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Molecular response of resistant and susceptible apple genotypes to Erwinia amylovora infection

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Abstract

The leaves of apple cultivars resistant (cv. Free Redstar) and susceptible (cv. Idared) to fire blight were infiltrated with Erwinia amylovora. After 24 hours, differential gene expression was analysed using cDNA-AFLP technique. The expression pattern in the resistant cultivar, especially up-regulated genes encoding proteins involved in hypersensitive reaction and controlled cell death (BAX inhibitor and HIR protein), support the hypothesis that hypersensitive reaction is the main mechanism of resistance to fire blight in cv. Free Redstar. An important role in the resistance reaction is also played by proteins involved in signal transduction, especially serine/threonine kinase, which has been shown previously to confer resistance to fungal and bacterial pathogens in a number of plant species. A potential role in the defence against Erwinia amylovora was probably also β-1,3-glucanase (PR-2 protein), which was up-regulated in the resistant cultivar only. One of the proteins known to be involved in plant defense against pathogens – glutamate receptor – was up-regulated in the leaves of cv. Idared. Although the susceptible phenotype of this cultivar shows that expression of glutamate receptor only does not provide substantial resistance, it may be considered in gene pyramiding in apple breeding programmes.

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References

  • Aldwinckle, H. S., & Beer, S. V. (1978). Fire blight and its control. Horticultural Reviews, 1, 423–474.

    Google Scholar 

  • Afzal, A. J., Wood, A. J., & Lightfoot, D. A. (2008). Plant receptor-like serine threonine kinases: roles in signalling and plant defense. Molecular Plant-Microbe Interactions, 21, 507–517.

    Article  CAS  PubMed  Google Scholar 

  • Baldo, A., Norelli, J. L., Farrell, R. E., Bassett, C. L., Aldwinckle, H. S., & Malnoy, M. (2010). Identification of genes differentially expressed during interaction of resistant and susceptible apple cultivars (Malus × domestica) with Erwinia amylovora. BMC Plant Biology, 10, 1.

    Article  PubMed Central  PubMed  Google Scholar 

  • Babu, R. M., Sajeena, A., Samundeeswari, A. V., Sreedhar, A., Vidhyasekeran, P., & Reddy, M. S. (2003). Induction of bacterial blight (Xanthomonas oryzae pv. oryzae) resistance in rice by treatment with acibenzolar-S-methyl. Annals of Applied Biology, 143, 333–340.

    Article  CAS  Google Scholar 

  • Bachem, C., van der Hoeven, R., de Brujin, S., Vreugdenhil, D., Zabeau, M., & Visser, R. (1996). Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. The Plant Journal, 9(5), 745–753.

    Article  CAS  PubMed  Google Scholar 

  • Ben-Naim, O., Eshed, R., Parnis, A., Teper-Bamnolker, P., Shalit, A., Coupland, G., Samach, A., & Lifschitz, E. (2006). The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA. The Plant Journal, 46, 462–76.

    Article  CAS  PubMed  Google Scholar 

  • Bonasera, J. M., Kim, J. F., & Beer, S. V. (2006). PR genes of apple: identification and expression in response to elicitors and inoculation with Erwinia amylovora. BMC Plant Biology, 6, 23.

    Article  PubMed Central  PubMed  Google Scholar 

  • Bouche, N., & Fromm, H. (2004). GABA in plants: just a metabolite? Trends in Plant Science, 9(3), 110–115.

    Article  CAS  PubMed  Google Scholar 

  • Brisset, M. N., Cesbron, S., Thomson, S. V., & Paulin, J.-P. (2000). Acibenzolar-S-methyl induces the accumulation of defense-related enzymes in apple and protects from fire blight. European Journal of Plant Pathology, 106, 529–536.

    Article  CAS  Google Scholar 

  • Broggini, G. A. L., Wöhner, T., Fahrentrapp, J., Kost, T. D., Flachowsky, H., Peil, A., Hanke, M. V., Richter, K., Patocchi, A., & Gessler, C. (2014). Engineering fire blight resistance into the apple cultivar ‘Gala’ using the FB_MR5 CC-NBS-LRR resistance gene of Malus × robusta 5. Plant Biotechnology Journal, 12, 728–733.

