The precocious germination of cereal grains before harvest, also known as pre-harvest sprouting, is an important source of yield and quality loss in cereal production. Pre-harvest sprouting is a complex grain defect and is becoming an increasing challenge due to changing climate patterns. Resistance to sprouting is multi-genic, although a significant proportion of the sprouting variation in modern wheat cultivars is controlled by a few major quantitative trait loci, including Phs-A1 in chromosome arm 4AL. Despite its importance, little is known about the physiological basis and the gene(s) underlying this important locus. In this study, we characterized Phs-A1 and show that it confers resistance to sprouting damage by affecting the rate of dormancy loss during dry seed after-ripening. We show Phs-A1 to be effective even when seeds develop at low temperature (13 °C). Comparative analysis of syntenic Phs-A1 intervals in wheat and Brachypodium uncovered ten orthologous genes, including the Plasma Membrane 19 genes (PM19-A1 and PM19-A2) previously proposed as the main candidates for this locus. However, high-resolution fine-mapping in two bi-parental UK mapping populations delimited Phs-A1 to an interval 0.3 cM distal to the PM19 genes. This study suggests the possibility that more than one causal gene underlies this major pre-harvest sprouting locus. The information and resources reported in this study will help test this hypothesis across a wider set of germplasm and will be of importance for breeding more sprouting resilient wheat varieties.

Division of Plant and Crop Sciences School of Biosciences University of Nottingham LE12 5RD UK

Institute of Experimental Botany Centre of the Region Haná for Biotechnological and Agricultural Research Šlechtitelů 31 78371 Olomouc Czech Republic

John Innes Centre Norwich Research Park NR4 7UH UK

John Innes Centre Norwich Research Park NR4 7UH UK KWS UK Ltd Hertfordshire SG8 7RE UK

KWS UK Ltd Hertfordshire SG8 7RE UK

Lantmannen SE 268 81 Svalov Sweden

Limagrain UK Ltd Woolpit Business Park IP30 9UP UK

RAGT Seeds Essex CB10 1TA UK

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Albrecht T, Oberforster M, Kempf H, Ramgraber L, Schacht J, Kazman E, Zechner E, Neumayer A, Hartl L, Mohler V. 2015. Genome-wide association mapping of preharvest sprouting resistance in a diversity panel of European winter wheats. Journal of Applied Genetics 1–9. PubMed

Balasubramanian S, Sureshkumar S, Agrawal M, Michael TP, Wessinger C, Maloof JN, Clark R, Warthmann N, Chory J, Weigel D. 2006. The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana . Nature Genetics 38, 711–715. PubMed PMC

Barrero JM, Cavanagh C, Verbyla KL, et al. 2015. Transcriptomic analysis of wheat near-isogenic lines identifies PM19-A1 and A2 as candidates for a major dormancy QTL. Genome Biology 16, 93. PubMed PMC

Bykova NV, Hoehn B, Rampitsch C, Hu J, Stebbing JA, Knox R. 2011. Thiol redox-sensitive seed proteome in dormant and non-dormant hybrid genotypes of wheat. Phytochemistry 72, 1162–1172. PubMed

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 Biology 14, 340. PubMed PMC

Chen A, Li C, Hu W, Lau MY, Lin H, Rockwell NC, Martin SS, Jernstedt JA, Lagarias JC, Dubcovsky J. 2014. PHYTOCHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod. Proceedings of the National Academy of Sciences, USA 111, 10037–10044. PubMed PMC

Chen CX, Cai SB, Bai GH. 2008. A major QTL controlling seed dormancy and pre-harvest sprouting resistance on chromosome 4A in a Chinese wheat landrace. Molecular Breeding 21, 351–358.

Chitnis VR, Gao F, Yao Z, Jordan MC, Park SE, Ayele BT. 2014. After-ripening induced transcriptional changes of hormonal genes in wheat seeds: the cases of brassinosteroids, ethylene, cytokinin and salicylic acid. PLoS ONE 9, e87543. PubMed PMC

Faris JD, Zhang Z, Fellers JP, Gill BS. 2008. Micro-colinearity between rice, Brachypodium and T. monococcum at the wheat domestication locus Q. Functional & Integrative Genomics 8, 149–164. PubMed

Flanagan CA, Ma H. 1994. Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant arabidopsis flowers. Plant Molecular Biology 26, 581–595. PubMed

Flintham J, Adlam R, Bassoi M, Holdsworth M, Gale MD. 2002. Mapping genes for resistance to sprouting damage in wheat. Euphytica 126, 39–45.

