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PMID: 17409091 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): an analysis of quantitative trait loci.

Genetics ·Vol. 176 ·No. 1 ·2007-05-00 ·Pages 659-74

Willems G, Dräger DB, Courbot M, Godé C, Verbruggen N, Saumitou-Laprade P

Abstract

The species Arabidopsis halleri, an emerging model for the study of heavy metal tolerance and accumulation in plants, has evolved a high level of constitutive zinc tolerance. Mapping of quantitative trait loci (QTL) was used to investigate the genetic architecture of zinc tolerance in this species. A first-generation backcross progeny of A. halleri ssp. halleri from a highly contaminated industrial site and its nontolerant relative A. lyrata ssp. petraea was produced and used for QTL mapping of zinc tolerance. A genetic map covering most of the A. halleri genome was constructed using 85 markers. Among these markers, 65 were anchored in A. thaliana and revealed high synteny with other Arabidopsis genomes. Three QTL of comparable magnitude on three different linkage groups were identified. At all QTL positions zinc tolerance was enhanced by A. halleri alleles, indicating directional selection for higher zinc tolerance in this species. The two-LOD support intervals associated with these QTL cover 24, 4, and 13 cM. The importance of each of these three regions is emphasized by their colocalization with HMA4, MTP1-A, and MTP1-B, respectively, three genes well known to be involved in metal homeostasis and tolerance in plants.

