Abstract
Breeding resistant apple cultivars is a long-term solution to fire blight, a devastating bacterial disease caused by Erwinia amylovora. However, most resistance sources have been characterized in wild genetic backgrounds with poor fruit quality. Additionally, strong influences of environment and tree vigor on susceptibility, quantitative resistance, and the disease’s erratic nature make phenotyping challenging. This study examined levels of resistance/susceptibility to fire blight among and within 32 full-sib families (n = 314 seedlings) in a pedigree-connected apple germplasm set. In 2016 and 2017, multiple actively-growing shoots per tree (approximately 3 trees per seedling) were challenged with E. amylovora. Responses were quantified as proportions of current season’s shoot lengths that were blighted (SLB). Within a year, seedling responses were estimated using mean adjusted SLB best linear unbiased predictions (adjusted SLB BLUPs). Responses ranged from highly resistant to highly susceptible (0.04–0.97 adjusted SLB BLUPs across years) and were relatively consistent between years (Spearman’s R2 = 0.55). K-means clustering was used to classify seedlings into resistance/susceptibility groups based on incidence, adjusted SLB BLUPs, maximum SLB, and maximum age of wood infected. Most families, including crosses between susceptible parents, demonstrated quantitative variation for resistance/susceptibility. Families derived from ‘Enterprise’ demonstrated low relative susceptibility. Depending on the year and model, average narrow-sense heritability estimates ranged from 0.22–0.49. Phenotypic information (1) increases understanding of variation and inheritance of resistance/susceptibility to fire blight in germplasm relevant to US apple breeding programs and (2) could be used in pedigree-informed QTL analyses to detect loci associated with resistance/susceptibility.
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26 May 2020
A Correction to this paper has been published: https://doi.org/10.1007/s42161-020-00571-w
References
Aldwinckle HS, Preczewski JL (1976) Reaction of terminal shoots of apple cultivars to invasion by Erwinia amylovora. Phytopathology 66:1439–1444
Aldwinckle HS, Gustafson HL, Forsline PL (1999) Evaluation of the core subset of the USDA apple germplasm collection for resistance to fire blight. Acta Hort 489:269–272. https://doi.org/10.17660/ActaHortic.1999.489.46
Allard A, Bink MCAM, Martinez S, Kelner J-J, Legave J-M, di Guardo M, Di Pierro EA, Laurens F, van de Weg EW, Costes E (2016) Detecting QTLs and putative candidate genes involved in budbreak and flowering time in an apple multiparental population. J Exp Bot 67:2875–2888. https://doi.org/10.1093/jxb/erw130
Amyotte B, Bowen AJ, Banks T, Rajcan I, Somers DJ (2017) Mapping the sensory perception of apple using descriptive sensory evaluation in a genome wide association study. PLoS One 12:e0171710. https://doi.org/10.1371/journal.pone.0171710
Bates D, Maechler M, Bollker B, Walker S (2015) Fitting linear mixed-effects models using LME4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Brown S (2012) Apple. In: Badenes ML, Byrne DH (eds) Fruit breeding, handbook of plant breeding, Springer-Verlag, pp 329-367
Calenge F, Drouet D, Denancé C, van de Weg WE, Brisset MN, Paulin JP, Durel CE (2005) Identification of major QTL together with several minor additive or epistatic QTLs for resistance to fire blight in apple in two related progenies. Theor Appl Genet 111:128–135. https://doi.org/10.1007/s00122-005-2002-z
Chagné D, Crowhurst RN, Troggio M, Davey MW, Gilmore B, Lawley C, Vanderzande S, Hellens RP, Kumar S, Cestaro A, Velasco R, Main D, Rees JD, Iezzoni A, Mockler T, Wilhelm L, van de Weg E, Gardiner SE, Bassil N, Peace C (2012) Genome-wide SNP detection, validation, and development of an 8K SNP array for apple. PLoS One 7:e31745. https://doi.org/10.1371/journal.pone.0031745
de Villemereuil P (2012) Estimation of biological trait heritability using the animal model: how to use the MCMCglmm R package. http://devillemereuil.legtux.org/wp-content/uploads/2012/12/tuto_en.pdf (Accessed 7 October 2019)
Desnoues E, Norelli JL, Aldwinckle HS, Wisniewski ME, Evans KM, Malnoy M, Khan A (2018) Identification of novel strain-specific and environment-dependent minor QTLs linked to fire blight resistance in apple. Plant Mol Biol Rep 36:247–256. https://doi.org/10.1007/s11105-018-1076-0
