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TaELF3-1DL, a homolog of ELF3, is associated with heading date in bread wheat

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Abstract

Early flowering 3 (ELF3) is a regulator to modulate photoperiod flowering in Arabidopsis. The homologs of ELF3 in rice and barley also have been identified essential for regulation of flowering time. In the current study, TaELF3 genes, homologs of ELF3 in bread wheat (Triticum aestivum L.), were cloned by a comparative genomics approach and located on homologous group 1 chromosomes, designated as TaELF3-1AL, TaELF3-1BL, and TaELF3-1DL, respectively. A sequence-tagged site (STS) marker was developed based on sequence polymorphism at the TaELF3-1DL locus. A quantitative trait locus (QTL) for heading date (HD) co-segregating with TaELF3-1DL explained 7.7–20.6% of the phenotypic variance in a RIL mapping population derived from the Gaocheng 8901/Zhoumai 16 cross genotyped using the wheat 90K iSelect assay. The late HD allele of TaELF3-1DL was prevalently selected in China’s specific wheat-growing regions and other countries. This study produces novel information in better understanding HD and provides a reliable functional marker for molecular marker-assisted selection in wheat breeding.

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References

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

    Article  CAS  PubMed  Google Scholar 

  • Barrett B, Bayram M, Kidwell K (2002) Identifying AFLP and microsatellite markers for vernalization response gene Vrn-B1 in hexaploid wheat (Triticum aestivum L.) using reciprocal mapping populations. Plant Breed 121:400–406

    Article  CAS  Google Scholar 

  • Beales J, Turner A, Griffiths S, Snape JW, Laurie DA (2007) A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor Appl Genet 115:721–733

    Article  CAS  PubMed  Google Scholar 

  • Beniston M, Stephenson DB, Christensen OB, Ferro CAT, Frei C, Goyette S, Halsnaes K, Holt T, Jylhä (2007) Future extreme events in European climate: an exploration of regional climate model projections. Clim Chang 81:71–95

    Article  Google Scholar 

  • Bennett D, Izanloo A, Edwards J, Kuchel H, Chalmers K, Tester M, Reynolds M, Schnurbusch T, Langridge P (2012) Identification of novel quantitative trait loci for days to ear emergence and flag leaf glaucousness in a bread wheat (Triticum aestivum L.) population adapted to southern Australian conditions. Theor Appl Genet 124:697–711

    Article  PubMed  Google Scholar 

  • Boden SA, Weiss D, Ross JJ, Davies NW, Trevaskis B, Chandler PM, Swain SM (2014) EARLY FLOWERING3 regulates flowering in spring barley by mediating gibberellin production and FLOWERIN LOCUS T expression. Plant Cell 26:1557–1569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brenchley R, Spannagl M, Pfeifer M, Barker GL, D'Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo MC, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KF, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491:705–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen F, Gao M, Zhang J, Zuo A, Shang X, Cui D (2013) Molecular characterization of vernalization response and photoperiod response genes in bread wheat from the yellow and Huai valley of China. BMC Plant Biol 13:199

    Article  PubMed  PubMed Central  Google Scholar 

  • Covington MF, Panda S, Liu XL, Strayer CA, Wagner DR, Kay SA (2001) ELF3 modulates resetting of the circadian clock in Arabidopsis. Plant Cell 13:1305–1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubcovsky J, Loukoianov A, Fu D, Valarik M, Sanchez A, Yan L (2006) Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2. Plant Mol Biol 60:469–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dunford RP, Griffiths S, Christodoulou V, Laurie DA (2005) Characterisation of a barley (Hordeum vulgare L.) homologue of the Arabidopsis flowering time regulator GIGANTEA. Theor Appl Genet 110:925–931

    Article  CAS  PubMed  Google Scholar 

  • Faure S, Turner AS, Gruszka D, Christodoulou V, Davis SJ, von Korff M, Lauriea DA (2012) Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. Proc Natl Acad Sci U S A 109:8328–8333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu DL, Szucs P, Yan LL, Helguera M, Skinner JS, 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

    Article  CAS  Google Scholar 

  • Griffiths S, Simmonds J, Leverington M, Wang Y, Fish L, Sayers L, Alibert L, Orford S, Wingen L, Herry L, Faure S, Laurie D, Bilham L, Snape J (2009) Meta-QTL analysis of the genetic control of ear emergence in elite European winter wheat germplasm. Theor Appl Genet 119:383–395

    Article  CAS  PubMed  Google Scholar 

  • Hanocq E, Laperche A, Jaminon O, Lainé AL, Le Gouis J (2007) Most significant genome regions involved in the control of earliness traits in bread wheat, as revealed by QTL meta-analysis. Theor Appl Genet 114:569–584

    Article  CAS  PubMed  Google Scholar 

  • Hicks KA, Millar AJ, Carre IA, Somers DE, Straume M, Meeks-Wagner DR, Kay SA (1996) Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science 274:790–792

