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Development and validation of high-throughput and low-cost STARP assays for genes underpinning economically important traits in wheat

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Abstract

Key message

We developed and validated 56 gene-specific semi-thermal asymmetric reverse PCR (STARP) markers for 46 genes of important wheat quality, biotic and abiotic stress resistance, grain yield, and adaptation-related traits for marker-assisted selection in wheat breeding.

Abstract

Development of high-throughput, low-cost, gene-specific molecular markers is important for marker-assisted selection in wheat breeding. In this study, we developed 56 gene-specific semi-thermal asymmetric reverse PCR (STARP) markers for wheat quality, tolerance to biotic and abiotic stresses, grain yield, and adaptation-related traits. The STARP assays were validated by (1) comparison of the assays with corresponding diagnostic STS/CAPS markers on 40 diverse wheat cultivars and (2) characterization of allelic effects based on the phenotypic and genotypic data of three segregating populations and 305 diverse wheat accessions from China and 13 other countries. The STARP assays showed the advantages of high-throughput, accuracy, flexibility, simple assay design, low operational costs, and platform compatibility. The state-of-the-art assays of this study provide a robust and reliable molecular marker toolkit for wheat breeding programs.

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Abbreviations

AFLP:

Amplified fragment length polymorphism

AMAS primer:

Asymmetrically modified allele-specific primer

AS-probe:

Allele-specific probe

CAPS:

Cleaved amplified polymorphic sequences

FM:

Functional markers

GI:

Germination index

GL:

Grain length

HD:

Heading date

HI:

Hardness Index

HMW-GS:

High molecular weight glutenin subunits

KASP:

Kompetitive allele-specific PCR

KNS:

Kernel number per spike

LMW-GS:

Low molecular weight glutenin subunits

LOX:

Lipoxygenase

MAS:

Marker-assisted selection

MTxW:

Mixograph midline 8 min band width

NS:

Number of spikes

PAGE:

Polyacrylamide gel electrophoresis

PDS:

Phytoene desaturase

PEA primer:

Priming element-adjustable primer

PH:

Plant height

POD:

Peroxidase

PPO:

Polyphenol oxidase

RAPD:

Random amplification of polymorphic DNA

RFLP:

Restriction fragment length polymorphism

SKCS:

Single kernel characterization system

SSR:

Simple sequence repeat

STARP:

Semi-thermal asymmetric reverse PCR

TKW:

Thousand kernel weight

TS-PCR:

Temperature-switch PCR

YPC:

Yellow pigment content

ZDS:

Zeta-carotene desaturase

References

  • Andersen JR, Lübberstedt T (2003) Functional markers in plants. Trends Plant Sci 8:554–560

    CAS  PubMed  Google Scholar 

  • Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng DZ, Platt A, Tarone AM, Hu TT, Jiang R, Muliyati NW, Zhang X, Amer MA, Baxter I, Brachi B, Chory J, Dean C, Debieu M, de Meaux J, Ecker JR, Faure N, Kniskern JM, Jones JDG, Michael T, Nemri A, Roux F, Salt DE, Tang CL, Todesco M, Traw MB, Weigel D, Marjoram P, Borevitz JO, Bergelson J, Nordborg M (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465:627–631

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ayalew H, Tsang PW, Chu CG, Wang JZ, Liu SY, Chen CF, Ma XF (2019) Comparison of TaqMan, KASP and rhAmp SNP genotyping platforms in hexaploid wheat. PLoS ONE 14:e0217222

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bagge M, Xia XC, Lübberstedt T (2007) Functional markers in wheat. Curr Opin Plant Biol 10:211–216

    CAS  PubMed  Google Scholar 

  • Barbazuk WB, Emrich SJ, Chen HD, Li L, Schnable PS (2007) SNP discovery via 454 transcriptome sequencing. Plant J 51:910–918

    CAS  PubMed  PubMed Central  Google Scholar 

  • Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32:314–331

    CAS  PubMed  PubMed Central  Google Scholar 

  • Broccanello C, Chiodi X, Funk A, McGrath JM, Panella L, Stevanato P (2018) Comparison of three PCR-based assays for SNP genotyping in plants. Plant Methods 14:28

