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Arsenal of elevated defense proteins fails to protect tomato against Verticillium dahliae

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Abstract

Although the hypersensitive reaction in foliar plant diseases has been extensively described, little is clear regarding plant defense strategies in vascular wilt diseases affecting numerous economically important crops and trees. We have examined global genetic responses to Verticillium wilt in tomato (Lycopersicon esculentum Mill.) plants differing in Ve1 resistance alleles. Unexpectedly, mRNA analyses in the susceptible plant (Ve1−) based on the microarrays revealed a very heroic but unsuccessful systemic response involving many known plant defense genes. In contrast, the response is surprisingly low in plants expressing the Ve1+ R-gene and successfully resisting the pathogen. Similarly, whole-cell protein analyses, based on 2D gel electrophoresis and mass spectrometry, demonstrate large systemic increases in a variety of known plant defense proteins in the stems of susceptible plants but only modest changes in the resistant plant. Taken together, the results indicate that the large systemic increases in plant defense proteins do not protect the susceptible plant. Indeed, since a number of the highly elevated proteins are known to participate in the plant hypersensitive response as well as natural senescence, the results suggest that some or all of the disease symptoms, including ultimate plant death, actually may be the result of this exaggerated plant response.

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Abbreviations

CS cv:

Craigella susceptible

CR cv:

Craigella resistant

d.p.i:

Days post-inoculation

HR:

Hypersensitive response

IPG:

Immobilized pH gradient isoelectric focusing

MALDI-MS:

Matrix-assisted laser desorption/ionization-mass spectrometry

MMLV:

Maloney murine leukemia virus

pAP3:

32P-labeled anionic potato peroxidase

PR:

Pathogenesis-related

R-gene:

Resistance-gene

SAR:

Systemic acquired resistance

SDS:

Sodium dodecylsulphate

TVR:

Tomato Verticillium response

Vd1:

Verticillium dahliae, race 1

References

  • Alba R, Fei Z, Payton P, Liu JM, Moore SL, Debbie P, Cohn J, D’Ascenzo M, Gordon JS, Rose JK, Martin G, Tanksley SD, Bouzayen M, Jahn M, Giovannoni J (2004) EST’s, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. Plant J 39:697–714

    Article  PubMed  CAS  Google Scholar 

  • Beckman CH (1987) The nature of wilt diseases of plants. APS Press, St. Paul, pp 36–64

    Google Scholar 

  • Bernards MA, Fleming WD, Llewellyn DB, Priefer R, Yang X, Sabatino A, Plourde GL (1999) Biochemical characterization of the suberization-associated anionic peroxidase gene of potato. Plant Physiol 121:135–146

    Article  PubMed  CAS  Google Scholar 

  • Bishop CD, Cooper RM (1983) An ultrastructural study of root invasion in three vascular wilt diseases. Physiol Plant Pathol 22:15–27

    Google Scholar 

  • Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2003) The molecular analysis of leaf senescence—a genomics approach. Plant Biotech J 1:3–22

    Article  CAS  Google Scholar 

  • Busch LV, Smith E (1981) Susceptibility of Ontario-grown alflafa cultivars and certain Medicago species to Verticillium albo-atrum. Can J Plant Pathol 3:169–172

    Article  Google Scholar 

  • Castroverde CDM, Nazar RN, Robb J (2010) Defence genes in tomato. In: Aube ED, Poole FM (eds) Tomatoes: agricultural practices, pathogen interactions and health effects. Nova Science Publishers Inc, Hauppauge, pp 1–40

    Google Scholar 

  • Chen P, Lee B, Robb J (2004) Tolerance to a non-host isolate of Verticillium dahliae in tomato. Physiol Mol Plant Pathol 64:283–291

    Article  CAS  Google Scholar 

  • Dobinson KF, Tenuta GK, Lazarovits G (1996) Occurrence of race 2 of Verticillium dahliae in processing fields in southwestern Ontario. Can J Plant Pathol 18:55–58

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296

    Article  Google Scholar 

  • Fradin EF, Thomma BP (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Pathol 7:71–86

    Article  PubMed  CAS  Google Scholar 

  • Fradin EF, Zhang Z, Juarez-Ayala Castroverde CDM, Nazar RN, Robb J, Liu C-M, Thomma BPHJ (2009) Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol 150:320–332

    Article  PubMed  CAS  Google Scholar 

  • Gayoso C, Pomar F, Novo-Uzal E, Merino F, de Ilárduya OM (2010) The Ve-mediated resistance response of the tomato to Verticillium dahliae involves H2O2, peroxidase and lignins and drives PAL gene expression. BMC Plant Biol 10:232–250

    Article  PubMed  Google Scholar 

  • Gold J, Robb J (1995) The role of the coating response in Craigella tomatoes infected with Verticillium dahliae, races 1 and 2. Physiol Mol Plant Pathol 47:141–157

    Article  Google Scholar 

  • Hu X, Nazar RN, Robb J (1993) Quantification of Verticillium biomass in wilt disease development. Physiol Mol Plant Pathol 42:23–36

    Article  CAS  Google Scholar 

  • Hurkman WJ, Tanaka CK (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 81:802–806

    Article  PubMed  CAS  Google Scholar 

  • Kawchuk L, Hachey J, Lynch DR, Klcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R, Prufer D (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci USA 98:6511–6515

    Article  PubMed  CAS  Google Scholar 

  • Lam E (2004) Controlled cell death, plant survival and development. Nat Rev/Mol Cell Biol 5:305–315

