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Targeted mapping of Cdu1, a major locus regulating grain cadmium concentration in durum wheat (Triticum turgidum L. var durum)

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Abstract

Some durum wheat (Triticum turgidum L. var durum) cultivars have the genetic propensity to accumulate cadmium (Cd) in the grain. A major gene controlling grain Cd concentration designated as Cdu1 has been reported on 5B, but the genetic factor(s) conferring the low Cd phenotype are currently unknown. The objectives of this study were to saturate the chromosomal region harboring Cdu1 with newly developed PCR-based markers and to investigate the colinearity of this wheat chromosomal region with rice (Oryza sativa L.) and Brachypodium distachyon genomes. Genetic mapping of markers linked to Cdu1 in a population of recombinant inbred substitution lines revealed that the gene(s) associated with variation in Cd concentration resides in wheat bin 5BL9 between fraction breakpoints 0.76 and 0.79. Genetic mapping and quantitative trait locus (QTL) analysis of grain Cd concentration was performed in 155 doubled haploid lines from the cross W9262-260D3 (low Cd) by Kofa (high Cd) revealed two expressed sequence tag markers (ESMs) and one sequence tagged site (STS) marker that co-segregated with Cdu1 and explained >80% of the phenotypic variation in grain Cd concentration. A second, minor QTL for grain Cd concentration was also identified on 5B, 67 cM proximal to Cdu1. The Cdu1 interval spans 286 kbp of rice chromosome 3 and 282 kbp of Brachypodium chromosome 1. The markers and rice and Brachypodium colinearity described here represent tools that will assist in the positional cloning of Cdu1 and can be used to select for low Cd accumulation in durum wheat breeding programs targeting this trait. The isolation of Cdu1 will further our knowledge of Cd accumulation in cereals as well as metal accumulation in general.

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References

  • Alloway BJ, Steinnes E (1999) Anthropogenic additions of cadmium to soils. In: McLaughlin MJ, Singh BR (eds) Cadmium in soils and plants. Kluwer Academic, Dordrecht, pp 97–123

    Google Scholar 

  • Badawi M, Danyluk J, Boucho B, Houde M, Sarhan F (2007) The CBF gene family in hexaploid wheat and its relationship to the phylogenetic complex of cereal CBFs. Mol Genet Genomics 277:533–554

    Article  CAS  PubMed  Google Scholar 

  • Bassam BJ, Gresshoff PM (2007) Silver staining DNA in polyacrylamide gels. Nat Protoc 2:2649–2654

    Article  CAS  PubMed  Google Scholar 

  • Bennetzen JL (2000) Comparative sequence analysis of plant nuclear genomes: microcolinearity and its many exceptions. Plant Cell 12:1021–1029

    Article  CAS  PubMed  Google Scholar 

  • Bossolini E, Wicker T, Knobel PA, Keller B (2007) Comparison of orthologous loci from small grass genomes Brachypodium and rice: implications for wheat genomics and grass genome annotation. Plant J 49:704–717

    Article  CAS  PubMed  Google Scholar 

  • Campoli C, Matus-Cádiz MA, Pozniak C, Cattivelli L, Fowler DB (2009) Comparative expression of Cbf genes in the Triticeae under different acclimation induction temperatures. Mol Genet Genomics 282:141–152

    Article  CAS  PubMed  Google Scholar 

  • Cenci A, Chantret N, Kong X, Gu Y, Anderson O, Fahima T, Distelfeld A, Dubcvosky J (2003) Construction and characterization of a half million clone BAC library of durum wheat (Triticum turgidum ssp. durum). Theor Appl Genet 107:931–939

    Google Scholar 

  • Clarke JM, Leisle D, Kopytko GL (1997) Inheritance of cadmium concentration in five durum wheat crosses. Crop Sci 37:1722–1725

    Article  Google Scholar 

  • CODEX STAN 193-1995 (2009) Codex general standard for contaminants and toxins in foods and feed. Revision 5, 2009. Available at http://www.codexalimentarius.net/download/standards/17/CXS_193e.pdf

