Skip to main content
SpringerLink
Log in

Mechanisms of resistance/tolerance of Pyrus communis to Stemphylium vesicarium. A transcriptome analysis

  • Published:
Agroforestry Systems Aims and scope Submit manuscript

Abstract

Pyrus communis ‘Rocha’ is an economically important crop very susceptible to the pathogenic fungus Stemphylium vesicarium, the causal agent of brown spot disease. Knowledge on the complexity of mechanisms responsible for resistance to S. vesicarium infection is necessary for definition of strategies to improve defence responses in susceptible cultivars. To investigate the molecular mechanisms behind Pyrus communis defence responses to S. vesicarium, a 6624 (3312 × 2) cDNA microarray was constructed to identify genes differentially expressed between a resistant/tolerant cultivar (‘Ercolini’) and a susceptible cultivar (‘Rocha’). Both cultivars were compared to evaluate their genetic background differences prior to inoculation (T0h) and transcriptional changes along a time course infection with S. vesicarium (T6h and T24h). Two cDNA libraries, from ‘Rocha’ and ‘Ercolini’ pear cultivars, spotted in the microarray resulted on 146 differential expressed genes. Transcriptome analysis revealed several transcripts related to stress and defence, namely peroxidases, 3-dehydroquinate dehydratase/shikimate 5-dehydrogenase, thiazole biosynthetic enzyme, serpins, cytochromes P450, 2-methyl-6-phytylbenzoquinone methyltransferase, 6-phosphogluconate dehydrogenase, polyneuridine-aldehyde esterase precursor, lipoxygenases and PR proteins. The results suggest that resistance/tolerance of ‘Ercolini’ cultivar may result from the rapid activation of defence mechanisms while in ‘Rocha’ cultivar the defence mechanisms may be activated too late for inducing an efficient response to infection by S. vesicarium. Cell wall strengthening and biosynthesis of antifungal compounds may constitute efficient physical and chemical barriers to S. vesicarium infection and priming emerges as a putative mechanism of resistance/tolerance. The evidence gathered combined with knowledge on host/endophyte signalling in mycorrhiza leads us to suggest priming as a measure to brown spot disease control in ‘Rocha’ pear cultivar through symbiosis with mycorrhizal fungi in order to anticipate and induce a more efficient activation of defence mechanisms. Also the thiazole biosynthetic enzyme and the serpins appears as potential candidates for the development of molecular markers for resistance to infection.

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

Access this article

Log in via an institution

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

References

  • Ahn I-P, Kim S, Lee Y-H (2005) Vitamin B1 functions as an activator of plant disease resistance. Plant Physiol 138:1505–1515

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Almagro L, Ros LVG, Belchi-Navarro S, Bru R, Barceló AR, Pedreño MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Armengaud P, Breitling R, Amtmann A (2004) The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136:2556–2576

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aver’yanov AA, Lapikova VP, Pasechnik TD, Kuznetsov VV, Baker CJ (2007) Supression of early stages of fungus development by hydrogen peroxide at low concentrations. Plant Pathology J 6:242–247

    Article  Google Scholar 

  • Bairoch A, Apweiler R, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, O’Donovan C, Redaschi N, Yeh L-SL (2005) The universal protein resource (UniProt). Nucl Acids Res 33:D154–D159

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ballvora A, Ercolano MR, Weiß J, Meksem K, Bormann CA, Oberhagermann P, Salamini F, Gebhardt C (2002) The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J 30:361–371

    Article  CAS  PubMed  Google Scholar 

  • Belkhadir Y, Subramaniam R, Dangl JL (2004) Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol 7:391–399

    Article  CAS  PubMed  Google Scholar 

  • Beuning L, Bowen J, Persson H, Barraclough D, Bulley S, Macrae E (2004) Characterisation of Mal d 1-related genes in Malus. Plant Mol Biol 55:369–388

