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Phylogenetic analysis of PR genes in some pome fruit species with the emphasis on transcriptional analysis and ROS response under Erwinia amylovora inoculation in apple

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Abstract

Attempts were made to identify eight pathogenesis related (PR) genes (i.e., PR-1a, PR3-ch1, PR3-Ch2, PR3-Ch3, PR3-Ch4, PR3-Ch5, PR-5 and PR-8) from 27 genotypes of apple, quince and pear, which are induced in response to inoculation with the pathogen Erwinia amylovora, the causal agent of fire blight. Totally, 32 PR genes of different families were obtained, excepting PR3-Ch2 (amplified only in apple) and PR3-Ch4 (amplified only in apple and pear), the others were successfully amplified in all the genotypes of apple, quince and pear. Evolutionary, the genes of each family exhibited significant homology with each other, as the corresponded phylogenetic neighbor-joining-based dendrograms were taken into consideration. Meanwhile, according to the expression assay, it was deduced that the pathogen activity can significantly affect the expression levels of some selected PR genes of PR3-Ch2, PR3-Ch4, PR3-Ch5 and particularly Cat I in both resistant (MM-111) and semi-susceptible (MM-106) apple rootstocks. Lastly, it was concluded that the pathogen E. amylovora is able to stimulate ROS response, particularly using generation of hydrogen peroxide (H2O2) in both aforementioned apple rootstock.

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References

  • Abdollahi H, Rugini E, Ruzzi M, Muleo R (2004) In vitro system for studying the interaction between Erwinia amylovora and genotypes of pear. Plant Cell, Tissue Organ Cult 79:203–212

    Article  CAS  Google Scholar 

  • Azad MK, Nasiri J, Abdollahi H (2013) Genetic diversity of selected iranian quinces using SSRs from apples and pears. Bioch genet 51:426–442

    Article  Google Scholar 

  • Baldo A, Norelli JL, Farrell RE, Bassett CL, Aldwinckle HS, Malnoy M (2010) Identification of genes differentially expressed during interaction of resistant and susceptible apple cultivars (Malus × domestica) with Erwinia amylovora. BMC Plant Biol 10:1

    Article  PubMed Central  PubMed  Google Scholar 

  • Bonasera JM, Kim JF, Beer SV (2006) PR genes of apple: identification and expression in response to elicitors and inoculation with Erwinia amylovora. BMC Plant Biol 6:23

    Article  PubMed Central  PubMed  Google Scholar 

  • Bonn WG, van der Zwet T (2000) Distribution and economic importance of fire blight. In: Vanneste JL (ed) Fire blight the disease and its causative agent, Erwinia amylovora. CAB International, Wallingford

    Google Scholar 

  • Channuntapipat C, Sedgley M, Collins G (2001) Sequences of the cDNAs and genomic DNAs encoding the S1, S7, S8, and Sf alleles from almond, Prunus dulcis. Theor Appl Genet 103:1115–1122

    Article  CAS  Google Scholar 

  • Cornelis GR, van Gijsegem F (2000) Assembly and function of type III secretory systems. Annu Rev Microbiol 54:735–774

    Article  CAS  PubMed  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1:19–21

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ghahremani Z, Abdollahi H (2010) Induction of systemic acquired resistance by salicylic acid against fire blight in apple and pear. In: XII international workshop on fire blight 896, pp 155–163

  • Grant M, Lamb C (2006) Systemic immunity. Curr Opin Plant Biol 9:414–420

    Article  CAS  PubMed  Google Scholar 

  • Heyens K,  Valcke R (2006) Flourescence imaging of the infection pattern of apple leaves with erwinia amylovora. Acta hort 704:69–71

    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 53:493–511

    Article  CAS  PubMed  Google Scholar 

  • Jensen PJ, Makalowska I, Altman N, Fazio G, Praul C, Maximova SN, Crassweller RM, Travis JW, McNellis TW (2010) Rootstock-regulated gene expression patterns in apple tree scions. Tree Genet Genomes 6:57–72

    Article  Google Scholar 

  • Jensen PJ, Halbrendt N, Fazio G, Makalowska I, Altman N, Praul C, Maximova SN, Ngugi HK, Crassweller RM, Travis JW, McNellis TW (2012) Rootstock-regulated gene expression patterns associated with fire blight resistance in apple. BMC Genom 13:9

    Article  CAS  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Biol 48:251–275

    Article  CAS  Google Scholar 

  • Liu Z, Du L, Wan B (2005) Pathogenesis-related proteins in higher plants. Nat Prod Res Dev 17:229–234

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Malnoy M, Martens S, Norelli JL, Barny MA, Sundin GW, Smits TH, Duffy B (2012) Fire blight: applied genomic insights of the pathogen and host. Annu Rev Phytopathol 50:475–494

