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AFLP analysis of the pseudometallophyte Cistus ladanifer: comparison with cpSSRs and exploratory genome scan to investigate loci associated to soil variables

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Abstract

Aims

To assess the genetic patterns of colonisation of metalliferous areas by the pseudometallophyte Cistus ladanifer with AFLP genome scan, to compare those estimates with previous cpSSR results, and to identify loci potentially linked to tolerance to metalliferous soils.

Methods

Thirty-three populations were screened with AFLP markers. Statistical analyses included estimation of genetic diversity, hierarchical analysis of molecular variation and Bayesian analysis of geographical partitioning of genetic diversity. Mantel tests and Spearman’s correlation index were used to compare results obtained with AFLP and cpSSR. Generalized Estimating Equations (GEE) models were applied to correlate allele frequency distribution and soil variables (pH, Ca:Mg ratio and total contents of different trace metals).

Results

Metallicolous and non-metallicolous populations of C. ladanifer showed neither different levels of genetic diversity, nor genetic differentiation between population types. Incongruence in genetic diversity estimates between AFLP and cpSSR due to marker-specific properties was observed. Nonetheless, pairwise distance matrices computed with both markers were concordant. GEE analyses showed that the Mn total soil content has an important effect on the allele distribution in C. ladanifer. In contrast, the Ca:Mg ratio seems to have no selective effect. Moreover, we identified a particular band with a putative role in the species’ tolerance to high Mn concentrations in the soil.

Conclusions

The soil type had no influence over this species’ genetic structure. GEE showed their usefulness in revealing the association between soil variables and AFLP loci.

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References

  • Alados CL, Navarro T, Cabezudo B (1999) Tolerance assessment of Cistus ladanifer to serpentine soils by developmental stability analysis. Plant Ecol 143:51–66

    Article  Google Scholar 

  • Alvarenga PM, Araújo MF, Silva JAL (2004) Elemental uptake and root-leaves transfer in Cistus ladanifer L. growing in a contaminated pyrite mining area (Aljustrel-Portugal). Water Air Soil Poll 152:81–96

    Article  CAS  Google Scholar 

  • Ater M, Lefèbvre C, Gruber W, Meerts P (2000) A phytogeochemical survey of the flora of ultramafic and adjacent normal soils in North Morocco. Plant Soil 218:127–135

    Article  CAS  Google Scholar 

  • Bastida F, Talavera S (2002) Temporal and spatial patterns of seed dispersal in two Cistus species (Cistaceae). Ann Bot 89:427–434

    Article  PubMed  Google Scholar 

  • Baumbach H, Hellwig FH (2007) Genetic differentiation of metallicolous and non-metallicolous populations of Armeria maritima (Mill.) Willd. taxa (Plumbaginaceae) in Central Europe. Plant Syst Evol 269:245–258

    Article  Google Scholar 

  • Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273

    Article  PubMed  CAS  Google Scholar 

  • Bonin A, Ehrich D, Manel S (2007) Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionist. Mol Ecol 16:3737–3758

    Article  PubMed  CAS  Google Scholar 

  • Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol S 36:243–266

    Article  Google Scholar 

  • Bucci G, González-Martínez SC, Le Provost G, Plomion C, Ribeiro MM, Sebastiani F, Alía R, Vendramin GG (2007) Range-wide phylogeography and gene zones in Pinus pinaster Ait. revealed by chloroplast microsatellite markers. Mol Ecol 16:2137–2153

    Article  PubMed  CAS  Google Scholar 

  • Carl G, Kuhn I (2007) Analyzing spatial autocorrelation in species distribution using Gaussian and logit models. Ecol Model 207:159–170

    Article  Google Scholar 

  • Carlier J, Leitão J, Fonseca F (2008) Population genetic structure of Cistus ladanifer L. (Cistaceae) and genetic differentiation from co-occurring Cistus species. Plant Spec Biol 23:141–151

    Article  Google Scholar 

  • Comes HP, Kadereit JW (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3:432–438

    Article  Google Scholar 

  • Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843

    Article  PubMed  Google Scholar 

  • Corander J, Sirén J, Arjas E (2008) Bayesian spatial modelling of genetic population structure. Comput Stat 23:111–129

    Article  Google Scholar 

  • de la Fuente V, Rufo L, Rodríguez N, Amils R, Zuluaga J (2010) Metal accumulation screening of the Río Tinto flora (Huelva, Spain). Biol Trace Elem Res 134:318–341