Durel C-E, Denancé C, Brisset MN (2009) 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 52:139–147. https://doi.org/10.1139/g08-111
Emeriewen OF, Malnoy M, Richter K, Kilian A, Hanke M-V, Peil A (2014) Evidence of a major QTL for fire blight resistance in apple wild species Malus fusca. Acta Hort 1056:289–294. https://doi.org/10.17660/ActaHortic.2014.1056.49
Emeriewen OF, Peil A, Richter K, Zini E, Hanke MV, Malnoy M (2017) 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 148:1011–1018. https://doi.org/10.1007/s10658-017-1152-6
Emeriewen OF, Wöhner T, Flachowsky H, Peil A (2019) Malus hosts-Erwinia amylovora interactions: strain pathogenicity and resistance mechanisms. Front Plant Sci 10:551. https://doi.org/10.3389/fpls.2019.00551
Fischer C, Richter K (1999) Results of fire blight resistance in the Pillnitz apple breeding programme. Acta Hort 489:279–285. https://doi.org/10.17660/ActaHortic.1999.489.48
Furbank RT, Tester M (2011) Phenomics – technologies to relieve the phenotyping bottleneck. Trends Plant Sci 16:635–644. https://doi.org/10.1016/j.tplants.2011.09.005
Gardiner SE, Norelli JL, de Silva N, Fazio G, Peil A, Malnoy M, Horner M, Bowatte D, Carlisle C, Wiedow C, Wan Y, Bassett CL, Baldo AM, Cleton J-M, Richter K, Aldwinckle HS, Bus VGM (2012) Putative resistance gene markers associated with quantitative trait loci for fire blight resistance in Malus ‘Robusta 5’ accessions. BMC Genet 13:25
Gardner RG, Cummins JN, Aldwinckle HS (1980) Inheritance of fire blight resistance in Malus in relation to rootstock breeding. J Amer Soc Hort Sci 105:912–916
Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22. https://doi.org/10.18637/jss.v033.i02
Hampson CR, Sholberg PL (2008) Estimating combining ability for fire blight resistance in apple progenies. Acta Hort 793:337–343. https://doi.org/10.17660/ActaHortic.2008.793.50
Harshman JM, Evans KM, Allen H, Potts R, Flamenco J, Aldwinckle HS, Wisniewski ME, Norelli JL (2017) Fire blight resistance in wild accessions of Malus sieversii. Plant Dis 101:1738–1745. https://doi.org/10.1094/PDIS-01-17-0077-RE
Kellerhals M, Schütz S, Patocchi A (2017) Breeding for host resistance to fire blight. J Plant Pathol 99:37–43. https://doi.org/10.4454/jpp.v99i0.3923
Khan MA, Duffy B, Gessler C, Patocchi A (2006) QTL mapping of fire blight resistance in apple. Mol Breeding 17:299–306. https://doi.org/10.1007/s11032-006-9000-y
Khan MA, Zhao Y, Korban SS (2013) Identification of genetic loci associated with fire blight resistance in Malus through combined use of QTL and association mapping. Physiol Plant 148:344–353. https://doi.org/10.1111/ppl.12068
Korban SS, Ries SM, Klopmeyer MJ, Morrisey JF, Hattermann DR (1988) Genotypic responses of scab-resistant apple cultivars/selections to two strains of Erwinia amylovora and the inheritance of resistance to fire blight. Ann Appl Biol 113:101–105
Kostick SA, Norelli JL, Evans KM (2019) Novel metrics to classify fire blight resistance of 94 apple cultivars. Plant Path 68:985–996. https://doi.org/10.1111/ppa.13012
Kumar S, Bolz RK, Alspach PA, Bus VGM (2010) Development of a recurrent apple breeding programme in New Zealand: a synthesis of results, and a proposed revised breeding strategy. Euphytica 173:207–222. https://doi.org/10.1007/s10681-009-0090-6
Kuznetsova AM, Brockhoff PB, Christensen RHB (2017) LMERTest package: tests in linear mixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13
Lee SA, Ngugi HK, Halbrendt NO, O’Keefe G, Lehman B, Travis JW, Sinn JP, McNellis TW (2010) Virulence characteristics accounting for fire blight disease severity in apple trees and seedlings. Phytopathology 100:539–550. https://doi.org/10.1094/PHYTO-100-6-0539
Lesspinasse Y, Paulin JP (1990) Apple breeding programme for fire blight resistance: strategy used and first results. Acta Hort 273:285–295. https://doi.org/10.17660/ActaHortic.1990.273.42
Luby JJ, Alspach PA, Bus VGM, Orguzie NC (2002) Field resistance to fire blight in a diverse apple (Malus sp.) germplasm collection. J Am Soc Hortic Sci 127:245–253
Mohan SK, Fallahi E, Bijman VP (2002) Evaluation of apple varieties for susceptibility to Erwinia amylovora by artificial inoculation under field conditions. Acta Hort 590:373–375. https://doi.org/10.17660/ActaHortic.2002.590.56