    Article  CAS  PubMed  Google Scholar 

  • Mayer M, Oberhuber C, Loncaric I, Heissenberger B, Keck M, Scheiner O, Hoffmann-Sommergruber K (2011) Fire blight (Erwinia amylovora) affects Mal d 1-related allergenicity in apple. Eur J Plant Pathol 131:1–7

    Article  CAS  Google Scholar 

  • McManus PS, Stockwell VO, Sundin GW, Jones AL (2002) Antibiotic use in plant agriculture. Annu Rev Phytopathol 40:443–465

    Article  CAS  PubMed  Google Scholar 

  • Moradi A, Nasiri J, Abdollahi H, Almasi M (2012) Development and evaluation of a loop-mediated isothermal amplification assay for detection of Erwinia amylovora based on chromosomal DNA. Eur J Plant Pathol 133:609–620

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Google Scholar 

  • Norelli JL, Farrell RE Jr, Bassett CL, Baldo AM, Lalli DA, Aldwinckle HS, Wisniewski ME (2009) Rapid transcriptional response of apple to fire blight disease revealed by cDNA suppression subtractive hybridization analysis. Tree Genet Genomes 5:27–40

    Article  Google Scholar 

  • Pester D, Milčevičová R, Schaffer J, Wilhelm E, Blümel S (2012) Erwinia amylovora expresses fast and simultaneously hrp/dsp virulence genes during flower infection on apple trees. PLoS ONE 7:e32583

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sarowar S, Kim YJ, Kim EN, Kim KD, Hwang BK, Islam R, Shin JS (2005) Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Rep 24:216–224

    Article  CAS  PubMed  Google Scholar 

  • Sarowar S, Zhao Y, Soria-Guerra RE, Ali S, Zheng D, Wang D, Korban SS (2011) Expression profiles of differentially regulated genes during the early stages of apple flower infection with Erwinia amylovora. J Exp Bot 62:4851–4861

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sklodowska M, Gajewska E, Kuzniak E, Wielanek M, Mikicinski A, Sobiczewski P (2011) Antioxidant profile and polyphenol oxidase activities in apple leaves after Erwinia amylovora infection and pretreatment with a benzothiadiazole-type resistance inducer (BTH). J Phytopathol 159:495–504

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants, H2O2 accumulation in papillae and hypersensitive response during barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Van Loon LC (1997) Induced resistance in plants and the role of pathogenesis-related proteins. Eur J Plant Pathol 103:753–765

    Article  Google Scholar 

  • Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR1 type proteins. Physiol Mol Plant Pathol 55:85–97

    Article  Google Scholar 

  • Venisse JS, Gullner G, Brisset MN (2001) Evidence for the involvement of an oxidative stress in the initiation of infection of pear by Erwinia amylovora. Plant Physiol 125:2164–2172

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Venisse JS, Malnoy M, Faize M, Paulin JP, Brisset MN (2002) Modulation of defense responses of Malus (spp. during compatible and incompatible interactions with Erwinia amylovora. Mol Plant Microbe Interact 15:1204–1212

    Article  CAS  PubMed  Google Scholar 

  • Vrancken K, Schoofs H, Deckers T, Valcke R (2012) Real time qPCR expression analysis of some stress related genes in leaf tissue of Pyrus communis cv. Conference after infection with Erwinia amylovora. Trees Struct Funct 26:67–73

    Article  CAS  Google Scholar 

  • Vrancken K, Holtappels M, Schoofs H, Deckers T, Valcke R (2013) Pathogenicity and infection strategies of the fire blight pathogen Erwinia amylovora in Rosaceae: state of the art. Microbiology 159:823–832

    Article  CAS  PubMed  Google Scholar 

  • Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Metraux JP, Ryals JA (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085–1094

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Author contributions

MH participated in performing the experimental work, molecular section. MRS participated in carrying out the Real time section of the work and assisted in manuscript revising. JN performed all the bioinformatics and data analysis, provided the manuscript draft and revised its final version. HA designed and supervised molecular section of the study, revised the manuscript and provided helpful discussions. MG participated in performing the experimental work, Reactive oxygen species (ROS) assay section. All the authors read and approved final version of the manuscript.

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Correspondence to Jaber Nasiri or Hamid Abdollahi.

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Hassani, M., Salami, S.A., Nasiri, J. et al. Phylogenetic analysis of PR genes in some pome fruit species with the emphasis on transcriptional analysis and ROS response under Erwinia amylovora inoculation in apple. Genetica 144, 9–22 (2016). https://doi.org/10.1007/s10709-015-9874-x

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  • DOI: https://doi.org/10.1007/s10709-015-9874-x

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