    Article  PubMed  CAS  Google Scholar 

  • Demoly JP, Montserrat P (1993) Cistus L. In: Castroviejo S, Aedo C, Cirujano S, Laínz M, Montserrat P, Morales R, Muñoz Garmendia F, Navarro C, Paiva J, Soriano C (eds) Flora Iberica, vol III. Real Jardín Botánico. CSIC, Madrid, pp 319–337

    Google Scholar 

  • Deng D, Lan C, Shu W (2007) The effects of heavy metal pollution on genetic diversity in zinc/cadmium hyperaccumulator Sedum alfredii populations. Plant Soil 297:83–92

    Article  CAS  Google Scholar 

  • Díez-Lázaro J (2008) Fitocorrección de suelos contaminados con metales pesados: Evaluación de plantas tolerantes y optimización del proceso mediante prácticas agronómicas. Ph.D. Thesis. Universidade de Santiago de Compostela, Spain

  • Dumolin S, Demesure B, Petit RJ (1995) Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theor Appl Genet 91:1253–1256

    Article  CAS  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  • Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer Associated, Sunderland

    Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • Friedland AJ (1990) The movement of metals through soils and ecosystems. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC, Boca Raton, pp 7–19

    Google Scholar 

  • Grivet D, Petit RJ (2002) Phylogeography of the common ivy (Hedera sp.) in Europe: genetic differentiation through space and time. Mol Ecol 11:1351–1362

    Article  PubMed  CAS  Google Scholar 

  • Gustafson DJ, Romano G, Latham RE, Morton JK (2003) Amplified fragment length polymorphism analysis of genetic relationships among the serpentine barrens endemic Cerastium velutinum Rafinesque var. villosissimum Pennell (Caryophyllaceae) and closely related Cerastium species. J Torrey Bot Soc 130:218–230

    Article  Google Scholar 

  • Guzmán B, Vargas P (2009) Long-distance colonization of the Western Mediterranean by Cistus ladanifer (Cistaceae) despite the absence of special dispersal mechanisms. J Biogeogr 36:954–968

    Article  Google Scholar 

  • Holderegger R, Herrmann D, Poncet B, Gugerli F, Thuiller W, Taberlet P, Gielly L, Rioux D, Brodbeck S, Aubert S, Manel S (2008) Land ahead: using genome scans to identify molecular markers of adaptive relevance. Plant Ecol Divers 1:273–283

    Article  Google Scholar 

  • Jiménez-Ambriz G, Petit C, Bourrié I, Dubois S, Olivieri I, Ronce O (2007) 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 Phytol 173:199–215

    Article  PubMed  Google Scholar 

  • Kremer A, Kleinschmit J, Cottrell J, Cundall EP, Deans JD, Ducousso A, König AO, Lowe AJ, Munro RC, Petit RJ, Stephan BR (2002) Is there a correlation between chloroplastic and nuclear divergence, or what are the roles of history and selection on genetic diversity in European oaks? Forest Ecol Manag 156:75–87

    Article  Google Scholar 

  • Lefèbvre C, Vernet P (1990) Microevolutionary processes on contaminated deposits. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC, Boca Raton, pp 285–299

    Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology, 2nd English ed. Elsevier, Amsterdam

    Google Scholar 

  • Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277

    Article  Google Scholar 

  • Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure of plant populations. Annu Rev Ecol Syst 15:65–95

    Article  Google Scholar 

  • Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99

    Article  PubMed  CAS  Google Scholar 

  • Mantel NA (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • Martín Bolaños M, Guinea López E (1949) Jarales y Jaras (Cistografia Hispanica). Ministerio de Agricultura, Madrid

    Google Scholar 

  • Médail F, Diadema K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36:1333–1345

    Article  Google Scholar 

  • Mengoni A, Gonnelli C, Galardi F, Gabbrielli R, Bazzicalupo M (2000) Genetic diversity and heavy metal tolerance in populations of Silene paradoxa L. (Caryophyllaceae): a RAPD analysis. Mol Ecol 9:1319–1324

    Article  PubMed  CAS  Google Scholar 

  • 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. Mol Ecol 10:1909–1916

    Article  PubMed  CAS  Google Scholar 

  • Mengoni A, Selvi F, Cusimano N, Galardi F, Gonnelli C (2006) Genetic diversity inferred from AFLP fingerprinting in populations of Onosma echioides (Boraginaceae) from serpentine and calcareous soils. Plant Biosyst 140:211–219

