Skip to main content
Log in

Expression profiling in HcrVf2-transformed apple plants in response to Venturia inaequalis

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Apple scab resistance is one of the most well-characterized plant–pathogen interactions in a woody plant species. While the HcrVf2 gene from the wild apple Malus floribunda 821 has proved capable of conferring scab resistance to the susceptible cv. Gala after genetic transformation, its identification represents only the first step in understanding the molecular mechanisms and, hence, the network of genes underlying the defence response. We used a PCR-based suppression subtractive hybridization to identify apple genes that are differentially expressed after Venturia inaequalis inoculation. Subtractive hybridization was performed between cDNA from challenged leaves of HcrVf2-resistant transgenic Gala and susceptible cv. Gala plants. A library of 523 unigenes was constructed and characterized by assigning a putative function via comparison with public databases. This set of pathogen-modulated apple genes includes many defence-related genes and is therefore an important source of information for understanding the molecular basis of the MalusV. inaequalis interaction.

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

Similar content being viewed by others

References

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

    PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K, Somerville CR, Thordal-Christensen H (2004) The PEN1 synthaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15:5118–5129

    Article  PubMed  CAS  Google Scholar 

  • Bachem CWB, van der Hoeven RS, de Bruijn SM, Vreugdenhil D, Zabeau M, Visser RGF (1996) Visualization of differential gene expression using a novel method of RNA fingerprint based on AFLP: analysis of gene expression during potato tuber development. Plant J 9:745–753

    Article  PubMed  CAS  Google Scholar 

  • Belfanti E, Silfverberg-Dilworth E, Tartarini S, Patocchi A, Barbieri M, Zhu J, Vinatzer B, Gianfranceschi L, Gessler C, Sansavini S (2004) The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc Natl Acad Sci USA 101:886–890

    Article  PubMed  CAS  Google Scholar 

  • Beuning LL, Bowen JH, Persson HA, Barraclough D, Bulley S, MacRae EA (2004) Characterisation of Mal d 1-related genes in Malus. Plant Mol Biol 55:369–388

    Article  PubMed  CAS  Google Scholar 

  • Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, Bergkamp R, Dirkse W, Van Staveren M, Stiekema W, Drost L, Ridley P, Hudson SA, Patel K, Murphy G, Piffanelli P, Wedler H, Wedler E, Wambutt R, Weitzenegger T, Pohl TM, Terryn N, Gielen J, Villarroel R, De Clerck R, Van Montagu M, Lecharny A, Auborg S, Gy I, Kreis M, Lao N, Kavanagh T, Hempel S, Kotter P, Entian KD, Rieger M, Schaeffer M, Funk B, Mueller-Auer S, Silvey M, James R, Montfort A, Pons A, Puigdomenech P, Douka A, Voukelatou E, Milioni D, Hatzopoulos P, Piravandi E, Obermaier B, Hilbert H, Düsterhöft A, Moores T, Jones JD, Eneva T, Palme K, Benes V, Rechman S, Ansorge W, Cooke R, Berger C, Delseny M, Voet M, Volckaert G, Mewes HW, Klosterman S, Schueller C, Chalwatzis N (1998) Analysis of 1.9Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391:485–488

    Article  PubMed  CAS  Google Scholar 

  • Blein JP, Coutos-Thévenot P, Mkarion D, Ponchet M (2002) From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci 7:293–296

    Article  PubMed  CAS  Google Scholar 

  • Borrás-Hidalgo O, Thomma BP, Collazo C, Chaćon O, Borrotto CJ, Ayra C, Portieles R, López Y, Pujol M (2006) EIL2 transcription factor and glutathione synthetase are required for defense of tobacco against tobacco blue mold. Mol Plant Microbe Interact 19:399–406

    Article  PubMed  Google Scholar 

  • Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Jhonson D, Luo S, McCurdy S, Foy M, Ewan M, Roth R, George D, Eletr S, Albrecht G, Vermaas E, Williams SR, Moon K, Burcham T, Pallas M, DuBridge RB, Kirchner J, Fearon K, Mao J, Corcoran K (2000) Gene expression analysis by massively parallel signature sequencing (MPSS) on microbeads arrays. Nat Biotechnol 18:597–598

    Article  Google Scholar 

  • Broekaert W, Lee HI Kush A, Chua NH, Raikhel N (1990) Wound-induced accumulation of mRNA containing a hevein sequence in laticifers of rubber tree (Hevea brasiliensis). Proc Natl Acad Sci USA 87:7633–7637

