Variability of zinc tolerance among and within populations of the pseudometallophyte species Arabidopsis halleri and possible role of directional selection

New Phytologist

Volumn 185, Issue 1, 2010, Pages 130-142

  Meyer, Claire Lise ^a   Kostecka, Alicja A ^b   Saumitou Laprade, Pierre ^a   Créach, Anne ^a   Castric, Vincent ^a   Pauwels, Maxime ^a   Frérot, Hélène ^a  

^a CNRS   (France)

^b POLISH ACADEMY OF SCIENCES   (Poland)

Author keywords

Arabidopsis halleri; Divergent selection; FST QST; Local adaptation; Quantitative trait; Zinc tolerance

Indexed keywords

MICROSATELLITE DNA; ZINC;

DICOTYLEDON; DIVERGENCE; GENETIC DIFFERENTIATION; GENETIC MARKER; HYDROPONICS; LOCAL ADAPTATION; MORPHOLOGY; PHENOTYPIC PLASTICITY; POLLUTION TOLERANCE; POLYMORPHISM; SELECTION; ZINC;

ADAPTATION; ARABIDOPSIS; ARTICLE; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; METABOLISM; PHENOTYPE; PHOTOSYNTHESIS; PHOTOSYSTEM II; PLANT; PLANT ROOT;

ADAPTATION, BIOLOGICAL; ARABIDOPSIS; MICROSATELLITE REPEATS; PHENOTYPE; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT ROOTS; PLANT SHOOTS; POLYMORPHISM, GENETIC; SELECTION, GENETIC; ZINC;

ARABIDOPSIS; ARABIDOPSIS HALLERI;

EID: 71249141133     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2009.03062.x     Document Type: Article

References (56)