    Article  CAS  PubMed  Google Scholar 

  • Cao, A., Xing, L., Wang, X., Yang, X., Wang, W., Sun, Y., Qian, C., Ni, J., Chen, Y., Liu, D., Wang, X., & Chen, P. (2011). Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. Proceedings of the National Academy of Sciences, 108, 7727–7732.

    Article  CAS  Google Scholar 

  • Carvalho, M. F., & Lazarowitz, S. G. (2004). Interaction of the movement protein NSP and the Arabidopsis acetyltransferase AtNSI is necessary for cabbage leaf curl Geminivirus infection and pathogenicity. Journal of Virology, 78, 11161–11171.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carvalho, M. F., Turgeon, R., & Lazarowitz, S. G. (2006). The genimivirus nuclear shuttle protein NSP inhibits the activity of AtNSI, a vascular expressed Arabidopsis acetyltransferase regulated with the sink-to-source transition. Plant Physiology, 140, 1317–1330.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chang, S., Puryear, J., & Cairney, J. (1993). A simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter, 11, 113–116.

    Article  CAS  Google Scholar 

  • Chizzali, C., Gaid, M. M., Asma, K., Belkheir, A. K., Hänsch, R., Richter, K., Flachowsky, H., Peil, A., Hanke, M. V., Liu, B., & Beerhues, L. (2012). Differential expression of biphenyl synthase gene family members in fire-blight-infected apple. Plant Physiology, 158, 864–875.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Creelman, R. A., Bell, E., & Mullet, J. E. (1992). Involvement of a lipoxygenase-like enzyme in abscisic acid biosynthesis. Plant Physiology, 99, 1258–1260.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Creelman, R. A., & Mullet, J. E. (1997). Biosynthesis and action of jasmonates in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 48, 355–381.

    Article  CAS  PubMed  Google Scholar 

  • de Bernonville, T. D., Gaucher, M., Guyot, S., Durel, C. E., Dat, J. F., & Brisset, M. N. (2011). The constitutive phenolic composition of two Malus × domestica genotypes is not responsible for their contrasted susceptibilities to fire blight. Environmental and Experimental Botany, 74, 65–73.

    Article  Google Scholar 

  • Dezar, C. A., Gago, G. M., Gonzales, D. H., & Chan, R. L. (2005). Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants. Translational Research, 14, 429–440.

    CAS  Google Scholar 

  • Duan, Y., Guo, J., Shi, X., Guan, X., Liu, F., Bai, P., Huang, L., & Kang, Z. (2013). Wheat hypersensitive-induced reaction genes TaHIR1 and TaHIR3 are involved in response to stripe rust fungus infection and abiotic stresses. Plant Cell Reports, 32, 273–283.

    Article  CAS  PubMed  Google Scholar 

  • Eichmann, R., Bischof, M., Weis, C., Shaw, J., Lacomme, C., Schweizer, P., Duchkov, D., Hensel, G., Kumlehn, J., & Hückelhoven, R. (2010). BAX INHIBITOR-1 is required for full susceptibility of barley to powdery mildew. Molecular Plant-Microbe Interaction, 23, 1217–1227.

    Article  CAS  Google Scholar 

  • Fahrentrapp, J., Broggini, G. A. L., Kellerhals, M., Peil, A., Richter, K., Zini, E., & Gessler, C. (2013). A candidate gene for fire blight resistance in Malus × robusta 5 is coding for a CC-NBS-LRR. Tree Genetics & Genomes, 9, 237–251.

    Article  Google Scholar 

  • Gong, Q., Li, P., Ma, S., Rupassara, S. I., & Bohnert, H. J. (2005). Salinity stress adaptation competence in the extremophile Thellungiella halophile in comparison with its relative Arabidopsis thaliana. The Plant Journal, 44, 826–839.

    Article  CAS  PubMed  Google Scholar 

  • Hardie, D. G. (1999). Plant protein serine/threonine kinases: classification and functions. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 97–131.

    Article  CAS  PubMed  Google Scholar 

  • Heyens, K., Valcke, R., Dumont, D., Robben, J., & Noben, J.-P. (2006). Differential expression of proteins in apple following inoculation with Erwinia amylovora. Acta Horticulturae, 704, 489–494.

