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Ascochyta blight disease of pea (Pisum sativum L.): defence-related candidate genes associated with QTL regions and identification of epistatic QTL

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Advances have been made in our understanding of Ascochyta blight resistance genetics through mapping candidate genes associated with QTL regions and demonstrating the importance of epistatic interactions in determining resistance.

Abstract

Ascochyta blight disease of pea (Pisum sativum L.) is economically significant with worldwide distribution. The causal pathogens are Didymella pinodes, Phoma medicaginis var pinodella and, in South Australia, P. koolunga. This study aimed to identify candidate genes that map to quantitative trait loci (QTL) for Ascochyta blight field disease resistance and to explore the role of epistatic interactions. Candidate genes associated with QTL were identified beginning with 101 defence-related genes from the published literature. Synteny between pea and Medicago truncatula was used to narrow down the candidates for mapping. Fourteen pea candidate sequences were mapped in two QTL mapping populations, A26 × Rovar and A88 × Rovar. QTL peaks, or the intervals containing QTL peaks, for the Asc2.1, Asc4.2, Asc4.3 and Asc7.1 QTL were defined by four of these candidate genes, while another three candidate genes occurred within 1.0 LOD confidence intervals. Epistasis involving QTL × background marker and background marker × background marker interactions contributed to the disease response phenotypes observed in the two mapping populations. For each population, five pairwise interactions exceeded the 5 % false discovery rate threshold. Two candidate genes were involved in significant pairwise interactions. Markers in three genomic regions were involved in two or more epistatic interactions. Therefore, this study has identified pea defence-related sequences that are candidates for resistance determination, and that may be useful for marker-assisted selection. The demonstration of epistasis informs breeders that the architecture of this complex quantitative resistance includes epistatic interactions with non-additive effects.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aubert G, Morin J, Jacquin F, Loridon K, Quillet MC, Petit A, Rameau C, Lejeune-Hénaut I, Huguet T, Burstin J (2006) Functional mapping in pea, as an aid to the candidate gene selection and for investigating synteny with the model legume Medicago truncatula. Theor Appl Genet 112:1024–1041

    Article  CAS  PubMed  Google Scholar 

  • Bonhomme M, André O, Badis Y, Ronfort J, Burgarella C, Chantret N, Prosperi JM et al (2014) High-density genome-wide association mapping implicates an F-box encoding gene in Medicago truncatula resistance to Aphanomyces euteiches. New Phytol 201:1328–1342

    Article  CAS  PubMed  Google Scholar 

  • Bordat A, Savois V, Nicolas M, Salse J, Chauveau A, Bourgeois M, Potier J, Houtin H, Rond C, Murat F, Marget P, Aubert G, Burstin J (2011) Translational genomics in legumes allowed placing in silico 5460 unigenes on the pea functional map and identified candidate genes in Pisum sativum L. Genes Genomes Genet 1:93–103

    CAS  Google Scholar 

  • Bretag TW, Ramsey M (2001) Foliar diseases caused by fungi: Ascochyta spp. In: Kraft JM, Pfleger PM (eds) Pea disease compendium. Americal Pathological Society, St. Paul, pp 24–28

    Google Scholar 

  • Broekaert WF, Delauré SL, De Bolle MFC, Cammue BPA (2006) The role of ethylene in host-pathogen interactions. Annu Rev Phytopathol 44:393–416

    Article  CAS  PubMed  Google Scholar 

  • Broman KW, Sen S (2009) A guide to QTL mapping with R/qtl. Springer, New York

    Book  Google Scholar 

  • Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: qTL mapping in experimental crosses. Bioinformatics 19:889–890

    Article  CAS  PubMed  Google Scholar 

  • Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60:183–205

    Article  CAS  PubMed  Google Scholar 

  • Buerstmayr M, Matiasch L, Mascher F, Vida G, Ittu M, Robert O, Holdgate S, Flath K, Neumayer A (2014) Buerstmayr H (2014) Mapping of quantitative adult plant field resistance to leaf rust and stripe rust in two European winter wheat populations reveals co-location of three QTL conferring resistance to both rust pathogens. Theor Appl Genet 127:2011–2028

    Article  PubMed  PubMed Central  Google Scholar 

  • Carillo E, Satovic Z, Aubert G, Boucherot K, Rubiales D, Fondevilla S (2014) Identification of quantitative trait loci and candidate genes for specific cellular resistance responses against Didymella pinodes in pea. Plant Cell Rep 33:1133–1145

