Candidate gene mapping identifies genomic variations in the fire blight susceptibility genes HIPM and DIPM across the Malus germplasm (original) (raw)

Abstract

Development of apple (Malus domestica) cultivars resistant to fire blight, a devastating bacterial disease caused by Erwinia amylovora, is a priority for apple breeding programs. Towards this goal, the inactivation of members of the HIPM and DIPM gene families with a role in fire blight susceptibility (S genes) can help achieve sustainable tolerance. We have investigated the genomic diversity of HIPM and DIPM genes in Malus germplasm collections and used a candidate gene-based association mapping approach to identify SNPs (single nucleotide polymorphisms) with significant associations to fire blight susceptibility. A total of 87 unique SNP variants were identified in HIPM and DIPM genes across 93 Malus accessions. Thirty SNPs showed significant associations (p

Loading...

Loading Preview

Sorry, preview is currently unavailable. You can download the paper by clicking the button above.

References (67)

  1. Vol:.(1234567890) Scientific RepoRtS | (2020) 10:16317 | https://doi.org/10.1038/s41598-020-73284-w
  2. Flachowsky, H. et al. Application of a high-speed breeding technology to apple (Malus×domestica) based on transgenic early flowering plants and marker-assisted selection. New Phytol. https ://doi.org/10.1111/j.1469-8137.2011.03813 .x (2011).
  3. Grattapaglia, D. & Resende, M. D. V. Genomic selection in forest tree breeding. Tree Genet. Genomes https ://doi.org/10.1007/s1129 5-010-0328-4 (2011).
  4. Kumar, S., Bink, M. C. A. M., Volz, R. K., Bus, V. G. M. & Chagné, D. Towards genomic selection in apple (Malus × domestica Borkh.) breeding programmes: prospects, challenges and strategies. Tree Genet. Genomes https ://doi.org/10.1007/s1129 5-011- 0425-z (2012).
  5. Resende, M. D. V. et al. Genomic selection for growth and wood quality in Eucalyptus: capturing the missing heritability and accelerating breeding for complex traits in forest trees. New Phytol. https ://doi.org/10.1111/j.1469-8137.2011.04038 .x (2012).
  6. Ghosh, S. et al. Speed breeding in growth chambers and glasshouses for crop breeding and model plant research. Nat. Protoc. https ://doi.org/10.1038/s4159 6-018-0072-z (2018).
  7. Khan, M. A., Zhao, Y. & Korban, S. S. Molecular mechanisms of pathogenesis and resistance to the bacterial pathogen Erwinia amylovora, causal agent of fire blight disease in rosaceae. Plant Mol. Biol. Rep. https ://doi.org/10.1007/s1110 5-011-0334-1 (2012).
  8. Norelli, J. L., Jones, A. L. & Aldwinckle, H. S. Fire blight management in the twenty-first century: using new technologies that enhance host resistance in apple. Plant Dis. https ://doi.org/10.1094/PDIS.2003.87.7.756 (2003).
  9. Luo, F., Evans, K., Norelli, J. L., Zhang, Z. & Peace, C. Prospects for achieving durable disease resistance with elite fruit quality in apple breeding. Tree Genet. Genomes https ://doi.org/10.1007/s1129 5-020-1414-x (2020).
  10. Muñoz-Sanz, J. V., Zuriaga, E., Cruz-García, F., McClure, B. & Romero, C. Self-(in)compatibility systems: target traits for crop- production, plant breeding, and biotechnology. Front. Plant Sci. https ://doi.org/10.3389/fpls.2020.00195 (2020).
  11. Longhi, S. et al. A candidate gene based approach validates Md-PG1 as the main responsible for a QTL impacting fruit texture in apple (Malus × domestica Borkh). BMC Plant Biol https ://doi.org/10.1186/1471-2229-13-37 (2013).