    CAS  Google Scholar 

  • Hückelhoven, R. (2004). BAX Inhibitor-1, an ancient cell death suppressor in animals and plants with prokaryotic relatives. Apoptosis, 9, 299–307.

    Article  PubMed  Google Scholar 

  • Iakimova, E. I., Michalczuk, L., & Woltering, E. J. (2005). Hypersensitive cell death in plants - its mechanisms and role in plant defence against pathogens. Journal of Fruit and Ornamental Plant Research, 13, 135–158.

    CAS  Google Scholar 

  • Iakimova, E. I., Sobiczewski, P., Michalczuk, L., Węgrzynowicz-Lesiak, E., Mikiciński, A., & Woltering, E. J. (2013). Morphological and biochemical characterization of Erwinia amylovora induced hypersensitive cell death in apple leaves. Plant Physiology and Biochemistry, 63, 292–305.

    Article  CAS  PubMed  Google Scholar 

  • Imani, J., Baltruschat, H., Stein, E., Jia, G., Vogelsberg, J., Kogel, K. H., & Hückelhoven, R. (2006). Expression of barley BAX Inhibitor-1 in carrots confers resistance to Botrytis cinerea. Molecular Plant Pathology, 7, 279–284.

    Article  CAS  PubMed  Google Scholar 

  • Jain, M., Nijhawan, A., Arora, R., Agarwal, P., Ray, S., Sharma, P., Kapoor, S., Tyagi, A. K., & Khurana, J. P. (2007). F-box protein in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiology, 143, 1467–1483.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Janssen, P., Coopman, R., Huys, G., Swings, J., Bleeker, M., Vos, P., Zabeau, M., & Kersters, K. (1996). Evaluation of the DNA fingerprinting method AFLP as a new tool in bacterial taxonomy. Microbiology, 142, 1881–1893.

    Article  CAS  PubMed  Google Scholar 

  • Jensen, P. J., Halbrendt, N., Fazio, G., Makalowska, I., Altman, N., Praul, C., Maximova, S. N., Ngugi, H. K., Crassweller, R. M., Travis, J. W., & McNellis, T. W. (2012). Rootstock-regulated gene expression patterns associated with fire blight resistance in apple. BMC Genomics, 13, 9–25.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jensen, P. J., Makalowska, I., Altman, N., Fazio, G., Praul, C., Maximova, S. N., Crassweller, R. M., Travis, J. W., & McNellis, T. W. (2010). Rootstock-regulated gene expression patterns in apple tree scions. Tree Genetics & Genomes, 6, 57–72.

    Article  Google Scholar 

  • Kang, S., Kim, H. B., Lee, H., Choi, J. Y., Heu, S., Oh, C. J., Kwon, S. I., & An, C. S. (2006). Overexpression in Arabidopsis of a plasma membrane-targeting glutamate receptor from small radish increases glutamate-mediated Ca2+ influx and delays fungal infection. Molecular Cell, 21, 418–427.

    CAS  Google Scholar 

  • Kawai-Yamada, M., Hori, Z., Ogawa, T., Ihara-Ohori, Y., Tamura, K., Nagano, M., Ishikawa, T., & Uchimiya, H. (2009). Loss of calmodulin binding to Bax inhibitor-1 affects Pseudomonas-mediated hypersensitive response-associated cell death in Arabidopsis thaliana. Journal of Biological Chemistry, 284, 27998–28003.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kellerhals, M., Franck, L., Baumgartner, I. O., Patocch, A., & Frey, J. E. (2011). Breeding for fire blight resistance in apple. Acta Horticulturae, 896, 385–389.

    Google Scholar 

  • Kellerhals, M., Baumgartner, I. O., Leumann, L., Frey, J. E., & Patocch, A. (2013). Progress in pyramiding desease resistances in apple breeding. Acta Horticulturae, 976, 487–491.

    Google Scholar 

  • Khan, M. A., Duffy, B., Gessler, C., & Patocchi, A. (2006). QTL mapping of fire blight resistance in apple. Molecular Breeding, 17, 299–306.

    Article  Google Scholar 

  • Kipreos, E. T., & Pagano, M. (2000). The F-box protein family. Genome Biology, 1(5), 3002.1–3002.7. reviews.