    Article  Google Scholar 

  • Choi HK, Mun JH, Kim DJ, Zhu H, Baek JM, Mudge J, Roe B, Ellis N, Doyle J, Kiss GB et al (2004) Estimating genome conservation between crop and model legume species. Proc Natl Acad Sci USA 101:15289–15294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cole SJ, Diener AC (2013) Diversity in receptor-like kinase genes is a major determinant of quantitative resistance to Fusarium oxysporum f.sp. matthioli. New Phytol 200:172–184

    Article  CAS  PubMed  Google Scholar 

  • Costanzo M, Baryshnikova A, Myers CL, Andrews B, Boone C (2011) Charting the genetic map of a cell. Current Opin Biotechnol 22:66–74

    Article  CAS  Google Scholar 

  • Davidson JA, Krysinska-Kaczmarek M, McKay HA, Scott ES (2012) Comparison of cultural growth and in planta quantification of Didymella pinodes, Phoma koolunga and Phoma medicaginis var. pinodella, causal agents of ascochyta blight on field pea (Pisum sativum). Mycologia 104:93–101

    Article  CAS  PubMed  Google Scholar 

  • Deulvot C, Charrel H, Marty A, Jacquin F, Donnadieu C, Lejeune-Hénaut I, Burstin J, Aubert G (2010) Highly-multiplexed SNP genotyping for genetic mapping and germplasm diversity studies in pea. BMC Genom 11:468

    Article  Google Scholar 

  • Diener A (2012) Visualizing and quantifying Fusarium oxysporum in the plant host. Mol Plant Microbe Interact 25:1531–1541

    Article  CAS  PubMed  Google Scholar 

  • Diener AC, Ausubel FM (2005) Resistance to Fusarium oxysporum 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 171:305–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doust AN, Lukens L, Olsen KM, Mauro-Herrera M, Meyer A, Rogers K (2014) Beyond the single gene: how epistasis and gene-by-environnment effects influence crop domestication. Proc Natl Acad Sci USA 111:6178–6183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fondevilla S, Satovic Z, Rubiales D, Moreno MT, Torres AM (2008) Mapping of quantitative trait loci for resistance to Mycosphaerella pinodes in Pisum sativum subsp syriacum. Mol Breed 21(4):439–454

    Article  CAS  Google Scholar 

  • Fondevilla S, Küster H, Krajinski F, Cubero JI, Rubiales D (2011) Identification of genes differentially expressed in a resistant reaction to Mycosphaerella pinodes in pea using microarray technology. BMC Genom 12:28

    CAS  Google Scholar 

  • Fondevilla S, Rotter B, Krezdorn N, Jüngling R, Winter P, Rubiales D (2014) Identification of genes involved in resistance to Didymella pinodes in pea by deepSuperSAGE transcriptome profiling. Plant Mol Biol Rep 32:258–269

    Article  CAS  Google Scholar 

  • Gilpin BJ, McCallum JA, Frew TJ, Timmerman-Vaughan GM (1997) A linkage map of the pea (Pisum sativum L.) genome containing cloned sequences of known function and expressed sequence tags (ESTs). Theor Appl Genet 95:1289–1299

    Article  CAS  Google Scholar 

  • Göhre V, Jones AME, Sklenár J, Robatzek S, Weber APM (2012) Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Mol Plant-Microbe Interact 25:1083–1092

    Article  PubMed  Google Scholar 

  • Hellens RP, Moreau C, Kui LW, Schwinn KE, Thomson SJ, Fiers MWEJ, Frew TJ, Murray SR, Hofer JMI, Jacobs JME, Davies KM, Allan AC, Bendahmane A, Coyne CJ, Timmerman-Vaughan GM, Ellis THN (2010) Identification of Mendel’s white flower character. PLoS One 5(10):e13230

    Article  PubMed  PubMed Central  Google Scholar 

  • Huard-Chauveau C, Perchepied L, Debieu M, Rivas S, Kroj T et al (2013) An atypical kinase under balancing selection confers broad-spectrum disease resistance in arabidopsis. PLoS Genet 9(9):e1003766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ibrahim A, Hofman-Bang J, Ahring BK (2001) Amplification and direct sequence analysis of the 23S rRNA gene from thermophilic bacteria. Biotechniques 30:414–420

    CAS  PubMed  Google Scholar 

  • Jain M, Misra G, Patel RK, Priya P, Jhanwar S, Khan AW, Shah N, Singh VK, Garg R, Jeena G, Sharma P, Kant C, Yadav M, Yadav G, Bhatia S, Tyagi AK, Chattopadhyay D (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J 74:715–729

