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A survey of EMS-induced biennial Beta vulgaris mutants reveals a novel bolting locus which is unlinked to the bolting gene B

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Abstract

Beta vulgaris is a facultative perennial species which exhibits large intraspecific variation in vernalization requirement and includes cultivated biennial forms such as the sugar beet. Vernalization requirement is under the genetic control of the bolting locus B on chromosome II. Previously, ethyl methanesulfonate (EMS) mutagenesis of an annual accession had yielded several mutants which require vernalization to bolt and behave as biennials. Here, five F2 populations derived from crosses between biennial mutants and annual beets were tested for co-segregation of bolting phenotypes with genotypic markers located at the B locus. One mutant appears to be mutated at the B locus, suggesting that an EMS-induced mutation of B can be sufficient to abolish annual bolting. Co-segregation analysis in four populations indicates that the genetic control of bolting also involves previously unknown major loci not linked to B, one of which also affects bolting time and was genetically mapped to chromosome IX.

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References

  • Abe J, Guan GP, Shimamoto Y (1997) A gene complex for annual habit in sugar beet (Beta vulgaris L.). Euphytica 94:129–135

    Article  Google Scholar 

  • Abegg FA (1936) A genetic factor for the annual habit in beets and linkage relationship. J Agric Res 53:493–511

    Google Scholar 

  • Alonso-Blanco C, Aarts MGM, Bentsink L, Keurentjes JJB, Reymond M, Vreugdenhil D, Koornneef M (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21:1877–1896

    Article  CAS  PubMed  Google Scholar 

  • Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121

    Article  Google Scholar 

  • Barzen E, Mechelke W, Ritter E, Seitzer JF, Salamini F (1992) RFLP markers for sugar beet breeding: chromosomal linkage maps and location of major genes for rhizomania resistance, monogermy and hypocotyl colour. Plant J 2:601–611

    Article  CAS  Google Scholar 

  • Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664

    Article  PubMed  Google Scholar 

  • Boudry P, Wieber R, Saumitou-Laprade P, Pillen K, Van Dijk H, Jung C (1994) Identification of RFLP markers closely linked to the bolting gene B and their significance for the study of the annual habit in beets (Beta vulgaris L.). Theor Appl Genet 88:852–858

    Article  CAS  Google Scholar 

  • Boudry P, McCombie H, Van Dijk H (2002) Vernalization requirement of wild beet Beta vulgaris ssp. maritima: among population variation and its adaptive significance. J Ecol 90:693–703

    Article  Google Scholar 

  • Butterfass T (1968) Die Zuordnung des Locus R der Zuckerrübe (Hypokotylfarbe) zum Chromosom II. Theor Appl Genet 38:348–350

    Article  Google Scholar 

  • Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD (2004) Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc Natl Acad Sci USA 101:15670–15675

    Article  CAS  PubMed  Google Scholar 

  • Chia TYP, Muller A, Jung C, Mutasa-Gottgens ES (2008) Sugar beet contains a large CONSTANS-LIKE gene family including a CO homologue that is independent of the early-bolting (B) gene locus. J Exp Bot 59:2735–2748

    Article  CAS  PubMed  Google Scholar 

  • Colasanti J, Coneva V (2009) Mechanisms of floral induction in grasses: something borrowed, something new. Plant Physiol 149:56–62

    Article  CAS  PubMed  Google Scholar 

  • Curth P (1960) Der Übergang in die reproduktive Phase der Zuckerrübe in Abhängigkeit von verschiedenen Umweltfaktoren. Deutsch Akademie Landwirtschaftswissenschaften zu Berlin, pp 7–80

  • Davies TJ, Barraclough TG, Chase MW, Soltis PS, Soltis DE, Savolainen V (2004) Darwin’s abominable mystery: insights from a supertree of the angiosperms. Proc Natl Acad Sci USA 101:1904–1909

    Article  CAS  PubMed  Google Scholar 

  • Distelfeld A, Dubcovsky J (2010) Characterization of the maintained vegetative phase deletions from diploid wheat and their effect on VRN2 and FT transcript levels. Mol Genet Genomics 283(3):223–232

