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Genome-wide linkage mapping of QTL for black point reaction in bread wheat (Triticum aestivum L.)

Abstract

Key message

Nine QTL for black point resistance in wheat were identified using a RIL population derived from a Linmai 2/Zhong 892 cross and 90K SNP assay.

Abstract

Black point, discoloration of the embryo end of the grain, downgrades wheat grain quality leading to significant economic losses to the wheat industry. The availability of molecular markers will accelerate improvement of black point resistance in wheat breeding. The aims of this study were to identify quantitative trait loci (QTL) for black point resistance and tightly linked molecular markers, and to search for candidate genes using a high-density genetic linkage map of wheat. A recombinant inbred line (RIL) population derived from the cross Linmai 2/Zhong 892 was evaluated for black point reaction during the 2011–2012, 2012–2013 and 2013–2014 cropping seasons, providing data for seven environments. A high-density linkage map was constructed by genotyping the RILs with the wheat 90K single nucleotide polymorphism (SNP) chip. Composite interval mapping detected nine QTL on chromosomes 2AL, 2BL, 3AL, 3BL, 5AS, 6A, 7AL (2) and 7BS, designated as QBp.caas-2AL, QBp.caas-2BL, QBp.caas-3AL, QBp.caas-3BL, QBp.caas-5AS, QBp.caas-6A, QBp.caas-7AL.1, QBp.caas-7AL.2 and QBp.caas-7BS, respectively. All resistance alleles, except for QBp.caas-7AL.1 from Linmai 2, were contributed by Zhong 892. QBp.caas-3BL, QBp.caas-5AS, QBp.caas-7AL.1, QBp.caas-7AL.2 and QBp.caas-7BS probably represent new loci for black point resistance. Sequences of tightly linked SNPs were used to survey wheat and related cereal genomes identifying three candidate genes for black point resistance. The tightly linked SNP markers can be used in marker-assisted breeding in combination with the kompetitive allele specific PCR technique to improve black point resistance.

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Abbreviations

ANOVA:

Analysis of variance

CIM:

Composite interval mapping

DH:

Doubled haploid

KASP:

Kompetitive allele specific PCR

LOD:

Logarithm of odds

LOX:

Lipoxygenase

MAS:

Marker-assisted selection

PAL:

Phenylalanine ammonialyase

POD:

Peroxidase

PPO:

Polyphenol oxidase

QTL:

Quantitative trait loci (locus)

RIL:

Recombinant inbred line

SNP:

Single nucleotide polymorphism

SSR:

Simple sequence repeat

References

  1. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Araji S, Grammer TA, Gertzen R, Anderson SD, Mikulic-Petkovsek M, Veberic R, Phu ML, Solar A, Leslie CA, Dandekar AM, Escobar MA (2014) Novel roles for the polyphenol oxidase enzyme in secondary metabolism and the regulation of cell death in walnut. Plant Physiol 164:1191–1203

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Avni R, Nave M, Eilam T, Sela H, Alekperov C, Peleg Z, Dvorak J, Korol A, Distelfeld A (2014) Ultra-dense genetic map of durum wheat × wild emmer wheat developed using the 90K iSelect SNP genotyping assay. Mol Breed 34:1549–1562

    CAS  Article  Google Scholar 

  4. Busman M, Desjardins AE, Proctor RH (2012) Analysis of fumonisin contamination and the presence of Fusarium in wheat with kernel black point disease in the US. Food Addit Contam 29:1092–1100

    CAS  Article  Google Scholar 

  5. Cabral AL, Jordan MC, McCartney CA, You FM, Humphreys DG, MacLachlan R, Pozniak CJ (2014) Identification of candidate genes, regions and markers for pre-harvest sprouting resistance in wheat (Triticum aestivum L.). BMC Plant Biol 14:340

    Article  PubMed  PubMed Central  Google Scholar 

  6. Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A, See D, Bai GH, Pumphrey M, Tomar L, Wong D, Kong S, Reynolds M, da Silva ML, Bockelman H, Talbert L, Anderson JA, Dreisigacker S, Baenziger S, Carter A, Korzun V, Morrell PL, Dubcovsky J, Morell MK, Sorrells ME, Hayden MJ, Akhunov E (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci USA 110:8057–8062

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Colasuonno P, Gadaleta A, Giancaspro A, Nigro D, Giove S, Incerti O, Mangini G, Signorile A, Simeone R, Blanco A (2014) Development of a high-density SNP-based linkage map and detection of yellow pigment content QTLs in durum wheat. Mol Breed 34:1563–1578

    CAS  Article  Google Scholar 

  8. Conner RL, Carefoot JM, Bole JB, Kozub GC (1992) The effect of nitrogen fertilizer and irrigation on black point incidence in soft white spring wheat. Plant Soil 140:41–47