    Article  Google Scholar 

  • Krattinger, S. G., Lagudah, E. S., Spielmeyer, W., Singh, R. P., Huerta-Espino, J., McFadden, H., Bossolini, E., Selter, L. L., & Keller, B. (2009). A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science, 323, 1360–1363.

    Article  CAS  PubMed  Google Scholar 

  • Kouzarides, T. (2000). Acetylation: a regulatory modification to rival phosphorylation? EMBO Journal, 19, 1176–1179.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kwak, K. J., Kim, J. Y., Kim, J. O., & Kang, H. (2007). Characterization of transgenic Arabidopsis plants overexpressing high mobility group B proteins under high salinity, drought or cold stress. Plant and Cell Physiology, 48, 221–231.

    Article  CAS  PubMed  Google Scholar 

  • Lespinasse, Y., Guérif, P., & Durel, C. E. (2011). Strategies for fire blight resistance breeding in pear (Pyrus communis); 30 years of experience. Acta Horticulturae, 909, 51–58.

    Google Scholar 

  • Leubner-Metzger, G., & Meins, F. (1999). Functions and regulation of plant ß-1,3-glucanases (PR-2). In S. K. Datta & S. Muthukrishnan (Eds.), Pathogenesis-related proteins in plants (pp. 49–73). Boca Raton, Florida, USA: CRC Press LLC.

    Google Scholar 

  • Malnoy, M., Jin, Q., Borejsza-Wysocka, E. E., He, S. Y., & Aldwinckle, H. S. (2007). Overexpression of the apple MpNPR1 gene confers increased disease resistance in Malus × domestica. Molecular Plant-Microbe Interaction, 20, 1568–1580.

    Article  CAS  Google Scholar 

  • Malnoy, M., Martens, S., Norelli, J. L., Barny, M. A., Sundin, G. W., Smits, T. H. M., & Duffy, B. (2012). Fire blight: applied genomic insights of the pathogen and host. Annual Review of Phytopathology, 50, 475–494.

    Article  CAS  PubMed  Google Scholar 

  • Manzoor, H., Kelloniemi, J., Chiltz, A., Wendehenne, D., Pugin, A., Poinssot, B., & Garcia-Brugger, A. (2013). Involvement of the glutamate receptor AtGLR3.3 in plant defense signalling and resistance to Hyaloperonospora arabidopsidis. The Plant Journal, 76, 466–480.

    Article  CAS  PubMed  Google Scholar 

  • Martinoia, E., Klein, M., Geisler, M., Bovet, L., Forestier, C., Kolukisaoglu, U., Müller-Röber, B., & Schulz, B. (2002). Multifunctionality of plant ABC transporters – more than just detoxifiers. Planta, 214, 345–355.

    Article  CAS  PubMed  Google Scholar 

  • Marrs, K. A. (1996). The functions and regulation of glutathione S-transferases in plant. Annual Review of Plant Physiology and Plant Molecular Biology, 47, 127–158.

    Article  CAS  PubMed  Google Scholar 

  • Mauch, F., Mauch-Mani, B., & Boller, T. (1988). Antifungal hydrolases in pea tissue II. Inhibition of fungal growth by combinations of chitinase and beta-1,3-glucanase. Plant Physiology, 88, 936–942.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McGarry, R. C., Barron, Y. D., Carvalho, M. F., Hill, J. E., Gold, D., Cheung, E., Kraus, W. L., & Lazarowitz, S. G. (2003). A novel Arabidopsis acetyltransferase interacts with the geminivirus movement protein NSP. Plant Cell, 15, 1605–1618.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Milčevičová, R., Gosch, C., Halbwirth, H., Stich, K., Hanke, M., Peil, A., Flachowsky, H., Rozhon, W., Jonak, C., Oufir, M., Hausman, J. F., Matušiková, I., Fluch, S., & Wilhelm, E. (2010). Erwinia amylovora-induced defense mechanism of two apple species that differ in susceptibility to fire blight. Plant Science, 179, 60–67.

    Article  Google Scholar 

  • Money, T., Reader, S., Qu, I., Dunford, R., & Moore, G. (1995). AFLP based mRNA fingerprinting. Nucleic Acids Research, 24, 2616–2617.

    Article  Google Scholar 

  • Norelli, J. L. (2004). Fire blight. In R. M. Goodman (Ed.), Encyclopedia of plant and crop science (pp. 443–447). NY: Marcel Dekker, Inc.