  12. Malnoy, M. et al. Fire blight: applied genomic insights of the pathogen and host. Annu. Rev. Phytopathol. https ://doi.org/10.1146/ annur ev-phyto -08121 1-17293 1 (2012).
  13. Busdieker-Jesse, N. L., Nogueira, L., Onal, H. & Bullock, D. S. The economic impact of new technology adoption on the U.S. apple industry. J. Agric. Resour. Econ. https ://doi.org/10.22004 /ag.econ.24625 4 (2016).
  14. Beckerman, J. L. & Sundin, G. W. Scab and fire blight of apple: issues in integrated pest management. Hortic. Rev. https ://doi. org/10.1002/97811 19281 269.ch8 (2016).
  15. Peil A, Hanke M V., Flachowsky H et al. Confirmation of the fire blight QTL of Malus × robusta 5 on linkage group 3. In: Acta Horticulturae (2008).
  16. Durel, C. E., Denancé, C. & Brisset, M. N. Two distinct major QTL for resistance to fire blight co-localize on linkage group 12 in apple genotypes 'Evereste' and Malus floribunda clone 821. Genome https ://doi.org/10.1139/G08-111 (2009).
  17. Emeriewen, O. et al. Identification of a major quantitative trait locus for resistance to fire blight in the wild apple species Malus fusca. Mol. Breed. https ://doi.org/10.1007/s1103 2-014-0043-1 (2014).
  18. Calenge, F. et al. Identification of a major QTL together with several minor additive or epistatic QTLs for resistance to fire blight in apple in two related progenies. Theor. Appl. Genet. https ://doi.org/10.1007/s0012 2-005-2002-z (2005).
  19. Khan, M. A., Duffy, B., Gessler, C. & Patocchi, A. QTL mapping of fire blight resistance in apple. Mol. Breed. https ://doi.org/10.1007/ s1103 2-006-9000-y (2006).
  20. Khan, M. A., Zhao, Y. F. & Korban, S. S. Identification of genetic loci associated with fire blight resistance in Malus through com- bined use of QTL and association mapping. Physiol. Plant https ://doi.org/10.1111/ppl.12068 (2013).
  21. Vogt, I. et al. Gene-for-gene relationship in the host-pathogen system Malus × robusta 5-Erwinia amylovora. New Phytol. https :// doi.org/10.1111/nph.12094 (2013).
  22. Broggini, G. A. L. et al. Engineering fire blight resistance into the apple cultivar 'Gala' using the FB_MR5 CC-NBS-LRR resistance gene of Malus × robusta 5. Plant Biotechnol. J. https ://doi.org/10.1111/pbi.12177 (2014).
  23. van Schie, C. C. N. & Takken, F. L. W. Susceptibility genes 101: how to be a good host. Annu. Rev. Phytopathol. https ://doi. org/10.1146/annur ev-phyto -10231 3-04585 4 (2014).
  24. Candresse, T., Le Gall, O., Maisonneuve, B., German-Retana, S. & Redondo, E. The use of green fluorescent protein-tagged recom- binant viruses to test Lettuce mosaic virus resistance in lettuce. Phytopathology https ://doi.org/10.1094/PHYTO .2002.92.2.169 (2002).
  25. Nicaise, V. et al. The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiol https ://doi.org/10.1104/pp.102.01785 5 (2003).
  26. Gao, Z. et al. The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor elF4E in cell-to- cell trafficking. Plant J https ://doi.org/10.1111/j.1365-313X.2004.02215 .x (2004).
  27. Gao, Z., Eyers, S., Thomas, C., Ellis, N. & Maule, A. Identification of markers tightly linked to sbm recessive genes for resistance to Pea seed-borne mosaic virus. Theor. Appl. Genet. https ://doi.org/10.1007/s0012 2-004-1652-6 (2004).
  28. Kang, B. C., Yeam, I., Frantz, J. D., Murphy, J. F. & Jahn, M. M. The pvr1 locus in Capsicum encodes a translation initiation factor elF4E that interacts with Tobacco etch virus VPg. Plant J. https ://doi.org/10.1111/j.1365-313X.2005.02381 .x (2005).
  29. Morales, M. et al. A physical map covering the nsv locus that confers resistance to Melon necrotic spot virus in melon (Cucumis melo L.). Theor. Appl. Genet. https ://doi.org/10.1007/s0012 2-005-0019-y (2005).