    Article  Google Scholar 

  • Metcalfe DB, Kunin WE (2006) The effects of plant density upon pollination success, reproductive effort and fruit parasitism in Cistus ladanifer L. (Cistaceae). Plant Ecol 185:41–47

    Article  Google Scholar 

  • Meudt HM, Clarke AC (2007) Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends Plant Sci 12:106–117

    Article  PubMed  CAS  Google Scholar 

  • 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. Mol Ecol 18:2050–2062

    Article  PubMed  Google Scholar 

  • Núñez-Olivera E, Martínez-Abaiga J, Escudero JC (1996) Adaptability of leaves of Cistus ladanifer to widely varying environmental conditions. Funct Ecol 10:636–646

    Article  Google Scholar 

  • Nyberg Berglund AB, Dahlgren S, Westerbergh A (2004) Evidence for parallel evolution and site-specific selection of serpentine tolerance in Cerastium alpinum during the colonization of Scandinavia. New Phytol 161:199–209

    Article  Google Scholar 

  • Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155

    Article  PubMed  CAS  Google Scholar 

  • Olalde M, Herrán A, Espinel S, Goicoechea PG (2002) White oak phylogeography in the Iberian Peninsula. Forest Ecol Manag 156:89–102

    Article  Google Scholar 

  • Pan W (2001) Model selection in estimating equations. Biometrics 57:529–534

    Article  PubMed  CAS  Google Scholar 

  • Papazoglou EG, Karantounias GA, Vemmos SN, Bouranis DL (2005) Photosynthesis and growth responses of giant reed (Arundo donax L.) to the heavy metals Cd and Ni. Environ Int 31:243–249

    Article  PubMed  CAS  Google Scholar 

  • Pauwels M, Willems G, Roosens N, Frérot H, Saumitou-Laprade P (2008) Merging methods in molecular and ecological genetics to study the adaptation of plants to anthropogenic metal-polluted sites: implications for phytoremediation. Mol Ecol 17:108–119

    Article  PubMed  CAS  Google Scholar 

  • Pérez-García F (1997) Germination of Cistus ladanifer seeds in relation to parent material. Plant Ecol 133:57–62

    Article  Google Scholar 

  • Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Poncet B, Herrmann D, Gugerli F, Taberlet P, Holderegger R, Gielly L, Rioux D, Thuiller W, Aubert S, Manel S (2010) Tracking genes of ecological relevance using a genome scan in two independent regional population samples of Arabis alpina. Mol Ecol 19:2896–2907

    Article  PubMed  CAS  Google Scholar 

  • Poschenrieder C, Bech J, Llugany M, Pace A, Fenés E, Barceló J (2001) Copper in plant species in a copper gradient in Catalonia (North East Spain) and their potential for phytoremediation. Plant Soil 230:247–256

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Quintela-Sabarís C (2011) Evolutionary origin and ecophysiology of metallicolous populations of Cistus ladanifer L. Ph.D. Thesis. Universidade de Santiago de Compostela, Spain

  • Quintela-Sabarís C, Vendramin GG, Castro-Fernández D, Fraga MI (2010) Chloroplast microsatellites reveal that metallicolous populations of the Mediterranean shrub Cistus ladanifer have multiple origins. Plant Soil 334:161–174

    Article  Google Scholar 

  • R Development Core Team (2007) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • Ribeiro MM, Mariette S, Vendramin GG, Szmidt AE, Plomion C, Kremer A (2002) Comparison of genetic diversity estimates within and among populations of maritime pine using chloroplast simple-sequence repeat and amplified fragment length polymorphism data. Mol Ecol 11:869–877

    Article  PubMed  CAS  Google Scholar 

  • Rohlf FJ (2002) NTSYSpc: numerical taxonomy system, ver. 2.11L. Exeter Publishing, Ltd, Setauket

    Google Scholar 

  • Ruttens A, Mench M, Colpaert JV, Boisson J, Carleer R, Vangronsveld J (2006) Phytostabilization of a metal contaminated sandy soil. I: influence of compost and/or inorganic metal immobilizing soil amendments on phytotoxicity and plant availability of metals. Environ Pollut 144:524–532

