Advertisement

Plant and Soil

, Volume 306, Issue 1–2, pp 105–116 | Cite as

The use of comparative genome analysis and syntenic relationships allows extrapolating the position of Zn tolerance QTL regions from Arabidopsis halleri into Arabidopsis thaliana

  • Nancy H. C. J. Roosens
  • Glenda Willems
  • Cécile Godé
  • Adeline Courseaux
  • Pierre Saumitou-Laprade
Regular Article

Abstract

Arabidopsis halleri is a species that has undergone natural selection for zinc (Zn) tolerance. Isolation of the quantitative trait loci (QTL) associated with this trait holds great promise for the identification of the main genes responsible for this adaptation. Using a segregating progeny produced by an interspecific cross, we previously constructed a genetic linkage map of A. halleri × A. lyrata petraea and mapped the three main QTL that confer Zn tolerance in A. halleri (Willems et al.). The goal of the present study is to compare the genetic linkage map of A. halleri × A. l. petraea to the annotated A. thaliana genome sequence to generate a tool for A. halleri genomic approaches. To achieve this aim, we constructed a genetic linkage map with 81 markers anchored on A. thaliana, including 23 genes known to be involved in metal homeostasis. First, this provided an extensive overview of the chromosomal rearrangements that have occurred since the divergence between A. thaliana and its closest relative A. halleri. Second, on the basis of the syntenic relationships assessed experimentally through this work, we transferred the QTL confidence intervals for Zn tolerance to the A. thaliana physical map, allowing access to all the genes localized in the corresponding regions. Third, we validated from the 23 genes involved in metal homeostasis the three ones localized in the QTL regions that can be considered the best candidates for conferring Zn tolerance.

Keywords

Arabidopsis halleri Zinc tolerance QTL mapping Synteny 

Notes

Acknowledgement

The authors thank Aude Bodin for technical support in the genetic mapping. This work was supported by funding from the Contrat de Plan Etat/Région Nord-Pas de Calais (PRC), from the European FEDER (contract no. 79/1769), from the BRG (contract no. 92), and from the INSU–CNRS program ACI ECCO (contract no. 04 2 9 FNS). G. Willems was funded by the European Research Training Network “Metalhome” (HPRN-CT-2002-00243), and N. Roosens by the Marie Curie intra-European Fellowship “Metolevol” (contract no. 024683 MEIF-CT-2005-0224683).