  30. Nieto, C. et al. An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant J. https :// doi.org/10.1111/j.1365-313X.2006.02885 .x (2006).
  31. Iyer-Pascuzzi, A. S. & McCouch, S. R. Recessive resistance genes and the Oryza sativa-Xanthomonas oryzae pv. oryzae pathosys- tem. Mol. Plant Microbe Interact. https ://doi.org/10.1094/MPMI-20-7-0731 (2007).
  32. Rakotomalala, M. et al. Resistance to rice yellow mottle virus in rice germplasm in Madagascar. Eur. J. Plant Pathol. https ://doi. org/10.1007/s1065 8-008-9282-5 (2008).
  33. Tyrka, M., Perovic, D., Wardyńska, A. & Ordon, F. A new diagnostic SSR marker for selection of the Rym4/Rym5 locus in barley breeding. J. Appl. Genet https ://doi.org/10.1007/BF031 95605 (2008).
  34. Jia, H. et al. Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol. J. https ://doi.org/10.1111/pbi.12677 (2017).
  35. Borejsza-Wysocka, E. E. et al. The fire blight resistance of apple clones in which DspE-interacting proteins are silenced. In X International Workshop on Fire Blight. Acta Hort. 704, 509-513 (2006).
  36. Malnoy, M. et al. Silencing of HIPM, the apple protein that interacts with HrpN of Erwinia amylovora. Acta Hortic. https ://doi. org/10.17660 /ActaH ortic .2008.793.38 (2008).
  37. Oh, C. S. & Beer, S. V. AtHIPM, an ortholog of the apple HrpN-interacting protein, is a negative regulator of plant growth and mediates the growth-enhancing effect of HrpN in arabidopsis. Plant Physiol. https ://doi.org/10.1104/pp.107.10343 2 (2007).
  38. Bocsanczy, A. M., Nissinen, R. M., Oh, C. S. & Beer, S. V. HrpN of Erwinia amylovora functions in the translocation of DspA/E into plant cells. Mol. Plant Pathol. https ://doi.org/10.1111/j.1364-3703.2008.00471 .x (2008).
  39. Campa, M. et al. HIPM is a susceptibility gene of Malus spp.: reduced expression reduces susceptibility to Erwinia amylovora. Mol. Plant Microbe Interact. https ://doi.org/10.1094/MPMI-05-18-0120-R (2019).
  40. Meng, X., Bonasera, J. M., Kim, J. F., Nissinen, R. M. & Beer, S. V. Apple proteins that interact with DspA/E, a pathogenicity effector of Erwinia amylovora, the fire blight pathogen. Mol. Plant Microbe Interact. https ://doi.org/10.1094/MPMI-19-0053 (2006).
  41. Pompili, V., Dalla Costa, L., Piazza, S., Pindo, M. & Malnoy, M. Reduced fire blight susceptibility in apple cultivars using a high- efficiency CRISPR/Cas9-FLP/FRT-based gene editing system. Plant Biotechnol. J. https ://doi.org/10.1111/pbi.13253 (2020).
  42. Duan, N. et al. Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat. Commun. https ://doi.org/10.1038/s4146 7-017-00336 -7 (2017).
  43. Bianco, L. et al. Development and validation of the Axiom Apple480K SNP genotyping array. Plant J. https ://doi.org/10.1111/ tpj.13145 (2016).
  44. Daccord, N. et al. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat. Genet. https ://doi.org/10.1038/ng.3886 (2017).
  45. Yang, S. et al. A next-generation marker genotyping platform (AmpSeq) in heterozygous crops: a case study for marker-assisted selection in grapevine. Hortic. Res. https ://doi.org/10.1038/hortr es.2016.2 (2016).
  46. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics https ://doi. org/10.1093/bioin forma tics/btu17 0 (2014).
  47. Wang, K., Li, M. & Hakonarson, H. ANNOVAR: Functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. https ://doi.org/10.1093/nar/gkq60 3 (2010).
  48. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics https ://doi.org/10.1093/bioin forma tics/btr33 0 (2011).
