Abstract
Cereal crop yield is greatly affected in many growing areas by abiotic stresses, mainly low temperature and drought. In order to find candidates for the tolerance genes for these stresses, 13 genes encoding for transcription factors and upstream regulators were screened by amplification and SSCP on six parental genotypes of three barley mapping populations (‘Nure’ × ‘Tremois’, ‘Proctor’ × ‘Nudinka’, and ‘Steptoe’ × ‘Morex’), and mapped as newly developed STS, SNP, and SSCP markers. A new consensus function map was then drawn using the three maps above, including 16 regulatory candidate genes (CGs). The positions of barley cold and drought tolerance quantitative trait loci (QTLs) presently described in the literature were added to the consensus map to find positional candidates from among the mapped genes. A cluster of six HvCBF genes co-mapped with the Fr-H2 cold tolerance QTL, while no QTLs for the same trait were positioned on chromosome 7H, where two putative barley regulators of CBF expression, ICE1 and FRY1, found by homology search, were mapped in this work. These observations suggest that CBF gene(s) themselves, rather than their two regulators, are at present the best candidates for cold tolerance. Four out of 12 drought tolerance QTLs of the consensus map are associated with regulatory CGs, on chromosomes 2H, 5H, and 7H, and two QTLs with effector genes, on chromosomes 5H and 6H. The results obtained could be used to guide MAS applications, allowing introduction into an ideal genotype of favourable alleles of tolerance QTLs.
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Abbreviations
- CG:
-
Candidate gene
- QTL:
-
Quantitative trait locus
- TF:
-
Transcription factor
- COR:
-
Cold regulated gene
- STS:
-
Sequence tagged site
- SNP:
-
Single nucleotide polymorphism
- SSCP:
-
Single strand conformation polymorphism
- CAPS:
-
Cleaved amplified polymorphic sequence
- ARMS:
-
Amplification refractory mutation system
References
Abe H, Urao T, Ito T, Seki M, Shonozaki K, Yammaguchi-Shinozaki K (2003) Arabidopsis AtMYC (bHLH) and AtMYB2 (MYB) function as transcription activators in abscisic acid signaling. Plant Cell 15:63–78
Blum A (1989) Osmotic adjustment and growth of barley genotypes under drought stress. Crop Sci 29:230–233
Casaretto J, Ho TD (2003) The transcription factors HvABI5 and HvVP1 are required for the abscisic acid induction of gene expression in barley aleurone cells. Plant Cell 15:271–284
Cattivelli L, Baldi P, Crosatti C, Di Fonzo N, Faccioli P, Grossi M, Mastrangelo AM, Pecchioni N, Stanca AM (2002) Chromosome regions and stress-related sequences involved in resistance to abiotic stress in Triticeae. Plant Mol Biol 48:649–665
Causse M, Duffe P, Gomez MC, Buret M, Damidaux R, Zamir D, Gur A, Chevalier C, Lemaire-Chamley M, Rothan C (2004) A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. J Exp Bot 55:1671–1685
Chandra Babu R, Zhang JA, Blum JA, Ho T-HD, Wu R, Nguyen HT (2004) HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Sci 166:855–862
Chen X, Salamini F, Gebhardt C (2001) A potato molecular-function map for carbohydrate metabolism and transport. Theor Appl Genet 102:284–295
Chinnusamy V, Ohta M, Kanrar S, Lee B, Hong X, Agarwal A, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Gene Dev 17:1043–1054
Choi DW, Rodriguez EM, Close TJ (2002) Barley Cbf3 gene identification, expression pattern, and map location. Plant Physiol 129:1–7
Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803
Diab AA, Teulat B, This D, Ozturk NZ, Benscher D, Sorrells ME (2004) Identification of drought-inducible genes and differentially expressed sequence tags in barley. Theor Appl Genet 109:1417–1425
Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552
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
Galiba G, Quarrie SA, Sutka J, Morgaunov A, Snape JW (1995) RFLP mapping of the vernalization (Vrn1) and frost resistance (Fr1) genes on chromosome 5A of wheat. Theor Appl Genet 90:1174–1179
Haake V, Cook D, Riechmann JL, Omaira P, Thomashow MF, Zang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Symp Ser 41:95–98
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 winterhardiness. Genome 36:66–71