    Article  CAS  PubMed  Google Scholar 

  • Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12:178–184

    Article  CAS  PubMed  Google Scholar 

  • El-Mezawy A, Dreyer F, Jacobs G, Jung C (2002) High-resolution mapping of the bolting gene B of sugar beet. Theor Appl Genet 105:100–105

    Article  CAS  PubMed  Google Scholar 

  • Gaafar RM, Hohmann U, Jung C (2005) Bacterial artificial chromosome-derived molecular markers for early bolting in sugar beet. Theor Appl Genet 110:1027–1037

    Article  CAS  PubMed  Google Scholar 

  • Greenup A, Peacock WJ, Dennis ES, Trevaskis B (2009) The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann Bot (Lond) (Epub ahead of print) doi:10.1093/aob/mcp063

  • Hansen M, Kraft T, Ganestam S, Sall T, Nilsson NO (2001) Linkage disequilibrium mapping of the bolting gene in sea beet using AFLP markers. Genet Res 77:61–66

    Article  CAS  PubMed  Google Scholar 

  • Hanson LE, Panella L (2003) Rhizoctonia root rot resistance of Beta PIs from USDA-ARS NPGS, 2003. Biol Cult Tests 19:FC012. doi:10.1094/BC19

  • Hautekeete NC, Piquot Y, Van Dijk H (2002) Life span in Beta vulgaris ssp. maritima: the effects of age at first reproduction and disturbance. J Ecol 90:508–516

    Article  Google Scholar 

  • He YH, Amasino RM (2005) Role of chromatin modification in flowering-time control. Trends Plant Sci 10:30–35

    Article  CAS  PubMed  Google Scholar 

  • Hohmann U, Jacobs G, Jung C (2005) An EMS mutagenesis protocol for sugar beet and isolation of non-bolting mutants. Plant Breed 124:317–321

    Article  Google Scholar 

  • Jung C, Müller AE (2009) Flowering time control and applications in plant breeding. Trends Plant Sci 14:563–573

    Article  CAS  PubMed  Google Scholar 

  • Koornneef M, Hanhart CJ, Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66

    Article  CAS  PubMed  Google Scholar 

  • Koornneef M, Alonso-Blanco C, Peeters AJM, Soppe W (1998a) Genetic control of flowering time in Arabidopsis. Annu Rev Plant Biol 49:345–370

    Article  CAS  Google Scholar 

  • Koornneef M, Alonso-Blanco C, Blankestijn-de Vries H, Hanhart CJ, Peeters AJM (1998b) Genetic interactions among late-flowering mutants of Arabidopsis. Genetics 148:885–892

    CAS  PubMed  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Laurent V, Devaux P, Thiel T, Viard F, Mielordt S, Touzet P, Quillet M (2007) Comparative effectiveness of sugar beet microsatellite markers isolated from genomic libraries and GenBank ESTs to map the sugar beet genome. Theor Appl Genet 115:793–805

    Google Scholar 

  • Letschert JPW (1993) Beta section Beta: biogeographical patterns of variation and taxonomy. Wageningen Agric Univ Papers 93:1–154

    Google Scholar 

  • Lexander K (1980) Present knowledge on sugar beet bolting mechanisms. In: Proc Int Inst Sugar Beet Res 43rd Winter Congress, pp 245–258

  • Li CX, Dubcovsky J (2008) Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J 55:543–554

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Zapater JM, Somerville CR (1990) Effect of light quality and vernalization on late-flowering mutants of Arabidopsis thaliana. Plant Physiol 92:770–776

    Article  CAS  PubMed  Google Scholar 

  • McGrath JM, Trebbi D, Fenwick A, Panella L, Schulz B, Laurent V, Barnes S, Murray SC (2007) An open-source first-generation molecular genetic map from a Sugarbeet × Table Beet cross and its extension to physical mapping. Crop Sci 47:27–44

    Article  Google Scholar 

  • Meier U (2001) Growth stages of mono-and dicotyledonous plants. Phenological growth stages and BBCH-identification keys of beet, 2nd edn. Federal Biological Research Centre for Agriculture and Forestry, Germany

    Google Scholar 

  • Michaels SD (2009) Flowering time regulation produces much fruit. Curr Opin Plant Biol 12:75–80

