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Genome-wide annotation and expression responses to biotic stresses of the WALL-ASSOCIATED KINASE - RECEPTOR-LIKE KINASE (WAK-RLK) gene family in Apple (Malus domestica)

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Abstract

The WALL ASSOCIATED-KINASE - RECETOR-LIKE KINASE (WAK-RLK) gene family has been reported to act as a sensor for disease. Apple (Malus domestica) can be affected by multiple biotic stresses, such as fungal diseases from Valsa mali (Vm), Alternariaalternata Apple Pathotype (AaAP), and Pythium ultimum (Pu). However, there has been no report of WAK-RLK genes involved in apple biotic stress response. In this paper, we performed a comprehensive study including genome-wide annotation, characterization and gene expression analysis of WAK-RLKs in apple (MdWAK-RLKs). We found 44 members based on structural domain identification. The number of amino acids, molecular weight, and theoretical pI of these identified members ranged from 302 to 998, 33.63 to 110.35 kD, and 5.1 to 9.26, respectively. Members of the family were anchored to 16 out of 17 chromosomes and were classified into six phylogenetic groups. We found two phylogenetic groups specific to the apple genome. Synteny analysis revealed that 11 gene pairs arose from segmental duplications and 7 gene clusters resulted from tandem duplications. Cis-elements in the promoter region of MdWAK-RLKs were found mainly in response to circadian rhythm, hormones, and multiple stresses. The large number of members that showed high expression in multiple tissues and differential expressed in response to stress revealed that the different functional roles of MdWAK-RLKs under physiological or pathological conditions. Several genes, such as MDP0000278283, MDP0000153539, MDP0000170906, and MDP0000251865, were significantly influenced by multiple diseases. This study provides new insights into the potential function of WAK-RLKs in Malus and in Rosaceae and its contribution to disease resistance.

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Abbreviations

AaAP:

Alternaria alternata Apple Pathotype

RLK:

Receptor Like Kinase

WAK-RLKs :

The WALL-ASSOCIATED-KINASE - RECETOR-LIKE KINASE

EGF:

Epidermal Growth Factor

OGs:

Oligogalacturonides

GDR:

Genome Database of Rosaceae species

NCBI:

The National Center for Biotechnology Information

TAIR:

The Arabidopsis Information Resources

MdWAK-RLKs :

Malus domestica WAK-RLKs

Pu :

Pythium ultimum

qRT-PCR:

quantitative Reverse-Transcription-Polymerase Chain Reaction

Vm :

Valsa mali

References

  • Abe, K., Iwanami, H., Kotoda, N., Moriya, S., & Takahashi, 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 Breeding, 129(2), 208–218.

    Article  CAS  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), 1–10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bassett, C. L., Baldo, A. M., Moore, J. T., Jenkins, R. M., Soffe, D. S., Wisniewski, M. E., Norelli, J. L., & Jr, R. E. F. (2014). Genes responding to water deficit in apple (malus x domestica borkh.) roots. BMC Plant Biology,14(1), 182.

  • Benschop, J. J., Mohammed, S., O'Flaherty, M., Heck, A. J., Slijper, M., & Menke, F. L. (2007). Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Molecular & Cellular Proteomics, 6(7), 1198–1214.

    Article  CAS  Google Scholar 

  • Brutus, A., Sicilia, F., Macone, A., Cervone, F., & De Lorenzo, G. (2010). A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proceedings of the National Academy of Sciences of the United States of America, 107(20), 9452–9457.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caillaud, M. C., Wirthmueller, L., Sklenar, J., Findlay, K., Piquerez, S. J., Jones, A. M., Robatzek, S., Jones, J. D. G., & Faulkner, C. (2014). The plasmodesmal protein PDLP1 localises to haustoria-associated membranes during downy mildew infection and regulates callose deposition. PLoS Pathogens, 10, e1004496.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Celton, J. M., Gaillard, S., Bruneau, M., Pelletier, S., Aubourg, S., Martin-Magniette, M. L., Navarro, L., Laurens, F., & Renou, J. P. (2014). Widespread anti-sense transcription in apple is correlated with siRNA production and indicates a large potential for transcriptional and/or post-transcriptional control. New Phytologist, 203(1), 287–299.