References

  1. Assuncao AGL, Schat H, Aarts MGM (2003) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:351–360CrossRefGoogle Scholar
  2. Basic N, Besnard G (2006) 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 119:479–487PubMedCrossRefGoogle Scholar
  3. Becher M, Talke IN, Krall L, Krämer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268PubMedGoogle Scholar
  4. Bechsgaard JS, Castric V, Charlesworth D, Vekemans X, Schierup MH (2006) The transition to self-compatibility in Arabidopsis thaliana and evolution within S-haplotypes over 10 Myr. Mol Biol Evol 23:1741–1750PubMedCrossRefGoogle Scholar
  5. 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 and Capsella rubella genomes. Plant Physiol 135:735–744PubMedCrossRefGoogle Scholar
  6. Clemens S, Palmgrem MG, Kramer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315PubMedCrossRefGoogle Scholar
  7. Chiang HC, Lo JC, Yeh KC (2006) Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ Sci Technol 40:6792–6798PubMedCrossRefGoogle Scholar
  8. Clauss MJ, Koch MA (2006) Poorly known relatives of Arabidopsis thaliana. Trends Plant Sci 11:449–459PubMedCrossRefGoogle Scholar
  9. Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal. Plant Physiol 14:1052–1065CrossRefGoogle Scholar
  10. Dräger DB, Desbrosses-Fonrouge AG, Krach C, Chardonnens AN, Meyer RC, Saumitou-Laprade P, Krämer U (2004) Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J 39:425–439PubMedCrossRefGoogle Scholar
  11. Filatov V, Dowdle J, Smirnoff N, Ford-Lloyd B, Newbury HJ, Macnair M (2006) Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation. Mol Ecol 15:3045–3059PubMedCrossRefGoogle Scholar
  12. Grotz N, Fox T, Connolly E, Park W, Guerinot ML, Eide D (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency PNAS 95:7220–7224Google Scholar
  13. Hansson B, Kawabe A, Preuss S, Kuittinen H, Charlesworth D (2006) Comparative gene mapping in Arabidopsis lyrata chromosomes 1 and 2 and the corresponding A. thaliana chromosome 1: recombination rates, rearrangements and centromere location. Genet Res 87:75–85PubMedCrossRefGoogle Scholar
  14. Koch MA, Kiefer M (2005) Genome evolution among cruciferous plants: a lecture from the comparison of the genetic maps of three diploid species Capsella rubella, Arabidopsis lyrata subsp. petraea, and A. thaliana. Am J Bot 92:761–767CrossRefGoogle Scholar
  15. Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175Google Scholar
  16. Kuittinen H, de Haan AA, Vogl C, Oikarinen S, Leppala J, Koch M, Mitchell-Olds T, Langley CH, Savolainen O (2004) Comparing the linkage maps of the close relatives Arabidopsis lyrata and A. thaliana. Genetics 168:1575–1584PubMedCrossRefGoogle Scholar
  17. Macnair MR, Bert V, Huitson SB, Saumitou-Laprade P, Petit D (1999) Zinc tolerance and hyperaccumulation are genetically independent characters. Proc R Soc Lond B Biol Sci 266:2175CrossRefGoogle Scholar
  18. Oetting WS, Lee HK, Flanders DJ, Wiesner GL,. Sellers TA et al (1995) Linkage analysis with multiplexed short tandem repeat polymorphism using infrared fluorescence and M13 tailed primers. Genomics 30:450–458PubMedCrossRefGoogle Scholar
  19. Pauwels M, Frerot H, Bonnin I, Saumitou-Laprade P (2006) A broad-scale analysis of population differentiation for Zn tolerance in an emerging model species for tolerance study: Arabidopsis halleri (Brassicaceae). J Evol Biol 19:1838–1850PubMedCrossRefGoogle Scholar
  20. 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 159:421–430CrossRefGoogle Scholar
  21. Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int J Phytoremediat 3:145–172CrossRefGoogle Scholar
  22. Saumitou-Laprade P, Rouwendal GJA, Cuguen J, Krens FA, Michaelis G (1993) Different CMS sources found in Beta vulgaris ssp. maritima: mitochondrial variability in wild populations revealed by a rapid screening procedure. Theor Appl Genet 85:529–535CrossRefGoogle Scholar
  23. Saumitou-Laprade P, Piquot Y, Raspé O, Bernard J, Vrieling K (1999) Plant DNA fingerprinting and profiling. In: JT Epplen, T Lubjuhn (eds) DNA profiling and DNA fingerprinting. Birkhauser, Basel, pp 17–38Google Scholar
  24. Van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, Verkleij JAC (1999) Overexpression of a novel Arabidopsis gene related to putative zinc transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol 119:1047–1055PubMedCrossRefGoogle Scholar
  25. Van Ooijen JW, Voorrips RE (2001) Joinmap 3.0, Software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The NetherlandsGoogle Scholar
  26. Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL 4.0, Software for the calculation of QTL positions on genetic maps. Plant Research International, Wageningen, The NetherlandsGoogle Scholar
  27. Voorrips RE (2002) Mapchart: Software for the graphical presentation of linkage maps and QTLs. Heredity 93:77–78CrossRefGoogle Scholar
  28. Weber M, Harada E, Vess C, von Roepenack-Lahaye E, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281PubMedCrossRefGoogle Scholar
  29. Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+–hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29:950–963PubMedCrossRefGoogle Scholar
  30. Willems G, Drager DB, Courbot M, Gode C, Verbruggen N, Saumitou-Laprade P (2007) The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): an analysis of quantitative trait loci. Genetics 176:659–674PubMedCrossRefGoogle Scholar
  31. Yogeeswaran K, Frary A, York TL, Amenta A, Lesser AH et al (2005) Comparative genome analyses of Arabidopsis spp.: inferring chromosomal rearrangement events in the evolutionary history of A. thaliana. Genome Res 15:505–515PubMedCrossRefGoogle Scholar
  32. Zhou J, Goldsbrough PB (1994) Functional homologs of fungal metallothionein genes from Arabidopsis. Plant Cell 6:875–884PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Nancy H. C. J. Roosens
    • 1
  • Glenda Willems
    • 1
  • Cécile Godé
    • 1
  • Adeline Courseaux
    • 1
  • Pierre Saumitou-Laprade
    • 1
  1. 1.Laboratoire de Génétique et Evolution des Populations Végétales, UMR CNRS 8016Université des Sciences et Technologies de LilleVilleneuve d’Ascq CedexFrance

Personalised recommendations