    Article  CAS  Google Scholar 

  • Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848–853

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Cheung AY (2004) Cell death in plant development and defense. In: Lockshin RA, Zakeri Z (eds) When cells die II: a comprehensive evaluation of apoptosis and programmed cell death. Wiley, Hoboken, pp 99–122

    Chapter  Google Scholar 

  • Pegg GF (1981) Biochemistry and physiology of pathogenesis. In: Mace ME, Bell AA, Beckman CH (eds) Fungal wilt diseases of plants. Academic Press Inc, USA

    Google Scholar 

  • Pegg GF, Brady BL (2002) Verticillium wilts, 1st edn. CABI Publishing, Wallingford, pp 193–253

    Book  Google Scholar 

  • Pegg GF, Street PFS (1984) Measurement of Verticillium albo-atrum in high and low resistance hop cultivars. Trans British Mycol Soc 82:99–106

    Article  Google Scholar 

  • Powelson ML, Rowe RC (1993) Biology and management of early dying of potatoes. Annu Rev Phytopathol 31:111–126

    Article  PubMed  CAS  Google Scholar 

  • Quirino BF, Noh Y-S, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282

    Article  PubMed  CAS  Google Scholar 

  • Robb J, Busch LV (1983) Structure and significance of “blocked” veins in Verticillium-infected chrysanthemum. Physiol Plant Pathol 23:35–53

    Article  Google Scholar 

  • Robb EJ, Nazar RN (1996) Factors contributing to successful PCR-based diagnostics for potato and other crops. In: Marshall G (ed) Diagnostics in crop production. British Crop Protection Council, Surrey, pp 75–84

    Google Scholar 

  • Robb EJ, Street PFS, Busch LV (1983) Basic fuchsin: a vascular dye in studies of Verticillium-infected chrysanthemum and tomato. Can J Bot 61:3355–3365

    Article  Google Scholar 

  • Robb EJ, Powell DA, Street PFS (1989) Vascular coating: a barrier to colonization by the pathogen in Verticillium wilt of tomato. Can J Bot 67:600–607

    Article  Google Scholar 

  • Robb EJ, Lee S-W, Mohan R, Kolattukudy PE (1991) Chemical characterization of stress-induced vascular coating in tomato. Plant Physiol 97:528–536

    Article  PubMed  CAS  Google Scholar 

  • Robb J, Castroverde CDM, Shittu HO, Nazar RN (2009) Patterns of defence gene expression in the tomato-Verticillium interaction. Botany 87:993–1006

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Savoie CJ, Aburatani S, Watanabe S, Eguchi Y, Muta S, Imoto S, Miyano S, Kuhara S, Tashiro K (2003) Use of gene networks from full genome microarray libraries to identify functionally relevant drug-affected genes and gene regulation cascades. DNA Res 10:19–25

    Article  PubMed  CAS  Google Scholar 

  • Schaible L, Cannon OS, Waddoups V (1951) Inheritance of resistance to Verticillium wilt in a tomato cross. Phytopathol 41:986–990

    Google Scholar 

  • Shittu HO, Castroverde CDM, Nazar RN, Robb J (2009) Plant-endophyte interplay protects tomato against a virulent Verticillium. Planta 229:415–426

    Article  PubMed  CAS  Google Scholar 

  • Straub C, Pazdrak K, Young TW, Stafford SJ, Wu Z, Je Wiktorowiczm, Haag AM, English RD, Soman KV, Kurosky A (2009) Toward the proteome of the human peripheral blood eosinophil. Proteomics Clin Appl 3:1151–1173

    Article  PubMed  CAS  Google Scholar 

  • Street PFS, Robb J, Ellis BE (1986) Secretion of vascular coating components by xylem parenchyma cells of tomatoes infected with Verticillium albo-atrum. Protoplasma 132:1–11

    Article  Google Scholar 

  • Tabaeizadeh Z, Agharbaoui Z, Harrak H, Poysa V (1999) Transgenic tomato plants expressing a Lycopersicon chilense chitinase gene demonstrate improved resistance to Verticillium dahliae race 2. Plant Cell Rep 19:197–202

    Article  CAS  Google Scholar 

  • Thomma BP, Nürnberger T, Joosten MH (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15

    Article  PubMed  CAS  Google Scholar 

  • Van Esse HP, Fradin EF, de Groot PJ, de Wit PJ, Thomma BP (2009) Tomato transcriptional responses to a foliar and a vascular fungal pathogen are distinct. Mol Plant Microbe Interact 22:245–258

    Article  PubMed  Google Scholar 

  • Van Loon LC (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  Google Scholar 

  • Van Ooijin G, Van der Burg HA, Cornelissen BJC, Takken FLW (2007) Structure and function of resistance proteins in solanaceous plants. Annu Rev Phytopathol 45:43–72

    Article  Google Scholar 

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Acknowledgments

Supported by NSERC, Canada (R.N.N. and J.R.), NIH, NHLBI (A.K.) and a Canadian Commonwealth Scholarship (H.O.S.).

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Authors and Affiliations

  1. Department of Molecular and Cellular Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Jane Robb, Hakeem Shittu & Ross N. Nazar

  2. Department of Biochemistry and Molecular Biology, University of Texas Medical Branch, Galveston, TX, 77555, USA

    Kizhake V. Soman & Alexander Kurosky

Authors
  1. Jane Robb
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  2. Hakeem Shittu
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  3. Kizhake V. Soman
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  4. Alexander Kurosky
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  5. Ross N. Nazar
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Correspondence to Ross N. Nazar.

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Robb, J., Shittu, H., Soman, K.V. et al. Arsenal of elevated defense proteins fails to protect tomato against Verticillium dahliae . Planta 236, 623–633 (2012). https://doi.org/10.1007/s00425-012-1637-7

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