Abstract
Key message
HvMKK3 alleles are temperature sensitive and are major contributors to environmental stability of preharvest sprouting in barley.
Abstract
Preharvest sprouting (PHS) can severely damage barley (Hordeum vulgare L.) malting quality, but PHS resistance is often negatively correlated with malting quality. Seed dormancy is closely related to PHS. Increased temperature during grain fill can decrease seed dormancy in barley, but genetic components of seed dormancy temperature sensitivity are poorly understood. Six years of PHS data were used to fit quantitative trait locus (QTL) x environment mixed models incorporating marker data from seed dormancy genes HvAlaAT1, HvGA20ox1, and HvMKK3 and weather covariates in spring and winter two-row malting barley. Variation in winter barley PHS was best modeled by average temperature range during grain fill and spring barley PHS by total precipitation during grain fill. Average high temperature during grain fill also accurately modeled PHS for both datasets. A highly non-dormant HvMKK3 allele determined baseline PHS susceptibility and HvAlaAT1 interactions with multiple HvMKK3 alleles conferred environmental sensitivity. Polygenic variation for PHS within haplotype was detected. Residual genotype and QTL by environment interaction variance indicated additional environmental and genetic factors involved in PHS. These models provide insight into genotype and environmental regulation of barley seed dormancy, a method for PHS forecasting, and a tool for breeders to improve PHS resistance.
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Raw data and R scripts are provided in the supplementary material.
References
Abe A, Takagi H, Fujibe T, Aya K, Kojima M et al (2012) OsGA20ox1, a candidate gene for a major QTL controlling seedling vigor in rice. Theor Appl Genet 125(4):647–657. https://doi.org/10.1007/s00122-012-1857-z
Alqudah AM, Schnurbusch T (2017) Heading date is not flowering time in spring barley. Front Plant Sci 8:896. https://doi.org/10.3389/fpls.2017.00896
Anderson JA, Sorrells ME, Tanksley SD (1993) RFLP analysis of genomic regions associated with resistance to preharvest sprouting in wheat. Crop Sci 33(3):453. https://doi.org/10.2135/cropsci1993.0011183X003300030008x
Benech-Arnold RL, Giallorenzi MC, Frank J, Rodriguez V (1999) Termination of hull-imposed dormancy in developing barley grains is correlated with changes in embryonic ABA levels and sensitivity. Seed Sci Res 9(1):39–47. https://doi.org/10.1017/S0960258599000045
Benech-Arnold RL, Gualano N, Leymarie J, Côme D, Corbineau F (2006) Hypoxia interferes with ABA metabolism and increases ABA sensitivity in embryos of dormant barley grains. J Exp Bot 57(6):1423–1430. https://doi.org/10.1093/jxb/erj122
Betts NS, Dockter C, Berkowitz O, Collins HM, Hooi M et al (2020) Transcriptional and biochemical analyses of gibberellin expression and content in germinated barley grain. J Exp Bot 71(6):1870–1884. https://doi.org/10.1093/jxb/erz546
Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: physiology of development, germination and dormancy, 3rd edn. Springer, New York
Biddulph TB, Mares DJ, Plummer JA, Setter TL (2005) Drought and high temperature increases preharvest sprouting tolerance in a genotype without grain dormancy. Springer, Euphytica, pp 277–283
Biddulph TB, Plummer JA, Setter TL, Mares DJ (2007) Influence of high temperature and terminal moisture stress on dormancy in wheat (Triticum aestivum L.). F. Crop. Res. 103(2):139–153. https://doi.org/10.1016/j.fcr.2007.05.005
Bonnardeaux Y, Li C, Lance R, Zhang XQ, Sivasithamparam K et al (2008) Seed dormancy in barley: identifying superior genotypes through incorporating epistatic interactions. Aust J Agric Res. https://doi.org/10.1071/AR07345
Bradford KJ, Benech-Arnold RL, Côme D, Corbineau F (2008) Quantifying the sensitivity of barley seed germination to oxygen, abscisic acid, and gibberellin using a population-based threshold model. J Exp Bot 59(2):335–347. https://doi.org/10.1093/jxb/erm315