    Article  CAS  PubMed  Google Scholar 

  • Bhuiyan NH, Selvaraj G, Wei Y, King J (2009) Gene expression profiling and silencing reveal that monolignol biosynthesis plays a critical role in penetration defence in wheat against powdery mildew invasion. J Exp Bot 60:509–521

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Borad V, Sriram S (2008) Pathogenesis-related proteins for the plant protection. Asian J Exp Sci 22:189–196

    Google Scholar 

  • Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC, Gaasterland T, Glenisson P, Holstege FCP, Kim IF, Markowitz V, Matese JC, Parkinson H, Robinson A, Sarkans U, Schulze-Kremer S, Stewart J, Taylor R, Vilo J, Vingron M (2001) Minimum information about a microarray experiment (MIAME)—toward standards for microarray data. Nat Genet 29:365–371

    Article  CAS  PubMed  Google Scholar 

  • Brechenmacher L, Weidmann S, van Tuinen D, Chatagnier O, Gianinazzi S, Franken P, Gianinazzi-Pearson V (2004) Expression profiling of up-regulated plant and fungal genes in early and late stages of Medicago truncatula-Glomus mosseae interactions. Mycorrhiza 14:253–262

    Article  CAS  PubMed  Google Scholar 

  • Breitling R, Armengaud P, Amtmann A, Herzyk P (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573:83–92

    Article  CAS  PubMed  Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  CAS  PubMed  Google Scholar 

  • Campos-Soriano L, García-Martínez J, Segundo BS (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13:579–592

    Article  CAS  PubMed  Google Scholar 

  • Casaretto JA, Zúñiga GE, Corcuera LJ (2004) Abscisic acid and jasmonic acid affect proteinase inhibitor activities in barley leaves. J Plant Physiol 161:389–396

    Article  CAS  PubMed  Google Scholar 

  • Cheng Z, Sattler S, Maeda H, Sakuragi Y, Bryant DA, DellaPenna D (2003) Highly divergent methyltransferases catalyze a conserved reaction in tocopherol and plastoquinone synthesis in cyanobacteria and photosynthetic eukaryotes. Plant Cell 15:2343–2356

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Corpet F, Gouzy J, Kahn D (1998) The ProDom database of protein domain families. Nucl Acids Res 26:323–326

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. J Exp Bot 60:391–408

    Article  CAS  PubMed  Google Scholar 

  • Danson J, Wasano K, Nose A (2000) Infection of rice plants with the sheath blight fungus causes an activation of pentose phosphate and glycolytic pathways. Eur J Plant Pathol 106:555–561

    Article  CAS  Google Scholar 

  • Delannoy E, Jalloul A, Assigbetsé K, Marmey P, Geiger JP, Lherminier J, Daniel JF, Martinez C, Nicole M (2003) Activity of class III peroxidases in the defense of cotton to bacterial blight. Mol Plant Microbe Interact 16:1030–1038

    Article  CAS  PubMed  Google Scholar 

  • Ding L, Hofius D, Hajirezaei M-R, Fernie AR, Börnke F, Sonnewald U (2007) Functional analysis of the essential bifunctional tobacco enzyme 3-dehydroquinate dehydratase/shikimate dehydrogenase in transgenic tobacco plants. J Exp Bot 58:2053–2067

    Article  CAS  PubMed  Google Scholar 

  • Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847

    Article  CAS  PubMed  Google Scholar 

  • Dogru E, Warzecha H, Seibel F, Haebel S, Lottspeich F, Stöckigt J (2000) The gene encoding polyneuridine aldehyde esterase of monoterpenoid indole alkaloid biosynthesis in plants is an ortholog of the α/β hydrolase super family. Eur J Biochem 267:1397–1406

    Article  CAS  PubMed  Google Scholar 

  • Duplessis S, Courty P-E, Tagu D, Martin F (2005) Transcript patterns associated with ectomycorrhiza development in Eucalyptus globules and Pisolithus microcarpus. New Phytol 165:599–611