    Article  CAS  PubMed  Google Scholar 

  • Jha AB, Tar’an B, Diapari M, Sindhu A, Shunmugam A, Bett K, Warkentin TD (2015) Allele diversity analysis to identify SNPs associated with ascochyta blight resistance in pea. Euphytica 202:189–197

    Article  CAS  Google Scholar 

  • Kaló P, Seres A, Taylor SA, Jakab J, Kevei Z, Kereszt A, Endre G, Ellis THN, Kiss GB (2004) Comparative mapping between Medicago sativa and Pisum sativum. Mol Gen Genomics 272:235–246

    Article  Google Scholar 

  • Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M (2014) Data, information, knowledge and principle: back to metabolism in KEGG. Nucl Acids Res 42:D199–D205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan TN, Timmerman-Vaughan GM, Rubiales D, Warkentin TD, Siddique KHM, Erskine W, Barbetti MJ (2013) Didymella pinodes and its management in field pea: challenges and opportunities. Field Crops Res 148:61–77

    Article  Google Scholar 

  • Knott CM (1987) A key for stages of development of the pea. Ann Appl Biol 111:233–244

    Article  Google Scholar 

  • Kruijt M, de Kock MJ, de Wit PJ (2005) Receptor-like proteins involved in plant disease resistance. Mol Plant Pathol 6:85–97

    Article  CAS  PubMed  Google Scholar 

  • Lai F-M, DeLong C, Mei K, Wignes T, Fobert PR (2002) Analysis of the DRR230 family of pea defensins: gene expression pattern and evidence of broad host-range antifungal activity. Plant Sci 163:855–864

    Article  CAS  Google Scholar 

  • Lehner B (2011) Molecular mechanisms of epistasis within and between genes. Trends Genet 27:323–331

    Article  CAS  PubMed  Google Scholar 

  • Lehner B, Crombie C, Tischler J, Fortunato A, Fraser AG (2006) Systematic mapping of genetic interactions in Caenorhabditis elegans identifies common modifiers of diverse signaling pathways. Nat Genet 38:896–903

    Article  CAS  PubMed  Google Scholar 

  • Lehti-Shiu MD, Zou C, Hanada K, Shiu SH (2009) Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 150:12–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leonforte A, Sudheesh S, Cogan NOI, Salisbury PA, Nicolas ME, Materne M, Forster JW, Kaur S (2013) SNP marker discovery, linkage map construction and identification of QTLs for enhanced salinity tolerance in field pea (Pisum sativum L.). BMC Plant Biol 13:161

    Article  PubMed  PubMed Central  Google Scholar 

  • Loridon K, McPhee K, Morin J, Dubreuil P, Pilet-Nayel ML, Aubert G, Rameau C, Baranger A, Coyne C, Lejeune-Hènaut I, Burstin J (2005) Microsatellite marker polymorphism and mapping in pea (Pisum sativum L.). Theor Appl Genet 111:1022–1031

    Article  CAS  PubMed  Google Scholar 

  • Madrid E, Barilli E, Gil J, Huguet T, Gentzbittel L, Rubiales D (2014) Detection of partial resistance quantitative trait loci against Didymella pinodes in Medicago truncatula. Mol Breeding 33:589–599

    Article  Google Scholar 

  • Maleck K, Levine A, Eulgem T, Morgan A, Schmid J et al (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26:403–410

    Article  CAS  PubMed  Google Scholar 

  • Margarido GRA, Souza AP, Garcia AAF (2007) OneMap: software for genetic mapping in outcrossing species. Hereditas 144:78–79

    Article  CAS  PubMed  Google Scholar 

  • Meuwissen TH, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829

    CAS  PubMed  PubMed Central  Google Scholar 

  • Naz AA, Kunert A, Flath K, Pillen K, Léon J (2012) Advanced backcross quantitative trait locus analysis in winter wheat: dissection of stripe rust seedling resistance and identification of favorable exotic alleles originated from a primary hexaploid wheat (Triticum turgidum ssp. dicoccoides × Aegilops tauschii). Mol Breeding 30:1219–1229

    Article  CAS  Google Scholar 

  • Prioul S, Frankewitz A, Deniot G, Morin G, Baranger A (2004) Mapping of quantitative trait loci for partial resistance to Mycosphaerella pinodes in pea (Pisum sativum L.), at the seedling and adult plant stages. Theor Appl Genet 108:1322–1334