    Article  Google Scholar 

  9. Conner RL, Davidson JGN (1988) Resistance in wheat to black point caused by Alternaria alternata and Cochliobolus sativus. Can J Plant Pathol 68:351–359

    Google Scholar 

  10. Cromey MG, Mulholland RI (1988) Black point of wheat: fungal associations, cultivar susceptibility, and effects on grain weight and germination. N Z J Agric Res 31:51–55

    Article  Google Scholar 

  11. Davis RM, Jackson LF (2009) UC IPM pest management guidelines: small grains. University of California ANR/Communication Services Diseases, Oakland

    Google Scholar 

  12. Desjardins AE, Busman M, Proctor RH, Stessman R (2007) Wheat kernel black point and fumonisin contamination by Fusarium proliferatum. Food Addit Contam 24:1131–1137

    CAS  Article  PubMed  Google Scholar 

  13. Dexter JE, Matsuo RR (1982) Effect of smudge and black point, mildewed kernels, and ergot on durum wheat quality. Cereal Chem 59:63–69

    Google Scholar 

  14. Dubiella U, Seybold H, Durian G, Komander E, Lassig R, Witte CP, Schulzeb WX, Romeisa T, Romeis T (2013) Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci USA 110:8744–8749

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Ellis SA, Gooding MJ, Thompson AJ (1996) Factors influencing the relative susceptibility of wheat cultivars (Triticum aestivum L.) to black point. Crop Prot 15:69–76

    Article  Google Scholar 

  16. Fernandez MR, Conner RL (2011) Black point and smudge in wheat. Prairie Soils Crops 4:158–164

    Google Scholar 

  17. Fernandez MR, Wang H, Singh AK (2014) Impact of seed discoloration on emergence and early plant growth of durum wheat at different soil gravimetric water contents. Can J Plant Pathol 36:509–516

    Article  Google Scholar 

  18. Fuerst EP, Okubara PA, Anderson JV, Morris CF (2014) Polyphenol oxidase as a biochemical seed defense mechanism. Front Plant Sci 5:689

    Article  PubMed  PubMed Central  Google Scholar 

  19. Gadaleta A, Giancaspro A, Giove SL, Zacheo S, Mangini G, Simeone R, Signorile A, Blanco A (2009) Genetic and physical mapping of new EST-derived SSRs on the A and B genome chromosomes of wheat. Theor Appl Genet 118:1015–1025

    CAS  Article  PubMed  Google Scholar 

  20. Gadaleta A, Giancaspro A, Nigro D, Giove SL, Incerti O, Simeone R, Piarulli L, Colasuonno P, Vale G, Cattivelli L, Blanco A (2014) A new genetic and deletion map of wheat chromosome 5A to detect candidate genes for quantitative traits. Mol Breed 34:1599–1611

    Article  Google Scholar 

  21. Gao FM, Wen WE, Liu JD, Rasheed A, Yin GH, Xia XC, Wu XX, He ZH (2015) Genome-wide linkage mapping of QTL for yield components, plant height and yield-related physiological traits in the Chinese wheat cross Zhou 8425B/Chinese Spring. Front Plant Sci 6:1099

    PubMed  PubMed Central  Google Scholar 

  22. Gupta PK, Rustgi S, Mir RR (2008) Array-based high-throughput DNA markers for crop improvement. Heredity 101:5–18

    CAS  Article  PubMed  Google Scholar 

  23. He HG, Zhu SY, Jiang ZN, Ji YY, Wang F, Zhao RH, Bie TD (2016) Comparative mapping of powdery mildew resistance gene Pm21 and functional characterization of resistance-related genes in wheat. Theor Appl Genet 129:819–829

    CAS  Article  PubMed  Google Scholar 

  24. Hudec K (2007) Pathogenicity of fungi associated with wheat and barley seedling emergence and fungicide efficacy of seed treatment. Biologia 62:287–291

    CAS  Article  Google Scholar 

  25. Iyer LM, Leipe DD, Koonin EV, Aravind L (2004) Evolutionary history and higher order classification of AAA + ATPases. J Struct Biol 146:11–31

    CAS  Article  PubMed  Google Scholar 

  26. Jungwirth H, Ring J, Mayer T, Schauer A, Büttner S, Eisenberg T, Carmona-Gutierreza D, Kuchlerb K, Madeo F (2008) Loss of peroxisome function triggers necrosis. FEBS Lett 582:2882–2886

