Abstract
The Rpv3 locus determines the ability to operate an isolate-specific hypersensitive response (HR) against Plasmopara viticola in grapevines that carry a resistant Rpv3 + haplotype. Artificial infection was performed on leaf discs of Rpv3 + and Rpv3 − grapevines with two distinct isolates of the pathogen (avrRpv3 + and avrRpv3 −). The plant response, including the establishment of HR and changes in expression of 33 genes, was compared to the development of the pathogen. HR was induced exclusively in the Rpv3 + host upon inoculation with the avrRpv3 + isolate of the pathogen, which is assumed to use avrRpv3 + effectors that are recognised by/through the plant Rpv3 + gene product. The limitation imposed on pathogen growth was the result of inducible responses elicited by the Rpv3 +–avrRpv3 + interaction. This host reaction relied on transcriptional induction of the HR-associated gene HSR1 and salicylic acid-induced pathogenesis-related (PR) genes PR-1 and PR-2 during the initial 24–48 h post-inoculation. These events had no parallel in the Rpv3 − host or upon infection with the avrRpv3 − isolate. The emerging model for Rpv3-mediated defence, which is dependent upon race-specific recognition, associated with up-regulation of PR-1 and PR-2 genes, and enforced by localised HR-type necrosis, is compatible with the cascade of events initiated by the products of NB-LRR and LRR-kinase receptor-like genes, such as those residing in the Rpv3 locus.
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Abbreviations
- DM:
-
Downy mildew
- ET:
-
Ethylene
- hpi:
-
Hours post-inoculation
- qPCR:
-
Quantitative PCR
- JA:
-
Jasmonic acid
- JA-Ile:
-
Jasmonoyl-iso-leucine
- MeJA:
-
Methyl-jasmonate
- PR:
-
Pathogenesis related
- R:
-
Resistance
- SA:
-
Salicylic acid
References
Bellin D, Peressotti E, Merdinoglu D, Wiedemann-Merdinoglu S, Adam-Blondon AF, Cipriani G, Morgante M, Testolin R, Di Gaspero G (2009) Resistance to Plasmopara viticola in grapevine ‘Bianca’ is controlled by a major dominant gene causing localised necrosis at the infection site. Theor Appl Genet 120:163–176
Cadle-Davidson L (2008) Variation within and between Vitis spp. for foliar resistance to the downy mildew pathogen Plasmopara viticola. Plant Dis 92:1577–1584
Chong J, Le Henanff G, Bertsch C, Walter B (2007) Identification, expression analysis and characterization of defense and signaling genes in Vitis vinifera. Plant Physiol Biochem 46:469–481
Cséfalvay L, Di Gaspero G, Matouš K, Bellin D, Ruperti B, Olejníčková J (2009) Pre-symptomatic detection of Plasmopara viticola infection in grapevine leaves using chlorophyll fluorescence imaging. Eur J Plant Pathol 125:291–302
Dai GH, Andary C, Mondolot-Cosson L, Boubals D (1995) Histochemical studies on the interaction between three species of grapevine, Vitis vinifera, V. rupestris and V. rotundifolia and the downy mildew fungus, Plasmopara viticola. Physiol Mol Plant Pathol 46:177–188
Deglène-Benbrahim L, Wiedemann-Merdinoglu S, Merdinoglu D, Walter B (2010) Evaluation of downy mildew resistance in grapevine by leaf dics bioassay with in vitro- and greenhouse-grown plants. Am J Enol Vitic 61:521–528
Di Gaspero G, Copetti D, Coleman C, Castellarin SD, Eibach R, Kozma P, Lacombe T, Gambetta G, Zvyagin A, Cindrić P, Kovács L, Morgante M, Testolin R (2011) Selective sweep at the Rpv3 locus during grapevine breeding for downy mildew resistance. Theor Appl Genet (submitted)
Díez-Navajas AM, Wiedemann-Merdinoglu S, Greif C, Merdinoglu D (2008) Nonhost versus host resistance to the grapevine downy mildew, Plasmopara viticola, studied at the tissue level. Phytopathology 98:776–780
Falk A, Feys BJ, Frost LN, Jones JD, Daniels MJ, Parker JE (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc Natl Acad Sci USA 96:3292–3297
Feys BJ, Moisan LJ, Newman MA, Parker JE (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J 20:5400–5411
