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Comparative iTRAQ proteomic profiling of susceptible and resistant apple cultivars infected by Alternaria alternata apple pathotype

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Abstract

Alternaria blotch, caused by the Alternaria alternata apple pathotype (A. alternata AP), is one of serious pathogen of apples. In order to better understand the molecular mechanisms that underlie the defense responses of apple resistance to Alternaria blotch disease, a comparative proteomic approach was applied to analyze of susceptible and resistant apple cultivars response to A. alternata AP infection using iTRAQ (isobaric tags for relative and absolute quantitation) technique. A total of 4225 proteins were identified, and 1226 proteins were quantified. Of the quantified proteins, 280 and 34 expressed differentially (fold change >1.5) at 72 h post-infection (HPI) in the susceptible (“Starking Delicious”) and the resistant (“Jonathan”) apple cultivars, respectively, compared with mock-inoculated controls. Most of the differentially expressed proteins (DEPs) were associated with host plant resistance to pathogens, including signal transduction, stress and defense, and photosynthesis metabolism. Among these proteins, beta-1,3-glucanase(PR2), thaumatin-like protein (PR5), and lipoxygenase were found in both susceptible and resistant hosts. However, endochitinase and (+)-neomenthol dehydrogenase were only detected in the resistant cultivar and increased in abundance in response to the pathogen attack. To study the role of pathogenesis-related (PR) proteins in the early infection process, their expressions at 6, 18, 36, and 72 HPI were analyzed by western blot. It showed that PR5 were accumulated to a high level at 6 HPI in “Jonathan,” while cannot be detected in “Starking Delicious” until 18 HPI. The above results suggested that endochitinase and (+)-neomenthol dehydrogenase, as well as PR5 which exerts function at early stage, play important roles in apple plant against A. alternata AP infestation.

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References

  • Abdallah NA, Shah D, Abbas D, Madkour M (2010) Stable integration and expression of a plant defensin in tomato confers resistance to fusarium wilt. GM Crops 1:344–350. doi:10.4161/gmcr.1.5.15091

    Article  PubMed  Google Scholar 

  • Abe K, Iwanami H, Kotoda N, Moriya S (2010) Evaluation of apple genotypes and Malus species for resistance to Alternaria blotch caused by Alternaria alternata apple pathotype using detached-leaf method. Plant Breed 129:208–218. doi:10.1111/j.1439-0523.2009.01672.x

    Article  CAS  Google Scholar 

  • Acharya K, Pal AK, Gulati A, Kumar S, Singh AK, Ahuja PS (2013) Overexpression of Camellia sinensis thaumatin-like protein, CsTLP in potato confers enhanced resistance to macrophomina phaseolina and Phytophthora infestans infection. Mol Biotechnol 54:609–622. doi:10.1007/s12033-012-9603-y

    Article  CAS  PubMed  Google Scholar 

  • Aggarwal K, Choe LH, Lee KH (2006) Shotgun proteomics using the iTRAQ isobaric tags. Briefings in Functional Genomics & Proteomics 5:112–120. doi:10.1093/bfgp/ell018

    Article  CAS  Google Scholar 

  • Bannenberg G, Martínez M, Hamberg M, Castresana C (2009) Diversity of the enzymatic activity in the lipoxygenase gene family of Arabidopsis thaliana. Lipids 44:85–95. doi:10.1007/s11745-008-3245-7

    Article  CAS  PubMed  Google Scholar 

  • Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant pathogen interactions. J Exp Bot 58:4019–4026. doi:10.1093/jxb/erm298

    Article  CAS  PubMed  Google Scholar 

  • Berger S, Papadopoulos M, Schreiber U, Kaiser W, Roitsch T (2004) Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato. Physiol Plant 122:419–428. doi:10.1111/j.1399-3054.2004.00433.x

    Article  CAS  Google Scholar 

  • Borges LL, Santana FA, Castro ISL, Arruda KMA, de Oliveira Ramos HJ, Moreira MA, de Barros EG (2013) Differentially expressed proteins during an incompatible interaction between common bean and the fungus Pseudocercospora griseola. Mol Breed 32:933–942. doi:10.1007/s11032-013-9922-0

    Article  CAS  Google Scholar 

  • Buron-Moles G, Wisniewski M, Viñas I, Teixidó N, Usall J, Droby S, Torres R (2015) Characterizing the proteome and oxi-proteome of apple in response to a host (Penicillium expansum) and a non-host (Penicillium digitatum) pathogen. J Proteome 114:136–151. doi:10.1016/j.jprot.2014.11.007