Hayes PM, Castro A, Marquez-Cedillo L, Corey A, Henson C, Jones BL, Kling J, Mather D, Matus I, Rossi C, Sato K (2003) Genetic diversity for quantitative inherited agronomic and malting quality traits. In: Von-Bothmer R et al. (eds) Diversity in barley. Elsevier Amsterdam, pp 201–226
Heun M, Kennedy AE, Anderson JA, Lapitan NLV, Sorrells ME, Tanksley SD (1991) Construction of a restriction fragment length polymorphism map for barley (Hordeum vulgare). Genome 35:1019–1025
Ishitani M, Xiong L, Stevenson B, Zhu J-K (1997) Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9:1935–1949
Islam AKMR, Shepherd KW, Sparrow DHB (1981) Isolation and characterization of euplasmic wheat-barley chromosome addition lines. Heredity 46:161–174
Ismail AM, Hall AE, Close TJ (1999) Allelic variation of a dehydrin gene cosegregates with chilling tolerance during seedling emergence. Proc Natl Acad Sci USA 96:13566–13570
Kleinhofs A, Kilian A, Saghai Maroof MA, Biyashev RM, Hayes PM, Chen FQ, Lapitan N, Fenwick A, Blake TK, Kanazin V, Ananiev E, Dahleen L, Kudrna D, Bollinger J, Knapp SJ, Liu B, Sorrells M, Heun M, Franckowiak JD, Hoffmann D, Skadsen R, Steffenson BJ (1993) A molecular, isozyme and morphological map of the barley (Hordeum vulgare L.) genome. Theor Appl Genet 86:705–712
Kleinhofs A, Graner A (2001) An integrated map of the barley genome. In: Phillips RL, Vasil IK (eds) DNA-based markers in plants. Kluwer, Dordrecht pp 187–199
Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181
Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, Zhu JK (2002) LOS2, a genetic locus acquired for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J 21:2692–2702
Limin AE, Fowler DB (2002) Developmental traits affecting low-temperature tolerance response in near-isogenic lines for the vernalization locus Vrn-A1 in wheat (Triticum aestivum L. em Thell). Ann Bot 89:579–585
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
Marè C, Mazzucotelli E, Crosatti C, Francia E, Stanca AM, Cattivelli L (2004) HvWRKY38: a new transcription factor involved in cold- and drought-response in barley. Plant Mol Biol 55:399–416
Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38:982–993
Morandini P, Salamini F (2003) Plant biotechnology and breeding: allied for years to come. Trends Plant Sci 8:70–75
Nguyen TT, Klueva N, Chamareck V, Aarti A, Magpantay G, Millena AC, Pathan MS, Nguyen HT (2004) Saturation mapping of QTL regions and identification of putative candidate genes for drought tolerance in rice. Mol Genet Genom 272:35–46
Orita M, Iwahana H, Kanazana H, Hayashi K, Sekiya T (1989) Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proc Natl Acad Sci USA 86:2766–2770
Palaisa KA, Morgante M, Williams M, Rafalski A (2003) Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15:1795–1806
Pan A, Hayes PM, Chen F, Chen THH, Blake T, Wright S, Karsai I, Bedo Z (1994) Genetic analysis of the components of winterhardiness in barley (Hordeum vulgare L). Theor Appl Genet 89:900–910
Pflieger S, Lefebvre V, Causse M (2001) The candidate gene approach in plant genetics: a review. Mol Breed 7:275–291
Rafalski A (2002) Application of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100
Reinheimer JL, Barr AR, Eglinton JK (2004) QTL mapping of chromosomal regions conferring reproductive frost tolerance in barley (Hordeum vulgare L). Theor Appl Genet 109:1267–1274
Roberts DWA (1990) Identification of loci on chromosome 5A of wheat involved in control of cold hardiness, vernalization, leaf length, rosette growth habit, and height of hardened plants. Genome 33:247–259
Robertson M, Swain SM, Chandler PM, Olszewski NE (1998) Identification of a negative regulator of gibberellin action, HvSPY, in barley. Plant Cell 10:995–1007
Rozen S, Skaletsky HJ (2000) Primer3 on the for general users and for biologist programmers. Meth Mol Biol 132:365–386
Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327
Schonfeld MA, Johnson RC, Carver BF, Mornhinweg DW (1988) Water relations in winter wheat as drought resistance indicator. Crop Sci 28:526–531
Schuurink RC, Shartzer SF, Fath A, Jones RL (1998) Characterization of a calmodulin-binding transporter from the plasma membrane of barley aleurone. Proc Natl Acad Sci USA 95:1944–1949
Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417
Singh K, Foley R, Onate-Sanches L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436
Skinner JS, von Zitzewitz J, Szucs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen THH, Hayes PM (2005a) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59:533–551