1. Al-Hiyaly SA, McNeilly T, Bradshaw AD. 1988. The effect of zinc contamination from electricity pylons - evolution in a replicated situation. New Phytologist 110 : 571 580.
2. Al-Shehbaz IA, O'Kane SLJ. 2002. Taxonomy and phylogeny of Arabidopsis (Brassicaceae). In : Somerville CR, Meyerowitz EM, eds. The Arabidopsis book. Rockville, MD, USA : American Society of Plant Biologists. doi :, http://www.aspb.org/publications/arabidopsis/
3. Antonovics J, Bradshaw AD, Turner RG. 1971. Heavy metal tolerance in plants. Advances in Ecological Research 7 : 1 85.
4. Arendt J, Reznick D. 2007. Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Science 23 : 26 32.
5. Assunção AGL, Da Costa Martins P, De Folter S, Vooijs R, Schat H, Aarts MGM. 2001. Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant, Cell & Environment 24 : 217 226.
6. Assunção AGL, Ten Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO. 2003. Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytologist 159 : 411 419.
7. Barrett RDH, Schluter D. 2007. Adaptation from standing variation. Trends in Ecology and Evolution 23 : 38 44.
8. Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M. 2001. Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis growth. Planta 212 : 696 709.
9. Bert V, Macnair MR, De Laguerie P, Saumitou-Lapdrade P, Petit D. 2000. Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri. New Phytologist 146 : 225 233.
10. Bert V, Bonin I, Saumitou-Laprade P, de Laguerie P, Petit D. 2002. Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytologist 155 : 47 57.
11. Bradshaw AD. 1952. Populations of Agrostis tenuis resistant to lead and zinc poisoning. Nature 169 : 1098.
12. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A. 2007. Zinc in plants. New Phytologist 173 : 677 702.
13. Cho M, Chardonnens AN, Dietz K-J. 2003. Differential heavy metal tolerance of Arabidopsis halleri and Arabidopsis thaliana: a leaf slice test. New Phytologist 158 : 287 293.
14. 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 ATPases. Plant Physiology 144 : 1052 1065.
15. Dechamps C, Lefèbvre C, Noret N, Meerts P. 2006. Reaction norms of life history traits in response to zinc in Thlaspi caerulescens from metalliferous and nonmetalliferous sites. New Phytologist 173 : 191 198.
16. Galardi F, Corrales I, Mengoni A, Pucci S, Barletti L, Barzanti R, Arnetoli M, Gabbrielli R, Gonnelli C. 2007. Intra-specific differences in nickel tolerance and accumulation in the Ni-hyperaccumulator Alyssum bertolonii. Environmental and Experimental Botany 60 : 377 384.
17. Genty B, Briantais JM, Baker NR. 1989. The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990 : 87 92.
18. Goudet J. 1995. Fstat version 1.2: a computer program to calculate F statistics. Journal of Heredity 86 : 485 486.
19. Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP. 2006. A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313 : 101 104.
20. Humphreys MO, Nicholls MK. 1984. Relationships between tolerance to heavy metals in Agrostis capillaris L. (A. tenuis Sibth.). New Phytologist 98 : 177 190.
21. Jiménez-Ambriz G, Petit C, Bourrié I, Dubois S, Olivieri S, Ronce O. 2006. Life history variation in the heavy metal tolerant plant Thlaspi caerulescens growing in a network of contaminated and noncontaminated sites in southern France: role of gene flow, selection and phenotypic plasticity. New Phytologist 173 : 199 215.
22. Koch M, Mummenhoff K, Hurka H. 1998. Systematics and evolution history of heavy metal tolerant Thlaspi caerulescens in Western Europe: evidence from genetic studies based on isozyme analysis. Biochemical Systematics and Ecology 26 : 823 838.
23. Küpper H, Lombi E, Zhao F-J, McGrath SP. 2000. Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212 : 75 84.
24. Küpper H, Parameswaran A, Leitenmaier B, Trtílek M, Šetlík I. 2007. Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytologist 175 : 655 674.
25. Llaurens V, Castric V, Austerlitz F, Vekemans X. 2008. High paternal diversity in the self-incompatible herb Arabidopsis halleri despite clonal reproduction and spatially restricted pollen dispersal. Molecular Ecology 17 : 1577 1588.
26. Macnair MR. 1983. The genetic control of copper tolerance in the yellow monkey flower, Mimulus guttatus. Heredity 50 : 283 293.
27. Macnair MR, Baker JM. 1994. Metal-tolerant plant: an evolutionary perspective. In : Farago ME ed. Plants and the chemical elements, biochemistry, uptake, tolerance and toxicity. New York, NY, USA : VCH, 68 83.
28. Macnair MR, Bert V, Huitson SB, Saumitou-Laprade P, Petit D. 1999. Zinc tolerance and hyperaccumulation are genetically independent characters. Proceedings of the Royal Society of London 266 : 2175 2179.
29. Macnair MR, Tilstone GH, Smith SE. 2000. The genetics of metal tolerance and accumulation in higher plants. In : Terry N, Banuelos G, Vangronsveld J, eds. Phytoremediation of contaminated soil and water. Boca Raton, FL, USA : CRC Press, 235 250.