    Article  CAS  Google Scholar 

  • Carter C, Pan S, Zouhar J, Avila EL, Girke T, Raikhel NV (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16:3285–3303. doi:10.1105/tpc.104.027078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Harmon AC (2006) Advances in plant proteomics. Proteomics 6:5504–5516. doi:10.1002/pmic.200600143

    Article  CAS  PubMed  Google Scholar 

  • Choi HW, Lee BG, Kim NH, Park Y, Lim CW, Song HK, Hwang BK (2008) A role for a menthone reductase in resistance against microbial pathogens in plants. Plant Physiol 148:383–401. doi:10.1104/pp.108.119461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci 98:13454–13459. doi:10.1073/pnas.231178298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dietz K (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107. doi:10.1146/annurev.arplant.54.031902.134934

    Article  CAS  PubMed  Google Scholar 

  • Dietz K, Jacob S, Oelze M, Laxa M, Tognetti V, de Miranda SMN, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57:1697–1709. doi:10.1093/jxb/erj160

    Article  CAS  PubMed  Google Scholar 

  • Fang X, Jost R, Finnegan PM, Barbetti MJ (2013) Comparative proteome analysis of the strawberry-Fusarium oxysporum f. sp. fragariae pathosystem reveals early activation of defense responses as a crucial determinant of host resistance. J Proteome Res 12:1772–1788. doi:10.1021/pr301117a

    Article  CAS  PubMed  Google Scholar 

  • Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz KJ (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J Biol Chem 280(13):12168–12180. doi:10.1074/jbc.M413189200

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Zhang H, Mandal SN, Wang C, Chen C, Ji W (2016) Quantitative proteomics reveals the central changes of wheat in response to powdery mildew. J Proteome 130:108–119. doi:10.1016/j.jprot.2015.09.006

    Article  CAS  Google Scholar 

  • Grover A (2012) Plant chitinases: genetic diversity and physiological roles. Crit Rev Plant Sci 31:57–73. doi:10.1080/07352689.2011.616043

    Article  CAS  Google Scholar 

  • Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720–1730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harimoto Y, Hatta R, Kodama M, Yamamoto M, Otani H, Tsuge T (2007) Expression profiles of genes encoded by the supernumerary chromosome controlling AM-toxin biosynthesis and pathogenicity in the apple pathotype of Alternaria alternata. Mol Plant-Microbe Interact 20:1463–1476. doi:10.1094/MPMI-20-12-1463

    Article  CAS  PubMed  Google Scholar 

  • Harimoto Y, Tanaka T, Kodama M, Yamamoto M, Otani H, Tsuge T (2008) Multiple copies of AMT2 are prerequisite for the apple pathotype of Alternaria alternata to produce enough AM-toxin for expressing pathogenicity. J Gen Plant Pathol 74:222–229. doi:10.1007/s10327-008-0089-1

    Article  CAS  Google Scholar 

  • Harteveld DOC, Akinsanmi OA, Becker MF, Drenth A (2014) Comparative fitness of Alternaria species causing leaf blotch and fruit spot of apple in Australia. Australas Plant Pathol 43:495–501. doi:10.1007/s13313-014-0297-4

    Article  CAS  Google Scholar 

  • Havanapan P, Bourchookarn A, Ketterman AJ, Krittanai C (2016) Comparative proteome analysis of rubber latex serum from pathogenic fungi tolerant and susceptible rubber tree (Hevea brasiliensis). J Proteome 131:82–92. doi:10.1016/j.jprot.2015.10.014

    Article  CAS  Google Scholar 

  • Herbers K, Takahata Y, Melzer M, Mock HP, Hajirezaei M, Sonnewald U (2000) Regulation of carbohydrate partitioning during the interaction of potato virus Y with tobacco. Mol Plant Pathol 1:51–59. doi:10.1046/j.1364-3703.2000.00007.x

    Article  CAS  PubMed  Google Scholar 

  • Hou M, Xu W, Bai H, Liu Y, Li L, Liu L, Liu B, Liu G (2012) Characteristic expression of rice pathogenesis-related proteins in rice leaves during interactions with Xanthomonas oryzae pv. oryzae. Plant Cell Rep 31:895–904. doi:10.1007/s00299-011-1210-z