Chono M, Honda I, Shinoda S, Kushiro T, Kamiya Y, Nambara E, Kawakami N, Kaneko S, Watanabe Y (2006) Field studies on the regulation of abscisic acid content and germinability during grain development of barley: molecular and chemical analysis of pre-harvest sprouting. J Exp Bot Oxf Acad. https://doi.org/10.1093/jxb/erj215
Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413:217–226. https://doi.org/10.1042/BJ20080625
Danquah A, de Zélicourt A, Boudsocq M, Neubauer J, Frei dit Frey N et al (2015) Identification and characterization of an ABA-activated MAP kinase cascade in Arabidopsis thaliana. Plant J 82(2):232–244. https://doi.org/10.1111/tpj.12808
de Mendiburu F, Yaseen M (2020) agricolae: Statistical Procedures for Agricultural Research. R package version 1.4.0, https://myaseen208.github.io/agricolae/https://cran.r-project.org/package=agricolae
Depauw RM, Mccaig TN (1991) Components of variation, heritabilities and correlations for indices of sprouting tolerance and seed dormancy in Triticum spp. Euphytica 52:221–229
Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171(3):501–523. https://doi.org/10.1111/j.1469-8137.2006.01787.x
Gao W, Clancy JA, Han F, Prada D, Kleinhofs A et al (2003) Molecular dissection of a dormancy QTL region near the chromosome 7 (5H) L telomere in barley. Theor Appl Genet 107(3):552–559. https://doi.org/10.1007/s00122-003-1281-5
Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml user guide. Hemel Hempstead, HP1 1ES, UK
Goldbach H, Michael G (1976) Abscisic acid content of barley grains during ripening as affected by temperature and variety. Crop Sci 16(6):797–799. https://doi.org/10.2135/cropsci1976.0011183x001600060015x
Gong X, Li C, Zhou M, Bonnardeaux Y, Yan G (2014) Seed dormancy in barley is dictated by genetics, environments and their interactions. Euphytica 197(355):368. https://doi.org/10.1007/s10681-014-1072-x
Gualano NA, Benech-Arnold RL (2009) The effect of water and nitrogen availability during grain filling on the timing of dormancy release in malting barley crops. Euphytica 168(3):291–301. https://doi.org/10.1007/s10681-009-9948-x
Han F, Ullrich SE, Clancy JA, Romagosa I (1999) Inheritance and fine mapping of a major barley seed dormancy QTL. Plant Sci 143(1):113–118. https://doi.org/10.1016/S0168-9452(99)00028-X
Hickey LT, Lawson W, Arief VN, Fox G, Franckowiak J et al (2012) Grain dormancy QTL identified in a doubled haploid barley population derived from two non-dormant parents. Euphytica 188(1):113–122. https://doi.org/10.1007/s10681-011-0577-9
Hori K, Sato K, Takeda K (2007) Detection of seed dormancy QTL in multiple mapping populations derived from crosses involving novel barley germplasm. Theor Appl Genet 115(6):869–876. https://doi.org/10.1007/s00122-007-0620-3
Jacobsen JV, Pearce DW, Poole AT, Pharis RP, Mander LN (2002) Abscisic acid, phaseic acid and gibberellin contents associated with dormancy and germination in barley. Physiol Plant 115(3):428–441. https://doi.org/10.1034/j.1399-3054.2002.1150313.x
King RW (1976) Abscisic acid in developing wheat grains and its relationship to grain growth and maturation. Planta 132(1):43–51. https://doi.org/10.1007/BF00390329
Lenoir C, Corbineau F, Come D (1986) Barley (Hordeum vulgare) seed dormancy as related to glumella characteristics. Physiol Plant 68(2):301–307. https://doi.org/10.1111/j.1399-3054.1986.tb01930.x
Li CD, Tarr A, Lance RCM, Harasymow S, Uhlmann J, Westcot S, Young KJ, Grime CR, Cakir M, Broughton S, Appels R (2003) A major QTL controlling seed dormancy and pre-harvest sprouting/grain α-amylase in two-rowed barley (Hordeum vulgare L.). Aust J Agric Res 54(12):1303. https://doi.org/10.1071/AR02210
Li C, Ni P, Francki M, Hunter A, Zhang Y et al (2004) Genes controlling seed dormancy and pre-harvest sprouting in a rice-wheat-barley comparison. Funct Integr Genom 4(2):84–93. https://doi.org/10.1007/s10142-004-0104-3
Lin R, Horsley RD, Lapitan NLV, Ma Z, Schwarz PB (2009) QTL mapping of dormancy in barley using the Harrington/Morex and Chevron/Stander mapping populations. Crop Sci 49(3):841. https://doi.org/10.2135/cropsci2008.05.0269