30. Meerts P, Van Isaker I. 1997. Heavy metal tolerance and hyperaccumulation in metallicolous and nonmetallicolous populations of Thlaspi caerulescens from continental Europe. Plant Ecology 133 : 221 231.
31. Mengoni A, Barabesi C, Gonelli C, Galardi F, Gabbrielli R, Bazzicalupo M. 2001. Genetic diversity of heavy metal-tolerant populations in Silene paradoxa L. (Caryophyllaceae): a chloroplast microsatellite analysis. Molecular Ecology 10 : 1909 1916.
32. Meyer CL, Vitalis R, Saumitou-Laprade P, Castric V. 2009. Genomic pattern of adaptive divergence in Arabidopsis halleri, a model species for tolerance to heavy metal. Molecular Ecology 18 : 2050 2062.
33. van de Mortel JE, Villanueva LA, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, Ver Loren van Themaat E, Koornneef M, Aarts MGM. 2006. Large expression differences in genes for iron and Zinc homeostasis, stress response, zand lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiology 142 : 1127 1147.
34. Mundry R, Sommer C. 2007. Discriminant function analysis with nonindependent data: consequence and an alternative. Animal Behaviour 74 : 965 976.
35. Nielsen R. 2005. Molecular signatures of natural selection. Annual Review of Genetics 39 : 197 218.
36. O'Kane SL, Al-Shehbaz IA. 2003. Phylogenetic position and generic limits of Arabidopsis (Brassicaceae) based on sequences of nuclear ribosomal DNA. Annals of the Missouri Botanical Garden 90 : 603 612.
37. Pauwels M, Saumitou-Laprade P, Holl C, Petit D, Bonin I. 2005. Multiple origins of metallicolous populations of the pseudometallophyte Arabidopsis halleri (Brassicaceae) in central Europe: the cpDNA testimony. Molecular Ecology 14 : 4403 4414.
38. Pauwels M, Frérot H, Bonin 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). Journal of Evolutionary Biology 19 : 1838 1850.
39. Reznick DN, Ghalambor CK. 2001. The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112-113 : 183 198.
40. Roosens NCJ, Willems G, Saumitou-Laprade P. 2008a. Using Arabidopsis to explore zinc tolerance and hyperaccumulation. Trends in Plant Science 13 : 208 215.
41. Roosens NCJ, Willems G, Godé C, Courseaux A, Saumitou-Laprade P. 2008b. The use of comparative genome analysis and syntenic relationships allows extrapolating the position of Zn tolerance QTL regions from Arabidopsis halleri into Arabidopsis thaliana. Plant and Soil 306 : 105 116.
42. Schat H, Ten Bookum WM. 1992. Genetic control of copper tolerance in Silene vulgaris. Heredity 68 : 219 229.
43. Schat H, Vooijs R. 1997. Multiple tolerance and co-tolerance to heavy metals in Silene vulgaris: a co-segregation analysis. New Phytologist 136 : 489 496.
44. Schat H, Kuiper E, Ten Bookum WM, Vooijs R. 1993. A general model for the genetic control of copper tolerance in Silene vulgaris: evidence from crosses between plants from different tolerant populations. Heredity 70 : 142 147.
45. Schat H, Vooijs R, Kuiper E. 1996. Identical major gene loci for heavy metal tolerances that have independently evolved in different local populations and subspecies of Silene vulgaris. Evolution 50 : 1888 1895.
46. Siegel S, Castellan NJ. 1988. Non parametric statistics for the behavioural sciences. New York, NY, USA : MacGraw-Hill.
47. Smith SE, Macnair MR. 1998. Hypostatic modifiers cause variation in degree of copper tolerance in Mimulus guttatus. Heredity 80 : 760 768.
48. Van Rossum F, Bonnin I, Fénart S, Pauwels M, Petit D, Saumitou-Laprade P. 2004. Spatial genetic structure within a metallicolous population of Arabidopsis halleri, a clonal, self-incompatible, and heavy metal tolerant species. Molecular Ecology 13 : 2959 2967.
49. Vekemans X, Lefèbvre C. 1997. On the evolution of heavy-metal tolerant populations in Armeria maritima: evidence from allozyme variation and reproductive barriers. Journal of Evolutionary Biology 10 : 175 191.
50. Von Frenckell-Insam BAK, Hutchinson TC. 1993. Occurrence of heavy metal tolerance and co-tolerance in Deschampsia cespitosa (L.) Beauv. From European and Canadian populations. New Phytologist 125 : 555 564.
51. Waldmann P, Garcia-Gil MR, Sillanpaa MJ. 2005. Comparing Bayesian estimates of genetic differentiation of molecular markers and quantitative traits: an application to Pinus sylvestris. Heredity 94 : 623 629.
52. Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38 : 1358 1370.
53. ST. Molecular Ecology 17 : 1885 1896.
54. Wilkins DA. 1978. The measurement of tolerance to edaphic factors by means of root growth. New Phytologist 80 : 623 633.
55. Willems G, Dräger DB, Courbot M, Godé 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 : 659 674.
56. Wu L, Bradshaw AD, Thurman DA. 1975. The potential for evolution of heavy metal tolerance in plants. III. The rapid evolution of copper tolerance in Agrostis stolonifera. Heredity 34 : 165 187.