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A perennial ryegrass CBF gene cluster is located in a region predicted by conserved synteny between Poaceae species

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Abstract

CBF/DREB1 proteins are the most important regulators of the cold temperature signaling pathway in many plants. CBF genes are candidates for low-temperature tolerance QTL in wheat and barley. Ten novel putative CBF cDNAs of perennial ryegrass (Lolium perenne L.) have been isolated from cold-treated leaf tissue. Their primary structures contain some conserved motifs, characteristic of the gene class. Phylogenetic analysis revealed that LpCBF genes were attributable to the HvCBF3-, and HvCBF4-subgroups following the previously proposed classification of barley CBF genes. RT-PCR analysis revealed that the expression of LpCBF genes was rapidly induced in response to low temperature and that the expression pattern under the low-temperature conditions for a long period was different between the various LpCBF genes. Five of the ten LpCBF genes were assigned to the genetic linkage map using the p150/112 reference mapping population. LpCBFIb, LpCBFII, LpCBFIIIb and LpCBFIIIc were mapped on LG5 forming a cluster within 2.2 cM, while LpCBFVb was located on LG1. Based on comparative genetic studies, conserved synteny for CBF gene family was observed between the Triticeae cereals and perennial ryegrass. Information on the perennial ryegrass CBF genes at both the molecular and genetic level obtained in this study would be useful for the further study on the role of CBF genes and low-temperature tolerance in grasses.

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References

  • Alm V, Fang C, Busso CS, Devos KM, Vollan K, Grieg Z, Rognli OA (2003) A linkage map of meadow fescue (Festuca pratensis Huds.) and comparative mapping with other Poaceae species. Theor Appl Genet 108:25–40

    Article  PubMed  CAS  Google Scholar 

  • Alm V, Busso CS, Larsen A, Humphreys MW, Rognli OA (2006) Quantitative trait loci for frost tolerance, winter survival and drought tolerance in meadow fescue (Festuca pratensis Huds.), and comparative mapping with cereals. Genetics (in press)

  • Alonso-Blanco C, Gomez-Mena C, Llorente F, Koornneef M, Salinas J, Martinez-Zapater JM (2005) Genetic and molecular analyses of natural variation indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis. Plant Physiol 139:1304–1312

    Article  PubMed  CAS  Google Scholar 

  • Armstead IP, Turner LB, Farrell M, Skot L, Gomez P, Montoya T, Donnison IS, King IP, Humphreys MO (2004) Synteny between a major heading-date QTL in perennial ryegrass (Lolium perenne L.) and the Hd3 heading-date locus in rice. Theor Appl Genet 108:822–828

    Article  PubMed  CAS  Google Scholar 

  • Bert PF, Charmet G, Sourdille P, Hayward MD, Balfourier F (1999) A high-density molecular map for ryegrass (Lolium perenne) using AFLP markers. Theor Appl Genet 99:445–452

    Article  CAS  Google Scholar 

  • Choi DW, Rodriguez EM, Close TJ (2002) Barley Cbf3 gene identification, expression pattern, and map location. Plant Physiol 129:1781–1787

    Article  PubMed  CAS  Google Scholar 

  • Cogan NO, Ponting RC, Vecchies AC, Drayton MC, George J, Dracatos PM, Dobrowolski MP, Sawbridge TI, Smith KF, Spangenberg GC, Forster JW (2006) Gene-associated single nucleotide polymorphism discovery in perennial ryegrass (Lolium perenne L.). Mol Gen Genomics, available on-line

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high salt- and cold- responsive gene expression. Plant J 33:751–763

    Article  PubMed  CAS  Google Scholar 

  • Faville MJ, Vecchies AC, Schreiber M, Drayton MC, Hughes LJ, Jones ES, Guthridge KM, Smith KF, Sawbridge T, Spangenberg GC, Bryan GT, Forster JW (2004) Functionally associated molecular genetic marker map construction in perennial ryegrass (Lolium perenne L.). Theor Appl Genet 110:12–32