    Article  CAS  PubMed  Google Scholar 

  • de Oliveira, L. F. V., Christoff, A. P., de Lima, J. C., de Ross, B. C. F., Sachetto-Martins, G., Margis-Pinheiro, M., & Margis, R. (2014). The Wall-associated Kinase gene family in rice genomes. Plant Science, 229(229), 181–192.

  • Depuydt, S., & Hardtke, C. S. (2011). Hormone signalling crosstalk in plant growth regulation. Current Biology, 21(9), R365–R373.

    Article  CAS  PubMed  Google Scholar 

  • Diener, A. C., & Ausubel, F. M. (2005). Resistance to fusarium oxysproum 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics, 171(1), 305–321.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn, R.D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R.Y., Eddy, S.R., Heger, A., Hetherington, K., Holm, L., Mistry, J., Sonnhammer, E.L.L., Tate, J., & Punta, M. (2014). Pfam: the protein families database. Nucleic acids research, 42(D1), 222–230.

  • Giorno, F., Guerriero, G., Baric, S., & Mariani, C. (2012). Heat shock transcriptional factors in Malus domestica: identification, classification and expression analysis. BMC Genomics,13, 639

  • Gendron, J. M., & Wang, Z. Y. (2007). Multiple mechanisms modulate brassinosteroid signaling. Current Opinion in Plant Biology, 10(5), 436–441.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanada, K., Zou, C., Lehti-Shiu, M. D., Shinozaki, K., & Shiu, S. H. (2008). Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiology, 148(2), 993–1003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou, X., Tong, H., Selby, J., DeWitt, J., Peng, X., & He, Z. H. (2005). Involvement of a cell wall-associated kinase, WAKL4, in Arabidopsis mineral responses. Plant Physiology, 139(4), 1704–1716.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu, B., Jin, J., Guo, A. Y., Zhang, H., Luo, J., Gao, G. 2015. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics, 31(8), 1296–1297.

  • Hurni, S., Scheuermann, D., Krattinger, S. G., Kessel, B., Wicker, T., Herren, G., Fitze, M. N., Breen, J., Presterl, T., Ouzunova, M., & Keller, B. (2015). The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase. Proceedings of the National Academy of Sciences of the United States of America, 112(28), 8780–8785.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamber, T., Buchmann, J. P., Pothier, J. F., Smits, T. H., Wicker, T., & Duffy, B. (2016). Fire blight disease reactome: RNA-seq transcriptional profile of apple host plant defense responses to Erwinia amylovora pathogen infection. Scientific Reports, 6.

  • Kaur, R., Singh, K., & Singh, J. (2013). A root-specific wall-associated kinase gene, HvWAK1, regulates root growth and is highly divergent in barley and other cereals. Functional & Integrative Genomics, 13(2), 167–177.

    Article  CAS  Google Scholar 

  • Kohorn, B. D. (2001). WAKs; cell wall associated kinases. Current Opinion in Cell Biology, 13(5), 529–533.

    Article  CAS  PubMed  Google Scholar 

  • Kohorn, B. D., & Kohorn, S. L. (2012). The cell wall-associated kinases, WAKs, as pectin receptors. Frontiers in Plant Science, 3, 88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohorn, B. D., Kobayashi, M., Johansen, S., Riese, J., Huang, L. F., Koch, K., Fu, S., Dotson, A., & Byers, N. (2006). An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. The Plant Journal, 46(2), 307–316.

    Article  CAS  PubMed  Google Scholar 

  • Lally, D., Ingmire, P., Tong, H. Y., & He, Z. H. (2001). Antisense expression of a cell wall–associated protein kinase, WAK4, inhibits cell elongation and alters morphology. The Plant Cell, 13(6), 1317–1332.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., Higgins, D. G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23(21), 2947–2948

  • Lehti-Shiu, M. D., Zou, C., & Shiu, S. H. (2012). Origin, diversity, expansion history, and functional evolution of the plant Receptor-Like Kinase/Pelle family. In Receptor-Like Kinases in Plants (pp. 1–22). Berlin Heidelberg: Springer.