Liu A, Gao F, Kanno Y, Jordan MC, Kamiya Y et al (2013) 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. https://doi.org/10.1371/journal.pone.0056570
Liu Y, Fang J, Xu F, Chu J, Yan C et al (2014) Expression patterns of ABA and GA metabolism genes and hormone levels during rice seed development and imbibition: a comparison of dormant and non-dormant rice cultivars. J Genet Genom 41(6):327–338. https://doi.org/10.1016/j.jgg.2014.04.004
Malosetti M, Voltas J, Romagosa I, Ullrich SE, van Eeuwijk FA (2004) Mixed models including environmental covariables for studying QTL by environment interaction. Kluwer Academic Publishers, New York
Mao X, Zhang J, Liu W, Yan S, Liu Q et al (2019) The MKKK62-MKK3-MAPK7/14 module negatively regulates seed dormancy in rice. Rice 12(1):2. https://doi.org/10.1186/s12284-018-0260-z
Martinez SA, Tuttle KM, Takebayashi Y, Seo M, Campbell KG et al (2016) The wheat ABA hypersensitive ERA8 mutant is associated with increased preharvest sprouting tolerance and altered hormone accumulation. Euphytica 212(2):229–245. https://doi.org/10.1007/s10681-016-1763-6
Martinez SA, Shorinola O, Conselman S, See D, Skinner DZ et al (2020) Exome sequencing of bulked segregants identified a novel TaMKK3-A allele linked to the wheat ERA8 ABA-hypersensitive germination phenotype. Theor Appl Genet 133(3):719–736. https://doi.org/10.1007/s00122-019-03503-0
Nagel M, Alqudah AM, Bailly M, Rajjou L, Pistrick S et al (2019) Novel loci and a role for nitric oxide for seed dormancy and preharvest sprouting in barley. Plant Cell Environ. https://doi.org/10.1111/pce.13483
Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A et al (2011) A wheat homolog of MOTHER of FT and TFL1 acts in the regulation of germination. Plant Cell 23(9):3215–3129. https://doi.org/10.1105/tpc.111.088492
Nakamura S, Pourkheirandish M, Morishige H, Kubo Y, Nakamura M et al (2016) Mitogen-activated protein kinase kinase 3 regulates seed dormancy in barley. Curr Biol 26(6):775–781. https://doi.org/10.1016/J.CUB.2016.01.024
Neyhart JL, Sweeney D, Sorrells M, Kapp C, Kephart KD et al (2019) Registration of the S2MET barley mapping population for multi-environment genomewide selection. J Plant Regist. https://doi.org/10.3198/jpr2018.06.0037crmp
Oberthur L, Blake TK, Dyer WE, Ullrich SE (1995) Genetic analysis of seed dormancy in barley (Hordeum vulgare L.). J Agric Genom 1: 1–10. https://www.cabdirect.org/cabdirect/abstract/20063161122 (Accessed 7 May 2019)
Pérez-Flores L, Carrari F, Osuna-Fernández R, Rodríguez MV, Enciso S et al (2003) Expression analysis of a GA 20-oxidase in embryos from two sorghum lines with contrasting dormancy: Possible participation of this gene in the hormonal control of germination. J Exp Bot 54(390):2071–2079. https://doi.org/10.1093/jxb/erg233
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org
Rodríguez MV, Margineda M, González-Martín JF, Insausti P, Benech-Arnold RL (2001) Predicting preharvest sprouting susceptibility in barley. Agron J 93(5):1071. https://doi.org/10.2134/agronj2001.9351071x
Rodríguez MV, Mendiondo GM, Cantoro R, Auge GA, Luna V et al (2012) Expression of seed dormancy in grain sorghum lines with contrasting pre-harvest sprouting behavior involves differential regulation of gibberellin metabolism genes. Plant Cell Physiol 53(1):64–80. https://doi.org/10.1093/pcp/pcr154
Sato K, Yamane M, Yamaji N, Kanamori H, Tagiri A et al (2016) Alanine aminotransferase controls seed dormancy in barley. Nat Commun 7(1):11625. https://doi.org/10.1038/ncomms11625
Shorinola O, Balcárková B, Hyles J, Tibbits JFG, Hayden MJ et al (2017) Haplotype analysis of the pre-harvest sprouting resistance locus Phs-A1 reveals a causal role of TaMKK3-A in global germplasm. Front Plant Sci 8:1555. https://doi.org/10.3389/fpls.2017.01555
Song S, Wang G, Wu H, Fan X, Liang L et al (2020) OsMFT2 is involved in the regulation of ABA signaling-mediated seed germination through interacting with OsbZIP23/66/72 in rice. Plant J 103(2):532–546. https://doi.org/10.1111/tpj.14748