    Article  PubMed  CAS  Google Scholar 

  • Broekaert W, Cammue BPA, De Bolle MFC, Thevissen K, De Samblanx GW, Osborn RW (1997) Antimicrobial peptides from plants. Crit Rev Plant Sci 16:297–323

    Article  CAS  Google Scholar 

  • Butt A, Mousley C, Morris K, Beynon J, Can C, Holub E, Greenberg JT, Buchanan-Wollaston V (1998) Differential expression of a senescence-enhanced metallothionein gene in Arabidopsis in response to isolates of Peronospora parasitica and Pseudomonas syringae. Plant J 16:209–221

    Article  PubMed  CAS  Google Scholar 

  • Cabral KM, Almeida SM, Valente AP, Almeida FC, Kurtenbach E (2003) Production of the active antifungal Pisum sativum defensin 1 (Psd1) in Pichia pastoris: overcoming the inefficiency of the STE13 protease. Protein Expr Purif 31:115–122

    Article  PubMed  CAS  Google Scholar 

  • Cheng Q, Zhang B, Zhuge Q, Zeng YR, Wang MX, Huang MR (2006) Expression profiles of two novel lipoxygenase genes in Populus deltoides. Plant Sci 170:1027–1035

    Article  CAS  Google Scholar 

  • Chevalier M, Lespinasse Y, Renaudin S (1991) A microscopic study of the different classes of symptoms coded by the Vf gene in apple for resistance to scab (Venturia inaequalis). Plant Pathol 40:249–256

    Article  Google Scholar 

  • Crouzet J, Trombik T, Fraisse AS, Boutry M (2006) Organization and function of the plant pleiotropic drug resistance ABC transporter family. FEBS Lett 13:1123–1130

    Article  Google Scholar 

  • Degenhardt J, Al-Masri AN, Kürkcüoglu S, Szankowski I, Gau AE (2005) Characterization by suppression subtractive hybridization of transcripts that are differentially expressed in leaves of apple scab-resistant and susceptible cultivars of Malus domestica. Mol Gen Genomics 273:326–335

    Article  CAS  Google Scholar 

  • Devoto A, Muskett PR, Shirasu K (2003) Role of ubiquitination in the regulation of plant disease against pathogens. Curr Opin Plant Biol 6:307–311

    Article  PubMed  CAS  Google Scholar 

  • Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030

    Article  PubMed  CAS  Google Scholar 

  • Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37

    Article  PubMed  CAS  Google Scholar 

  • Dowd C, Wilson IW, McFadden H (2004) Gene expression profile changes in cotton root and hypocotyl tissues in response to infection with Fusarium oxysporum f. sp. vasinfectum. Mol Plant Microbe Interact 17:654–667

    Article  PubMed  CAS  Google Scholar 

  • Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10:71–78

    Article  PubMed  CAS  Google Scholar 

  • Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–97

    Article  PubMed  CAS  Google Scholar 

  • Froehlich JE, Itoh A, Howe GA (2001) Tomato allene oxide synthase and fatty acid hydroperoxide lyase, two cytochrome P450s involved in oxylipin metabolism, are targeted to different membranes of chloroplast envelop. Plant Physiol 125:306–317

    Article  PubMed  CAS  Google Scholar 

  • Gao AG, Hakimi SM, Mittanck CA, Wu Y, Woerner BM, Stark DM, Shah DM, Liang J, Rommens CM (2000) Fungal pathogen protection in potato by expression of a plant defensin peptide. Nat Biotechnol 18:1307–1310

    Article  PubMed  CAS  Google Scholar 

  • Gau AE, Koutb M, Piotrowski M, Kloppstech K (2004) Accumulation of pathogenesis-related proteins in the apoplast of a susceptible cultivar of apple (Malus domestica cv. Elstar) after infection by Venturia inaequalis and constitutive expression of PR genes in the resistant cultivar Remo. Eur J Plant Pathol 110:703–711

    Article  CAS  Google Scholar 

  • Gilroy E, Hein I, Van der Hoorn RAL, Boevink P, Venter E, McLellan H, Kaffarnik F, Hrubikova K, Shaw J, Holeva M, Lopez E, Hidalgo O, Pritchard L, Loake G, Lacomme C, Birch P (2007) Involvement of cathepsin B in the plant disease resistance hypersensitive response. Plant J 52:1–13

    Article  PubMed  CAS  Google Scholar 

  • Hammond-Kosack KE, Jones JDG (1997) Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48:575–607