    Google Scholar 

  • Leisso, R., Leisso, R., & Mazzola, M. (2016, December). Apple replant disease and the-omics: interaction of apple rootstock metabolome and the soil microbiome. In American Phytopathological Society Annual Meeting (Vol. 106, p. S4).

    Google Scholar 

  • Lescot, M., Déhais, P., Thijs, G., Marchal, K., Moreau, Y., Peer, Y. V. D., Rouzé, P., & Rombauts, S. (2002). Plantcare, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research, 30(1), 325–327.

  • Li, H., Zhou, S. Y., Zhao, W. S., Su, S. C., & Peng, Y. L. (2009). A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Molecular Biology, 69(3), 337–346.

    Article  CAS  PubMed  Google Scholar 

  • Lim, C. W., Yang, S. H., Shin, K. H., Lee, S. C., & Kim, S. H. (2015). The AtLRK10L1. 2, Arabidopsis ortholog of wheat LRK10, is involved in ABA-mediated signaling and drought resistance. Plant Cell Reports, 34(3), 447–455.

    Article  CAS  PubMed  Google Scholar 

  • Mangwanda, R., Myburg, A. A., & Naidoo, S. (2015). Transcriptome and hormone profiling reveals Eucalyptus grandis defence responses against Chrysoporthe austroafricana. BMC Genomics, 16(1), 319.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matsubayashi, Y., Ogawa, M., Morita, A., & Sakagami, Y. (2002). An LRR receptor kinase involved in perception of a peptide plant hormone. phytosulfokine. Science, 296(5572), 1470–1472.

    CAS  PubMed  Google Scholar 

  • Meier, S., Ruzvidzo, O., Morse, M., Donaldson, L., Kwezi, L., & Gehring, C. (2010). The Arabidopsis wall associated kinase-like 10 gene encodes a functional guanylyl cyclase and is co-expressed with pathogen defense related genes. PLOS one, 5(1), e8904.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nguyen, Q. N., Lee, Y. S., Cho, L. H., Jeong, H. J., An, G., & Jung, K. H. (2015). Genome-wide identification and analysis of Catharanthus roseus RLK1-like kinases in rice. Planta, 241(3), 603–613.

    Article  CAS  PubMed  Google Scholar 

  • Osakabe, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., & Tran, L. S. P. (2013). Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. Journal of Experimental Botany, 64(2), 445–458.

    Article  CAS  PubMed  Google Scholar 

  • Peleg, Z., & Blumwald, E. (2011). Hormone balance and abiotic stress tolerance in crop plants. Current Opinion in Plant Biology, 14(3), 290–295.

    Article  CAS  PubMed  Google Scholar 

  • Rizzon, C., Ponger, L., & Gaut, B. S. (2006). Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Computational Biology, 2(9), e115.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Robert-Seilaniantz, A., Grant, M., & Jones, J. D. (2011). Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytopathology, 49, 317–343.

    Article  CAS  PubMed  Google Scholar 

  • Scheer, J. M., & Ryan, C. A. (2002). The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proceedings of the National Academy of Sciences of the United States of America, 99(14), 9585–9590.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schultz, J., Milpetz, F., Bork, P., Ponting, C. P. (1998). SMART, a simple modular architecture research tool: identification of signaling domains. Proceedings of the National Academy of Sciences, 95(11), 5857–5864.

  • Shin, S., Lv, J., Fazio, G., Mazzola, M., & Zhu, Y. (2014). Transcriptional regulation of ethylene and jasmonate mediated defense response in apple (Malus domestica) root during Pythium ultimum infection. Horticulture research, 1, 14053.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shin, S., Zheng, P., Fazio, G., Mazzola, M., Main, D., & Zhu, Y. (2016a). Transcriptome changes specifically associated with apple (Malus domestica) root defense response during Pythium ultimum infection. Physiological and Molecular Plant Pathology, 94, 16–26.