    CAS  Article  PubMed  Google Scholar 

  27. Kahl SM, Ulrich A, Kirichenko AA, Müller ME (2015) Phenotypic and phylogenetic segregation of Alternaria infectoria from small-spored Alternaria species isolated from wheat in Germany and Russia. J Appl Microbiol 119:1637–1650

    CAS  Article  PubMed  Google Scholar 

  28. Kosambi DD (1943) The estimation of map distance from recombination values. Annu Eugen 12:172–175

    Article  Google Scholar 

  29. Kumar J, Schäfer P, Hückelhoven R, Langen G, Baltruschat H, Stein E, Nagarajan S, Kogel KH (2002) Bipolaris sorokiniana, a cereal pathogen of global concern: cytological and molecular approaches towards better control. Mol Plant Pathol 3:185–195

    CAS  Article  PubMed  Google Scholar 

  30. Kumar S, Kawałek A, van der Klei IJ (2014) Peroxisomal quality control mechanisms. Curr Opin Microbiol 22:30–37

    CAS  Article  PubMed  Google Scholar 

  31. Lehmensiek A, Campbell AW, Williamson PM, Michalowitz M, Sutherland MW, Daggard G (2004) QTLs for black point resistance in wheat and the identification of potential markers for use in breeding programs. Plant Breed 123:410–416

    CAS  Article  Google Scholar 

  32. Li HH, Ye GY, Wang JK (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374

    Article  PubMed  PubMed Central  Google Scholar 

  33. Li WL, Faris JD, Chittoor JM, Leach JE, Hulbert SH, Liu DJ, Chen PD, Gill BS (1999) Genomic mapping of defense response genes in wheat. Theor Appl Genet 98:226–233

    CAS  Article  Google Scholar 

  34. Liu X, Yang LH, Zhou XY, Zhou MP, Lu Y, Ma LJ, Ma HX, Zhang ZY (2013) Transgenic wheat expressing Thinopyrum intermedium MYB transcription factor TiMYB2R-1 shows enhanced resistance to the take-all disease. J Exp Bot 64:2243–2253

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Liu ZX, Liu F, Li BQ, Wang J, Zhu XL, Wang GX (2005) Breeding and cultivation technique of new winter wheat variety-Linmai No. 2. Chin Agric Bull 21:188–192

    Google Scholar 

  36. Mak Y, Willows RD, Roberts TH, Wrigley CW, Sharp PJ, Copeland L (2006) Black point is associated with reduced levels of stress, disease and defence related proteins in wheat grain. Mol Plant Pathol 7:177–189

    CAS  Article  PubMed  Google Scholar 

  37. Marasas WFO (2001) Discovery and occurrence of the fumonisins: a historical perspective. Environ Health Persp 109:239–243

    CAS  Article  Google Scholar 

  38. March TJ, Able JA, Schultz C, Able AJ (2007) A novel late embryogenesis abundant protein and peroxidase associated with black point in barley grains. Proteomics 7:3800–3808

    CAS  Article  PubMed  Google Scholar 

  39. Palacios SA, Susca A, Haidukowski M, Stea G, Cendoya E, Ramírez ML, Chulze SN, Farnochi MC, Moretti A, Torres AM (2015) Genetic variability and fumonisin production by Fusarium proliferatum isolated from durum wheat grains in Argentina. Int J Food Microbiol 201:35–41

    CAS  Article  PubMed  Google Scholar 

  40. Perelló A, Moreno M, Sisterna M (2008) Alternaria infectoria species-group associated with black point of wheat in Argentina. Plant Pathol 57:379

    Article  Google Scholar 

  41. Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiol 130:15–21

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Qi LL, Echalier B, Chao S, Lazo GR, Butler GE, Anderson OD, Dubcovsky J (2004) A chromosome bin map of 16,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Qin YX, Wang MC, Tian YC, He WX, Han L, Xia GM (2012) Over-expression of TaMYB33 encoding a novel wheat MYB transcription factor increases salt and drought tolerance in Arabidopsis. Mol Biol Rep 39:7183–7192

    CAS  Article  PubMed  Google Scholar 

  44. Regnier T, Macheix JJ (1996) Changes in wall bound phenolic acids, phenylalanine and tyrosine ammonia-lyases, and peroxidases in developing durum wheat grains (Triticum turgidum L. var. durum). J Agric Food Chem 44:1727–1730

    CAS  Article  Google Scholar 

  45. Russo MA, Ficco DBM, Laido G, Marone D, Papa R, Blanco A, Gadaleta A, Vita PD, Mastrangelo AM (2014) A dense durum wheat × T. dicoccum linkage map based on SNP markers for the study of seed morphology. Mol Breed 34:1579–1597