    Article  CAS  PubMed  Google Scholar 

  • El-kereamy A, Jayasankar S, Taheri A, Errampalli D, Paliyath G (2009) Expression analysis of a plum pathogenesis related 10 (PR10) protein during brown rot infection. Plant Cell Rep 28:95–102

    Article  CAS  PubMed  Google Scholar 

  • El-Sayed M, Verpoorte R (2007) Catharanthus terpenoid indole alkaloids: biosynthesis and regulation. Phytochem Rev 6:277–305

    Article  CAS  Google Scholar 

  • Facchini PJ (2001) Alkaloid biosynthesis in plants: biochemistry, cell biology, molecular regulation, and metabolic engineering applications. Annu Rev Plant Physiol Plant Mol Biol 52:29–66

    Article  CAS  PubMed  Google Scholar 

  • Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ferreira FJ, Guo C, Coleman JR (2008) Reduction of plastid-localized carbonic anhydrase activity results in reduced Arabidopsis seedling survivorship. Plant Physiol 147:585–594

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Figueiredo A, Fortes AM, Ferreira S, Sebastiana M, Choi YH, Sousa L, Acioli-Santos B, Pessoa F, Verpoorte R, Pais MS (2008) Transcriptional and metabolic profiling of grape (Vitis vinifera L.) leaves unravel possible innate resistance against pathogenic fungi. J Exp Bot 59:3371–3381

    Article  CAS  PubMed  Google Scholar 

  • Fonseca S, Hackler L Jr, Zvara A, Ferreira S, Baldé A, Dudits D, Pais MS, Puskas LG (2004) Monitoring gene expression during pear fruit development, ripening and senescence using cDNA microarrays. Plant Sci 167:457–469

    Article  CAS  Google Scholar 

  • Fonseca S, Monteiro L, Barreiro MG, Pais MS (2005) Expression of genes encoding cell wall modifying enzymes is induced by cold storage and reflects changes in pear fruit texture. J Exp Bot 56:2029–2036

    Article  CAS  PubMed  Google Scholar 

  • Fortes AM, Santos F, Choi YH, Silva MS, Figueiredo A, Sousa L, Pessoa F, Acioli-Santos B, Sebastiana M, Palme K, Malhó R, Verpoorte R, Pais MS (2008) Organogenic nodule development in hop (Humulus lupulus L.): transcript and metabolic responses. BMC Genomics. doi:10.1186/1471-2164-9-445

    PubMed Central  PubMed  Google Scholar 

  • García-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386

    Article  PubMed  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 

  • Gechev TS, Minkov IN, Hille J (2005) Hydrogen peroxide-induced cell death in Arabidopsis: transcriptional and mutant analysis reveals a role of an oxoglutarate-dependent dioxygenase gene in the cell death process. IUBMB Life 57:181–188

    Article  CAS  PubMed  Google Scholar 

  • Ghosh M (2006) Antifungal properties of haem peroxidase from Acorus calamus. Ann Bot 98:1145–1153

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gibly A, Bonshtien A, Balaji V, Debbie P, Martin GB, Sessa G (2004) Identification and expression profiling of tomato genes differentially regulated during a resistance response to Xanthomonas campestris pv. vesicatoria. MPMI 17:1212–1222

    Article  CAS  PubMed  Google Scholar 

  • Gjetting T, Carver TLW, Skøt L, Lyngkjær MF (2004) Differential gene expression in individual papilla-resistant and powdery mildew-infected barley epidermal cells. MPMI 17:729–738

    Article  CAS  PubMed  Google Scholar 

  • Gowri G, Bugos RC, Campbell WH, Maxwell CA, Dixon RA (1991) Stress responses in alfalfa (Medicago sativa L.). X. Molecular cloning and expression of S-adenosyl-l-methionine: caffeic acid 3-O-methyltransferase, a key enzyme of lignin biosynthesis. Plant Physiol 97:7–14