    Google Scholar 

  • Norelli, J. L., Farrell, R. E., Bassett, C. L., Baldo, A. M., Lalli, D. A., Aldwinckle, H. S., & Wisniewski, M. E. (2009). Rapid transcriptional response of apple to fore blight disease revealed by cDNA suppression subtractive hybridization analysis. Tree Genetics & Genomes, 5, 27–40.

    Article  Google Scholar 

  • Park, D. H., Mirabella, R., Bronstein, P. A., Preston, G. M., Haring, M. A., Lim, C. K., Collmer, A., & Schuurink, R. C. (2010). Mutations in γ-aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. The Plant Journal, 64, 318–330.

    Article  CAS  PubMed  Google Scholar 

  • Parravicini, G., Gessler, C., Denance, C., Lassere-Zuber, P., Vergne, E., Brisset, M. N., Patocchi, A., Durel, C. E., & Brioggini, G. A. L. (2011). Identification of serine/threonine kinase and nucleotide-binding site–leucine-rich repeat (NBS-LRR) genes in the fire blight resistance quantitative trait locus of apple cultivar ‘Evereste’. Molecular Plant Pathology, 12, 493–505.

    Article  CAS  PubMed  Google Scholar 

  • Peng, H. Z., Lin, E. P., Sang, Q. L., Yao, S., Jin, Q. Y., Hua, X. Q., & Zhu, M. Y. (2007). Molecular cloning, expression analyses and primary evolution studies of REV- and TB1-like genes in bamboo. Tree Physiology, 27, 1273–1281.

    Article  CAS  PubMed  Google Scholar 

  • Pontais, I., de Bernonville, T. D., Paulin, J.-P., & Brisset, M.-N. (2008). A microarray approach to analyse transcriptional changes in apple after infection by Ervinia amylovora. Acta Horticulturae, 793, 187–188.

    CAS  Google Scholar 

  • Price, M. B., Jelesko, J., & Okumoto, S. (2012). Glutamate receptor homologs in plants: functions and evolutionary origins. Frontiers in Plant Science, 3, 235.

    Article  PubMed Central  PubMed  Google Scholar 

  • Rivera, E., Codina, J. C., Olea, F., de Vincente, A., & Perez-Garcia, A. (2002). Differential expression of β-1,3-glucanase in susceptible and resistant melon cultivars in response to infection by Sphaerotheca fusca. Physiological and Molecular Plant Pathology, 61, 257–265.

    Article  Google Scholar 

  • Robson, F., Costa, M. M., Hepworth, S. R., Vizir, I., Piñeiro, M., Reeves, P. H., Putterill, J., & Coupland, G. (2001). Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. The Plant Journal, 28, 619–631.

    Article  CAS  PubMed  Google Scholar 

  • Roxas, V. P., Smith, R. K., Allen, E. R., & Allen, R. D. (1997). Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nature Biotechnology, 15, 988–991.

    Article  CAS  PubMed  Google Scholar 

  • Ryugo, K., Okuse, I., & Fujii, Y. (1990). Correlation between fire blight resistance and phenolic levels in pears. Acta Horticulturae, 273, 335–338.

    Article  Google Scholar 

  • Sarowar, S., Zhao, Y., Soria-Guerra, R. E., Ali, S., Zheng, D., Wang, D., & Korban, S. S. (2011). Expression profiles of differentially regulated genes during the early stages of apple flower infection with Erwinia amylovora. Journal of Experimental Botany, 62, 4851–4861.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Siedow, J. N. (1991). Plant lipoxygenase: structure and function. Annual Review of Plant Physiology and Plant Molecular Biology, 42, 145–188.

    Article  CAS  Google Scholar 

  • Sobiczewski, P., Zurawicz, E., Berczynski, S., & Lewandowski, M. (2004). Terminal shoot susceptibility of new polish apple cultigens to fire blight. Folia Horticulturae, 16, 149–157.

    Google Scholar 

  • Sobiczewski, P., Żurawicz, E., Berczyński, S., Mikiciński, A., & Lewandowski, M. (2008). The importance of the type of Erwinia amylovora inoculum in screening of apple genotypes susceptibility to fire blight. Journal of Fruit and Ornamental Plant Researct, 16, 305–313.