Skinner JS, von Zitzewitz J, Marquez-Cedillo L, Filichkin T, Szücs P, Amundsen K, Stockinger EJ, Thomashow MF, Chen THH, Hayes PM (2005b) Barley contains a large CBF gene family associated with quantitative cold tolerance traits. In: Chen THH, Uemura M, Fujikawa S (eds) Cold Hardiness in Plants: Molecular Genetics, Cell Biology and Physiology. CAB International, Oxon, UK, pp 30–52
Stam P, Van Ooijen JW (1995) JOINMAP version 2.0: Software for the calculation of genetic linkage maps. Center Plant Breeding Reproduction Res, Agric Res Dep, Wageningen, The Netherlands
Sutka J, Galiba G, Vagujfalvi A, Gill BS, Snape JW (1999) Physical mapping of the Vrn-A1 and Fr1 genes on chromosome 5A of wheat using deletion lines. Theor Appl Genet 99:199–202
Teulat B, This D, Khairallah M, Borries C, Ragot C, Sourdille P, Leroy P, Monneveux P, Charrier A (1998) Several QTLs involved in osmotic-adjustment trait variation in barley (Hordeum vulgare L.). Theor Appl Genet 96:688–698
Teulat B, Borries C, This D (2001) New QTLs identified for plant water status, water-soluble carbohydrate and osmotic adjustment in a barley population grown in a growth-chamber under two water regimes. Theor Appl Genet 103:161–170
Teulat B, Merah O, Sirault X, Borries C, Waugh R, This D (2002) QTLs for grain carbon isotope discrimination in field-grown barley. Theor Appl Genet 106:118–126
Teulat B, Zoumarou-Wallis N, Rotter B, BenSalem M, Bahri H, This D (2003) QTL for relative water content in field-grown barley and their stability across Mediterranean environments. Theor Appl Genet 108:181–188
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Ann Rev Plant Physiol Plant Mol Biol 50:571–599
Thomashow MF, Gilmour SJ, Stockinger EJ, Jaglo-Ottosen KR, Zarka DG (2001) Role of the Arabidopsis CBF transcriptional activators in cold acclimation. Physiol Plant 112:171–175
Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler IV ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289
Vannini C, Locatelli F, Bracale M, Magnani E, Marsoni M, Osnato M, Mattana M, Baldoni E, Coraggio I (2004) Overexpression of the rice Osmyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants. Plant J 37:115–127
Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211
von Zitzewitz J, Szucs P, Dubcovsky J, Yan L, Francia E, Pecchioni N, Casas A, Chen THH, Hayes PM, Skinner JS (2005) Structural and functional characterization of barley vernalization genes. Plant Mol Biol 59:449–467
Wissenbach M, Uberlacker B, Vogt F, Becker D, Salamini F, Rohde W (1993) Myb genes from Hordeum vulgare: tissue-specific expression of chimeric Myb promoter/Gus genes in transgenic tobacco. Plant J 4:411–422
Xiong L, Lee H, Ishitani M, Lee H, Zhang C, Zhu JK (2001) FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev 15:1971–1984
Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell (Suppl) S165–S183
Xue GP (2002) An AP2 domain transcription factor HvCBF1 activates expression of cold-responsive genes in barley through interaction with a (G/a)(C/t)CGAC motif. Biochim Biophys Acta 1577:63–72
Xue GP (2003) The DNA-binding activity of an AP2 transcriptional activator HvCBF2 involved in regulation of low-temperature responsive genes in barley is modulated by temperature. Plant J 33:373–383
Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94
Ye S, Dhillon S, Ke X, Collins AR, Day IN (2001) An efficient procedure for genotyping single nucleotide polymorphisms. Nucl Acid Res 29:e88
Acknowledgements
The authors wish to thank Dr. S. Salvi, Università di Bologna, for the consensus map construction by means of the software JoinMap 2.0. This work was supported by grants from MiUR (Ministero dell’Università e della Ricerca Scientifica) “Progetto FIRB FUNCTIONMAP” (ID: RBAU01MHMR_004), and partially supported by EU INCOA3 Project MABDE No. ICA3-2002-10073.
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Communicated by J. W. Snape
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Tondelli, A., Francia, E., Barabaschi, D. et al. Mapping regulatory genes as candidates for cold and drought stress tolerance in barley. Theor Appl Genet 112, 445–454 (2006). https://doi.org/10.1007/s00122-005-0144-7
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DOI: https://doi.org/10.1007/s00122-005-0144-7