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Shaw BP, Sahu SK, Mishra RK (2004) Heavy metal induced oxidative damage in terrestrial plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants: from molecules to ecosystems, 2nd edn. Springer, Berlin, pp 84–126

    Google Scholar 

  • Simões MP, Madeira M, Gazarini L (2009) Ability of Cistus L. shrubs to promote soil rehabilitation in extensive oak woodlands of Mediterranean areas. Plant Soil 323:249–265

    Article  Google Scholar 

  • Staton JL, Schizas NV, Chandler GT, Coull BC, Quattro JM (2001) Ecotoxicology and population genetics: the emergence of “Phylogeographic and Evolutionary Ecotoxicology”. Ecotoxicology 10:217–222

    Article  PubMed  CAS  Google Scholar 

  • Storey JD (2002) A direct approach to false discovery rates. J Roy Stat Soc B 64:479–498

    Article  Google Scholar 

  • Talavera S, Gibbs PE, Herrera J (1993) Reproductive biology of Cistus ladanifer (Cistaceae). Plant Syst Evol 186:123–134

    Article  Google Scholar 

  • Tordoff GM, Baker AJM, Willis AJ (2000) Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41:219–228

    Article  PubMed  CAS  Google Scholar 

  • Vekemans X (2002) AFLP-SURV version 1.0. Distributed by the author. Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles, Belgium

  • Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151

    Article  PubMed  CAS  Google Scholar 

  • Vendramin GG, Anzidei M, Madaghiele A, Bucci G (1998) Distribution of genetic diversity in Pinus pinaster Ait. as revealed by chloroplast microsatellites. Theor Appl Genet 97:456–463

    Article  CAS  Google Scholar 

  • Vos P, Hagers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Friters A, Pot J, Paleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  PubMed  CAS  Google Scholar 

  • Wenzel WW, Lombi E, Adriano D (2004) Root and rhizosphere processes in metal hyperaccumulation and phytoremediation technology. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants: from molecules to ecosystems, 2nd edn. Springer, Berlin, pp 313–344

    Google Scholar 

  • White TL, Adams WT, Neale DB (2007) Forest genetic. CAB International, Oxfordshire

    Book  Google Scholar 

  • Yan J, Fine JP (2004) Estimating equations for association structures. Stat Med 23:859–880

    Article  PubMed  Google Scholar 

  • Ye ZH, Baker AJM, Wong MH, Willis AJ (1997) Zinc, lead and cadmium tolerance, uptake and accumulation by Typha latifolia. New Phytol 136:469–480

    Article  CAS  Google Scholar 

  • Zhivotovsky LA (1999) Estimating population structure in diploids with multilocus dominant DNA markers. Mol Ecol 8:907–913

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Dr. Isabel Evaristo (INRB L-INIA) collaborated in the optimization of the AFLP protocol. Alessio Mengoni and two anonymous referees provided useful comments that improved the manuscript. Miguel González Szamocki revised the English usage.

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Authors and Affiliations

  1. Departamento de Botánica, Facultade de Bioloxía, Universidade de Santiago de Compostela, Santiago de Compostela, 15782, Spain

    Celestino Quintela-Sabarís, Daniel Castro-Fernández & Maria Isabel Fraga

  2. Departamento de Recursos Naturais e Desenvolvimento Sustentável, Escola Superior Agrária, 6001-909, Castelo Branco, Portugal

    Maria Margarida Ribeiro

  3. Laboratoire d’Ecologie Alpine (LECA), CNRS UMR 5553, Grenoble Université, BP 53, 2233 Rue de la Piscine, 38041, Grenoble Cedex 9, France

    Bénédicte Poncet

  4. INRB L-INIA Molecular Biology Laboratory, Avª da República, Quinta do Marquês, 2780-159, Oeiras, Portugal

    Rita Costa

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  1. Celestino Quintela-Sabarís
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  2. Maria Margarida Ribeiro
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  3. Bénédicte Poncet
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  4. Rita Costa
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  5. Daniel Castro-Fernández
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Correspondence to Celestino Quintela-Sabarís.

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Quintela-Sabarís, C., Ribeiro, M.M., Poncet, B. et al. AFLP analysis of the pseudometallophyte Cistus ladanifer: comparison with cpSSRs and exploratory genome scan to investigate loci associated to soil variables. Plant Soil 359, 397–413 (2012). https://doi.org/10.1007/s11104-012-1221-8

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