  • Dubcovsky J, Ramakrishna W, SanMiguel PJ, Busso CS, Yan L, Shiloff BA, Bennetzen JL (2001) Comparative sequence analysis of collinear barley and rice bacterial artificial chromosomes. Plant Physiol 125:1342–1353

    Article  CAS  PubMed  Google Scholar 

  • Dutilleul C, Jourdain A, Bourguignon J, Hugouvieux V (2008) The Arabidopsis putative selenium-binding protein family: expression study and characterization of SBP1 as a potential new player in cadmium detoxification processes. Plant Physiol 147:239–251

    Article  CAS  PubMed  Google Scholar 

  • Erayman M, Sandhu D, Sidhu D, Dilbirligi M, Baenziger PS, Gill KS (2004) Demarcating the gene-rich regions of the wheat genome. Nucleic Acids Res 32:3546–3565

    Article  CAS  PubMed  Google Scholar 

  • Faris JD, Haen KM, Gill BS (2000) Saturation mapping of a gene-rich recombination hot spot region in wheat. Genetics 154:823–835

    CAS  PubMed  Google Scholar 

  • Faris JD, Zhang Z, Fellers JP, Gill BS (2008) Micro-colinearity between rice, Brachypodium, and Triticum monococcum at the wheat domestication locus Q. Funct Integr Genomics 8:149–164

    Article  CAS  PubMed  Google Scholar 

  • Ferenc Bálint A, Szira F, Röder MS, Galiba G, Börner A (2009) Mapping of loci affecting copper tolerance in wheat—the possible impact of the vernalization gene Vrn-A1. Environ Exp Bot 65:369–375

    Article  Google Scholar 

  • Feuillet C, Keller B (2002) Comparative genomics in the grass family: molecular characterization of grass genome structure and evolution. Ann Bot 89:3–10

    Article  CAS  PubMed  Google Scholar 

  • Francki M, Carter M, Ryan K, Hunter A, Bellgard M, Appels R (2004) Comparative organization of wheat homoeologous group 3S and 7L using wheat–rice synteny and identification of potential markers for genes controlling xanthophyll content in wheat. Funct Integr Genomics 4:118–130

    Article  CAS  PubMed  Google Scholar 

  • Gill KS, Gill BS, Endo TR, Boiko EV (1996) Identification and high-density mapping of gene-rich regions in chromosome group 5 of wheat. Genetics 143:1001–1012

    CAS  PubMed  Google Scholar 

  • Grant CA, Buckley WT, Bailey LD, Selles F (1998) Cadmium accumulation in crops. Can J Plant Sci 78:1–17

    CAS  Google Scholar 

  • Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390:301–310

    Article  CAS  PubMed  Google Scholar 

  • Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648

    Article  CAS  PubMed  Google Scholar 

  • Harris NS, Taylor GS (2001) Remobilization of cadmium in maturing shoots of near-isogenic lines of durum wheat that differ in grain cadmium accumulation. J Exp Bot 52:1473–1481

    Article  CAS  PubMed  Google Scholar 

  • Harris NS, Taylor GJ (2004) Cadmium uptake and translocation in seedlings of near isogenic lines of durum wheat that differ in grain cadmium accumulation. BMC Plant Biol 4:4

    Article  PubMed  Google Scholar 

  • Hart JJ, Welch RM, Norvell WA, Kochian LV (2006) Characterization of cadmium uptake, translocation and storage in near-isogenic lines of durum wheat that differ in grain cadmium concentration. New Phytol 172:261–271

    Article  CAS  PubMed  Google Scholar 

  • Huo N, Lazo GR, Vogel JP, You FM, Ma Y, Hayden DM, Coleman-Derr D, Hill TA, Dvorak J, Anderson OD, Luo M-C, Gu YQ (2008) The nuclear genome of Brachypodium distachyon: analysis of BAC end sequences. Funct Integr Genomics 8:135–147

    Article  CAS  PubMed  Google Scholar 

  • Iqbal M, Navabi A, Yang R-C, Salmon DF, Spaner D (2007) Molecular characterization of vernalization response genes in Canadian spring wheat. Genome 50:511–516

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa S, Ae N, Yano M (2005) Chromosomal regions with quantitative trait loci controlling cadmium concentration in brown rice (Oryza sativa). New Phytol 168:345–350