    Article  CAS  PubMed  Google Scholar 

  • Jarvis P, López-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids. Nat Rev Mol Cell Biol 14:787–802. doi:10.1038/nrm3702

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Yang L, Qi Y, Lu Y, Huang Z, Chen L (2015) Root iTRAQ protein profile analysis of two Citrus species differing in aluminum-tolerance in response to long-term aluminum-toxicity. BMC Genomics 16. doi:10.1186/s12864-015-2133-9

  • Johnson RD, Johnson L, Itoh Y, Kodama M, Otani H, Kohmoto K (2000) Cloning and characterization of a cyclic peptide synthetase gene from Alternaria alternata apple pathotype whose product is involved in AM-toxin synthesis and pathogenicity. Mol Plant-Microbe Interact 13:742–753. doi:10.1094/MPMI.2000.13.7.742

    Article  CAS  PubMed  Google Scholar 

  • Jones AME, Thomas V, Truman B, Lilley K, Mansfield J, Grant M (2004) Specific changes in the Arabidopsis proteome in response to bacterial challenge: differentiating basal and R-gene mediated resistance. Phytochemistry 65:1805–1816. doi:10.1016/j.phytochem.2004.04.005

    Article  CAS  PubMed  Google Scholar 

  • Joo G (2005) Purification and characterization of an extracellular chitinase from the antifungal biocontrol agent Streptomyces halstedii. Biotechnol Lett 27:1483–1486. doi:10.1007/s10529-005-1315-y

    Article  CAS  PubMed  Google Scholar 

  • Jung K (2007) Growth inhibition effect of pyroligneous acid on pathogenic fungus, Alternaria mali, the agent of alternaria blotch of apple. Biotechnol Bioprocess Eng 12:318–322. doi:10.1007/BF02931111

    Article  CAS  Google Scholar 

  • Kallberg Y, Oppermann U, Jörnvall H, Persson B (2002) Short-chain dehydrogenases/reductases (SDRs)—coenzyme-based functional assignments in completed genomes. Eur J Biochem 269:4409–4417. doi:10.1046/j.1432-1033.2002.03130.x

    Article  CAS  PubMed  Google Scholar 

  • Kaur P, Jost R, Sivasithamparam K, Barbetti MJ (2011) Proteome analysis of the Albugo candida-Brassica juncea pathosystem reveals that the timing of the expression of defence-related genes is a crucial determinant of pathogenesis. J Exp Bot 62:1285–1298. doi:10.1093/jxb/erq365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosová K, Vítámvás P, Prášil IT, Renaut J (2011) Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J Proteome 74:1301–1322. doi:10.1016/j.jprot.2011.02.006

    Article  Google Scholar 

  • Lee D, Back C, Win NKK, Choi K, Kim K, Kang I, Choi C, Yoon T, Uhm JY, Jung H (2011) Biological characterization of Marssonina coronaria associated with apple blotch disease. Mycobiology 39:200–205. doi:10.5941/MYCO.2011.39.3.200

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Y, Aldwinckle HS, Sutton T, Tsuge T, Kang G, Cong P, Cheng ZM (2013) Interactions of apple and the Alternaria alternata apple pathotype. Crit Rev Plant Sci 32:141–150. doi:10.1080/07352689.2012.722026

    Article  Google Scholar 

  • Li Y, Hirst PM, Wan Y, Liu Y, Zhou Q, Gao H, Guo Y, Zhao Z, Wang L, Han M (2012) Resistance to Marssonina coronaria and Alternaria alternata apple pathotype in the major apple cultivars and rootstocks used in China. Hortscience 47:1241–1244

    Google Scholar 

  • Li ZT, Dhekney SA, Gray DJ (2011) PR-1 gene family of grapevine: a uniquely duplicated PR-1 gene from a Vitis interspecific hybrid confers high level resistance to bacterial disease in transgenic tobacco. Plant Cell Rep 30:1–11. doi:10.1007/s00299-010-0934-5

    Article  PubMed  Google Scholar 

  • Liu D, He X, Li W, Chen C, Ge F (2012) Molecular cloning of a thaumatin-like protein gene from Pyrus pyrifolia and overexpression of this gene in tobacco increased resistance to pathogenic fungi. Plant Cell, Tissue and Organ Culture (PCTOC) 111:29–39. doi:10.1007/s11240-012-0167-0