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Graciet E, Lebreton S, Gontero B (2004) Emergence of new regulatory mechanisms in the Benson–Calvin pathway via protein-protein interactions: a glyceraldehyde-3-phosphate dehydrogenase/CP12/phosphoribulokinase complex. J Exp Bot 55:1245–1254

    Article  CAS  PubMed  Google Scholar 

  • Habib H, Fazili KM (2007) Plant protease inhibitors: a defense strategy in plants. Biotechnol Mol Biol Rev 2:068–085

    Google Scholar 

  • Halbwirth H (2010) The creation and physiological relevance of divergent hydroxylation patterns in the flavonoid pathway. Int J Mol Sci 11:595–621

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Halterman D, Zhou F, Wei F, Wise RP, Schulze-Lefert P (2001) The MLA6 coiled-coil, NBS-LRR protein confers AvrMla6-dependent resistance specificity to Blumeria graminis f. sp. hordei in barley and wheat. Plant J 25:335–348

    Article  CAS  PubMed  Google Scholar 

  • Hammond-Kosack KE, Parker JE (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14:177–193

    Article  CAS  PubMed  Google Scholar 

  • He X-Z, Wang X, Dixon RA (2006) Mutational analysis of the Medicago glycosyltransferase UGT71G1 reveals residues that control regioselectivity for (iso)flavonoid glycosylation. J Biol Chem 281:34441–34447

    Article  CAS  PubMed  Google Scholar 

  • Hématy K, Cherk C, Somerville S (2009) Host–pathogen warfare at the plant cell wall. Curr Opin Plant Biol 12:406–413

    Article  PubMed  CAS  Google Scholar 

  • Herrmann KM (1995) The shikimate pathway: early steps in the biosynthesis of aromatic compounds. Plant Cell 7:907–919

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann-Sommergruber K (2002) Pathogenesis-related (PR)-proteins identified as allergens. Biochem Soc Trans 30:930–935

    Article  CAS  PubMed  Google Scholar 

  • Hohnjec N, Vieweg MF, Pühler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137:1283–1301

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, Chory J (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22:2825–2827

    Article  CAS  PubMed  Google Scholar 

  • Howe G, Lee GI, Itoh A, Li L, DeRocher AE (2000) Cytochrome P450-dependent metabolism of oxylipins in tomato. Cloning and expression of allene oxide synthase and fatty acid hydroperoxide lyase. Plant Physiol 123:711–724

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hussein MM, Balbaa LK, Gaballah MS (2007) Developing a salt tolerant cowpea using alpha tocopherol. J Appl Sci Res 3:1234–1239

    CAS  Google Scholar 

  • Jansen RMC, Miebach M, Kleist E, Van Henten EJ, Wildt J (2009) Release of lipoxygenase products and monoterpenes by tomato plants as an indicator of Botrytis cinerea-induced stress. Plant Biol 11:859–868

    Article  CAS  PubMed  Google Scholar 

  • Jones AME, Thomas V, Bennett MH, Mansfield J, Grant M (2006) Modifications to the Arabidopsis defense proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae. Plant Physiol 142:1603–1620

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defences. J Chem Ecol 38:651–664

    Article  CAS  PubMed  Google Scholar 

  • Karamloo F, Scheurer S, Wangorsch A, May S, Haustein D, Vieths S (2001) Pyr c 1, the major allergen from pear (Pyrus communis), is a new member of the Bet v 1 allergen family. J Chromatogr B 756:281–293

    Article  CAS  Google Scholar 

  • Kasprzewska A (2003) Plant Chitinases—regulation and function. Cell Mol Biol Lett 8:809–824

    CAS  PubMed  Google Scholar 

  • Kim JH, Cheon YM, Kim B-G, Ahn J-H (2008) Analysis of flavonoids and characterization of the OsFNS gene involved in flavone biosynthesis in rice. J Plant Biol 51:97–101