    Article  PubMed  CAS  Google Scholar 

  • Hu G, deHart AKA, 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

    Article  PubMed  CAS  Google Scholar 

  • Hückelhoven R (2007) Cell-wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45:2.1–2.27

    Article  Google Scholar 

  • Jensen PJ, Rytter J, Detwiler EA, Travis JW, McNellis TW (2003) Rootstock effects on gene expression patterns in apple tree scions. Plant Mol Biol 493:493–511

    Article  Google Scholar 

  • Kalde M, Barth M, Somssich IE, Lippok B (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defence signaling pathways. Mol Plant Microbe Interact 16:295–305

    Article  PubMed  CAS  Google Scholar 

  • Kästner B, Tenhaken R, Kauss H (1998) Chitinase in cucumber hypocotyls is induced by germinating fungal spores and by fungal elicitor in synergism with inducers of acquired resistance. Plant J 13:447–454

    Article  Google Scholar 

  • Ko TS, Lee S, Schaefer SC, Korban SK (2003) Characterization of a tissue-specific and developmentally regulated β-1,3-glucanase gene family in Prunus persica. Plant Physiol Biochem 41:955–963

    Article  CAS  Google Scholar 

  • Komjanc M, Festi S, Rizzotti L, Cattivelli L, Cervone F, De Lorenzo G (1999) A leucine-rich repeat receptor-like protein kinase (LRPKm1) gene is induced in Malus × domestica by Venturia inaequalis infection and salicylic acid treatment. Plant Mol Biol 40:945–957

    Article  PubMed  CAS  Google Scholar 

  • Koo JC, Chun HJ, Park HC, Kim MC, Koo YD, Koo SC, Ok HM, Park SJ, Lee SH, Yun DJ, Lim CO, Bahk JD, Lee SY, Cho MJ (2002) Over-expression of a seed specific hevein-like antimicrobial peptide from Pharbitis nil enhances resistance to a fungal pathogen in transgenic tobacco plants. Plant Mol Biol 50:441–452

    Article  PubMed  CAS  Google Scholar 

  • Krüger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, Mulder L, Jones JDG (2002) A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296:744–747

    Article  PubMed  Google Scholar 

  • Lay FT, Brugliera F, Anderson MA (2003) Isolation and properties of floral defensins from ornamental tobacco and petunia. Plant Physiol 131:1283–1293

    Article  PubMed  CAS  Google Scholar 

  • Li L, Steffens JC (2002) Over-expression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215:239–247

    Article  PubMed  CAS  Google Scholar 

  • Li B, Xu X (2002) Infection and development of apple scab (Venturia inaequalis) on old leaves. J Phytopathol 150:687–691

    Article  Google Scholar 

  • Liang P, Pardee AB (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257:967–971

    Article  PubMed  CAS  Google Scholar 

  • Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P (2005) Pre- and Post-invasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180–1183

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Schiff M, Serino G, Deng XW, Dinesh-Kumar SP (2002) Role of SCF-ubiquitin ligase and the COP9 signalosome in the N gene-mediated resistance response to tobacco mosaic virus. Plant Cell 14:1483–1496

    Article  PubMed  CAS  Google Scholar 

  • Logemann E, Wu SC, Schröder J, Schmelzer E, Somssich IE, Hahlbrock K (1995) Gene activation by UV light, fungal elicitor or fungal infection in Petroselinum crispum is correlated with repression of cell cycle-related genes. Plant J 8:9865–876

    Google Scholar 

  • Lopez C, Soto M, Restrepo S, Piègu B, Cooke R, Delseny M, Tohme J, Verdier V (2005) Gene expression profile in response to Xanthomonas axonopodis pv. manihotis infection in cassava using a cDNA microarray. Plant Mol Biol 57:393–410

    Article  PubMed  CAS  Google Scholar 

  • Mahalingam R, Gomez-Buitrago A, Eckardt N, Shah N, Guevara-Garcia A, Day P, Raina R, Fedoroff NV (2003) Characterizing the stress/defense transcriptome of Arabidopsis. Genome Biol 4:R20

    Article  PubMed  Google Scholar 

  • Matsumura H, Reich S, Ito A, Saitoh H, Kamoun S, Winter P, Kahl G, Reuter M, Kruger DH, Terauchi R (2003) Gene expression analysis of plant host–pathogen interactions by SuperSAGE. Proc Natl Acad Sci USA 100:15718–15723

    Article  PubMed  CAS  Google Scholar 

  • Mysore K, Ryu CM (2004) Nonhost resistance: how much do we know? Trends Plant Sci 2:97–104

