Skip to main content
Log in

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

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

Cfu:

Colony forming units

JA:

Jasmonic acid

MeSA:

Methyl salicylate

SA:

Salicylic acid

SAR:

Systemic acquired resistance

ISR:

Induced systemic response

spr2 :

Suppressor of prosystemin-mediated responses2

References

  • 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 55:178–186

    Article  CAS  Google Scholar 

  • Ahn IP, Lee SW, Suh SC (2007) Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPR1. Mol Plant Microbe Interact 20:759–768

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • 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 21:954–971

    Article  CAS  PubMed  Google Scholar 

  • 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 174:524–533

    Google Scholar 

  • Bhattarai KK, Li Q, Liu Y, Dinesh-Kumar SP, Kaloshian I (2007) The Mi-1-mediated pest resistance requires Hsp90 and Sgt11. Plant Physiol 144:312–323

    Article  CAS  PubMed  Google Scholar 

  • Brown JK, Czosnek H (2002) Whitefly transmission of plant viruses. Adv Bot Res 36:65–92

    Article  Google Scholar 

  • 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 21:244–259

    Article  CAS  PubMed  Google Scholar 

  • 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 177:175–180

    Article  Google Scholar 

  • Chen M-S (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15:101–114

    Article  Google Scholar 

  • 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 102:18771–18772

    Article  Google Scholar 

  • 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 21

  • Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant–pathogen interactions. Trends Plant Sci 7:210–216

    Article  CAS  PubMed  Google Scholar 

  • 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 19:1062–1071

    Article  CAS  PubMed  Google Scholar 

  • Czosnek H, Laterrot H (1997) A worldwide survey of tomato yellow leaf curl viruses. Arch Virol 142:1391–1406

    Article  CAS  PubMed  Google Scholar 

  • 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 43:284–298

    Article  CAS  PubMed  Google Scholar 

  • 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 277:33105–33114

    Article  CAS  PubMed  Google Scholar 

  • Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57:747–754

    Article  CAS  PubMed  Google Scholar 

  • 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 135:325–334

    Article  CAS  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    Article  CAS  PubMed  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868

    Article  CAS  PubMed  Google Scholar 

  • 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 137:44–60

    Article  Google Scholar 

  • Felton GW (2005) Indigestion is a plant’s best defense. Proc Natl Acad Sci USA 102:18771–18772

    Article  CAS  PubMed  Google Scholar 

  • Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824

    Article  CAS  PubMed  Google Scholar 

  • 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 220:447–454

    Article  CAS  PubMed  Google Scholar 

  • 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 10:591–600

    Article  CAS  PubMed  Google Scholar 

  • 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 315–322

  • 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 269:2414–2420

    Article  CAS  PubMed  Google Scholar 

  • 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 68:138–148

    Article  CAS  Google Scholar 

  • Hoelmer KA, Osborne LS, Yokomi RK (1991) Foliage disorders in Florida associated with feeding by sweetpotato whitefly, Bemisia tabaci. Florida Entomol 74:162–166

    Article  Google Scholar 

  • Howe GA (2004) Jasmonates as signals in the wound response. J Plant Growth Regul 23:223–237

    CAS  Google Scholar 

  • Howe GA, Ryan CA (1999) Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 153:1411–1421

    CAS  PubMed  Google Scholar 

  • Jiménez-Delgadillo MR (1999) Evaluación y caracterización fisiológica de rizobacterias empleadas como posibles agentes de biocontrol. MSc Dissertation. Cinvestav I.P.N. Unidad Irapuato, México

  • Jones DR (2003) Plant viruses transmitted by whiteflies. Eur J Plant Pathol 109:195–219

    Article  Google Scholar 

  • 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 122:67–74

    Article  PubMed  Google Scholar 

  • Kazan K, Manners JM (2008) Jasmonate signaling: toward an integrated view. Plant Physiol 146:1459–1468

    Article  CAS  PubMed  Google Scholar 

  • Kempema LA, Cui X, Holzer FM, Walling LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Plant Physiol 143:849–865

    Article  CAS  PubMed  Google Scholar 

  • Kloepper JW, Tuzun S, Ku J (1992) Proposed definitions related to induced disease resistance. Biocontrol Sci Technol 2:349–351

    Article  Google Scholar 

  • Kloepper JW, Ryu CM, Zhang SA (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    Article  CAS  PubMed  Google Scholar 

  • Koornneef A, Pieterse CMJ (2008) Cross-talk in defense signaling. Plant Physiol 146:839–844

    Article  CAS  PubMed  Google Scholar 

  • 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 147:1358–1368

    Article  CAS  PubMed  Google Scholar 

  • 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 85:1301–1305

    Article  Google Scholar 

  • 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 15:1646–1661

    Article  CAS  PubMed  Google Scholar 

  • 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 279:2101–2108

    Article  CAS  PubMed  Google Scholar 

  • 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 179–188

    Google Scholar 

  • Maynard DN, Cantliffe DJ (1989) Squash silverleaf and irregular ripening: new vegetable disorders in Florida. Fla Coop Ext Ser IFAS VC-37, pp 4