    Article  CAS  Google Scholar 

  • Koch H-G, Schneider D (2007) Folding, assembly, and stability of transmembrane cytochromes. Curr Chem Biol 1:59–74

    CAS  Google Scholar 

  • Kolomiets MV, Chen H, Gladon RJ, Braun EJ, Hannapel DJ (2000) A leaf lipoxygenase of potato induced specifically by pathogen infection. Plant Physiol 124:1121–1130

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kreft O, Hoefgen R, Hesse H (2003) Functional analysis of cystathionine γ-synthase in genetically engineered potato plants. Plant Physiol 131:1843–1854

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Krepinsky K, Plaumann M, Martin W, Schnarrenberger C (2001) Purification and cloning of chloroplast 6-phosphogluconate dehydrogenase from spinach. Eur J Biochem 268:2678–2686

    Article  CAS  PubMed  Google Scholar 

  • Lammens W, Le Roy K, Schroeven L, Van Laere A, Rabijns A, Van den Ende W (2009) Structural insights into glycoside hydrolase family 32 and 68 enzymes: functional implications. J Exp Bot 60:727–740

    Article  CAS  PubMed  Google Scholar 

  • Lavania M, Chauhan PS, Chauhan SVS, Singh HB, Nautiyal CS (2006) Induction of plant defense enzymes and phenolics by treatment with plant growth–promoting rhizobacteria Serratia marcescens NBRI1213. Curr Microbiol 52:363–368

    Article  CAS  PubMed  Google Scholar 

  • Li J, Brader G, Palva ET (2008) Kunitz trypsin inhibitor: an antagonist of cell death triggered by phytopathogens and fumonisin B1 in Arabidopsis. Mol Plant 1:482–495

    Article  CAS  PubMed  Google Scholar 

  • Liu J-J, Ekramoddoullah AKM (2006) The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol Mol Plant Pathol 68:3–13

    Article  CAS  Google Scholar 

  • Llorente I, Montesinos E (2002) Effect of relative humidity and interrupted wetness periods on brown spot severity of pear caused by Stemphylium vesicarium. Phytopathology 92:99–104

    Article  CAS  PubMed  Google Scholar 

  • Llorente I, Montesinos E (2006) Brown spot of pear: an emerging disease of economic importance in Europe. Plant Dis 90:1368–1375

    Article  Google Scholar 

  • Llorente I, Vilardell P, Bugiani R, Gherardi I, Montesinos E (2000) Evaluation of BSPcast disease warning system in reduced fungicide use programs for management of brown spot of pear. Plant Dis 84:631–637

    Article  Google Scholar 

  • Loizeau K, Gambonnet B, Guo-Fang Z, Curien G, Jabrin S, Van Der Straeten D, Lambert WE, Rébeillé F, Ravanel S (2007) Regulation of one-carbon metabolism in Arabidopsis: the N-terminal regulatory domain of cystathionine γ-synthase is cleaved in response to folate starvation. Plant Physiol 145:491–503

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Matringe M, Ksas B, Rey P, Havaux M (2008) Tocotrienois, the unsaturated forms of vitamin E, can function as antioxidants and lipid protectors in tobacco leaves. Plant Physiol 147:764–778

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Memelink J, Verpoorte R, Kijne JW (2001) ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 6:212–219

    Article  CAS  PubMed  Google Scholar 

  • Mendgen K, Hahn M, Deising H (1996) Morphogenesis and mechanisms of penetration by pathogenic fungi. Annu Rev Phytopathol 34:367–386

    Article  CAS  PubMed  Google Scholar 

  • Minic Z (2008) Physiological roles of plant glycoside hydrolases. Planta 227:723–740

    Article  CAS  PubMed  Google Scholar 

  • Minic Z, Jouanin L (2006) Plant glycoside hydrolases involved in cell wall polysaccharide degradation. Plant Physiol Biochem 44:435–449