    Article  Google Scholar 

  • Mysore KS, D’Ascenzo MD, He X, Martin GB (2003) Overexpression of the disease resistance gene Pto in tomato induces gene expression changes similar to immune responses in human and fruitfly. Plant Physiol 132:1901–1912

    Article  PubMed  CAS  Google Scholar 

  • Nürnberger T, Scheel D (2001) Signal transmission in the plant immune response. Trends Plant Sci 6:372–379

    Article  PubMed  Google Scholar 

  • Patocchi A, Vinatzer BA, Gianfranceschi L, Tartarini S, Zhang HB, Sansavini S, Gessler C (1999) Construction of a 550 kb BAC contig spanning the genomic region containing the apple resistance gene Vf. Mol Gen Genet 262:884–891

    Article  PubMed  CAS  Google Scholar 

  • Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC (2005) NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against Tobacco Mosaic Virus. Curr Biol 15:968–973

    Article  PubMed  CAS  Google Scholar 

  • Peterman TK, Sequeira AS, Samia JA, Lunde EE (2006) Molecular cloning and characterization of patellin1, a novel sec14-related protein, from zucchini (Cucurbita pepo). J Plant Physiol 163:1150–1158

    Article  PubMed  CAS  Google Scholar 

  • Ramonell KM, Zhang B, Ewing RM, Chen Y, Xu D, Stacey G, Somerville S (2002) Microarray analysis of chitin elicitation in Arabidopsis thaliana. Mol Plant Pathol 3:301–311

    Article  CAS  Google Scholar 

  • Ramonell KM, Berrocal-Lobo M, Koh S, Wan J, Edwards H, Stacey G, Somerville S (2005) Loss-of-function mutations in chitin responsive genes show increased susceptibility to the powdery mildew pathogen Erysiphe cichoracearum. Plant Physiol 138:1027–1036

    Article  PubMed  CAS  Google Scholar 

  • Rivas S, Mucyn T, van den Burg HA, Vervoort J, Jones JDG (2002) An ~400 kDa membrane-associated complex that contains one molecule of the resistance protein Cf-4. Plant J 29:783–796

    Article  PubMed  CAS  Google Scholar 

  • Rowland O, Ludwig AA, Merrick CJ, Baillieul F, Tracy FE, Durrant WE, Fritz-Laylin L, Nekrasov V, Sjölander K, Yoshioka H, Jones JDG (2005) Functional analysis of Avr9/Cf-9 rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato. Plant Cell 17:295–310

    Article  PubMed  CAS  Google Scholar 

  • Rushton PJ, Reinstadler A, Lipka V, Lippok B, Somssich IE (2002) Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling. Plant Cell 14:749–762

    Article  PubMed  CAS  Google Scholar 

  • Schena M, Shalon D, Davis RW, Brown PO (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270:467–470

    Article  PubMed  CAS  Google Scholar 

  • Shibuya N, Minami E (2001) Oligosaccharide signaling for defense responses in plants. Physiol Mol Plant Pathol 59:223–233

    Article  CAS  Google Scholar 

  • Silfverberg-Dilworth E, Patocchi A, Gessler C (2006) Evaluation of in vitro grown apple shoot sensitivity to Venturia inaequalis using a detached leaf assay. IOBC–WPRS Bull 29:67–74 (Gessler C, Triloff P, eds)

    Google Scholar 

  • Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806

    Article  PubMed  CAS  Google Scholar 

  • Takemoto D, Jones DA, Hardham AR (2003) GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J 33:775–792

    Article  PubMed  CAS  Google Scholar 

  • Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330

    Article  PubMed  CAS  Google Scholar 

  • Terras FRG, Eggermont K, Kovaleva V, Raikhel NV, Osborn RW, Kester A, Rees SB, Torrekens S, Van Leuven F, Vanderleyden J, Cammue BPA, Broekaert WF (1995) Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell 7:573–588

    Article  PubMed  CAS  Google Scholar 

  • Thipyapong P, Hunt MD, Steffens JC (2004) Antisense downregulation of polyphenol oxidase results in enhanced disease susceptibility. Planta 220:105–107

    Article  PubMed  CAS  Google Scholar 

  • Thomma BP, Cammue BP, Thevissen K (2002) Plant defensins. Planta 216:193–202

    Article  PubMed  CAS  Google Scholar 

  • Tyerman SD, Niemietz M, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Env 25:173–194

    Article  CAS  Google Scholar 

  • Valsangiacomo C, Gessler C (1988) Role of the cuticular membrane in ontogenic and Vf resistance of apple leaves against Venturia inaequalis. Phytopathology 78:1066–1069