Gao F, Shu X, Ali MB, Howard S, Li N, Winterhagen P, Qiu W, Gassmann W (2010) A functional EDS1 ortholog is differentially regulated in powdery mildew resistant and susceptible grapevines and complements an Arabidopsis eds1 mutant. Planta 231:1037–1047
Hu G, deHart AK, Li Y, Ustach C, Handley V, Navarre R, Hwang CF, Aegerter BJ, Williamson VM, Baker B (2005) EDS1 in tomato is required for resistance mediated by TIR-class R genes and the receptor-like R gene Ve. Plant J 42:376–391
Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329
Jürges G, Kassemeyer H–H, Dürrenberger M, Düggelin M, Nick P (2009) The mode of interaction between Vitis and Plasmopara viticola Berk. & Curt. Ex de Bary depends on the host species. Plant Biol 11:886–898
Kast WK, Stark-Urnau M, Seidel M, Gemmrich AR (2001) Inter-isolate variation of virulence of Plasmopara viticola on resistant vine varieties. Bull OILB/SROP 24:45–49
Kortekamp A, Zyprian E (2003) Characterization of Plasmopara-resistance in grapevine using in vitro plants. J Plant Physiol 160:1393–1400
Laudert D, Weiler EW (2002) Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signaling. Plant J 15:675–684
McDowell JM, Cuzick A, Can C, Beynon J, Dangl JL, Holub EB (2000) Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation. Plant J 22:523–529
Munson TV (1909) Foundations of American grape culture. T.V. Munson & Son, Denison 252 pp
Mur LA, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262
Penninckx IA, Thomma BP, Buchala A, Métraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113
Peressotti E, Wiedemann-Merdinoglu S, Delmotte F, Bellin D, Di Gaspero G, Testolin R, Merdinoglu D, Mestre P (2010) Breakdown of resistance to grapevine downy mildew upon limited deployment of a resistant variety. BMC Plant Biol 10:147
Polesani M, Bortesi L, Ferrarini A, Zamboni A, Fasoli M, Zadra C, Lovato A, Pezzotti M, Delledonne M, Polverari A (2010) General and species-specific transcriptional responses to downy mildew infection in a susceptible (Vitis vinifera) and a resistant (V. riparia) grapevine species. BMC Genomics 11:117
Repka V (2002) Evidence for the involvement of cysteine proteases in the regulation of methyl jasmonate-induced cell death in grapevine. Vitis 41:115–121
Repka V, Fischerová I, Silhárová K (2001) Methyl jasmonate induces a hypersensitive-like response of grapevine in the absence of avirulent pathogens. Vitis 40:5–10
Schröder S, Telle S, Nick P, Thines M (2011) Cryptic diversity of Plasmopara viticola (Oomycota, Peronosporaceae) in North America. Org Divers Evol. doi:10.1007/s13127-010-0035-x
Shirasu K, Schulze-Lefert P (2003) Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways. Trends Plant Sci 8:252–258
Sivasankar S, Sheldrick B, Rothstein SJ (2000) Expression of allene oxide synthase determines defence gene activation in tomato. Plant Physiol 122:1335–1342
Thomma BP, Penninckx IA, Broekaert WF, Cammue BP (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13:63–68
Unger S, Büche C, Boso S, Kassemeyer HH (2007) The course of colonization of two different Vitis genotypes by Plasmopara viticola indicates compatible and incompatible host–pathogen interaction. Phytopathology 97:780–786
Zimmerli L, Stein M, Lipka V, Schulze-Lefert P, Somerville S (2004) Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. Plant J 40:633–646
Acknowledgments
This research was supported by funds from the Italian Ministry of Agriculture (VIGNA project) and from the Regional Government of Friuli Venezia Giulia (Grapevine Breeding Project). We thank Courtney Coleman for proofreading the manuscript.
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Casagrande, K., Falginella, L., Castellarin, S.D. et al. Defence responses in Rpv3-dependent resistance to grapevine downy mildew. Planta 234, 1097–1109 (2011). https://doi.org/10.1007/s00425-011-1461-5
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DOI: https://doi.org/10.1007/s00425-011-1461-5