Flintham J, Holdsworth M, Jack P, Kettlewell PS, Phillips A. 2011. An integrated approach to stabilising HFN in wheat: screens, genes and understanding. Project Report 480. HGCA, Agriculture and Horticulture Development Board.

Flintham JE. 2000. Different genetic components control coat-imposed and embryo-imposed dormancy in wheat. Seed Science Research 10, 43–50.

Gao F, Ayele BT. 2014. Functional genomics of seed dormancy in wheat: advances and prospects. Frontiers in Plant Science 5, 458. PubMed PMC

Gao F, Rampitsch C, Chitnis VR, Humphreys GD, Jordan MC, Ayele BT. 2013. a Integrated analysis of seed proteome and mRNA oxidation reveals distinct post-transcriptional features regulating dormancy in wheat (Triticum aestivum L.). Plant Biotechnology Journal 11, 921–932. PubMed

Gao X, Hu CH, Li HZ, Yao YJ, Meng M, Dong L, Zhao WC, Chen QJ, Li XY. 2013. b Factors affecting pre-harvest sprouting resistance in wheat (Triticum aestivum L.): a review. The Journal of Animal and Plant Sciences 23, 556–565.

Gerjets T, Scholefield D, Foulkes MJ, Lenton JR, Holdsworth MJ. 2010. An analysis of dormancy, ABA responsiveness, after-ripening and pre-harvest sprouting in hexaploid wheat (Triticum aestivum L.) caryopses. Journal of Experimental Botany 61, 597–607. PubMed PMC

Glover NM, Daron J, Pingault L, Vandepoele K, Paux E, Feuillet C, Choulet F. 2015. Small-scale gene duplications played a major role in the recent evolution of wheat chromosome 3B. Genome Biology 16, 188. PubMed PMC

Heijmans K, Morel P, Vandenbussche M. 2012. MADS-box genes and floral development: the dark side. Journal of Experimental Botany 63, 5397–5404. PubMed

Himi E, Maekawa M, Miura H, Noda K. 2011. Development of PCR markers for Tamyb10 related to R-1, red grain color gene in wheat. Theoretical and Applied Genetics 122, 1561–1576. PubMed

Himi E, Noda K. 2005. Red grain colour gene (R) of wheat is a Myb-type transcription factor. Euphytica 143, 239–242.

Imtiaz M, Ogbonnaya FC, Oman J, van Ginkel M. 2008. Characterization of quantitative trait loci controlling genetic variation for preharvest sprouting in synthetic backcross-derived wheat lines. Genetics 178, 1725–1736. PubMed PMC

International Wheat Genome Sequencing Consortium (IWGSC) 2014. A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345, 1251788. PubMed

Irish VF, Sussex IM. 1990. Function of the apetala-1 gene during Arabidopsis floral development. The Plant Cell 2, 741–753. PubMed PMC

Iyer LM, Burroughs AM, Aravind L. 2006. The ASCH superfamily: novel domains with a fold related to the PUA domain and a potential role in RNA metabolism. Bioinformatics 22, 257–263. PubMed

Kato K, Nakamura W, Tabiki T, Miura H, Sawada S. 2001. Detection of loci controlling seed dormancy on group 4 chromosomes of wheat and comparative mapping with rice and barley genomes. Theoretical and Applied Genetics 102, 980–985.

Kottearachchi NS, Uchino N, Kato K, Miura H. 2006. Increased grain dormancy in white-grained wheat by introgression of preharvest sprouting tolerance QTLs. Euphytica 152, 421–428.