    Article  CAS  PubMed  Google Scholar 

  • Moon J, Lee H, Kim M, Lee I (2005) Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol 46:292–299

    Article  CAS  PubMed  Google Scholar 

  • Munerati O (1931) L’eredità della tendenza alla annualità nella commune barbabietola, coltivata, Ztschr Züchtung, Reihe A. Pflanzenzüchtung 17:84–89

    Google Scholar 

  • Nilsson O, Lee I, Blazquez MA, Weigel D (1998) Flowering-time genes modulate the response to LEAFY activity. Genetics 150:403–410

    CAS  PubMed  Google Scholar 

  • Owen FW (1954) The significance of single gene reactions in sugar beets. Proc Am Soc Sugar Beet Technol 8:392–398

    Google Scholar 

  • Owen FW, Carsner E, Stout M (1940) Photothermal induction of flowering in sugar beets. J Agric Res 61:101–124

    Google Scholar 

  • Putterill J, Laurie R, Macknight R (2004) It’s time to flower: the genetic control of flowering time. Bioessays 26:363–373

    Article  CAS  PubMed  Google Scholar 

  • Reeves PA, He Y, Schmitz RJ, Amasino RM, Panella LW, Richards C (2007) Evolutionary conservation of the FLC mediated vernalization response: evidence from the sugar beet (Beta vulgaris). Genetics 176:295–307

    Article  CAS  PubMed  Google Scholar 

  • Schneider K, Kulosa D, Soerensen T, Möhring S, Heine M, Durstewitz G, Polley A, Weber E, Jamsari J, Lein J, Hohmann U, Tahiro E, Weisshaar B, Schulz B, Koch G, Jung C, Ganal M (2007) Analysis of DNA polymorphisms in sugar beet (Beta vulgaris L.) and development of an SNP-based map of expressed genes. Theor Appl Genet 115:601–615

    Article  CAS  PubMed  Google Scholar 

  • Stout M (1945) Translocation of the reproductive stimulus in sugar beet. Bot Gaz 107:86–95

    Article  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 

  • Turck F, Fornara F, Coupland G (2008) Regulation and identity of Florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594

    Article  CAS  PubMed  Google Scholar 

  • Utz HF, Melchinger AE (1996) PLABQTL: a program for composite interval mapping of QTL. J Quant Trait Loci 2:1–5

    Google Scholar 

  • Van Dijk H, Boudry P (1991) Genetic variation for life histories in Beta maritima. Int Board Plant Genet Resour 7:44–55

    Google Scholar 

  • Van Dijk H, Boudry P, McCombre H, Vernet P (1997) Flowering time in wild beet (Beta vulgaris ssp. maritima) along a latitudinal cline. Acta Oecol 18:47–60

    Article  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap® 3.0. Software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The Netherlands

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Farrona S, Vincent C, Joecker A, Schoof H, Turck F, Alonso-Blanco C, Coupland G, Albani MC (2009) PEP1 regulates perennial flowering in Arabis alpina. Nature 459:423–427

    Article  CAS  PubMed  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 USA 100:6263–6268

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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 USA 103:19581–19586

    Article  CAS  PubMed  Google Scholar 

  • Zeevaart JA (2008) Leaf-produced floral signals. Curr Opin Plant Biol 11:541–547

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The project was funded by the Deutsche Forschungsgemeinschaft under grant no. DFG JU 205/14-1. S. F. Abou-Elwafa is supported by a scholarship from the Ministry of Higher Education, Egypt. We thank Uwe Hohmann for propagation of mutants, Gretel Schulze-Buxloh for marker sequence information, Monika Bruisch and Erwin Danklefsen for technical assistance in the field and greenhouse, and Martina Bach and Monika Dietrich for technical assistance in the laboratory.

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Correspondence to Andreas E. Müller.

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Communicated by T. Luebberstedt.

B. Büttner and S. F. Abou-Elwafa contributed equally to this work.

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Büttner, B., Abou-Elwafa, S.F., Zhang, W. et al. A survey of EMS-induced biennial Beta vulgaris mutants reveals a novel bolting locus which is unlinked to the bolting gene B . Theor Appl Genet 121, 1117–1131 (2010). https://doi.org/10.1007/s00122-010-1376-8

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