Exp Bot 56:663–671CrossRefPubMedGoogle Scholar
  71. Thompson GA, Goggin FL (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J Exp Bot 57:755–766CrossRefPubMedGoogle Scholar
  72. Thompson AR, Vierstra RD (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 8:165–173CrossRefPubMedGoogle Scholar
  73. Ton J, Van Pelt JA, Van Loon LC, Pieterse CMJ (2002) Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol Plant Microbe Interact 15:27–34CrossRefPubMedGoogle Scholar
  74. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121CrossRefPubMedGoogle Scholar
  75. van de Ven WTG, LeVesque CS, Perring TM, Walling LL (2000) Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. Plant Cell 12:1409–1423PubMedGoogle Scholar
  76. Van der Ent S, Verhagen BWM, Van Doorn R, Bakker D, Verlaan MG, Pel MJC, Joosten RG, Proveniers MCG, Van Loon LC, Ton J, Pieterse CMJ (2008) MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 146:1293–1304CrossRefPubMedGoogle Scholar
  77. Van Hulten M, Pelser M, van Loon LC, Pieterse CMJ, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci USA 103:5602–5607CrossRefPubMedGoogle Scholar
  78. Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483CrossRefPubMedGoogle Scholar
  79. Van Oosten VR, Bodenhausen N, Reymond P, Van Pelt JA, Van Loon LC, Dicke M, Pieterse CMJ (2008) Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Mol Plant Microbe Interact 21:919–930CrossRefPubMedGoogle Scholar
  80. Van Peer R, Niemann GJ, Schippers B (1991) Induced resistance and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81:728–733CrossRefGoogle Scholar
  81. Van Wees SCM, Pieterse CMJ, Trijssenaar A, Van’t Westende YAM, Hartog F, Van Loon LC (1997) Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol Plant Microbe Interact 10:716–724CrossRefPubMedGoogle Scholar
  82. van Wees SCM, de Swart EAM, van Pelt JA, van Loon LC, Pieterse CMJ (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:8711–8716CrossRefPubMedGoogle Scholar
  83. Verhagen BWM, Glazebrook J, Zhu T, Chang H-S, Van Loon LC, Pieterse CMJ (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol Plant Microbe Interact 17:895–908CrossRefPubMedGoogle Scholar
  84. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216PubMedGoogle Scholar
  85. Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866CrossRefPubMedGoogle Scholar
  86. Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875CrossRefPubMedGoogle Scholar
  87. Zehnder G, Kloepper JW, Yao C, Wei G (1997a) Induction of systemic resistance in cucumber against cucumber beetles (Coleoptera: Chrysomelidae) by plant growth-promoting rhizobacteria. Biol Microb Control 90:391–396Google Scholar
  88. Zehnder G, Kloepper JW, Tuzun S, Yao C, Wei G, Chambliss O, Shelby R (1997b) Insect feeding on cucumber mediated by rhizobacteria-induced plant resistance. Entomol Exp Appl 83:81–85CrossRefGoogle Scholar
  89. Zehnder GW, Yao C, Murphy JF, Sikora EJ, Kloepper JW (2000) Induction of resistance in tomato against cucumber mosaic cucumovirus by plant growth-promoting rhizobacteria. Biocontrol 45:127–137CrossRefGoogle Scholar
  90. Zehnder GW, Murphy JF, Sikora EJ, Kloepper JW (2001) Application of rhizobacteria for induced resistance. Eur J Plant Pathol 107:39–50CrossRefGoogle Scholar
  91. Zhang S, Reddy MS, Kloepper JW (2002a) Development of assays for assessing induced systemic resistance by plant growth-promoting rhizobacteria against blue mold of tobacco. Biol Control 23:79–86CrossRefGoogle Scholar
  92. Zhang S, Moyne AL, Reddy MS, Kloepper JW (2002b) The role of salicylic acid in induced systemic resistance elicited by plant growth-promoting rhizobacteria against blue mold of tobacco. Biol Control 25:288–296CrossRefGoogle Scholar
  93. Zhao Y, Thilmony R, Bender CL, Schaller A, He SY, Howe GA (2003) Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36:485–499CrossRefPubMedGoogle Scholar
  94. Zhao H, Lu J, Lu S, Zhou Y, Wei J, Song Y, Wang T (2005) Isolation and functional characterization of a cinnamate 4-hydroxylase promoter from Populus tomentosa. Plant Sci 168:1157–1162CrossRefGoogle Scholar
  95. Zhu-Salzman K, Salzman RA, Ahn JE, Koiwa H (2004) Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol 134:420–431CrossRefPubMedGoogle Scholar
  96. Zhu-Salzman K, Bi J-L, Liu T-X (2005) Molecular strategies of plant defence and insect counter-defence. Insect Sci 12:3–15Google Scholar
  97. Zonia LE, Stebbins NE, Polacco JC (1995) Essential role of urease in germination of nitrogen-limited Arabidopsis thaliana seeds. Plant Physiol 107:1097–1103CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • José Humberto Valenzuela-Soto
    • 1
  • María Gloria Estrada-Hernández
    • 1
  • Enrique Ibarra-Laclette
    • 1
  • John Paul Délano-Frier
    • 1
  1. 1.Unidad de Biotecnología e Ingeniería Genética de Plantas, Cinvestav - IrapuatoIrapuatoMexico

Personalised recommendations