  • 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 97:1096–1105

    Article  CAS  PubMed  Google Scholar 

  • 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 347–351

  • 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 208:212–219

    Article  CAS  PubMed  Google Scholar 

  • 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 84:779–784

    Article  Google Scholar 

  • Nabity PD, Zavala JA, DeLucia EH (2008) Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Ann Bot 103:655–663

    Article  PubMed  Google Scholar 

  • 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 86:2697–2707

    Article  Google Scholar 

  • Oliveira MRV, Henneberry TJ, Anderson P (2001) History, current status and collaborative research projects for Bemisia tabaci. Crop Prot 20:709–723

    Article  Google Scholar 

  • 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 18:2–9

    Article  CAS  Google Scholar 

  • Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116

    Article  CAS  PubMed  Google Scholar 

  • Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: From molecular mechanisms to ecology. Trends Plant Sci 12:564–569

    Article  CAS  PubMed  Google Scholar 

  • 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 8:1225–1237

    Article  CAS  PubMed  Google Scholar 

  • 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 10:1571–1580

    Article  CAS  PubMed  Google Scholar 

  • 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 4:535–544

    Article  CAS  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Google Scholar 

  • 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 11:544–554

    Article  CAS  PubMed  Google Scholar 

  • Raudenbush SW, Bryk AS (2002) Hierarchical linear models: applications and data analysis methods, 2nd edn. Sage, Thousand Oaks

    Google Scholar 

  • Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404–411

    Article  CAS  PubMed  Google Scholar 

  • 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 16:616–628

    Article  CAS  PubMed  Google Scholar 

  • 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 29:546–557

    Article  PubMed  Google Scholar 

  • 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 49:565–577

    Article  CAS  PubMed  Google Scholar 

  • 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 130:1022–1031

    Article  CAS  PubMed  Google Scholar 

  • 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):S10

    Article  PubMed  Google Scholar 

  • 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 80:822

    Google Scholar 

  • 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 56:663–671

    Article  CAS  PubMed  Google Scholar 

  • Thompson GA, Goggin FL (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J Exp Bot 57:755–766

    Article  CAS  PubMed  Google Scholar 

  • Thompson AR, Vierstra RD (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 8:165–173

    Article  CAS  PubMed  Google Scholar 

  • 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 15:27–34

    Article  CAS  PubMed  Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121

    Article  CAS  PubMed  Google Scholar 

  • 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 12:1409–1423

    PubMed  Google Scholar 

  • 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 146:1293–1304

    Article  PubMed  Google Scholar 

  • 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 103:5602–5607

    Article  PubMed  Google Scholar 

  • Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    Article  PubMed  Google Scholar 

  • 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 21:919–930

    Article  PubMed  Google Scholar 

  • 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 81:728–733

    Article  Google Scholar 

  • 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 10:716–724

    Article  PubMed  Google Scholar 

  • 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 97:8711–8716

    Article  PubMed  Google Scholar 

  • 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 17:895–908

    Article  CAS  PubMed  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    CAS  PubMed  Google Scholar 

  • Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866

    Article  CAS  PubMed  Google Scholar 

  • Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875

    Article  CAS  PubMed  Google Scholar 

  • 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 90:391–396

    Google Scholar 

  • 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 83:81–85

    Article  Google Scholar 

  • 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 45:127–137

    Article  Google Scholar 

  • Zehnder GW, Murphy JF, Sikora EJ, Kloepper JW (2001) Application of rhizobacteria for induced resistance. Eur J Plant Pathol 107:39–50

    Article  Google Scholar 

  • 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 23:79–86

    Article  Google Scholar 

  • 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 25:288–296

    Article  Google Scholar 

  • 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 36:485–499

    Article  CAS  PubMed  Google Scholar 

  • 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 168:1157–1162

    Article  CAS  Google Scholar 

  • Zhu-Salzman K, Salzman RA, Ahn JE, Koiwa H (2004) Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol 134:420–431

    Article  CAS  PubMed  Google Scholar 

  • Zhu-Salzman K, Bi J-L, Liu T-X (2005) Molecular strategies of plant defence and insect counter-defence. Insect Sci 12:3–15

    CAS  Google Scholar 

  • Zonia LE, Stebbins NE, Polacco JC (1995) Essential role of urease in germination of nitrogen-limited Arabidopsis thaliana seeds. Plant Physiol 107:1097–1103

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John Paul Délano-Frier.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 265 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Valenzuela-Soto, J.H., Estrada-Hernández, M.G., Ibarra-Laclette, E. et al. Inoculation of tomato plants (Solanum lycopersicum) with growth-promoting Bacillus subtilis retards whitefly Bemisia tabaci development. Planta 231, 397–410 (2010). https://doi.org/10.1007/s00425-009-1061-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-009-1061-9

Keywords

Navigation