    PubMed  PubMed Central  Google Scholar 

  • Chen F, Zhang FY, Cheng XY, Morris C, Xu HX, Dong ZD, Zhan KH, Cui DQ (2010) Association of Puroindoline b-B2 variants with grain traits, yield components and flag leaf size in bread wheat (Triticum aestivum L.) varieties of the Yellow and Huai Valleys of China. J Cereal Sci 52:247–253

    CAS  Google Scholar 

  • Chen XY, Cao XY, Zhang YJ, Islam S, Zhang JJ, Yang RC, Liu JJ, Li GY, Appels R, Keeble-Gagnere G, Ji WQ, He ZH, Ma WJ (2016) Genetic characterization of cysteine-rich type-b avenin-like protein coding genes in common wheat. Sci Rep 6:30692

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ching A, Caldwell KS, Jung M, Dolan M, Smith OS, Tingey S, Morgante M, Rafalski AJ (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet 3:19

    PubMed  PubMed Central  Google Scholar 

  • Close TJ, Bhat PR, Lonardi S, Wu YH, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, Bozdag S, Roose ML, Moscou MJ, Chao SM, Varshney RK, Szucs P, Sato K, Hayes PM, Matthews DE, Kleinhofs A, Muehlbauer GJ, DeYoung J, Marshall DF, Madishetty K, Fenton RD, Condamine P (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genom 10:582

    Google Scholar 

  • Cormier F, Throude M, Ravel C, Gouis J, Leveugle M, Lafarge S, Exbrayat F, Duranton N, Praud S (2015) Detection of NAM-A1 natural variants in bread wheat reveals differences in haplotype distribution between a worldwide core collection and European elite germplasm. Agronomy 5:143–151

    CAS  Google Scholar 

  • Crawford AC, Francki MG (2013) Lycopene-ε-cyclase (e-LCY3A) is functionally associated with quantitative trait loci for flour b* colour on chromosome 3A in wheat (Triticum aestivum L.). Mol Breeding 31:737–741

    CAS  Google Scholar 

  • Cui F, Zhao CH, Ding AM, Li J, Wang L, Li XF, Bao YG, Li JM, Wang HG (2014) Construction of an integrative linkage map and QTL mapping of grain yield-related traits using three related wheat RIL populations. Theor Appl Genet 127:659–675

    PubMed  Google Scholar 

  • De la Vega FM, Lazaruk KD, Rhodes MD, Wenz MH (2005) Assessment of two flexible and compatible SNP genotyping platforms: TaqMan® SNP genotyping assays and the SNPlex™ genotyping system. Mutat Res 573:111–135

    PubMed  Google Scholar 

  • Díaz A, Zikhali M, Turner AS, Isaac P, Laurie DA (2012) Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum). PLoS ONE 7:e33234

    PubMed  PubMed Central  Google Scholar 

  • Dong CH (2011) Cloning of genes associated with grain yellow pigment content in common wheat and development of functional markers. Dissertation, Agricultural University of Hebei Province

  • Dong CH, Ma ZY, Xia XC, Zhang LP, He ZH (2012) Allelic variation at the TaZds-A1 locus on wheat chromosome 2A and development of a functional marker in common wheat. J Integr Agric 11:1067–1074

    CAS  Google Scholar 

  • Dong LL, Wang FM, Liu T, Dong ZY, Li AL, Jing RL, Mao L, Li YW, Liu X, Zhang KP, Wang DW (2014) Natural variation of TaGASR7-A1 affects grain length in common wheat under multiple cultivation conditions. Mol Breeding 34:937–947

    CAS  Google Scholar 

  • Dreisigacker S, Sukumaran S, Guzmán C, He XY, Lan CX, Bonnett D, Crossa J (2016) Molecular marker-based selection tools in spring bread wheat improvement: CIMMYT experience and prospects. Mol Breed Sustain Crop Improv 2:421–474

    Google Scholar 

  • Ellis H, Spielmeyer W, Gale R, Rebetzke J, Richards A (2002) “Perfect” markers for the Rht-B1b and Rht-D1b dwarfing genes in wheat. Theor Appl Genet 105:1038–1042

    CAS  PubMed  Google Scholar 

  • Eujayl I, Sorrells ME, Baum M, Wolters P, Powell W (2002) Isolation of EST-derived microsatellite markers for genotyping the A and B genomes of wheat. Theor Appl Genet 104:399–407