  49. Bradbury, P. J. et al. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics https ://doi. org/10.1093/bioin forma tics/btm30 8 (2007).
  50. Singh, J. & Khan, A. Distinct patterns of natural selection determine sub-population structure in the fire blight pathogen, Erwinia amylovora. Sci. Rep. https ://doi.org/10.1038/s4159 8-019-50589 -z (2019).
  51. R Core Team. R: A language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. (R Foundation forStatistical Computing, 2020).
  52. Desnoues, E. et al. Identification of novel strain-specific and environment-dependent minor QTLs linked to fire blight resistance in apples. Plant Mol. Biol. Rep. https ://doi.org/10.1007/s1110 5-018-1076-0 (2018).
  53. Charrad, M., Ghazzali, N., Boiteau, V. & Niknafs, A. Nbclust: An R package for determining the relevant number of clusters in a data set. J. Stat. Softw. https ://doi.org/10.18637 /jss.v061.i06 (2014).
  54. Browning, S. R. & Browning, B. L. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet. https ://doi.org/10.1086/52198 7 (2007).
  55. Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. https ://doi.org/10.1086/51979 5 (2007).
  56. Barrett, J. C., Fry, B., Maller, J. & Daly, M. J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics https ://doi.org/10.1093/bioin forma tics/bth45 7 (2005).
  57. Pavan, S., Jacobsen, E., Visser, R. G. F. & Bai, Y. Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol. Breed. https ://doi.org/10.1007/s1103 2-009-9323-6 (2010).
  58. Zaidi, S. S., Mukhtar, M. S. & Mansoor, S. Genome editing: targeting susceptibility genes for plant disease resistance. Trends Bio- technol. https ://doi.org/10.1016/j.tibte ch.2018.04.005 (2018).
  59. Borejsza-Wysocka, E. E. et al. The fire blight resistance of apple clones in which DspE-interacting proteins are silenced. Acta Hortic. https ://doi.org/10.17660 /actah ortic .2006.704.80 (2006).
  60. Udoh, L. I. et al. Candidate gene sequencing and validation of SNP markers linked to carotenoid content in cassava (Manihot esculenta Crantz). Mol. Breed. https ://doi.org/10.1007/s1103 2-017-0718-5 (2017).
  61. Parravicini, G. et al. 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' . Mol. Plant Pathol. https ://doi.org/10.111 1/j.1364-3703.2010.00690 .x (2011).
  62. Fahrentrapp, J. et al. A candidate gene for fire blight resistance in Malus × robusta 5 is coding for a CC-NBS-LRR. Tree Genet. Genomes https ://doi.org/10.1007/s1129 5-012-0550-3 (2013).
  63. Emeriewen, O. F. et al. Fire blight resistance of Malus ×arnoldiana is controlled by a quantitative trait locus located at the distal end of linkage group 12. Eur. J. Plant Pathol. https ://doi.org/10.1007/s1065 8-017-1152-6 (2017).
  64. Singh, J. et al. Root system traits impact early fire blight susceptibility in apple (Malus × domestica). BMC Plant Biol. https ://doi. org/10.1186/s1287 0-019-2202-3 (2019).
  65. Quamme, H. A. & Bonn, W. G. Virulence of Erwinia amylovora and its influence on the determination of fire blight resistance of pear cultivars and seedlings. Can. J. Plant Pathol. https ://doi.org/10.1080/07060 66810 95013 45 (1981).
  66. Norelli, J. L. Differential host × pathogen interactions among cultivars of apple and strains of Erwinia amylovora. Phytopathology https ://doi.org/10.1094/phyto -74-136 (1984).
  67. Emeriewen, O. F., Wöhner, T., Flachowsky, H. & Peil, A. Malus hosts-Erwinia amylovora interactions: strain pathogenicity and resistance mechanisms. Front. Plant Sci. https ://doi.org/10.3389/fpls.2019.00551 (2019).