MeSH Terms
Adaptation, Physiological/drug effects,genetics Arabidopsis/classification,drug effects,genetics Chromosome Mapping Chromosome Segregation/genetics Clone Cells Epistasis, Genetic Genetic Markers Lod Score Quantitative Trait Loci/genetics Zinc/pharmacology
Chemicals
Genetic Markers Zinc
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Willems Glenda
Laboratoire de Génétique et Evolution des Populations Végétales, UMR CNRS 8016, FR CNRS 1818, Université des Sciences et Technologies de Lille-Lille1, F-59655 Villeneuve d'Ascq Cedex, France.
Dräger Dörthe B
Courbot Mikael
Godé Cécile
Verbruggen Nathalie
Saumitou-Laprade Pierre
References (54)
54 references, click to expand
  1. Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation.
    Plant Physiol. 1999 Mar;119(3):1047-55 PMID: 10069843
  2. Zinc tolerance and hyperaccumulation are genetically independent characters.
    Proc Biol Sci. 1999 Nov 7;266(1434):2175-9 PMID: 10649632
  3. The evolutionary genetics of adaptation: a simulation study.
    Genet Res. 1999 Dec;74(3):207-14 PMID: 10689798
  4. Genetic and molecular dissection of naturally occurring variation.
    Curr Opin Plant Biol. 2001 Apr;4(2):130-5 PMID: 11228435
  5. Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences.
    Am J Bot. 2001 Mar;88(3):534-44 PMID: 11250830
  6. Mapping quantitative trait loci in plants: uses and caveats for evolutionary biology.
    Nat Rev Genet. 2001 May;2(5):370-81 PMID: 11331903
  7. Finding the molecular basis of quantitative traits: successes and pitfalls.
    Nat Rev Genet. 2001 Jun;2(6):437-45 PMID: 11389460
  8. Molecular mechanisms of plant metal tolerance and homeostasis.
    Planta. 2001 Mar;212(4):475-86 PMID: 11525504
  9. The genetic architecture of quantitative traits.
    Annu Rev Genet. 2001;35:303-39 PMID: 11700286
  10. Cellular mechanisms for heavy metal detoxification and tolerance.
    J Exp Bot. 2002 Jan;53(366):1-11 PMID: 11741035
  11. A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions.
    Genetics. 2001 Dec;159(4):1701-16 PMID: 11779808
  12. Understanding quantitative genetic variation.
    Nat Rev Genet. 2002 Jan;3(1):11-21 PMID: 11823787
  13. Mapping and analysis of quantitative trait loci in experimental populations.
    Nat Rev Genet. 2002 Jan;3(1):43-52 PMID: 11823790
  14. Quantitative trait loci for inflorescence development in Arabidopsis thaliana.
    Genetics. 2002 Mar;160(3):1133-51 PMID: 11901129
  15. Cross-species microsatellite markers for elucidating population genetic structure in Arabidopsis and Arabis (Brassicaeae).
    Mol Ecol. 2002 Mar;11(3):591-601 PMID: 11918792
  16. MapChart: software for the graphical presentation of linkage maps and QTLs.
    J Hered. 2002 Jan-Feb;93(1):77-8 PMID: 12011185
  17. The population genetics of adaptation: the adaptation of DNA sequences.
    Evolution. 2002 Jul;56(7):1317-30 PMID: 12206234
  18. Finding genes that underlie complex traits.
    Science. 2002 Dec 20;298(5602):2345-9 PMID: 12493905
  19. QTL architecture of resistance and tolerance traits in Arabidopsis thaliana in natural environments.
    Mol Ecol. 2003 May;12(5):1153-63 PMID: 12694279
  20. Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass.
    Plant J. 2003 Jul;35(2):164-76 PMID: 12848823
  21. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri.
    Plant J. 2004 Jan;37(2):251-68 PMID: 14690509
  22. 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. 2004 Jan;37(2):269-81 PMID: 14690510
  23. Theoretical basis of the Beavis effect.
    Genetics. 2003 Dec;165(4):2259-68 PMID: 14704201
  24. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis.
    Plant Cell. 2004 May;16(5):1327-39 PMID: 15100400
  25. The Arabidopsis genome sequence as a tool for genome analysis in Brassicaceae. A comparison of the Arabidopsis and Capsella rubella genomes.
    Plant Physiol. 2004 Jun;135(2):735-44 PMID: 15208421
  26. A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens.
    FEBS Lett. 2004 Jul 2;569(1-3):140-8 PMID: 15225623
  27. Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels.
    Plant J. 2004 Aug;39(3):425-39 PMID: 15255871
  28. Quantitative trait locus analyses and the study of evolutionary process.
    Mol Ecol. 2004 Sep;13(9):2505-22 PMID: 15315666
  29. Spatial genetic structure within a metallicolous population of Arabidopsis halleri, a clonal, self-incompatible and heavy-metal-tolerant species.
    Mol Ecol. 2004 Oct;13(10):2959-67 PMID: 15367112
  30. Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase.
    Plant Physiol. 2004 Nov;136(3):3814-23 PMID: 15516513
  31. Comparing the linkage maps of the close relatives Arabidopsis lyrata and A. thaliana.
    Genetics. 2004 Nov;168(3):1575-84 PMID: 15579708
  32. Evolution of genome size in Brassicaceae.
    Ann Bot. 2005 Jan;95(1):229-35 PMID: 15596470
  33. The genetic theory of adaptation: a brief history.
    Nat Rev Genet. 2005 Feb;6(2):119-27 PMID: 15716908
  34. Comparative genome analyses of Arabidopsis spp.: inferring chromosomal rearrangement events in the evolutionary history of A. thaliana.
    Genome Res. 2005 Apr;15(4):505-15 PMID: 15805492
  35. MTP1 mops up excess zinc in Arabidopsis cells.
    Trends Plant Sci. 2005 Jul;10(7):313-5 PMID: 15946891
  36. Multiple origin of metallicolous populations of the pseudometallophyte Arabidopsis halleri (Brassicaceae) in central Europe: the cpDNA testimony.
    Mol Ecol. 2005 Dec;14(14):4403-14 PMID: 16313601
  37. Poorly known relatives of Arabidopsis thaliana.
    Trends Plant Sci. 2006 Sep;11(9):449-59 PMID: 16893672
  38. Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation.
    Mol Ecol. 2006 Sep;15(10):3045-59 PMID: 16911220
  39. Comparative cDNA-AFLP analysis of Cd-tolerant and -sensitive genotypes derived from crosses between the Cd hyperaccumulator Arabidopsis halleri and Arabidopsis lyrata ssp. petraea.
    J Exp Bot. 2006;57(12):2967-83 PMID: 16916885
  40. A broad-scale analysis of population differentiation for Zn tolerance in an emerging model species for tolerance study: Arabidopsis halleri (Brassicaceae).
    J Evol Biol. 2006 Nov;19(6):1838-50 PMID: 17040381
  41. 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. 2005 Apr;92(4):761-7 PMID: 21652456
  42. THE POPULATION GENETICS OF ADAPTATION: THE DISTRIBUTION OF FACTORS FIXED DURING ADAPTIVE EVOLUTION.
    Evolution. 1998 Aug;52(4):935-949 PMID: 28565213
  43. AFLP: a new technique for DNA fingerprinting.
    Nucleic Acids Res. 1995 Nov 11;23(21):4407-14 PMID: 7501463
  44. Structure, organization and expression of the metallothionein gene family in Arabidopsis.
    Mol Gen Genet. 1995 Aug 21;248(3):318-28 PMID: 7565594
  45. Mapping polygenes.
    Annu Rev Genet. 1993;27:205-33 PMID: 8122902
  46. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis.
    Genomics. 1994 Jan 1;19(1):137-44 PMID: 8188214
  47. Comparative recombination distances among Zea mays L. inbreds, wide crosses and interspecific hybrids.
    Genetics. 1995 Dec;141(4):1573-81 PMID: 8601495
  48. Linkage analysis with multiplexed short tandem repeat polymorphisms using infrared fluorescence and M13 tailed primers.
    Genomics. 1995 Dec 10;30(3):450-8 PMID: 8825630
  49. The evolution of apical dominance in maize.
    Nature. 1997 Apr 3;386(6624):485-8 PMID: 9087405
  50. An interspecific backcross of Lycopersicon esculentum x L. hirsutum: linkage analysis and a QTL study of sexual compatibility factors and floral traits.
    Genetics. 1997 Oct;147(2):861-77 PMID: 9335620
  51. QTL analysis in plants; where are we now?
    Heredity (Edinb). 1998 Feb;80 ( Pt 2):137-42 PMID: 9503632
  52. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus).
    Genetics. 1998 May;149(1):367-82 PMID: 9584110
  53. Analysis of natural allelic variation at flowering time loci in the Landsberg erecta and Cape Verde Islands ecotypes of Arabidopsis thaliana.
    Genetics. 1998 Jun;149(2):749-64 PMID: 9611189
  54. Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data.
    Genetics. 1998 Aug;149(4):2099-104 PMID: 9691061
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
DOI
10.1534/genetics.106.064485
Published
2007-05-00
Epub
2007-00-03
Pages
659-74
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1893047
Subset
IM
External Links
PubMed source DOI: 10.1534/genetics.106.064485 PMC Full Text View journal details
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