    Article  CAS  PubMed  Google Scholar 

  • Iwaki K, Nishida J, Yanagisawa T, Yoshida H, Kato K (2002) Genetic analysis of Vrn-B1 for vernalization requirement by using linked dCAPS markers in bread wheat (Triticum aestivum L.). Theor Appl Genet 104:571–576

    Article  CAS  PubMed  Google Scholar 

  • Kim WY, Hicks KA, Somers DE (2005) Independent roles for EARLY FLOWERING 3 and ZEITLUPE in the control of circadian timing, hypocotyl length, and flowering time. Plant Physiol 139:1557–1569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kippes N, Debernardi JM, Vasquez-Gross HA, Akpinar BA, Budak H, Kato K, Chao S, Akhunov E, Dubcovsky J (2015) Identification of the VERNALIZATION 4 gene reveals the origin of spring growth habit in ancient wheats from South Asia. Proc Natl Acad Sci U S A 112:E5401–E5410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosambi DD (1943) The estimation of map distance from recombination values. Ann Eugenics 12:172–175

    Article  Google Scholar 

  • Lagudah ES, Appels R, McNeil D (1991) The Nor-D3 locus of Triticum tauschii: natural variation and genetic linkage to markers in chromosome 5. Genome 34:387–395

    Article  CAS  Google Scholar 

  • Le Gouis J, Bordes J, Ravel C, Heumez E, Faure S, Praud S, Galic N, Remoué C, Balfourier F, Allard V, Rousset M (2012) Genome-wide association analysis to identify chromosomal regions determining components of earliness in wheat. Theor Appl Genet 124:597–611

    Article  CAS  PubMed  Google Scholar 

  • 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 

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

    Article  CAS  PubMed  Google Scholar 

  • Matsubara K, Ogiso-Tanaka E, Hori K, Ebana K, Ando T, Yano M (2012) Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering. Plant Cell Physiol 53:709–716

    Article  CAS  PubMed  Google Scholar 

  • McWatters HG, Bastow RM, Hall A, Millar AJ (2000) The ELF3 zeitnehmer regulates light signaling to the circadian clock. Nature 408:716–720

    Article  CAS  PubMed  Google Scholar 

  • Mühleisen J, Piepho HP, Maurer HP, Longin CFH, Reif JC (2013) Yield stability of hybrids versus lines in wheat, barley, and triticale. Theor Appl Genet 127:309–316

    Article  PubMed  Google Scholar 

  • Nishida H, Yoshida T, Kawakami K, Fujita M, Long B, Akashi Y, Laurie DA, Kato K (2013) Structural variation in the 5′ upstream region of photoperiod-insensitive alleles Ppd-A1a and Ppd-B1a identified in hexaploid wheat (Triticum aestivum L.), and their effect on heading time. Mol Breed 31:27–37

    Article  CAS  Google Scholar 

  • Ravel C, Praud S, Murigeux A, Canaguier A, Sapet F, Dufour P, Chalhoub B, Brunel D, Beckert M, Charmet G (2006) Single nucleotide polymorphism frequency in a set of selected lines of bread wheat (Triticum aestivum L.). Genome 49:1131–1139

    Article  CAS  PubMed  Google Scholar 

  • Reif JC, Maurer HP, Korzun V, Ebmeyer E, Miedaner T, Würschum T (2011) Mapping QTLs with main and epistatic effects underlying grain yield and heading time in soft winter wheat. Theor Appl Genet 123:283–292

    Article  PubMed  Google Scholar 

  • Rousset M, Bonnin I, Remoue C, Falque M, Rhone B, Veyrieras JB, Madur D, Murigneux A, Balfourier F, Le Gouis J, Santoni S, Goldringer I (2011) Deciphering the genetics of flowering time by an association study on candidate genes in bread wheat (Triticum aestivum L.). Theor Appl Genet 123:907–926

    Article  PubMed  Google Scholar 

  • Seki M, Chono M, Nishimura T, Sato M, Yoshimura Y, Matsunaka H, Fujita M, Oda S, Kubo K, Kiribuchi-Otobe C, Kojima H, Nishida H, Kato K (2013) Distribution of photoperiod-insensitive allele Ppd-A1a and its effect on heading time in Japanese wheat cultivars. Breed Sci 63:309–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shitsukawa N, Iqari C, Shimada S, Kitagawa S, Sakamoto K, Saito H (2007) The einkorn wheat (Triticum monococcum) mutant, maintained vegetative phase, is caused by a deletion in the VRN1 gene. Genes Genet Syst 82:167–170

    Article  CAS  PubMed  Google Scholar 

  • Snape W, Butterworth K, Whitechurch E, Worland AJ (2001) Waiting for fine times: genetics of flowering time in wheat. Euphytica 119:185–190

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stelmakh AF (1998) Genetic systems regulating flowering response in wheat. Euphytica 100:359–369

    Article  Google Scholar 

  • Strasser B, Alvarez MJ, Califano A, Cerdan PD (2009) A complementary role for ELF3 and TFL1 in the regulation of flowering time by ambient temperature. Plant J 58:629–640

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Thines B, Harmon FG (2010) Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock. Proc Natl Acad Sci U S A 107:3257–3262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trevaskis B, Hemming MN, Dennis ES, Peacock WJ (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:352–357