    Article  CAS  Google Scholar 

  • Mazzeo MF, Cacace G, Ferriello F, Puopolo G, Zoina A, Ercolano MR, Siciliano RA (2014) Proteomic investigation of response to forl infection in tomato roots. Plant Physiol Biochem 74:42–49. doi:10.1016/j.plaphy.2013.10.031

    Article  CAS  PubMed  Google Scholar 

  • Mehta A, Brasileiro AC, Souza DS, Romano E, Campos MA, Grossi-de-Sa MF, Silva MS, Franco OL, Fragoso RR, Bevitori R, Rocha TL (2008) Plant-pathogen interactions: what is proteomics telling us? FEBS J 275:3731–3746. doi:10.1111/j.1742-4658.2008.06528.x

    Article  CAS  PubMed  Google Scholar 

  • Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002) H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J 29:257–268. doi:10.1046/j.0960-7412.2001.01215.x

    Article  CAS  PubMed  Google Scholar 

  • Munhoz CF, Santos AA, Arenhart RA, Santini L, Monteiro Vitorello CB, Vieira M (2015) Analysis of plant gene expression during passion fruit-Xanthomonas axonopodis interaction implicates lipoxygenase 2 in host defence. Ann Appl Biol 167:135–155. doi:10.1111/aab.12215

    Article  CAS  Google Scholar 

  • Oide S, Bejai S, Staal J, Guan N, Kaliff M, Dixelius C (2013) A novel role of PR2 in abscisic acid (ABA) mediated, pathogen-induced callose deposition in Arabidopsis thaliana. New Phytol 200:1187–1199. doi:10.1111/nph.12436

    Article  CAS  PubMed  Google Scholar 

  • Otani H (2000) Host recognition by plant pathogens and role of host-specific toxins. J Gen Plant Pathol 66:278–280

    Article  Google Scholar 

  • Petriccione M, Salzano AM, Di Cecco I, Scaloni A, Scortichini M (2014) Proteomic analysis of the Actinidia deliciosa leaf apoplast during biotrophic colonization by Pseudomonas syringae pv. actinidiae. J Proteome 101:43–62. doi:10.1016/j.jprot.2014.01.030

    Article  CAS  Google Scholar 

  • Roberts JW (1924) Morphological characters of Alternaria mali Roberts. J Agric Res 27:699–712

    Google Scholar 

  • Rouhier N, Gelhaye E, Gualberto JM, Jordy MN, De Fay E, Hirasawa M, Duplessis S, Lemaire SD, Frey P, Martin F, Manieri W, Knaff DB, Jacquot JP (2004) Poplar peroxiredoxin Q. A thioredoxin-linked chloroplast antioxidant functional in pathogen defense. Plant Physiol 134:1027–1038. doi:10.1104/pp.103.035865

  • Rouhier N, Jacquot J (2002) Plant peroxiredoxins: alternative hydroperoxide scavenging enzymes. Photosynth Res 74:259–268. doi:10.1023/A:1021218932260

    Article  CAS  PubMed  Google Scholar 

  • Safavi K, Zareie R, Tabatabaei BES (2012) Constitutive expression of thaumatin-like protein (TLP-3) in transgenic tobacco plants leads to enhance resistance to Alternaria alternata. Arch Phytopathol Plant Protect 45:161–169. doi:10.1080/03235408.2010.507947

    Article  CAS  Google Scholar 

  • Sakamoto Y, Nakade K, Konno N (2011) Endo-beta-1,3-glucanase GLU1, from the fruiting body of Lentinula edodes, belongs to a new glycoside hydrolase family. Appl Environ Microbiol 77:8350–8354. doi:10.1128/AEM.05581-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep 32:1085–1098. doi:10.1007/s00299-013-1441-2

    Article  CAS  PubMed  Google Scholar 

  • Schaller MD (2001) Biochemical signals and biological responses elicited by the focal adhesion kinase. Biochim Biophys Acta 1540:1–21

    Article  CAS  PubMed  Google Scholar 

  • Sofi TA, Beig MA, Dar GH, Ahmad M, Hamid A, Ahangar FA, Padder BA, Shah MD (2013) Cultural, morphological, pathogenic and molecular characterization of Alternaria mali associated with alternaria leaf blotch of apple. Afr J Biotechnol 12:370–381. doi:10.5897/AJB12.2735