Spielmeyer W, Ellis M, Robertson M, Ali S, Lenton JR et al (2004) Isolation of gibberellin metabolic pathway genes from barley and comparative mapping in barley, wheat and rice. Theor Appl Genet 109(4):847–855. https://doi.org/10.1007/s00122-004-1689-6
Sreenivasulu N, Usadel B, Winter A, Radchuk V, Scholz U et al (2008) Barley grain maturation and germination: Metabolic pathway and regulatory network commonalities and differences highlighted by new MapMan/PageMan profiling tools. Plant Physiol 146(4):1738–1758. https://doi.org/10.1104/pp.107.111781
Sweeney DW, Rooney TE, Walling JG, Sorrells ME (2021) Interactions of the barley SD1 and SD2 seed dormancy loci influence preharvest sprouting, seed dormancy, and malting quality. Crop Sci. https://doi.org/10.1002/csc2.20641
Torada A, Koike M, Ogawa T, Takenouchi Y, Tadamura K et al (2016) A causal gene for seed dormancy on wheat chromosome 4A encodes a MAP kinase kinase. Curr Biol 26:782–787. https://doi.org/10.1016/j.cub.2016.01.063
Ullrich SE, Lee H, Clancy JA, del Blanco IA, Jitkov VA, Kleinhofs A, Han F, Prada D, Romagosa I, Molina-Cano JL (2009) Genetic relationships between preharvest sprouting and dormancy in barley. Euphytica 168(3):331–345. https://doi.org/10.1007/s10681-009-9936-1
van Beckum JMM, Libbenga KR, Wang M (1993) Abscisic acid and gibberellic acid-regulated responses of embryos and aleurone layers isolated from dormant and nondormant barley grains. Physiol Plant 89(3):483–489. https://doi.org/10.1111/j.1399-3054.1993.tb05202.x
van Eeuwijk FA, Malosetti M, Yin X, Struik PC, Stam P (2005) Statistical models for genotype by environment data: from conventional ANOVA models to eco-physiological QTL models. Aust J Agric Res 56:883–894. https://doi.org/10.1071/AR05153
Verbyla AP (2019) A note on model selection using information criteria for general linear models estimated using REML. Aust N Z J Stat 61(1):39–50. https://doi.org/10.1111/anzs.12254
Vetch JM, Walling JG, Sherman J, Martin JM, Giroux MJ (2020) Mutations in the HvMKK3 and HvAlaAT1 genes affect barley preharvest sprouting and after-ripened seed dormancy. Crop Sci. https://doi.org/10.1002/csc2.20178
Walker-Simmons M, Sesing J (1990) Temperature effects on embryonic abscisic acid levels during development of wheat grain dormancy. J Plant Growth Regul 9(1):51–56. https://doi.org/10.1007/BF02041941
Wei W, Min X, Shan S, Jiang H, Cao J et al (2019) Isolation and characterization of TaQsd1 genes for period of dormancy in common wheat (Triticum aestivum L.). Mol Breed. https://doi.org/10.1007/s11032-019-1060-x
Acknowledgements
We would like to thank David Benscher, Amy Fox, and James Tanaka for field and phenotyping assistance, Jean-Luc Jannink, Marnin Wolfe, Shantel Martinez and Travis Rooney for formative discussions early in the conception of the project, and Arunas Verbyla for sharing updated icREML R scripts. This work was supported by New York Agriculture and Markets, the American Malting Barley Association (AMBA), and the Brewers Association (BA). Partial funding for this project was provided by USDA National Institute of Food and Agriculture Grant 2017-67007-25939 (Wheat-CAP) and Hatch Project 149-945.
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This study was funded by New York Agriculture and Markets, American Malting Barley Association, Brewers Association, USDA National Institute of Food and Agriculture Grant 2017-67007-25939 (Wheat-CAP), Hatch Project 149-945.
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MES supervised the overall project; DWS and KHK were responsible for investigation; DWS developed methodology, analyzed and curated data, and prepared the manuscript; MES, DWS, and KHK contributed to funding acquisition and editing of the manuscript.
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Sweeney, D.W., Kunze, K.H. & Sorrells, M.E. QTL x environment modeling of malting barley preharvest sprouting. Theor Appl Genet 135, 217–232 (2022). https://doi.org/10.1007/s00122-021-03961-5
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DOI: https://doi.org/10.1007/s00122-021-03961-5