    Article  CAS  PubMed  Google Scholar 

  • Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wei JX, Zhang Y, Liu JD, 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

    Article  CAS  PubMed  Google Scholar 

  • Worland AJ (1996) The influence of flowering time genes on environmental adaptability in European wheats. Euphytica 89:49–57

    Article  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci U S A 100:6263–6268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L, Helguera M, Kato K, Fukuyama S, Sherman J, Dubcovsky J (2004a) Allelic variation at the VRN-1 promoter region in polyploidy wheat. Theor Appl Genet 109:1677–1686

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004b) The wheat VRN2 gene is a flowering repressor downregulated by vernalization. Science 303:1640–1644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci U S A 103:19581–19586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida R, Fekih R, Fujiwara S, Oda A, Miyata K, Tomozoe Y, Nakagawa M, Niinuma K, Hayashi K, Ezura H, Coupland G, Mizoguchi T (2009) Possible role of EARLY FLOWERING 3 (ELF3) in clock-dependent floral regulation by SHORT VEGETATIVE PHASE (SVP) in Arabidopsis thaliana. New Phytol 182:838–850

    Article  CAS  PubMed  Google Scholar 

  • Zagotta MT, Hicks KA, Jacobs CI, Young JC, Hangarter RP, Wagner R (1996) The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J 10:691–702

    Article  CAS  PubMed  Google Scholar 

  • Zakhrabekova S, Gough SP, Braumann I, Muller AH, Lundqvist J, Ahmann K, Dockter C, Matyszczak I, Kurowska M, Druka A, Waugh R, Graner A, Stein N, Steuernagel B, Lundqvist U, Hansson M (2012) Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley. Proc Natl Acad Sci U S A 109:4326–4331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Wang Y, Wu S, Yang J, Liu H, Zhou Y (2012) A single nucleotide polymorphism at the Vrn-D1 promoter region in common wheat is associated with vernalization response. Theor Appl Genet 125:1697–1704

    Article  PubMed  Google Scholar 

  • Zhang X, Gao M, Wang S, Chen F, Cui D (2015) Allelic variation at the vernalization and photoperiod sensitivity loci in Chinese winter wheat cultivars (Triticum aestivum L.). Front. Plant Sci 6:470

    Google Scholar 

  • Zhao J, Huang X, Ouyang X, Chen W, Du A, Zhu L, Wang S, Deng XW, Li S (2012) OsELF3-1, an ortholog of Arabidopsis EARLY FLOWERING3, regulates rice circadian rhythm and photoperiodic flowering. PLoS One 7:e43705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zikhali M, Wingen LU, Griffiths S (2016) Delimitation of the Earliness per se D1 (Eps-D1) flowering gene to a subtelomeric chromosomal deletion in bread wheat (Triticum aestivum). J Exp Bot 67:287–299

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by National Key Technology R&D Program of China (2014BAD01B05), National Natural Science Foundation of China (3151663, 31461143021), CAAS Science and Technology Innovation Program, and National Key Basic Research Program of China (2014Cb138105).

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Authors and Affiliations

  1. College of Agronomy, Shandong Agricultural University, Taian, Shandong, 271018, China

    Jinping Wang, Honggang Wang & Shubing Liu

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

    Jinping Wang, Weie Wen, Mamoona Hanif, Xianchun Xia, Jindong Liu, Li Yang, Shuanghe Cao & Zhonghu He

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

    Zhonghu He

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  1. Jinping Wang
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  2. Weie Wen
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  3. Mamoona Hanif
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  4. Xianchun Xia
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Correspondence to Shuanghe Cao or Zhonghu He.

Electronic supplementary material

Fig. S1

Alignment of HvELF3, TaELF3–1AL, TaELF3–1BL and TaELF3–1DL (TIFF 5187 kb)

High Resolution Image (GIF 2633 kb)

Fig. S2

Frequency distributions of HD in the Gaocheng 8901/Zhoumai 16 RIL population. a, Anyang 2013; b, Suixi 2013; c, Anyang 2014; d, Suixi 2014. HD of the parents, Gaocheng 8901 and Zhoumai 16, are indicated by arrows (TIFF 254 kb)

High Resolution Image (GIF 227 kb)

Table S1

Genotypes of TaELF3–1DLa and TaELF3–1DLb in 283 Chinese and foreign wheat cultivars (DOCX 27 kb)

Table S2

Characteristics of TaELF3–1AL, TaELF3–1BL and TaELF3–1DL (DOCX 13 kb)

Table S3

Association analysis of TaELF3–1DL with HD of RILs developed from the Gaocheng 8901/Zhoumai 16 cross (DOCX 17 kb)

Table S4

QTL analysis for HD in the Gaocheng 8901/Zhoumai 16 RIL population (DOCX 16 kb)

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Wang, J., Wen, W., Hanif, M. et al. TaELF3-1DL, a homolog of ELF3, is associated with heading date in bread wheat. Mol Breeding 36, 161 (2016). https://doi.org/10.1007/s11032-016-0585-5

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