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa S, Abe T, Kuramata M, Yamaguchi M, Ando T, Yamamoto T, Yano M (2010) A major quantitative trait locus for increasing cadmium-specific concentration in rice grain is located on the short arm of chromosome 7. J Exp Bot 61:923–934

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru Y, Suzuki M, Kobayashi T, Takahashi M, Nakanishi H, Mori S, Nishizawa N (2005) OsZIP4, a novel zinc-regulated zinc transporter in rice. J Exp Bot 56:3207–3214

    Google Scholar 

  • Itoh T, Tanaka T, Barrero RA, Yamasaki C, Fujii Y, Hilton PB, Antonio BA, Aono H, Apweiler R, Bruskiewich R et al (2007) Curated genome annotation of Oryza sativa ssp japonica and comparative genome analysis with Arabidopsis thaliana. Genome Res 17:175–183

    Article  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 

  • Karaba A, Dixit S, Greco R, Aharoni A, Trijatmiko KR, Marsch-Martinez N, Krishnan A, Nataraja KN, Udayakumar M, Pereira A (2007) Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. Proc Natl Acad Sci USA 104:15270–15275

    Article  CAS  PubMed  Google Scholar 

  • Kashiwagi T, Shindoh K, Hirotsu N, Ishimaru K (2009) Evidence for separate translocation pathways in determining cadmium accumulation in grain and aerial plant parts in rice. BMC Plant Biol 9:8

    Article  PubMed  Google Scholar 

  • Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50:207–218

    Article  CAS  PubMed  Google Scholar 

  • Klein M, Burla B, Martinoia E (2006) The multidrug resistance-associated protein (MRP/ABC) subfamily of ATP-binding cassette transporters in plants. FEBS Lett 580:1112–1122

    Article  CAS  PubMed  Google Scholar 

  • Knox AK, Li C, Vágújfalvi A, Galiba G, Stockinger E, Dubcovsky J (2008) Identification of candidate CBF genes for the frost tolerance locus Fr-Am2 in Triticum monococcum. Plant Mol Biol 67:257–270

    Article  CAS  PubMed  Google Scholar 

  • Knox RE, Pozniak CJ, Clarke FR, Clarke JM, Houshmand S, Singh AK (2009) Chromosomal location of the cadmium uptake gene (Cdu1) in durum wheat. Genome 52:741–747

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Mohan A, Balyan HS, Gupta PK (2009) Orthology between genomes of Brachypodium, wheat and rice. BMC Res Notes 2:93

    Article  PubMed  Google Scholar 

  • Lagudah ES, McFadden H, Singh RP, Huerta-Espino J, Bariana HS, Spielmeyer W (2006) Molecular genetic characterization of the Lr34/Yr18 slow rusting resistance gene region in wheat. Theor Appl Genetics 114:21–30

    Article  CAS  Google Scholar 

  • Li W, Gill BS (2002) The colinearity of the Sh2/A1 orthologous region in rice sorghum and maize is interrupted and accompanied by genome expansion in the Triticeae. Genetics 160:1153–1162

    CAS  PubMed  Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428

    Article  CAS  Google Scholar 

  • Lu H, Faris JD (2006) Macro- and micro-colinearity between the genomic region of wheat chromosome 5B containing the Tsn1 gene and the rice genome. Funct Integr Genomics 6:90–105

    Article  CAS  PubMed  Google Scholar 

  • Lu H-J, Fellers JP, Friesen TL, Meinhardt SW, Faris JD (2006) Genomic analysis and marker development for the Tsn1 locus in wheat using bin-mapped ESTs and flanking BAC contigs. Theor Appl Genet 112:1132–1142

    Article  CAS  PubMed  Google Scholar 

  • McLaughlin MJ, Parker DR, Clarke JM (1999) Metals and micronutrients—food safety issues. Field Crops Res 60:143–163

    Article  Google Scholar 

  • Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, Vavasseur A, Richaud P (2009) AtHMA3, a P 1B -ATPase Allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149:894–904

    Article  CAS  PubMed  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35:D883–D887

    Article  CAS  PubMed  Google Scholar 

  • Parker DR, Norvell WA (1999) Advances in solution culture methods for plant mineral nutrition research. Adv Agron 65:151–213