Laurie DA, Bennett MD. 1988. The production of haploid wheat plants from wheat × maize crosses. Theoretical and Applied Genetics 76, 393–397. PubMed

Lee SB, Lee SJ, Kim SY. 2015. AtERF15 is a positive regulator of ABA response. Plant Cell Reports 34, 71–81. PubMed

Lei L, Zhu X, Wang S, Zhu M, Carver BF, Yan L. 2013. TaMFT-A1 is associated with seed germination sensitive to temperature in winter wheat. PLoS ONE 8, e73330. PubMed PMC

Li C, Ni P, Francki M, Hunter A, et al. 2004. Genes controlling seed dormancy and pre-harvest sprouting in a rice-wheat-barley comparison. Functional & Integrated Genomics 4, 84–93. PubMed

Licausi F, Ohme-Takagi M, Perata P. 2013. APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytologist 199, 639–649. PubMed

Liu A, Gao F, Kanno Y, Jordan MC, Kamiya Y, Seo M, Ayele BT. 2013. a Regulation of wheat seed dormancy by after-ripening is mediated by specific transcriptional switches that induce changes in seed hormone metabolism and signaling. PLoS ONE 8, e56570. PubMed PMC

Liu S, Sehgal SK, Li J, Lin M, Trick HN, Yu J, Gill BS, Bai G. 2013. b Cloning and characterization of a critical regulator for preharvest sprouting in wheat. Genetics 195, 263–273. PubMed PMC

Lohwasser U, Rehman, Arif MA, Börner A. 2013. Discovery of loci determining pre-harvest sprouting and dormancy in wheat and barley applying segregation and association mapping. Biologia Plantarum 57, 663–674.

Mares D, Mrva K. 2014. Wheat grain preharvest sprouting and late maturity alpha-amylase. Planta 240, 1167–1178. PubMed

Mares D, Mrva K, Cheong J, Williams K, Watson B, Storlie E, Sutherland M, Zou Y. 2005. A QTL located on chromosome 4A associated with dormancy in white- and red-grained wheats of diverse origin. Theoretical and Applied Genetics 111, 1357–1364. PubMed

Nakamura S, Abe F, Kawahigashi H, et al. 2011. A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. The Plant Cell 23, 3215–3229. PubMed PMC

Ogbonnaya FC, Imtiaz M, DePauw RM. 2007. Haplotype diversity of preharvest sprouting QTLs in wheat. Genome 50, 107–118. PubMed

Ogbonnaya FC, Imtiaz M, Ye G, Hearnden PR, Hernandez E, Eastwood RF, van, Ginkel M, Shorter SC, Winchester JM. 2008. Genetic and QTL analyses of seed dormancy and preharvest sprouting resistance in the wheat germplasm CN10955. Theoretical and Applied Genetics 116, 891–902. PubMed

Rodriguez MV, Toorop PE, Benech-Arnold RL. 2011. Challenges facing seed banks in relations to seed quality. In: Kermode AR, ed. Seed dormancy: methods and protocols, method in molecular biology, Vol 773 New York: Humana Press, 17–40. PubMed

Preston JC, Christensen A, Malcomber ST, Kellogg EA. 2009. MADS-box gene expression and implications for developmental origins of the grass spikelet. American Journal of Botany 96, 1419–1429. PubMed

Smith SM, Maughan PJ. 2015. SNP genotyping using KASPar assays. Methods in Molecular Biology 1245, 243–256. PubMed

Torada A, Ikeguchi S, Koike M. 2005. Mapping and validation of PCR-based markers associated with a major QTL for seed dormancy in wheat. Euphytica 143, 251–255.

Torada A, Koike M, Ikeguchi S, Tsutsui I. 2008. Mapping of a major locus controlling seed dormancy using backcrossed progenies in wheat (Triticum aestivum L.). Genome 51, 426–432. PubMed

Trenberth KE. 2011. Changes in precipitation with climate change. Climate Research 47, 123–138.

Tyagi S, Gupta PK. 2012. Meta-analysis of QTLs involved in pre-harvest sprouting tolerance and dormancy in bread wheat. Triticeae Genomics and Genetic 3, 9–24.

Walker-Simmons M. 1987. ABA levels and sensitivity in developing wheat embryos of sprouting resistant and susceptible cultivars. Plant Physiology 84, 61–66. PubMed PMC

Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F. 2002. Ecological responses to recent climate change. Nature 416, 389–395. PubMed

Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J. 2003. Positional cloning of the wheat vernalization gene VRN1. Proceedings of the National Academy of Sciences, USA 100, 6263–6268. PubMed PMC

Haplotype Analysis of the Pre-harvest Sprouting Resistance Locus Phs-A1 Reveals a Causal Role of TaMKK3-A in Global Germplasm

A High Resolution Radiation Hybrid Map of Wheat Chromosome 4A