    Article  CAS  PubMed  Google Scholar 

  • Prioul-Gervais S, Deniot G, Receveur EM, Frankewitz A, Fourmann M, Rameau C, Pilet-Nayel ML, Baranger A (2007) Candidate genes for quantitative resistance to Mycosphaerella pinodes in pea (Pisum sativum L.). Theor Appl Genet 114:971–984

    Article  CAS  PubMed  Google Scholar 

  • Pushpavalli R, Krishnamurthy L, Thudi M, Gaur PM, Rao MV, Siddique KHM, Colmer TD, Turner NC, Varshney RK, Vadez V (2015) Two key genomic regions harbour QTLs for salinity tolerance in ICCV 2 × JG 11 derived chickpea (Cicer arietinum L.) recombinant inbred lines. BMC Plant Biol 15:124

    Article  PubMed  PubMed Central  Google Scholar 

  • Rouse MN, Talbert LE, Singh D, Sherman JD (2014) Complementary epistasis involving Sr12 explains adult plant resistance to stem rust in Thatcher wheat (Triticum aestivum L.). Theor Appl Genet 127:1549–1559

    Article  CAS  PubMed  Google Scholar 

  • Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K, Fujishiro T, Katoh M, Kohara M, Kishida Y, Minami C, Nakayama S, Nakazaki N, Shimizu Y, Shinpo S, Takahashi C, Wada T, Yamada M, Ohmido N, Hayashi M, Fukui K, Baba T, Nakamichi T, Mori H, Tabata S (2008) Genome structure of the legume, Lotus japonicus. DNA Res 15:227–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  CAS  PubMed  Google Scholar 

  • Shen Y, Diener AC (2013) Arabidopsis thaliana RESISTANCE TO FUSARIUM OXYSPORUM 2 implicates tyrosine-sulfated peptide signaling in susceptibility and resistance to root infection. PLoS Genet 9(5):e1003525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sindhu A, Ramsay L, Anderson LA, Stonehouse R, Li R, Condie J, Shunmagam ASK, Liu Y, Jha AB, Diapari M, Burstin J, Aubert G, Tar’an B, Bett KE, Warkentin TD, Sharpe AG (2014) Gene-based SNP discovery and genetic mapping in pea. Theor Appl Genet 127:2225–2241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh A, Knox RE, DePauw RM, Singh AK, Cuthbert RD, Campbell HL, Shorter S, Bhavani S (2014) Stripe rust and leaf rust resistance QTL mapping, epistatic interactions, and co-localization with stem rust resistance loci in spring wheat evaluated over three continents. Theor Appl Genet 127:2465–2477

    Article  CAS  PubMed  Google Scholar 

  • Snitkin ES, Segrè D (2011) Epistatic interaction maps relative to multiple metabolic phenotypes. PLoS Genet 7:e1001294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • St Clair DA (2010) Quantitative disease resistance and quantitative resistance loci in breeding. Annu Rev Phytopath 48:247–268

    Article  CAS  Google Scholar 

  • Tang H, Krishnakumar V, Bidwell S, Rosen B, Chan A, Zhou S, Gentzbittel L, Childs KL, Yandell M, Gundlach H, Mayer KFX, Schwartz DC, Town CD (2014) An improved genome release (version Mt4.0) for the model legume Medicago truncatula. BMC Genom 15:312

    Article  Google Scholar 

  • Tar’an B, Warkentin T, Somers DJ, Miranda D, Vandenberg A, Blade S, Woods S, Bing D, DeKoeyer D, Penner G (2003) Quantitative trait loci for lodging resistance, plant height and partial resistance to Mycosphaerella blight in Weld pea (Pisum sativum L.). Theor Appl Genet 107:1482–1491

    Article  PubMed  Google Scholar 

  • Tayeh N, Bahrman N, Devaux R, Bluteau A, Prosperi JM, Delbreil B, Lejeune-Hénaut I (2013) A high-density genetic map of the Medicago truncatula major freezing tolerance QTL on chromosome 6 reveals colinearity with a QTL related to freezing damage in Pisum sativum linkage group VI. Mol Breeding 32:279–289

    Article  CAS  Google Scholar 

  • Thimm O, Blaesing OE, Gibon Y, Nagel A, Meyer S, Krueger P, Selbig J, Mueller LA, Rhee SY, Stitt M (2004) Mapman: a user-driven tool to display genomics datasets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Article  CAS  PubMed  Google Scholar 

  • Timmerman GM, Frew TJ, Miller AM, Weeden NF, Jermyn WJ (1993) Linkage mapping of sbm-1, a gene conferring resistance to pea seed-borne mosaic virus, using molecular markers in Pisum sativum. Theor Appl Genet 85:609–615