    Article  CAS  Google Scholar 

  • Parker DR, Norvell WA, Chaney RL (1995) GEOCHEM-PC: a chemical speciation program for IBM and compatible personal computers. In: Loeppert RH, Schwab AP, Goldberg S (eds) Chemical equilibrium and reaction models. SSSA Spec, Publ. 42, Soil Science Society of America, Madison, WI, pp 253–269

  • Paux E, Sourdille P, Salse J, Saintenac C, Choulet F, Leroy P, Korol A, Michalak M, Kianian S, Spielmeyer W, Lagudah E, Somers D, Kilian A, Alaux M, Vautrin S, Bergès H, Eversole K, Appels R, Safar J, Simkova H, Dolezel J, Bernard M, Feuillet C (2008) A physical map of the 1-gigabase bread wheat chromosome 3B. Science 322:101–104

    Article  CAS  PubMed  Google Scholar 

  • Penner GA, Clarke J, Bezte LJ, Leisle D (1995) Identification of RAPD markers linked to a gene governing cadmium uptake in durum wheat. Genome 38:543–547

    CAS  PubMed  Google Scholar 

  • Pozniak CJ, Fox SL, Knott DR (2009) CDC Verona durum wheat. Can J Plant Sci 89:321–324

    Article  Google Scholar 

  • Qi LL, Echalier B, Chao S, Lazo GR, Butler GE, Anderson OD, Akhunov ED, Dvorak J, Linkiewicz AM, Ratnasiri A et al (2004) A chromosome bin map of 16, 000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712

    Article  CAS  PubMed  Google Scholar 

  • Ramakrishna W, Dubcovsky J, Park Y-J, Busso C, Emberton J, SanMiguel P, Bennetzen JL (2002) Different types and rates of genome evolution detected by comparative sequence analysis of orthologous segments from four cereal genomes. Genetics 162:1389–1400

    CAS  PubMed  Google Scholar 

  • Saintenac C, Falque M, Martin OC, Paux E, Feuillet C, Sourdille P (2009) Detailed recombination studies along chromosome 3B provide new insights on crossover distribution in wheat (Triticum aestivum L.). Genetics 181:393–403

    Article  CAS  PubMed  Google Scholar 

  • Salt DE, Rauser WE (1995) MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol 107:1293–1301

    CAS  PubMed  Google Scholar 

  • Satarug S, Moore MR (2004) Adverse health effects of chronic exposure to low-level cadmium in foodstuffs and cigarette smoke. Environ Health Perspect 112:1099–1103

    Article  CAS  PubMed  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. A poor man’s approach to genotyping for research and high-throughput diagnostics. Nat Biotechnol 16:233–235

    Article  Google Scholar 

  • Song WY, Sohn EJ, Martinoia E, Lee YJ, Yang YY, Jasinski M, Forestier C, Hwang I, Lee Y (2003) Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat Biotechnol 21:914–919

    Article  CAS  PubMed  Google Scholar 

  • Soric R, Loncaric Z, Kovacevic V, Brkic I, Simic D (2009) A major gene for leaf cadmium accumulation in maize (Zea mays L.). In: The proceedings of the international plant nutrition colloquim XVI, UC Davis. Available at http://escholarship.org/uc/item/1q48v6cf

  • Sorrells ME, LaRota M, Bermudez-Kandianis CE, Greene RA, Kantety R, Munkvold JD, Miftahudin, Mahmoud A, Ma X, Gustafson PJ et al (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827

    CAS  PubMed  Google Scholar 

  • Stockinger EJ, Skinner JS, Gardner KG, Francia E, Pecchioni N (2007) Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. Plant J 51:308–321

    Article  CAS  PubMed  Google Scholar 

  • Stolt JP, Sneller FEC, Bryngelsson T, Lunborg T, Schat H (2003) Phytochelation and cadmium accumulation in wheat. Environ Exp Bot 49:21–28

    Article  CAS  Google Scholar 

  • Szira F, Ferenc Bálint A, Vágújfalvi A, Galiba G (2008) Are Cbf genes involved in copper tolerance? Acta Biol Szeged 52:205–207