    Article  CAS  Google Scholar 

  • Shin, K. H., Yang, S. H., Lee, J. Y., Lim, C. W., Lee, S. C., Brown, J. W., & Kim, S. H. (2015). Alternative splicing of mini-exons in the arabidopsis leaf rust receptor-like kinase lrk10 genes affects subcellular localisation. Plant Cell Reports, 34(3), 495–505.

  • Shin, S. Y., Chung, H., Kim, S. Y., & Nam, K. H. (2016b). BRI1-EMS-suppressor 1 gain-of-function mutant shows higher susceptibility to necrotrophic fungal infection. Biochemical and Biophysical Research Communications, 470(4), 864–869.

    Article  CAS  PubMed  Google Scholar 

  • Shiu, S. H., Karlowski, W. M., Pan, R., Tzeng, Y. H., Mayer, K. F., & Li, W. H. (2004). Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. The Plant Cell, 16(5), 1220–1234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sivaguru, M., Ezaki, B., He, Z. H., Tong, H., Osawa, H., Baluška, F., Volkmann, D., & Matsumoto, H. (2003). Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis. Plant Physiology, 132(4), 2256–2266.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739.

  • Velasco, R., Zharkikh, A., Affourtit, J., Dhingra, A., Cestaro, A., Kalyanaraman, A., Fontana, P., Bhatnagar, S. K., Troggio, M., Pruss, D., Salvi, S., Pindo, M., Baldi, P., Castelletti, S., Cavaiuolo, M., Coppola, G., Costa, F., Cova, V., Ri, A. D., Goremykin, V., Komjanc, M., Longhi, S., Magnago, P., Malacarne, G., Malnoy, M., Micheletti, D., Moretto, M., Perazzolli, M., Si-Ammour, A., Vezzulli, S., Zini, E., Eldredge, G., Fitzgerald, L. M., Gutin, N., Lanchbury, J., Macalma, T., Mitchell, J. T., Reid, J., Wardell, B., Kodira, C., Chen, Z., Desany, B., Niazi, F., Palmer, M., Koepke, T., Jiwan, D., Schaeffer, S., Krishnan, V., Wu, C., Chu, V. T., King, S. T., Vick, J., Tao, Q., Mraz, A., Stormo, A., Stormo, K., Bogden, R., Ederle, D., Stella, A., Vecchietti, A., Kater, M. M., Masiero, S., Lasserre, P., Lespinasse, Y., Allan, A. C., Bus, V., Chagné, D., Crowhurst, R. N., Gleave, A. P., Lavezzo, E., Fawcett, J. A., Proost, S., Rouzé, P., Sterck, L., Toppo, S., Lazzari, B., Hellens, R. P., Durel, C., Gutin, A., Bumgarner, R. E., Gardiner, S. E., Skolnick, M., Egholm, M., Peer, Y. V., & Salamin, F. (2010). The genome of the domesticated apple (Malus × domestica Borkh.). Nature Genetics, 42(10), 833–839.

    Article  CAS  PubMed  Google Scholar 

  • Verica, J. A., & He, Z. H. (2002). The Cell Wall-Associated Kinase (WAK) and WAK-Like Kinase Gene Family. Plant Physiology, 129(2), 455–459.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner, T. A., & Kohorn, B. D. (2001). Wall-associated kinases are expressed throughout plant development and are required for cell expansion. The Plant Cell, 13(2), 303–318.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, W., Barnaby, J. Y., Tada, Y., Li, H., Tör, M., Caldelari, D., Lee, D., Fu, X., & Dong, X. (2011). Timing of plant immune responses by a central circadian regulator. Nature, 470(7332), 110–114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Y., Tang, H., DeBarry, J. D., Tan, X., Li, J., Wang, X., Lee, T., Jin, H., Marler, B., Guo, H., Kissinger, J. C., & Paterson, A. H. (2012). MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 40(7), e49–e49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, S., Hu, T., Wang, Y., Luo, Y., Michailides, T. J., & Cao, K. (2016). New understanding on infection processes of Valsa canker of apple in China. European Journal of Plant Pathology, 146(3), 531–540.