    Article  CAS  PubMed  Google Scholar 

  • Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, Ohkawa Y, Ohashi Y (2008) Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (121/180). Mol Genet Genomics 279:415–427

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moffett P, Farnham G, Peart J, Baulcombe DC (2002) Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J 21:4511–4519

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Monteiro S, Barakat M, Piçarra-Pereira MA, Teixeira AR, Ferreira RB (2003) Osmotin and thaumatin from grape: a putative general defense mechanism against pathogenic fungi. Phytopathology 93:1505–1512

    Article  CAS  PubMed  Google Scholar 

  • Montesinos E, Moragrega C, Llorente I, Vilardell P, Bonaterra A, Ponti I, Bugiani R, Cavanni P, Brunelli A (1995) Development and evaluation of an infection model for Stemphylium vesicarium on pear based on temperature and wetness duration. Phytopathology 85:586–592

    Article  Google Scholar 

  • Moy P, Qutob D, Chapman BP, Atkinson I, Gijzen M (2004) Patterns of gene expression upon infection of soybean plants by Phytophthora sojae. MPMI 17:1051–1062

    Article  CAS  PubMed  Google Scholar 

  • Nafisi M, Goregaoker S, Botanga CJ, Glawischnig E, Olsen CE, Halkier BA, Glazebrook J (2007) Arabidopsis cytochrome P450 monooxygenase 71A13 catalyzes the conversion of indole-3-acetaldoxime in camalexin synthesis. Plant Cell 19:2039–2052

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Niederman T, Genetet I, Bruyere T, Gees R, Stinzi A, Legrand M, Fritig B, Mosinger E (1995) Pathogenesis-related PR-1 proteins are antifungal: isolation and characterization of three 14 kidodalton proteins of tomato and of a basic PR-1 of tobacco with inhibitory activity against Phytophythora infestans. Plant Physiol 108:17–27

    Article  Google Scholar 

  • O’Connor SE, Maresh JJ (2006) Chemistry and biology of monoterpene indole alkaloid biosynthesis. Nat Prod Rep 23:532–547

    Article  PubMed  CAS  Google Scholar 

  • Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M (1999) KEGG: Kyoto encyclopedia of genes and genomes. Nucl Acids Res 27:29–34

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1186/1471-2164-11-117

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcón-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534

    Article  CAS  PubMed  Google Scholar 

  • Pühringer H, Moll D, Hoffmann-Sommergruber K, Watillon B, Katinger H, Machado MLC (2000) The promoter of an apple Ypr10 gene, encoding the major allergen Mal d 1, is stress- and pathogen-inducible. Plant Sci 152:35–50

    Article  Google Scholar 

  • Quiroga M, Guerrero C, Botella M, Barcelo A, Amaya I, Medina M, Alonso F, Forchetti S, Tigier H, Valpuesta V (2000) A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiol 122:1119–1127

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Radwan O, Mouzeyar S, Nicolas P, Bouzidi MF (2005) Induction of a sunflower CC-NBS-LRR resistance gene analogue during incompatible interaction with Plasmopara halstedii. J Exp Bot 56:567–575

    Article  CAS  PubMed  Google Scholar 

  • Rancé I, Fournier J, Esquerré-Tugayé M-T (1998) The incompatible interaction between Phytophthora parasítica var. nicotianae race 0 and tobacco is suppressed in transgenic plants expressing antisense lipoxygenase sequences. Proc Natl Acad Sci USA 95:6554–6559

    Article  PubMed Central  PubMed  Google Scholar 

  • Raschke M, Bürkle L, Müller N, Nunes-Nesi A, Fernie AR, Arigoni D, Amrhein N, Fitzpatrick TB (2007) Vitamin B1 biosynthesis in plants requires the essential iron-sulfur cluster protein, THIC. PNAS 104:19637–19642

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reiter W-D, Vanzin GF (2001) Molecular genetics of nucleotide sugar interconversion pathways in plants. Plant Mol Biol 47:95–113

