Skip to main content
SpringerLink
Log in

Gene polymorphisms for elucidating the genetic structure of the heavy-metal hyperaccumulating trait in Thlaspi caerulescens and their cross-genera amplification in Brassicaceae

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Genetic polymorphism was investigated in Thlaspi caerulescens J. & C. Presl at 15 gene regions, of which seven have been identified to putatively play a role in heavy-metal tolerance or hyperaccumulation. Single nucleotide and length polymorphisms were assessed at four cleaved amplified polymorphic sequences (CAPS) and 11 simple sequence repeat (microsatellite) loci, respectively. The utility of these loci for genetic studies in T. caerulescens was measured among seven natural populations (135 individuals). Fourteen loci rendered polymorphism, and the number of alleles per locus varied from 2 to 5 and 1 to 27 for CAPS and microsatellites, respectively. Up to 12 alleles per locus were detected in a population. The global observed heterozygosity per population varied between 0.01 and 0.31. Additionally, cross-species/genera amplification of loci was investigated on eight other Brassicaceae (five individuals per population). Overall, 70% of the cross-species/genera amplifications were successful, and among them, more than 40% provided intraspecific polymorphisms within a single population. This indicates that such markers may, as well, allow comparative population genetic or mapping studies between and within several Brassicaceae, particularly for genes involved in traits such as heavy-metal tolerance and/or hyperaccumulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Assunçao AGL, Schat H, Aarts MGM (2003a) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:351–360

    Article  CAS  Google Scholar 

  • Assunçao AGL, Ten Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003b) A cosegregation analysis of zinc (Zn) accumulation and Zn tolerance in the Zn hyperaccumulator Thlaspi caerulescens. New Phytol 159:383–390

    Article  CAS  Google Scholar 

  • Assunçao AGL, Pieper B, Vromans J, Lindhout P, Aarts MGM, Schat H (2006) Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analysis of zinc accumulation. New Phytol 170:21–32

    Article  PubMed  CAS  Google Scholar 

  • Basic N, Keller C, Fontanillas P, Vittoz P, Besnard G, Galland N (2006a) Cadmium hyperaccumulation and reproductive traits in natural Thlaspi caerulescens populations. Plant Biol 8:64–72

    Article  CAS  Google Scholar 

  • Basic N, Salamin N, Keller C, Galland N, Besnard G (2006b) Genetic differentiation of Thlaspi caerulescens natural populations in relation to their cadmium hyperaccumulation capacity. Biochem Syst Ecol 34: DOI 10.1016/j.bse.2006.04.001

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc Roy Soc Lond Ser B 263:1619–1626

    Article  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.03, logiciel sous Windows™ pour la génétique des populations. Laboratoire Génome, Populations, Interactions CNRS UMR 5000, Université de Montpellier II, Montpellier (France). http://www.univ-montp2.fr/∼genetix/genetix/genetix.htm

  • Bernard C, Roosens N, Czernic P, Lebrun M, Verbruggen N (2004) A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett 569:140–148

    Article  PubMed  CAS  Google Scholar 

  • Bert V, Meerts P, Saumitou-Laprade P, Salis P, Gruber W, Verbruggen N (2003) Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant Soil 249:9–18

    Article  CAS  Google Scholar 

  • Boivin K, Acarkan A, Mbulu RS, Clarenz O, Schmidt R (2004) The Arabidopsis genome sequence as a tool for genome analysis in Brassicaceae: a comparison of the Arabidopsis thaliana and Capsella rubella genomes. Plant Physiol 135:735–744

    Article  PubMed  CAS  Google Scholar 

  • Bon MC, Hurard C, Gaskin J, Risterucci AM (2005) Polymorphic microsatellite markers in polyploidy Lepidium draba L. ssp. draba (Brassicaceae) and cross-species amplification in closely related taxa. Mol Ecol Notes 5:68–70

    Article  CAS  Google Scholar 

  • Bovet L, Eggmann T, Meylan-Bettex M, Polier J, Kammer P, Marin E, Feller U, Martinoia E (2003) Transcript levels of AtMRPs after cadmium treatment: induction of AtMRP3. Plant Cell Environ 26:371–381

    Article  CAS  Google Scholar 

  • Clauss MJ, Cobban H, Mitchell-Olds T (2002) Cross-species microsatellite markers for elucidating population genetic structure in Arabidopsis and Arabis (Brassicaeae). Mol Ecol 11:591–601

    Article  PubMed  CAS  Google Scholar 

  • Dubois S, Cheptou PO, Petit C, Meerts P, Poncelet M, Vekemans X, Lefèbvre C, Escarré J (2003) Genetic structure and mating systems of metallicolous and nonmetallicolous populations of Thlaspi caerulescens. New Phytol 157:633–641

    Article  Google Scholar 

  • Durka W, Bossdorf O, Gautschi B (2004) Isolation and characterization of microsatellite loci in the invasive Alliaria petiolata (Brassicaceae). Mol Ecol Notes 4:173–175

    Article  CAS  Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler IV ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    Article  PubMed  CAS  Google Scholar 

  • Frerot H, Petit C, Lefebvre C, Gruber W, Collin C, Escarré J (2003) Zinc and cadmium accumulation in controlled crosses between metallicolous and nonmetallicolous populations of Thlaspi caerulescens (Brassicaceae). New Phytol 157:643–648

    Article  CAS  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html

  • Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461–485

    Article  PubMed  CAS  Google Scholar 

  • Koch M, Mummenhoff K, Hurka H (1998) Systematics and evolutionary history of heavy metal tolerant Thlaspi caerulescens in Western Europe: evidence from genetic studies based on isozyme analysis. Biochem Syst Ecol 26:823–838