    CAS  PubMed  Google Scholar 

  • Fu DL, Szücs P, Yan LL, Helguera M, Skinner JS, von Zitzewitz J, Hayes PM, Dubcovsky J (2005) Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol Gen Genomics 273:54–65

    CAS  Google Scholar 

  • 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 

  • Geng HW, Xia XC, Zhang LP, Qu YY, He ZH (2012) Development of functional markers for a lipoxygenase gene TaLox-B1 on chromosome 4BS in common wheat. Crop Sci 52:568–576

    CAS  Google Scholar 

  • Giroux MJ, Morris CF (1997) A glycine to serine change in puroindoline b is associated with wheat grain hardness and low levels of starch-surface friabilin. Theor Appl Genet 95:857–864

    CAS  Google Scholar 

  • Giroux MJ, Morris CF (1998) Wheat grain hardness results from highly conserved mutations in the friabilin components puroindoline a and b. Proc Natl Acad Sci USA 95:6262–6266

    CAS  PubMed  Google Scholar 

  • Grover A, Sharma PC (2016) Development and use of molecular markers: past and present. Crit Rev Biotechnol 36:290–302

    CAS  PubMed  Google Scholar 

  • Guillemaut P, Maréchal-Drouard L (1992) Isolation of plant DNA: a fast, inexpensive, and reliable method. Plant Mol Biol Rep 10:60–65

    CAS  Google Scholar 

  • Hackauf B, Wehling P (2002) Identification of microsatellite polymorphisms in an expressed portion of the rye genome. Plant Breeding 121:17–25

    CAS  Google Scholar 

  • He XY, He ZH, Zhang LP, Sun DJ, Morris CF, Fuerst EP, Xia XC (2007) Allelic variation of polyphenol oxidase (PPO) genes located on chromosomes 2A and 2D and development of functional markers for the PPO genes in common wheat. Theor Appl Genet 115:47–58

    CAS  PubMed  Google Scholar 

  • He XY, Zhang YL, He ZH, Wu YP, Xiao YG, Ma CX, Xia XC (2008) Characterization of phytoene synthase 1 gene (Psy1) located on common wheat chromosome 7A and development of a functional marker. Theor Appl Genet 116:213–221

    CAS  PubMed  Google Scholar 

  • He XY, He ZH, Ma W, Appels R, Xia XC (2009) Allelic variants of phytoene synthase 1 (Psy1) genes in Chinese and CIMMYT wheat cultivars and development of functional markers for flour colour. Mol Breeding 23:553–563

    CAS  Google Scholar 

  • IWGSC (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:7191

    Google Scholar 

  • Jatayev S, Kurishbayev A, Zotova L, Khasanova G, Serikbay D, Zhubatkanov A, Botayeva M, Zhumalin A, Turbekova A, Soole K, Langridge P, Shavrukov Y (2017) Advantages of Amplifluor-like SNP markers over KASP in plant genotyping. BMC Plant Biol 17:254

    PubMed  PubMed Central  Google Scholar 

  • Jia AL, Ren Y, Gao FM, Yin GH, Liu JD, Guo L, Zheng JZ, He ZH, Xia XC (2018) Mapping and validation of a new QTL for adult-plant resistance to powdery mildew in Chinese elite bread wheat line Zhou8425B. Theor Appl Genet 131:1063–1071

    PubMed  Google Scholar 

  • Jin H, Wen W, Liu JD, Zhai SN, Zhang Y, Yan J, Liu ZY, Xia XC, He ZH (2016) Genome-wide QTL mapping for wheat processing quality parameters in a Gaocheng 8901/Zhoumai 16 recombinant inbred line population. Front Plant Sci 7:1032

    PubMed  PubMed Central  Google Scholar 

  • Kage U, Kumar A, Dhokane D, Karre S, Kushalappa AC (2016) Functional molecular markers for crop improvement. Crit Rev Biotechnol 36:917–930

    CAS  PubMed  Google Scholar 

  • Klindworth DL, Saini J, Long YM, Rouse MN, Faris JD, Jin Y, Xu SS (2017) Physical mapping of DNA markers linked to stem rust resistance gene Sr47 in durum wheat. Theor Appl Genet 130:1135–1154