    Article  Google Scholar 

  • Van Loon LC, Rep M, Pieterse CMJ (2006) Significance of the inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:7.1–7.28

    Google Scholar 

  • Velculescu VE, Zhang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene expression. Science 270:484–487

    Article  PubMed  CAS  Google Scholar 

  • Vinatzer BA, Patocchi A, Gianfranceschi L, Tartarini S, Zhang HB, Gessler C, Sansavini S (2001) Apple contains receptor-like genes homologous to the Cladosporium fulvum resistance gene family of tomato with a cluster of genes cosegregating with Vf apple scab resistance. Mol Plant Microbe Interact 14:508–515

    Article  PubMed  CAS  Google Scholar 

  • Wang KLC, Yoshida H, Lurin C, Ecker JR (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428:945–950

    Article  PubMed  CAS  Google Scholar 

  • Wiermer M, Feys BJ, Parker JE (2005) Plant immunity: the EDS1 regulatory node. Curr Opin Plant Biol 8:383–389

    Article  PubMed  CAS  Google Scholar 

  • Wilkins TA, Smart LB (1996) Isolation of RNA from plant tissue. In: Krieg PA (ed) A laboratory guide to RNA: isolation, analysis, and synthesis. Wiley-Liss, New York, pp 21–42

    Google Scholar 

  • Williams EB, Kuc J (1969) Resistance in Malus to Venturia inaequalis. Ann Rev Phytopathol 7:223–246

    Article  CAS  Google Scholar 

  • Xia Y, Suzuki H, Borevitz J, Blount J, Guo Z, Patel K, Dixon RA, Lamb C (2004) An extracellular aspartic protease function in Arabidopsis disease resistance signaling. EMBO J 23:980–88

    Article  PubMed  CAS  Google Scholar 

  • Xu ML, Korban SS (2002) A cluster of four receptor-like genes resides in the Vf locus that confers resistance to apple scab disease. Genetics 162:1995–2006

    PubMed  CAS  Google Scholar 

  • Yang SH, Berberich T, Miyazaki A, Sano H, Kusano T (2003) Ntdin, a tobacco senescence-associated gene, is involved in molybdenum cofactor biosynthesis. Plant Cell Physiol 44:1037–1044

    Article  PubMed  CAS  Google Scholar 

  • Yoshida H, Nagata M, Saito K, Wang KLC, Ecker JR (2005) Arabidopsis ETO1 specifically interacts with and negatively regulates type 2 1-aminocyclopropane-1-carboxylate synthases. BMC Plant Biol 5:14 doi:10.1186/1471-2229-5-14

    Article  PubMed  Google Scholar 

  • Zhang Z, Feechan A, Pedersen C, Newman MA, Qiu JL, Olesen KL, Thordal-Christensen H (2007) A SNARE-protein has opposing functions in penetration resistance and defence signalling pathways. Plant J 49:302–312

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zou J, Rodriguez-Zas S, Aldea M, Li M, Zhu J, Gonzalez DO, Vodkin LO, DeLucia E, Clough SJ (2005) Expression profiling soybean response to Pseudomonas syringae reveals new defence-related genes and rapid HR-specific downregulation of photosynthesis. Mol Plant Microbe Interact 18:1161–1174

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Dott. Enrico Belfanti for the plant material, Dr. Gaetano Perrotta for his assistance during the sequencing of the SSH library and with sequence analysis and Dr. Vanina Ziosi for her help with the library screening.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roberta Paris.

Additional information

Communicated by J. Davis

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

List of the 558 single-pass sequences of the apple SSH library (DOC 602 KB)

Table S1

List of the 334 unigenes identified by SSH and similar to known genes available in public databases. 264 clones were derived from the ‘forward’ subtraction, 59 from the ‘reverse’ and 11 from both the procedures (XLS 103 KB)

Table S2

List of ESTs that (1) did not match any sequence in the database (NO HIT), (2) match sequences of unknown function (UNCLASSIFIED); (3) match sequences of unclear function (UNCLEAR FUNCTION); (4) match transposon-related sequences (TRANSPOSONS) (XLS 58.0 KB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Paris, R., Cova, V., Pagliarani, G. et al. Expression profiling in HcrVf2-transformed apple plants in response to Venturia inaequalis . Tree Genetics & Genomes 5, 81–91 (2009). https://doi.org/10.1007/s11295-008-0177-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-008-0177-6

Keywords

Navigation