    Google Scholar 

  • Sobiczewski, P., Peil, A., Mikicinski, A., Richter, K., Lewandowski, M., Zurawicz, E., & Kellerhals, M. (2015). Susceptibility of apple genotypes from European genetic resources to fire blight (Erwinia amylovora). European Journal of Plant Pathology, 141, 51–62.

    Article  Google Scholar 

  • Stein, M., Dittgen, J., Sánchez-Rodríguez, C., Hou, B. H., Molina, A., Schulze-Lefert, P., Lipka, V., & Somerville, S. (2006). Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to non-host resistance to inappropriate pathogens that enter by direct penetration. Plant Cell, 18, 731–746.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Swiderski, M. R., & Innes, R. W. (2001). The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. The Plant Journal, 26, 101–112.

    Article  CAS  PubMed  Google Scholar 

  • Taura, T., Siomi, M. C., & Siomi, H. (2005). The molecular mechanisms of mRNA export. In T. Tzfira & V. Citovsky (Eds.), Nuclear import and export in plants and animals (pp. 161–174). USA: Kluwer Academic/Plenum Publishers.

    Chapter  Google Scholar 

  • van der Zwet, T., & Beer, S. V. (1995). Fire blight – its nature, prevention and control. USDA Washington, Agriculture Information Bulletins, 631.

  • van der Zwet, T., & Keil, H. L. (1979). Fire blight, a bacterial disease of rosaceous plants. Washington, DC: USDA Agriculture Handbook. No. 510.

    Google Scholar 

  • Venisse, J. S., Gullner, G., & Brisset, M. N. (2001). Evidence for the involvement of an oxidative stress in the initiation of infection of pear by Erwinia amylovora. Plant Physiology, 125, 2164–2172.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Venisse, J. S., Malnoy, M., Faize, M., Paulin, J.-P., & Brisset, M. N. (2002). Modulation of defense responses of Malus spp. during compatible and incompatible interactions with Erwinia amylovora. Molecular Plant-Microbe Interactions, 15, 1204–1212.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Tang, C., Huang, X., Li, F., Chen, X., Zhang, G., Sun, Y., Han, D., & Kang, Z. (2012). Wheat BAX inhibitor-1 contributes to wheat resistance to Puccinia striiformis. Journal of Experimental Botany, 63, 4571–4584.

    Article  CAS  PubMed  Google Scholar 

  • Xu, L., Liu, Z.-Y., Zhang, K., Lu, Q., Liang, J., & Zhang, X.-Y. (2013). Characterization of the Pinus massoniana transcriptional response to Bursaphelenchus xylophilus infection using suppression subtractive hybridization. International Journal of Molecular Sciences, 14, 11356–11375.

    Article  PubMed Central  PubMed  Google Scholar 

  • Yang, Y., Fu, Z., Su, Y., Zhang, X., Li, G., Guo, J., Que, Y., & Xu, L. (2014). A cytosolic glucose-6-phosphate dehydrogenase gene, ScG6PDH, plays a positive role in response to various abiotic stresses in sugarcane. Scientific Reports. doi:10.1038/srep07090.

    Google Scholar 

  • Zhou, J., Loh, Y.-T., Bressan, R. A., & Martin, G. A. (1995). The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell, 83, 925–935.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, L., Cheung, M.-Y., Li, M.-W., Fu, Y., Sun, Z., Sun, S.-M., & Lam, H.-M. (2010). Rice hypersensitive induced reaction protein 1 (OsHIR1) associates with plasma membrane and triggers hypersensitive cell death. BMC Plant Biology, 10, 290–299.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zoeller, M., Stingl, N., Krischke, M., Fekete, A., Waller, F., Berger, S., & Mueller, M. J. (2012). Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiology, 160, 365–378.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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  1. Research Institute of Horticulture, Konstytucji 3 Maja 1/3, 96-100, Skierniewice, Poland

    Monika Markiewicz & Lech Michalczuk

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Markiewicz, M., Michalczuk, L. Molecular response of resistant and susceptible apple genotypes to Erwinia amylovora infection. Eur J Plant Pathol 143, 515–526 (2015). https://doi.org/10.1007/s10658-015-0704-x

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