    CAS  PubMed  Google Scholar 

  • Kolchanov NA, Kochetov AV, Salina EA, Pershina LA, Khlestkina EK, Shumny VK (2017) Status and prospects of marker-assisted and genomic plant breeding. Her Russ Acad Sci 87:125–131

    Google Scholar 

  • Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4:403–410

    CAS  PubMed  Google Scholar 

  • Lagudah ES, Krattinger SG, Herrera-Foessel S, Singh RP, Huerta-Espino J, Spielmeyer W, Brown-Guedira G, Selter LL, Keller B (2009) Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theor Appl Genet 119:889–898

    CAS  PubMed  Google Scholar 

  • Lei L, Zhu XK, Wang SW, Zhu MR, Carver BF, Yan LL (2013) TaMFT-A1 is associated with seed germination sensitive to temperature in winter wheat. PLoS ONE 8:e73330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li XP, Zhao XQ, He X, Zhao GY, Li B, Liu DC, Zhang AM, Zhang XY, Tong YP, Li ZS (2011) Haplotype analysis of the genes encoding glutamine synthetase plastic isoforms and their association with nitrogen-use- and yield-related traits in bread wheat. New Phytol 189:449–458

    CAS  PubMed  Google Scholar 

  • Li FJ, Wen WE, He ZH, Liu JD, Jin H, Cao SH, Geng HW, Yan J, Zhang PZ, Wan YX, Xia XC (2018) Genome-wide linkage mapping of yield-related traits in three Chinese bread wheat populations using high-density SNP markers. Theor Appl Genet 131:1903–1924

    PubMed  Google Scholar 

  • Liang D, Tang JW, Pena RJ, Singh R, He XY, Shen XY, Yao DN, Xia XC, He ZH (2010) Characterization of CIMMYT bread wheats for high- and low-molecular weight glutenin subunits and other quality-related genes with SDS-PAGE, RP-HPLC and molecular markers. Euphytica 172:235–250

    CAS  Google Scholar 

  • Liu SX, Chao S, Anderson J (2008) New DNA markers for high molecular weight glutenin subunits in wheat. Theor Appl Genet 118:177–183

    CAS  PubMed  Google Scholar 

  • Liu YN, He ZH, Appels R, Xia XC (2012) Functional markers in wheat: current status and future prospects. Theor Appl Genet 125:1–10

    CAS  PubMed  Google Scholar 

  • Liu SB, Sehgal SK, Li JR, Lin M, Trick HN, Yu JM, Gill BS, Bai GH (2013) Cloning and characterization of a critical regulator for preharvest sprouting in wheat. Genetics 195:263–273

    CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ (1999) Allelic discrimination using fluorogenic probes and the 5′ nuclease assay. Genet Anal Biomol Eng 14:143–149

    CAS  Google Scholar 

  • Livak KJ, Flood SJA, Marmaro J, Giusti W, Deetz K (1995) Oligonucieotides with fluorescent dyes at opposite ends provied a quenched probe system useful for detecting PCR product and nucleic-acid hybridization. PCR Methods Appl 4:357–362

    CAS  PubMed  Google Scholar 

  • Long YM, Chao WS, Ma GJ, Xu SS, Qi LL (2017) An innovative SNP genotyping method adapting to multiple platforms and throughputs. Theor Appl Genet 130:597–607

    CAS  PubMed  Google Scholar 

  • Ma DY, Yan J, He ZH, Wu L, Xia XC (2012) Characterization of a cell wall invertase gene TaCwi-A1 on common wheat chromosome 2A and development of functional markers. Mol Breeding 29:43–52

    CAS  Google Scholar 

  • Mammadov J, Aggarwal R, Buyyarapu R, Kumpatla S (2012) SNP markers and their impact on plant breeding. Int J Plant Genomics 2012:728398

    PubMed  PubMed Central  Google Scholar 

  • Miedaner T, Korzun V (2012) Marker-assisted selection for disease resistance in wheat and barley breeding. Phytopathology 102:560–566

    PubMed  Google Scholar 

  • Muterko A, Salina E (2019) Divergence of VRN-B3 alleles during the evolution of domesticated wheat. Mol Genet Genomics 294:263–275