Norelli JL, Jones AL, Aldwinckle HS (2003) Fire blight management in the twenty-first century: using new technologies that enhance host resistance in apple. Plant Dis 87:756–765. https://doi.org/10.1094/PDIS.2003.87.7.756
Peace CP (2017) DNA-informed breeding of rosaceous crops: promises, progress and prospects. Hortic Res 4:17006. https://doi.org/10.1038/hortres.2017.6
Peace CP, Luby JJ, van de Weg WE, Bink MCAM, Iezzoni AF (2014) A strategy for developing representative germplasm sets for systematic QTL validation, demonstrated for apple, peach, and sweet cherry. Tree Genet Genomes 10:1679–1694. https://doi.org/10.1007/s11295-014-0788-z
Peil A, Garcia-Libreros T, Richter K, Trognitz C, Trognitz B, Hanke M-V, Flachowsky H (2007) Strong evidence for a fire blight resistance gene of Malus robusta located on linkage group 3. Plant Breed 126:470–475. https://doi.org/10.1111/j.1439-0523.2007.01408.x
Peil A, Bus VMG, Geider K, Richter K, Flachowsky H, Hanke MV (2009) Improvement of fire blight resistance in apple and pear. Int J Plant Breed 3:1–27
Piepho HP, Möhring J, Melchinger AE, Büchse A (2008) BLUP for phenotypic selection in plant breeding and variety testing. Euphytica 161:209–228. https://doi.org/10.1007/s10681-007-9449-8
van de Weg E, Di Guardo M, Jänsch M, Socquet-Juglard D, Costa F, Baumgartner I, Broggini GAL, Kellerhals M, Troggio M, Laurens F, Durel C-E, Patocchi A (2018) Epistatic fire blight resistance QTL alleles in the apple cultivar ‘Enterprise’ and selection X-6398 discovered and characterized through pedigree-informed analysis. Mol Breeding 38. https://doi.org/10.1007/s11032-017-0755-0
van der Zwet T, Orolaza-Halbrendt N, Zeller W (2012) Fire blight: history, biology and management. APS Press, Saint Paul
Vanderzande S, Howard NP, Cai L, Da Silva LC, Antanaviviute L, Bink MCAM, Kruisselbrink JW, Bassil N, Gasic K, Iezzoni A, van de Weg E, Peace C (2019) High-quality, genome-wide SNP genotypic data for pedigreed germplasm of diploid outbreeding species apple, peach, and sweet cherry through a common workflow. PLoS One 14:e0210928. https://doi.org/10.1371/journal.pone.0210928
Verma S, Evans E, Guan Y, Luby JJ, Rosyara UR, Howard NP, Bassil N, Bink MCAM, van de Weg WE, Peace CP (2019) Two large-effect QTLs, Ma and Ma3, determine genetic potential for acidity in apple fruit: breeding insights from a multi-family study. Tree Genet Genomes 15. https://doi.org/10.1007/s11295-019-1324-y
Wilson AJ, Réale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26. https://doi.org/10.1111/j.1365-2656.2009.01639.x
Wolak ME (2012) Nadiv: an R package to create relatedness matrices for estimating non-additive genetic variances in animal models. Methods Ecol Evol 3:792–796. https://doi.org/10.1111/j.2041-210X.2012.00213.x
Xu Y, Crouch JH (2008) Marker-assisted selection in plant breeding: from publications to practice. Crop Sci 48:391–407. https://doi.org/10.2135/cropsci2007.04.0191
Acknowledgements
The authors would like to thank Nancy Buchanan, Schaefer Buchanan, Lisa Brutcher, Jamie Coggins, and Bonnie Schonberg of the Washington State University (WSU) Tree Fruit Research and Extension Center for their assistance and/or technical expertise with carrying out these field inoculation experiments. Additionally, the authors would like to thank the WSU Columbia View orchard farm crew for maintaining the planting throughout the duration of this study. This study was partially funded by Washington Tree Fruit Research Commission projects # CP-15-100 (A, B, & C) and CP-12-104 (A & B), United States Department of Agriculture – National Institute of Agriculture award # 2016-68004-24770, United States Department of Agriculture – National Institute of Agriculture – Specialty Crop Research Initiative project ‘RosBREED: combining disease resistance and horticultural quality in new rosaceous cultivars’ (2014-51181-22378), and United States Department of Agriculture – National Institute of Agriculture Hatch project 1014919.
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Kostick, S.A., Norelli, J.L., Teh, S.L. et al. Quantitative variation and heritability estimates of fire blight resistance in a pedigree-connected apple germplasm set. J Plant Pathol 103 (Suppl 1), 65–75 (2021). https://doi.org/10.1007/s42161-020-00543-0
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DOI: https://doi.org/10.1007/s42161-020-00543-0