    Article  PubMed  CAS  Google Scholar 

  • Francia E, Rizza F, Cattivelli L, Stanca AM, Galiba G, Tóth B, Hayes PM, Skinner JS, Pecchioni N (2004) Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) × ‘Tremois’ (spring) barley map. Theor Appl Genet 108:670–680

    Article  PubMed  CAS  Google Scholar 

  • Galiba G, Quarrie SA, Sutka J, Morgounov A, Snape JW (1995) RFLP mapping ofvernalization (Vrn1) and frost resistance (Fr1) on chromosome 5A of wheat. Theor Appl Genet 90:1174–1179

    Article  CAS  Google Scholar 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54:767–781

    Article  PubMed  CAS  Google Scholar 

  • Hayes PM, Blake T, Chen THH, Tragoonrung S, Chen F, Pan A, Liu B (1993) Quantitative trait loci on barley (Hordeum vulgare L.) chromosome 7 associated with components of winter hardiness. Genome 36:66–71

    CAS  PubMed  Google Scholar 

  • Jaglo-Ottosen KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    Article  PubMed  CAS  Google Scholar 

  • Jaglo-Ottosen KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 12:910–917

    Article  Google Scholar 

  • Jensen LB, Andersen JR, Frei U, Xing Y, Taylor C, Holm PB, Lübberstedt T (2005) QTL mapping of vernalization response in perennial ryegrass (Lolium perenne L.) reveals co-location with an orthologue of wheat VRN1. Theor Appl Genet 110:527–536

    Article  PubMed  CAS  Google Scholar 

  • Jones ES, Mahoney NL, Hayward MD, Armstead IP, Jones JG, Humphreys MO, Kishida T, Yamada T, Balfourier F, Charmet G, Forster JW (2002) An enhanced molecular marker-based genetic map of perennial ryegrass (Lolium perenne L.) reveals comparative relationships with other Poaceae genomes. Genome 45:282–295

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi F, Takumi S, Kume S, Ishibashi M, Ohno R, Murai K, Nakamura C (2005) Regulation by Vrn-1/Fr-1 chromosomal intervals of CBF-mediated Cor/Lea gene expression and freezing tolerance in common wheat. J Exp Bot 56:887–895

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Laurie DA, Pratchett N, Bezant JH, Snape JW (1995) RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter spring barley (Hordeum vulgare L.) cross. Genome 38:575–585

    CAS  PubMed  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    Article  PubMed  CAS  Google Scholar 

  • Miller AK, Galiba G, Dubcovsky J (2006) A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-A m 2 in Triticum monococcum. Mol Gen Genomics 275:193–203

    Article  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) The isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    PubMed  CAS  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2006) Regulons inovolved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant 126:62–71

    Article  CAS  Google Scholar 

  • Nakayama S, Tsurumi Y, Larsen A, Takai T, Iriki N (2001) Breeding forage grasses for winter survival. In: Iriki N et al (eds) Low temperature plant microbe interactions under snow, Hokkaido National Agricultural Experiment Station, Sapporo, pp 169–180

    Google Scholar 

  • Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 101:3985–3990

    Article  PubMed  CAS  Google Scholar 

  • Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45:1042–1052

    Article  PubMed  CAS  Google Scholar 

  • Sim S, Chang T, Curley J, Warnke SE, Barker RE, Jung G (2005) Chromosomal rearrangements differentiating the ryegrass genome from the Triticeae, oat, and rice genomes using common heterologous RFLP probes. Theor Appl Genet 110:1011–1019

    Article  PubMed  CAS  Google Scholar 

  • Skinner JS, von Zitzewitz J, Szűcs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen THH, Hayes PM (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59:533–551

    Article  PubMed  CAS  Google Scholar 

  • Skinner JS, Szűcs P, von Zitzewitz J, Marquez-Cedillo L, Filichkin T, Stockinger EJ, Thomashow MF, Chen THH, Hayes PM (2006) Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis. Theor Appl Genet 112:832–842

    Article  PubMed  CAS  Google Scholar 

  • Snape JW, Semikhodskii A, Fish L, Sarma RN, Quarrie SA et al (1997) Mapping of frost tolerance loci in wheat and comparative mapping with other cereals. Acta Agron Hung 45:265–270

    Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040

    Article  PubMed  CAS  Google Scholar 

  • Stockinger EJ, Cheng H, Skinner JS (2006) Structural organization of barley CBF genes coincident with a QTL for cold hardiness. In: Chen THH, Uemura M, Fujikawa S (eds) Cold hardiness in plants. CABI Publishing, Wallingford, pp 53–63

    Google Scholar 

  • Sutka J, Snape JW (1989) Location of a gene for frost resistance on chromosome 5A of wheat. Euphytica 42:41–44

    Article  Google Scholar 

  • Tang MJ, Lu SY, Jing YX (2005) Isolation and identification of a cold-inducible gene encoding a putative DRE-binding transcription factor from Festuca arundinacea. Plant Physiol Biochem 43:233–239

    Article  PubMed  CAS  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  PubMed  CAS  Google Scholar 

  • Tondelli A, Francia E, Barabaschi D, Aprile A, Skinner JS, Stockinger EJ, Stanca AM, Pecchioni N (2006) Mapping regulatory genes as candidates for cold and drought stress tolerance in barley. Theor Appl Genet 112:445–454

    Article  PubMed  CAS  Google Scholar 

  • Toth B, Galiba G, Feher E, Sutka J, Snape JW (2003) Mapping genes affecting flowering time and frost resistance on chromosome 5B of wheat. Theor Appl Genet 107:509–514

    Article  PubMed  CAS  Google Scholar 

  • Vágújfalvi A, Galiba G, Cattivelli L, Dubcovsky J (2003) The cold regulated transcriptional activator Cbf3 is linked to the frost tolerance locus Fr-A2 on wheat chromosome 5A. Mol Gen Genome 269:60–67

    Google Scholar 

  • Wilkins PW (1991) Breeding perennial ryegrass for agriculture. Euphytica 52:201–214

    Article  Google Scholar 

  • Xiong Y, Fei SZ (2006) Functional and phylogenetic analysis of a DREB/CBF-like gene in perennial ryegrass (Lolium perenne L.). Planta 224:878–888

    Article  PubMed  CAS  Google Scholar 

  • Xue GP (2002) Characterisation of the DNA-binding profile of barley HvCBF1 using an enzymatic method for rapid, quantitative and high-throughput analysis of the DNA-binding activity. Nucleic Acids Res 30:e77

    Article  PubMed  Google Scholar 

  • Yamada T, Jones ES, Cogan NOI, Vecchies AC, Nomura T, Hisano H, Shimamoto Y, Smith KF, Hayward MD, Forster JW (2004) QTL analysis of morphological, developmental, and winter hardiness-associated traits in perennial ryegrass. Crop Sci 44:925–935

    Article  CAS  Google Scholar 

  • Zhao TJ, Sun S, Liu Y, Liu JM, Liu Q, Yan YB, Zhou HM (2006) Regulating the drought-responsive element (DRE)-mediated signaling pathway by synergic functions of trans-active and trans-inactive DRE binding factors in Brassica napus. J Biol Chem 281:10752–10759

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

We gratefully acknowledge Dr. Sohei Kobayashi, Dr. Kazuhiro Tase and Mr. Yasuharu Sanada for their technical advice, and Miss Mayumi Hata and Miss Mayuko Kawamura for their technical assistance. This work was supported, in part, by Grants-in Aid for Scientific Research (No. 17380163) from the Ministry of Education, Science, Sports and Culture, Japan. The authors thank Prof. Michael Hayward (Rhydgoch Genetics, Aberystwyth, UK) and Dr. Toshinori Komatsu for careful critical reading of the manuscript.

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Correspondence to T. Yamada.

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Communicated by H. H. Geiger.

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Tamura, K., Yamada, T. A perennial ryegrass CBF gene cluster is located in a region predicted by conserved synteny between Poaceae species. Theor Appl Genet 114, 273–283 (2007). https://doi.org/10.1007/s00122-006-0430-z

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  • DOI: https://doi.org/10.1007/s00122-006-0430-z

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