    CAS  PubMed  Google Scholar 

  • Myakishev MV, Khripin Y, Hu S, Hamer DH (2001) High-throughput SNP genotyping by allele-specific PCR with universal energy-transfer-labeled primers. Genome Res 11:163–169

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A, Matsumoto T, Utsugi S, Ogawa T, Handa H, Ishida H, Mori M, Kawaura K, Ogihara Y, Miura H (2011) A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell 23:3215–3229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Neff MM, Neff JD, Chory J, Pepper AE (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14:387–392

    CAS  PubMed  Google Scholar 

  • Newton CR, Graham A, Heptinstall LE, Powell SJ, Summers C, Kalsheker N, Smith JC, Markham AF (1989) Analysis of any point mutation in DNA. The amplification refractory mutation system (ARMS). Nucleic Acids Res 17:2503–2516

    CAS  PubMed  PubMed Central  Google Scholar 

  • Powell N, Ji XM, Ravash R, Edlington J, Dolferus R (2012) Yield stability for cereals in a changing climate. Funct Plant Biol 39:539–552

    PubMed  Google Scholar 

  • Qi LL, Foley ME, Cai XW, Gulya TJ (2016) Genetics and mapping of a novel downy mildew resistance gene, Pl18, introgressed from wild Helianthus argophyllus into cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 129:741–752

    CAS  PubMed  Google Scholar 

  • Qi LL, Talukder ZI, Hulke BS, Foley ME (2017) Development and dissection of diagnostic SNP markers for the downy mildew resistance genes PlArg and Pl8 and marker-assisted gene pyramiding in sunflower (Helianthus annuus L.). Mol Genet Genomics 292:551–563

    CAS  PubMed  Google Scholar 

  • Ramirez-Gonzalez RH, Uauy C, Caccamo M (2015) PolyMarker: a fast polyploid primer design pipeline. Bioinformatics 31:2038–2039

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rasheed A, Xia XC (2019) From markers to genome-based breeding in wheat. Theor Appl Genet 132:767–784

    CAS  PubMed  Google Scholar 

  • Rasheed A, Wen WE, Gao FM, Zhai SN, Jin H, Liu JD, Guo Q, Zhang YJ, Dreisigacker S, Xia XC, He ZH (2016) Development and validation of KASP assays for genes underpinning key economic traits in bread wheat. Theor Appl Genet 129:1843–1860

    CAS  PubMed  Google Scholar 

  • Raza A, Razzaq A, Mehmood SS, Zou XL, Zhang XK, Lv Y, Xu JS (2019) Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants 8:34

    CAS  PubMed Central  Google Scholar 

  • Riley MC, Aubrey W, Young M, Clare A (2013) PD5: a general purpose library for primer design software. PLoS ONE 8:e80156

    PubMed  PubMed Central  Google Scholar 

  • Schwarz G, Sift A, Wenzel G, Mohler V (2003) DHPLC scoring of a SNP between promoter sequences of HMW glutenin x-type alleles at the Glu-D1 locus in wheat. J Agric Food Chem 51:4263–4267

    CAS  PubMed  Google Scholar 

  • 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 Breeding 33:1–14

    CAS  Google Scholar 

  • Shi JQ, Li RY, Qiu D, Jiang CC, Long Y, Morgan C, Bancroft I, Zhao JY, Meng JL (2009) Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassica napus. Genetics 182:851–861

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • Sun CW, Zhang FY, Yan XF, Zhang XF, Dong ZD, Cui DQ, Chen F (2017) Genome-wide association study for 13 agronomic traits reveals distribution of superior alleles in bread wheat from the Yellow and Huai Valley of China. Plant Biotechnol J 15:953–969

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tabone T, Mather DE, Hayden MJ (2009) Temperature Switch PCR (TSP): robust assay design for reliable amplification and genotyping of SNPs. BMC Genom 10:580

    Google Scholar 

  • Thiel T, Michalek W, Varshney RK, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422

    CAS  PubMed  Google Scholar 

  • Tyagi S, Kramer FR (1996) Molecular beacons: probes that fluoresce upon hybridization. Nat Biotechnol 14:303–308