    Article  CAS  Google Scholar 

  • Koch M, Haubold B, Mitchell-Olds T (2001) Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences. Am J Bot 88:534–544

    Article  PubMed  CAS  Google Scholar 

  • Kuittinen H, Aguadé M, Charlesworth D, Haan ADE, Lauga B, Mitchell-Olds T, Oikarinen S, Ramos-Onsins S, Stranger B, Van Tienderen P, Savolainen O (2002) Primers for 22 candidate genes for ecological adaptations in Brassicaceae. Mol Ecol Notes 2:258–262

    Article  CAS  Google Scholar 

  • Lakshmi PK, Arumugam N, Gupta V, Mukhopadhyay A, Sodhi YS, Pental D, Pradhan AK (2005) Mapping and tagging of seed coat colour and the identification of microsatellite markers for marker-assisted manipulation of the trait in Brassica juncea. Theor Appl Genet 111:8–14

    Article  CAS  Google Scholar 

  • Lasat MM, Pence NS, Garvin DF, Ebbs SD, Kochian LV (2000) Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J Exp Bot 51:71–79

    Article  PubMed  CAS  Google Scholar 

  • Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol 145:11–20

    Article  CAS  Google Scholar 

  • Lombi E, Tearall KL, Howarth JR, Zhao FJ, Hawkesford MJ, McGrath SP (2002) Influence of iron status on cadmium and zinc uptake by different ecotypes of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 128:1359–1367

    Article  PubMed  CAS  Google Scholar 

  • Lowe AJ, Jones AE, Raybould AF, Trick M, Moule CL, Edwards KJ (2002) Transferability and genome specificity of a new set of microsatellite primers among Brassica species of the U triangle. Mol Ecol Notes 2:7–11

    Article  CAS  Google Scholar 

  • Lowe AJ, Moule C, Trick M, Edwards KJ (2004) Efficient large-scale development of microsatellites for marker and mapping applications in Brassica crop species. Theor Appl Genet 108:1103–1112

    Article  PubMed  CAS  Google Scholar 

  • Lugon-Moulin N, Zhang M, Gadani F, Rossi L, Koller D, Krauss M, Wagner GJ (2004) Critical review of the science and options for reducing cadmium in tobacco (Nicotiana tabacum L.) and other plants. Adv Agron 83:111–180

    Article  CAS  Google Scholar 

  • Mäser P, Thomine S, Schroder JI, Waed JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667

    Article  PubMed  Google Scholar 

  • Peer WA, Mamoudian M, Lahner B, Reeves RD, Murphy AS, Salt DE (2003) Identifying model metal hyperaccumulating plants: germplasm analysis of 20 Brassicaceae accessions from a wide geographical area. New Phytol 159:421–430

    Article  CAS  Google Scholar 

  • Pence NS, Larsen PB, Ebbs SD, Letham DL, Lasat MM, Garvin DF, Eide D, Kochian LV (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci USA 98:9995–10000

    Google Scholar 

  • Plieske J, Struss D (2001) Microsatellite markers for genome analysis in Brassica. I. development in Brassica napus and abundance in Brassicaceae species. Theor Appl Genet 102:689–694

    Article  CAS  Google Scholar 

  • Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566

    Article  CAS  Google Scholar 

  • Roosens N, Leplae R, Bernard C, Verbruggen N (2005) Variations in plant metallothioneins: the heavy metal hyperaccumulator Thlaspi caerulescens as a case study. Planta 222:716–729

    Article  PubMed  CAS  Google Scholar 

  • Roosens N, Verbruggen N, Meerts P, Ximénez-Embún P, Smith JAC (2003) Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe. Plant Cell Environ 26:1657–1672

    Article  CAS  Google Scholar 

  • Suzuki N, Koizumi N, Sano H (2001) Screening of cadmium-responsive genes in Arabidopsis thaliana. Plant Cell Environ 24:1177–1188

    Article  CAS  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Van Oosterhout C, Weetman D, Hutchinson WF (2006) Estimation and adjustment of microsatellite null alleles in nonequilibrium populations. Mol Ecol Notes 6:255–256

    Article  Google Scholar 

  • Yang YW, Lai KN, Tai PY, Ma DP, Li WH (1999) Molecular phylogenetic studies of Brassica, Rorippa, Arabidopsis and allied genera based on the internal transcribed spacer region of 18S–25S rDNA. Mol Phylogenet Evol 13:455–462

    Article  PubMed  CAS  Google Scholar 

  • Zha HG, Jiang RF, Zhao FJ, Vooijs R, Schat H, Barker JHA, McGrath SP (2004) Co-segregation analysis of cadmium and zinc accumulation in Thlaspi caerulescens interecotypic crosses. New Phytol 163:299–312

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank N. Salamin and L. Bovet for methodological advices, D. Savova-Bianchi and C. Parisod for technical helps and C. Keller for providing plant material from Ganges and Prayon.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolution, Biophore, University of Lausanne, 1015, Lausanne, Switzerland

    N. Basic & G. Besnard

Authors
  1. N. Basic
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Besnard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. Besnard.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Basic, N., Besnard, G. Gene polymorphisms for elucidating the genetic structure of the heavy-metal hyperaccumulating trait in Thlaspi caerulescens and their cross-genera amplification in Brassicaceae. J Plant Res 119, 479–487 (2006). https://doi.org/10.1007/s10265-006-0011-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-006-0011-x

Keywords

Search

Navigation