    Article  CAS  PubMed  Google Scholar 

  • Timmerman-Vaughan GM, Frew TJ, Weeden NF (2000) Characterization and linkage mapping of R-gene analogous DNA sequences in pea (Pisum sativum L.). Theor Appl Genet 101:241–247

    Article  CAS  Google Scholar 

  • Timmerman-Vaughan GM, Frew TJ, Russell AC, Khan T, Butler R, Gilpin M, Murray S, Falloon K (2002) QTL mapping of partial resistance to field epidemics of ascochyta blight of pea. Crop Sci 42:2100–2111

    Article  CAS  Google Scholar 

  • Timmerman-Vaughan GM, Frew TJ, Butler R, Murray S, Gilpin M, Falloon K, Johnston P, Lakeman MB, Russell A, Khan T (2004) Validation of quantitative trait loci for Ascochyta blight resistance in pea (Pisum sativum L.), using populations from two crosses. Theor Appl Genet 109:1620–1631

    Article  CAS  PubMed  Google Scholar 

  • Untergrasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucl Acids Res 40:e115

    Article  Google Scholar 

  • Varshney RK, Song C, Saxena RK, Azam S, Yu S, Sharpe AG, Cannon S, Baek J, Rosen BD, Tar’an B, Millan T, Zhang X, Ramsay LD, Iwata A, Wang Y, Nelson W, Farmer AD, Gaur PM, Soderlund C, Penmetsa RV, Xu C, Bharti AK, He W, Winter P, Zhao S, Hane JK, Carrasquilla-Garcia N, Condie JA, Upadhyaya HD, Luo MC et al (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol 31:240–246

    Article  CAS  PubMed  Google Scholar 

  • Vazquez MD, Zemetra R, Peterson CJ, Mundt CC (2015) Identification of Cephalosporium stripe resistance quantitative trait loci in two recombinant inbred line populations of winter wheat. Theor Appl Genet 128:329–341

    Article  CAS  PubMed  Google Scholar 

  • Volt AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    Article  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weinreich DM, Watson RA, Chao L (2005) Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59:1165–1174

    Article  CAS  PubMed  Google Scholar 

  • Wroth JM (1999) Evidence suggests that Mycosphaerella pinodes infection of Pisum sativum is inherited as a quantitative trait. Euphytica 107:193–204

    Article  Google Scholar 

  • Wu Q, VanEtten HD (2004) Introduction of pland and fungal genes into pea (Pisum sativum L.) hairy roots reduces their ability to produce pisatin and affects their response to a fungal pathogen. Mol Plant Microb Interact 17:798–804

    Article  CAS  Google Scholar 

  • Würschum T, Maurer HP, Dreyer F, Reif JC (2013) Effect of inter- and intragenic epistasis on the heritability of oil content in rapeseed (Brassica napus L.). Theor Appl Genet 126:435–441

    Article  PubMed  Google Scholar 

  • Young ND, Debelle F, Oldroyd GE, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KF, Gouzy J, Schoof H, Van de Peer Y, Proost S, Cook DR, Meyers BC, Spannagl M, Cheung F, De Mita S, Krishnakumar V, Gundlach H, Zhou S, Mudge J, Bharti AK, Murray JD, Naoumkina MA, Rosen B, Silverstein KA, Tang H, Rombauts S, Zhao PX, Zhou P et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu LX, Lorenz A, Rutkoski J, Singh RP, Bhavani S, Huerta-Espino J, Sorrells ME (2011) Association mapping and gene-gene interaction for stem rust resistance in CIMMYT spring wheat germplasm. Theor Appl Genet 123:1257–1268

    Article  CAS  PubMed  Google Scholar 

  • Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48:592–605

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Samantha Baldwin, David Chagné and Vincent Bus for critical reading of the manuscript, and Donna Gibson for the Fig. 2 graphics. Funding was provided in part by the New Zealand Foundation for Research Science and Technology and the New Zealand Ministry for Business Innovation and Employment through Core funding to Plant & Food Research.

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Correspondence to Gail M. Timmerman-Vaughan.

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Timmerman-Vaughan, G.M., Moya, L., Frew, T.J. et al. Ascochyta blight disease of pea (Pisum sativum L.): defence-related candidate genes associated with QTL regions and identification of epistatic QTL. Theor Appl Genet 129, 879–896 (2016). https://doi.org/10.1007/s00122-016-2669-3

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