    CAS  PubMed  Google Scholar 

  • Tyagi S, Bratu DP, Kramer FR (1998) Multicolor molecular beacons for allele discrimination. Nat Biotechnol 16:49–53

    CAS  PubMed  Google Scholar 

  • Van Tienderen PH, De Haan AA, Van der Linden CG, Vosman B (2002) Biodiversity assessment using markers for ecologically important traits. Trends Ecol Evol 17:577–582

    Google Scholar 

  • Varshney RK, Graner A, Sorrells ME (2005) Genomics-assisted breeding for crop improvement. Trends Plant Sci 10:621–630

    CAS  PubMed  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Vandelee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang LH, Zhao XL, He ZH, Ma W, Appels R, Pena RJ, Xia XC (2009) Characterization of low-molecular-weight glutenin subunit Glu-B3 genes and development of STS markers in common wheat (Triticum aestivum L.). Theor Appl Genet 118:525–539

    CAS  PubMed  Google Scholar 

  • Wang LH, Li GY, Pena RJ, Xia XC, He ZH (2010) Development of STS markers and establishment of multiplex PCR for Glu-A3 alleles in common wheat (Triticum aestivum L.). J Cereal Sci 51:305–312

    CAS  Google Scholar 

  • Wang SC, Wong DB, Forrest K, Allen A, Chao SM, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, Lillemo M, Mather D, Appels R, Dolferus 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, Int Wheat Genome S (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wei B, Jing RL, Wang CS, Chen JB, Mao XG, Chang XP, Jia JZ (2009) Dreb1 genes in wheat (Triticum aestivum L.): development of functional markers and gene mapping based on SNPs. Mol Breeding 23:13–22

    CAS  Google Scholar 

  • Wei JX, Geng HW, Zhang Y, Liu JD, Wen W, Zhang Y, 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  PubMed  Google Scholar 

  • Welsh J, McClelland M (1990) Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res 18:7213–7218

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whitcombe D, Theaker J, Guy SP, Brown T, Little S (1999) Detection of PCR products using self-probing amplicons and fluorescence. Nat Biotechnol 17:804–807

    CAS  PubMed  Google Scholar 

  • Xu X, Liu X, Ge S, Jensen JD, Hu FY, Li X, Dong Y, Gutenkunst RN, Fang L, Huang L, Li JX, He WM, Zhang GJ, Zheng XM, Zhang FM, Li YR, Yu C, Kristiansen K, Zhang XQ, Wang J, Wright M, McCouch S, Nielsen R, Wang J, Wang W (2011) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30:105–111

    CAS  PubMed  Google Scholar 

  • Yang Y, Ma YZ, Xu ZS, Chen XM, He ZH, Yu Z, Wilkinson M, Jones HD, Shewry PR, Xia LQ (2007) Isolation and characterization of Viviparous-1 genes in wheat cultivars with distinct ABA sensitivity and pre-harvest sprouting tolerance. J Exp Bot 58:2863–2871

    CAS  PubMed  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Zhang YJ, Liu JD, Xia XC, He ZH (2014a) TaGS-D1, an ortholog of rice OsGS3, is associated with grain weight and grain length in common wheat. Mol Breed 34:1097–1107

    CAS  Google Scholar 

  • Zhang YJ, Miao XL, Xia XC, He ZH (2014b) Cloning of seed dormancy genes (TaSdr) associated with tolerance to pre-harvest sprouting in common wheat and development of a functional marker. Theor Appl Genet 127:855–866

    CAS  PubMed  Google Scholar 

  • Zhang B, Liu X, Xu WN, Chang JZ, Li A, Mao XG, Zhang XY, Jing RL (2015) Novel function of a putative MOC1 ortholog associated with spikelet number per spike in common wheat. Sci Rep 5:12211

    PubMed  PubMed Central  Google Scholar 

  • Zhang PF, He ZH, Tian XL, Gao FM, Xu DG, Liu JD, Wen WE, Fu LP, Li GY, Sui XX, Xia XC, Wang CP, Cao SH (2017) Cloning of TaTPP-6AL1 associated with grain weight in bread wheat and development of functional marker. Mol Breed 37:78

    Google Scholar 

  • Zhao Y, Mette MF, Gowda M, Longin CFH, Reif JC (2014) Bridging the gap between marker-assisted and genomic selection of heading time and plant height in hybrid wheat. Heredity 112:638–645