    Google Scholar 

  • Takahashi R, Ishimaru Y, Senoura T, Shimo HM, Nakanishi H, Nishizawa NK (2009) Characterization of OsNramp1, a metal transporter from rice. In: The proceedings of the international plant nutrition colloquium XVI, Department of Plant Sciences, UC Davis. Available at http://escholarship.org/uc/item/2vh9z40

  • Tanhuanpää P, Kalendar R, Schulman AH, Kiviharju E (2007) A major gene for grain cadmium accumulation in oat (Avena sativa L.). Genome 50:588–594

    Article  PubMed  Google Scholar 

  • Tezuka K, Miyadate H, Katou K, Kodama I, Matsumoto S, Kawamoto T, Masaki S, Satoh H, Yamagucji M, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2009) A single recessive gene controls cadmium translocation in the cadmium hyperaccumulating rice cultivar Cho-Ko-Kohu. Theor Appl Genet 120:1175–1182

    Article  PubMed  Google Scholar 

  • Ueno D, Kono I, Yokosho K, Ando T, Yano M, Ma JF (2009) A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol 182:644–653

    Article  CAS  PubMed  Google Scholar 

  • Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688

    Article  CAS  PubMed  Google Scholar 

  • Valárik M, Linkiewicz A, Dubcovsky J (2006) A microcolinearity study at the earliness per se gene Eps-Am 1 region reveals an ancient duplication that preceded the wheat–rice divergence. Theor Appl Genetics 112:945–957

    Article  Google Scholar 

  • van Ooijen JW (1999) LOD significance thresholds for QTL analysis in experimental populations of diploid species. Heredity 83:613–624

    Article  PubMed  Google Scholar 

  • Van Ooijen JW (2004) MapQTL v5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma BV, Wageningen

  • van Ooijen JW, Voorrips RE (2004) JoinMap Version 4.0, Software for the calculation of genetic linkage maps. Kyazma BV, Wageningen

    Google Scholar 

  • Vogeli-Lange R, Wagner GJ (1990) Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves. Implication of a transport function for cadmium-binding peptides. Plant Physiol 92:1086–1093

    Article  CAS  PubMed  Google Scholar 

  • Wojas S, Hennig J, Plaza S, Geisler M, Siemianowski O, Sklodowska A, Ruszczynska A, Bulska E, Antosiewicz DM (2009) Ectopic expression of Arabidopsis ABC transporter MRP7 modifies cadmium root-to-shoot transport and accumulation. Environ Pollut 157:2781–2789

    Article  CAS  PubMed  Google Scholar 

  • Xue D, Chen M, Zhang G (2009) Mapping of QTLs associated with cadmium tolerance and accumulation during seedling stage in rice (Oryza sativa L.). Euphytica 165:587–596

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yu GT, Cai X, Harris MO, Gu YQ, Luo MC, Xu SS (2009) Saturation and comparative mapping of the genomic region harboring Hessian Xy resistance gene H26 in wheat. Theor Appl Genet 118:1589–1599

    Article  CAS  PubMed  Google Scholar 

  • Zook EG, Greene FE, Morris ER (1970) Nutrient composition of selected wheats and products. VI. Distribution of manganese, copper, nickel, zinc, magnesium, lead, tin, cadmium, chromium, and selenium as determined by atomic absorption spectroscopy and colorimetry. Cereal Chem 47:720–731

    CAS  Google Scholar 

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Acknowledgments

We gratefully acknowledge the technical assistance of Ryan Babonich, Russell Lawrie, Charlene Tang, Jay Ross, and Marlin Olfert, and funding of this work by the National Science and Engineering Research Council (NSERC), Western Grains Research Foundation (WGRF), and the Agriculture and Agri-Food Canada Matching Investment Initiative.

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Correspondence to C. J. Pozniak.

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Communicated by C. Feuillet.

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Wiebe, K., Harris, N.S., Faris, J.D. et al. Targeted mapping of Cdu1, a major locus regulating grain cadmium concentration in durum wheat (Triticum turgidum L. var durum). Theor Appl Genet 121, 1047–1058 (2010). https://doi.org/10.1007/s00122-010-1370-1

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