    Article  Google Scholar 

  46. Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8018

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Semagn K, Babu R, Hearne S, Olsen M (2014) Single nucleotide polymorphism genotyping using Kompetitive Allele Specific PCR (KASP): overview of the technology and its application in crop improvement. Mol Breed 33:1–14

    CAS  Article  Google Scholar 

  48. Southwell RJ, Brown JF, Wong PT (1980) Effect of inoculum density, stage of plant growth and dew period on the incidence of black point caused by Alternaria alternata in durum wheat. Ann Appl Biol 96:29–35

    Article  Google Scholar 

  49. Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: JoinMap. Plant J 3:739–744

    CAS  Article  Google Scholar 

  50. Sun DJ, He ZH, Xia XC, Zhang LP, Morris CF, Apples R, Ma WJ, Wang H (2005) A novel STS marker for polyphenol oxidase activity in bread wheat. Mol Breed 16:209–218

    CAS  Article  Google Scholar 

  51. Tah PR, Lehmensiek A, Fox GP, Mace E, Sulman M, Bloustein G, Daggard GE (2010) Identification of genetic regions associated with black point in barley. Field Crop Res 115:61–66

    Article  Google Scholar 

  52. Tiwari VK, Wang SC, Sehgal S, Vrána J, Friebe B, Kubaláková M, Chhuneja P, Doležel J, Akhunov E, Kalia B, Sabir J, Gill BS (2014) SNP discovery for mapping alien introgressions in wheat. BMC Genom 15:273

    Article  Google Scholar 

  53. Tomás-Barberán FA, Espín JC (2001) Phenolic compounds and related enzymes as determinants of quality in fruits and vegetables. J Sci Food Agric 81:853–876

    Article  Google Scholar 

  54. Veldboom LR, Lee M (1996) Genetic mapping of quantitative trait loci in maize in stress and non-stress environments: I. Grain yield and yield components. Crop Sci 36:1310–1319

    CAS  Article  Google Scholar 

  55. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    CAS  Article  PubMed  Google Scholar 

  56. Walker KR, Able JA, Mather DE, Able AJ (2008) Black point formation in barley: environmental influences and quantitative trait loci. Aust J Agric Res 59:1021–1029

    CAS  Article  Google Scholar 

  57. Wang S, Basten CJ, Zeng ZB (2006) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm

  58. Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Stephen S, Barker G, Wieseke R, Plieske J, International Wheat Genome Sequencing Consortium, Lillemo M, Mather D, Appels R, Dulferos R, Brown-Guedira G, Korol A, Akhunova AR, Feuillet C, Salse J, Morgante M, Pozniak C, Luo MC, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E (2014) Characterization of polyploid wheat genomic diversity using the high-density 90,000 SNP array. Plant Biotechnol J 12:787–796

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. Wei JX, Geng HW, Zhang Y, Liu JD, Wen WE, Xia XC, Chen XM, He ZH (2015) Mapping quantitative trait loci for peroxidase activity and developing gene-specific markers for TaPod-A1 on wheat chromosome 3AL. Theor Appl Genet 128:2067–2076

    CAS  Article  PubMed  Google Scholar 

  60. Williamson PM (1997) Black point of wheat: in vitro production of symptoms, enzymes involved, and association with Alternaria alternata. Aust J Agri Res 48:13–19

    Article  Google Scholar 

  61. Yang F, Li W, Jørgensen HJ (2013) Transcriptional reprogramming of wheat and the hemibiotrophic pathogen Septoria tritici during two phases of the compatible interaction. PLoS One 8:e81606

    Article  PubMed  PubMed Central  Google Scholar 

  62. Zhai SN, He ZH, Wen WE, Jin H, Liu JD, Zhang Y, Liu ZY, Xia XC (2016) Genome-wide linkage mapping of flour color-related traits and polyphenol oxidase activity in common wheat. Theor Appl Genet 129:377–394

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Prof. R. A. McIntosh, Plant Breeding Institute, University of Sydney, for critical review of this manuscript. This study was supported by the National Natural Science Foundation of China (31461143021), Beijing Municipal Science and Technology Project (D151100004415003) and National Key Project (2016YFD0101802).

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Correspondence to Xianchun Xia.

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We declare that these experiments comply with the ethical standards in China.

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Communicated by I. D Godwin.

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Liu, J., He, Z., Wu, L. et al. Genome-wide linkage mapping of QTL for black point reaction in bread wheat (Triticum aestivum L.). Theor Appl Genet 129, 2179–2190 (2016). https://doi.org/10.1007/s00122-016-2766-3

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Keywords

  • Quantitative Trait Locus
  • Quantitative Trait Locus Analysis
  • Quantitative Trait Locus Mapping
  • Single Nucleotide Polymorphism Marker
  • Quantitative Trait Locus Region