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng J, Liu H, Wang YQ, Wang LF, Chang XP, Jing RL, Hao CY, Zhang XY (2014) TEF-7A, a transcript elongation factor gene, influences yield-related traits in bread wheat (Triticum aestivum L.). J Exp Bot 65:5351–5365

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Prof. R. A. McIntosh, Plant Breeding Institute, University of Sydney, for reviewing this manuscript. This work was funded by the National Natural Science Foundation of China (31461143021, 31961143007, 31971929), the National Key Research and Development Program of China (2016YFD0101802, 2016YFE0108600), and CAAS Science and Technology Innovation Program.

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Authors and Affiliations

  1. Institute of Crop Sciences, National Wheat Improvement Center, Chinese Academy of Agricultural Sciences (CAAS), 12 Zhongguancun South Street, Beijing, 100081, China

    Yuying Wu, Ming Li, Zhonghu He, Shuanghe Cao & Xianchun Xia

  2. International Maize and Wheat Improvement Center (CIMMYT) China Office, c/o CAAS, 12 Zhongguancun South Street, Beijing, 100081, China

    Zhonghu He

  3. Global Wheat Program, International Maize and Wheat Improvement Center (CIMMYT), Apdo. Postal 6-641, 06600, Mexico, DF, Mexico

    Susanne Dreisigacker

  4. Department of Cell Biology, Zunyi Medical University, 201 Dalian Road, Zunyi, 563099, Guizhou, China

    Weie Wen

  5. Institute of Forage and Grassland Sciences, Heilongjiang Academy of Agricultural Sciences, 368 Xuefu Street, Harbin, 150086, Heilongjiang, China

    Hui Jin

  6. Crop Research Institute, Heilongjiang Academy of Agricultural Sciences, 368 Xuefu Street, Harbin, 150086, Heilongjiang, China

    Fengmei Gao

  7. Crop Research Institute, National Engineering Laboratory for Wheat and Maize, Key Laboratory of Wheat Biology and Genetic Improvement in the Northern Yellow-Huai Rivers Valley of Ministry of Agriculture and Rural Affairs, Shandong Academy of Agricultural Sciences, 202 Gongye North Road, Jinan, 250100, Shandong, China

    Shengnan Zhai & Faji Li

  8. Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, 7 Pengfei Road, Shenzhen, 518120, Guangdong, China

    Jindong Liu

  9. Farm of Seed Production of Gaoyi County, Gaoyi, 051330, Hebei, China

    Rongge Wang

  10. Crop Research Institute, Anhui Academy of Agricultural Sciences, 40 Nongke South Street, Hefei, 230001, Anhui, China

    Pingzhi Zhang & Yingxiu Wan

Authors
  1. Yuying Wu
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  2. Ming Li
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  3. Zhonghu He
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  4. Susanne Dreisigacker
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  5. Weie Wen
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  6. Hui Jin
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  7. Shengnan Zhai
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  8. Faji Li
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  9. Fengmei Gao
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  10. Jindong Liu
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  11. Rongge Wang
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  12. Pingzhi Zhang
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  13. Yingxiu Wan
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  14. Shuanghe Cao
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  15. Xianchun Xia
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Contributions

YYW designed all assays, executed the experiment, and wrote the paper. WEW, HJ, SNZ, FJL, FMG, JDL, RGW, PZZ, and YXW participated in field trials and collected phenotypic data. SHC helped in designing primers. ML, ZHH, and SD assisted in writing the paper. XCX designed the experiment and wrote the paper. All authors read the final version of the manuscript and approved for publication.

Corresponding author

Correspondence to Xianchun Xia.

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Conflict of interest

We declare no conflicts of interest in regard to this manuscript.

Ethical standards

These experiments complied with the ethical standards in China.

Additional information

Communicated by Mark E. Sorrells.

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Wu, Y., Li, M., He, Z. et al. Development and validation of high-throughput and low-cost STARP assays for genes underpinning economically important traits in wheat. Theor Appl Genet 133, 2431–2450 (2020). https://doi.org/10.1007/s00122-020-03609-w

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  • DOI: https://doi.org/10.1007/s00122-020-03609-w

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