    Article  CAS  PubMed  Google Scholar 

  • Roberts TH, Hejgaard J (2008) Serpins in plants and green algae. Funct Integr Genomics 8:1–27

    Article  CAS  PubMed  Google Scholar 

  • Salzer P, Bonanomi A, Beyer K, Vögeli-Lange R, Aeschbacher RA, Lange J, Wiemken A, Kim D, Cook DR, Boller T (2000) Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation, and pathogen infection. MPMI 13:763–777

    Article  CAS  PubMed  Google Scholar 

  • Sasaki Y, Asamizu E, Shibata D, Nakamura Y, Kaneko T, Awai K, Amagai M, Kuwata C, Tsugane T, Masuda T, Shimada H, K-i Takamiya, Ohta H, Tabata S (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res 8:153–161

    Article  CAS  PubMed  Google Scholar 

  • Sattler SE, Mène-Saffrané L, Farmer EE, Krischke M, Mueller MJ, DellaPenna D (2006) Nonenzymatic lipid peroxidation reprograms gene expression and activates defense markers in Arabidopsis tocopherol-deficient mutants. Plant Cell 18:3706–3720

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sebastiana M, Figueiredo A, Acioli B, Sousa L, Pessoa F, Baldé A, Pais MS (2009) Identification of plant genes involved on the initial contact between ectomycorrhizal symbionts (Castanea sativa—European chestnut and Pisolithus tinctorius). Eur J Soil Biol 45:275–282

    Article  CAS  Google Scholar 

  • Seifert GJ (2004) Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to outside. Curr Opin Plant Biol 7:277–284

    Article  CAS  PubMed  Google Scholar 

  • Shetty NP, Jergensen HJL, Jensen JD, Collinge DB, Shetty HS (2008) Roles of reative oxygen species in interactions between plants and pathogens. Eur J Plant Pathol 121:267–280

    Article  CAS  Google Scholar 

  • Shi B-J, Wang G-L (2008) Comparative study of genes expressed from rice fungus-resistant and susceptible lines during interactions with Magnaporthe oryzae. Gene 427:80–85

    Article  CAS  PubMed  Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sindelar L, Sindelarova M, Burketova L (1999) Changes in activity of glucose-6-phosphate and 6-phosphogluconate dehydrogenase isozymes upon potato virus Y infection in tobacco leaf tissues and protoplasts. Plant Physiol Bioch 37:195–201

    Article  CAS  Google Scholar 

  • Singh P, Bugiani R, Cavanni P, Nakajima H, Kodama M, Otani H, Kohmoto K (1999) Purification and biological characterization of host-specific SV-toxins from Stemphylium vesicarium causing brown spot of European pear. Phytopathology 89:947–953

    Article  CAS  PubMed  Google Scholar 

  • Spreitzer RJ, Salvucci ME (2002) RUBISCO: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53:449–475

    Article  CAS  PubMed  Google Scholar 

  • Suheri H, Price TV (2000) Infection of onion leaves by Alternaria porri and Stemphylium vesicarium and disease development in controlled environments. Plant Pathol 49:375–382

    Article  Google Scholar 

  • Teixeira de Sousa AJ (2000) Medidas a adoptar para a redução da incidência da “Stemphyliose” no pomar de pereira Rocha. In: 5º Encontro Rocha em Flor—Produção Integrada—Associação de Produtores Agrícolas da Sobrena (APAS), pp 33–38

  • Teixeira de Sousa AJ (2003) A “stemphyliose” na pereira Rocha. In: Sobreiro J, Lopes G (eds) Guia de Fruticultura. Centro Operativo e Tecnológico Hortofrutícola Nacional, Alcobaça, pp 1–8