    Article  Google Scholar 

  • Sutton TB (1991) Identification and distribution of Alternaria mali on apples in North Carolina and susceptibility of different varieties of apples to Alternaria blotch. Plant Dis 75:1045–1048

    Article  Google Scholar 

  • Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270. doi:10.1016/j.tplants.2012.02.010

    Article  CAS  PubMed  Google Scholar 

  • Van Loon LC, Rep M, Pieterse C (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162. doi:10.1146/annurev.phyto.44.070505.143425

    Article  CAS  PubMed  Google Scholar 

  • Vidigal P, Carvalho R, Amâncio S, Carvalho L (2013) Peroxiredoxins are involved in two independent signalling pathways in the abiotic stress protection in Vitis vinifera. Biol Plant 57(4):483–496. doi:10.1007/s10535-013-0346-9

    Article  Google Scholar 

  • Vidhyasekaran, P (2007). Fungal pathogenesis in plants and crops: molecular biology and host defense mechanisms. CRC Press

  • Vizcaíno JA, Csordas A, del-Toro N, Dianes JA, Griss J, Lavidas I, Mayer G, Perez-Riverol Y, Reisinger F, Ternent T, Xu QW, Wang R, Hermjakob H (2016). 2016 update of the PRIDE database and related tools. Nucleic Acids Res 44(D1): D447-D456 (PubMed ID: 26527722)

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058. doi:10.1093/aob/mct067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waters MT, Langdale JA (2009) The making of a chloroplast. EMBO J 28:2861–2873. doi:10.1038/emboj.2009.264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Li M, Jiao P, Tao H, Wei N, Ma F, Zhang J (2015) Dynamic transcription profiles of "Qinguan" apple (Malus × domestica) leaves in response to Marssonina coronaria inoculation. Front Plant Sci 6. doi:10.3389/fpls.2015.00842

  • Zhang S, Chen W, Xin L, Gao Z, Hou Y, Yu X, Zhang Z, Qu S (2014) Genomic variants of genes associated with three horticultural traits in apple revealed by genome re-sequencing. Horticulture Research 1:14045. doi:10.1038/hortres.2014.45

    Article  PubMed  PubMed Central  Google Scholar 

  • Zieske LR (2006) A perspective on the use of iTRAQ™ reagent technology for protein complex and profiling studies. J Exp Bot 57:1501–1508. doi:10.1093/jxb/erj168

    Article  CAS  PubMed  Google Scholar 

  • Zoeller M, Stingl N, Krischke M, Fekete A, Waller F, Berger S, Mueller MJ (2012) Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiol 160:365–378. doi:10.1104/pp.112.202846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the National Science Foundation of China (31171935) and the Fundamental Research Funds for the Central Universities (KYZ201310). We are also grateful to Prof. Guo Yunzhong in Northwest A&F University, China, for providing the strain of Alternaria alternata apple pathotype.

Data Archiving Statement

The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE (Vizcaíno et al. 2016) partner repository with the dataset identifier PXD005406 and 10.6019/PXD005406.”

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  1. Department of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    Weichen Ni, Longming Zhu, Renhe Sha, Jianmin Tao, Binhua Cai & Sanhong Wang

  2. National Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, 210095, China

    Longming Zhu

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  1. Weichen Ni
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Correspondence to Sanhong Wang.

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Communicated by D. Chagné

Electronic supplementary material

ESM 1 Supporting Information Figure S1. Data reproducibility reflected by Pearson correlation coefficients. Pair-wise Pearson correlation coefficient of all 12 samples (three replicates × four conditions) presented in red-white-green heat map format. Color scale as shown, generated with R script

(DOC 45 kb)

ESM 2 Supporting Information Excel S1. Proteins identified and quantified in the susceptible and resistant apple leaves infected by A. alternata AP

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ESM 3 Supporting Information Excel S2. KEGG_pathway_annotation of differential expression proteins

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ESM 4 Supporting Information Excel S3. Subcellular location of the identified protein

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ESM 5 Supporting Information Excel S4. Proteins detected specifically differential expression in the susceptible variety

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ESM 6 Supporting Information Excel S5. The differentially expressed proteins detected both in the resistant and susceptible cultivars

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Ni, W., Zhu, L., Sha, R. et al. Comparative iTRAQ proteomic profiling of susceptible and resistant apple cultivars infected by Alternaria alternata apple pathotype. Tree Genetics & Genomes 13, 23 (2017). https://doi.org/10.1007/s11295-017-1104-5

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