    Article  Google Scholar 

  • Weigel, D., Ahn, J. H., Blázquez, M. A., Borevitz, J. O., Christensen, S. K., Fankhauser, C., Ferrándiz, C., Kardailsky, I., Malancharuvil, E. J., Neff, M. M., Nguyen, J. T., Sato, S., Wang, Z. Y., Xia, Y., Dixon, R. A., Harrison, M. J., Lamb, C. J., Yanofsky, M. F., & Chory, J. (2000). Activation tagging in Arabidopsis. Plant Physiology, 122(4), 1003–1014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, T., Wang, Y., Zheng, Y., Fei, Z., Dandekar, A. M., Xu, K., Han, Z., & Cheng, L. (2015). Suppressing sorbitol synthesis substantially alters the global expression profile of stress response genes in apple (Malus domestica) leaves. Plant and Cell Physiology, 56(9), 1748–1761.

    Article  CAS  PubMed  Google Scholar 

  • Yin, Z., Ke, X., Kang, Z., & Huang, L. (2016). Apple resistance responses against Valsa mali revealed by transcriptomics analyses. Physiological and Molecular Plant Pathology, 93, 85–92. https://doi.org/10.1016/j.pmpp.2016.01.004.

    Article  CAS  Google Scholar 

  • Zhang, S., Chen, C., Li, L., Meng, L., Singh, J., Jiang, N., Deng, X., He, Z., & Lemaux, P. G. (2005). Evolutionary expansion, gene structure, and expression of the rice wall-associated kinase gene family. Plant Physiology, 139(3), 1107–1124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, K. X., Tian, W. E. N., Jun, D. O. N. G., BAI, T. H., Kun, W. A. N. G., & LI, C. Y. (2016). Comprehensive evaluation of tolerance to alkali stress by 17 genotypes of apple rootstocks. Journal of Integrative Agriculture, 15(7), 1499–1509.

    Article  CAS  Google Scholar 

  • Zhu, J. K. (2003). Regulation of ion homeostasis under salt stress. Current Opinion in Plant Biology, 6(5), 441–445.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, L., Ni, W., Liu, S., Cai, B., Xing, H., & Wang, S. (2017). Transcriptomics Analysis of Apple Leaves in Response to Alternaria alternata Apple Pathotype Infection. Frontiers in Plant Science, 8.

  • Zuo, W., Chao, Q., Zhang, N., Ye, J., Tan, G., Li, B., Xing, Y., Zhang, B., Liu, H., Fengler, K. A., Zhao, J., Zhao, X., Chen, Y., Lai, J., Yan, J., & Xu, M. (2015). A maize wall-associated kinase confers quantitative resistance to head smut. Nature Genetics, 47(2), 151–157.

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was funded by the Talent introduction Project of Gansu Agricultural University (GSAU-RCZX201712) and the National Natural Science Foundation of China (31501728) and the Ministry of Agriculture.

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  1. College of Horticulture, Gansu Agricultural University, Lanzhou, 730070, China

    Cunwu Zuo, Yulian Liu, Zhigang Guo, Juan Mao, Mingyu Chu & Baihong Chen

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  1. Cunwu Zuo
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  2. Yulian Liu
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  3. Zhigang Guo
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  4. Juan Mao
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Correspondence to Baihong Chen.

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All authors have received research grants from Gansu Agricultural University. All authors declared that they have no conflict of interest.

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Zuo, C., Liu, Y., Guo, Z. et al. Genome-wide annotation and expression responses to biotic stresses of the WALL-ASSOCIATED KINASE - RECEPTOR-LIKE KINASE (WAK-RLK) gene family in Apple (Malus domestica). Eur J Plant Pathol 153, 771–785 (2019). https://doi.org/10.1007/s10658-018-1591-8

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