  • Teixeira de Sousa AJ, Oliveira H, Rego MC, Sousa R, Valdiviesso T, Godinho JC, Branco JQ (1998) “Stemphyliose” da Pereira em Portugal. In: Novos Rumos na Produção das Plantas—Actas da 2ª Reunião Bienal da Sociedade Portuguesa de Fitopatologia, pp 68–75

  • Thompson CE, Fernandes CL, Souza ON, Salzano FM, Bonatto SL, Freitas LB (2006) Molecular modeling of pathogenesis-related proteins of family 5. Cell Biochem Biophys 44:385–394

    Article  CAS  PubMed  Google Scholar 

  • Tucker SL, Talbot NJ (2001) Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu Rev Phytopathol 39:385–417

    Article  CAS  PubMed  Google Scholar 

  • Vainonen JP, Vener AV, Aro E-M (2009) Determination of in vivo protein phosphorylation in photosynthetic membranes. In: Robbins P (ed) Plant signal transduction. Methods in molecular medicine, vol 479. Humana Press, Totowa, pp 1–14. doi:10.1007/978-1-59745-289-2_9

    Chapter  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Vanacker H, Carver TLW, Foyer CH (1998) Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117:1103–1114

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Véronési C, Rickauer M, Fournier J, Pouénat M-L, Esquerré-Tugayé M-T (1996) Lipoxygenase gene expression in the tobacco—Phytophthora parasitica nicotianae interaction. Plant Physiol 112:997–1004

    Article  PubMed Central  PubMed  Google Scholar 

  • Wan C-Y, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Annal Biochem 223:7–12

    Article  CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Werck-Reichhart D, Feyereisen R (2000) Cytochromes P450: a success story. Genome Biol 1(6):3003.1–3003.9

    Article  Google Scholar 

  • Wink M (2010) Secondary metabolites: deterring herbivores. eLS. doi:10.1002/9780470015902.a0000918.pub2

    Google Scholar 

  • Yang T, Poovaiah BW (2002) Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. PNAS 99:4097–4102

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Portuguese Science and Technology Foundation (FCT) under the PhD fellowship SFRH/BD/12374/2003 and partially financed by national funds through FCT under the Projects PEst-OE/BIA/UI4046/2011, PEst-OE/MAT/UI0006/2011 and PTDC/MAT/118335/2010. The authors wish to acknowledge to Dr. Sandra Fonseca by the kindly supply of controls used in microarrays and to Mr. Ernesto Rodrigues for the kindly supply of pear tree clones. The authors also wish to thank to Dr. Aladje Baldé and Dr. Pedro Sampaio for their valuable help and to Dr. Margarida Fortes, Dr. Mónica Sebastiana, Dr. Andreia Figueiredo and Dr. Filipa Monteiro for their valuable advices during this work.

Author information

Authors and Affiliations

  1. Plant Systems Biology Lab, Center for Biodiversity, Functional and Integrative Genomics (BioFIG), Science Faculty of Lisbon University (FCUL), C2, Piso 4, Sala 2.4.48, Campo Grande, 1749-016, Lisbon, Portugal

    Vanessa Tolentino Pereira & Maria Salomé Pais

  2. Department of Statistics and Operational Research, Center of Statistics and Aplications of the University of Lisbon, FCUL, CEAUL, Lisbon, Portugal

    Lisete Sousa

  3. National Institute of Agricultural Research (INIA), National Station of Fruit Culture Vieira Natividade (ENFVN), Estrada de Leiria, 2460-997, Alcobaça, Portugal

    António Teixeira de Sousa

Authors
  1. Vanessa Tolentino Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lisete Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. António Teixeira de Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Salomé Pais
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vanessa Tolentino Pereira.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pereira, V.T., Sousa, L., de Sousa, A.T. et al. Mechanisms of resistance/tolerance of Pyrus communis to Stemphylium vesicarium. A transcriptome analysis. Agroforest Syst 89, 991–1017 (2015). https://doi.org/10.1007/s10457-015-9831-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10457-015-9831-9

Keywords

Search

Navigation