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Using AFLP genome scanning to explore serpentine adaptation and nickel hyperaccumulation in Alyssum serpyllifolium

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Abstract

Background and aims

Alyssum section Odontarrhena is the largest single clade of Ni-hyperaccumulator plants, most of which are endemic to ultramafic (serpentine) soils. Alyssum serpyllifolium is a facultative hyperaccumulator able to grow both on limestone-derived and ultramafic soils. Analysis of different populations of this species with contrasting phenotypes could allow the identification of genes involved in Ni-hyperaccumulation and serpentine tolerance.

Methods

A glasshouse pot experiment on compost-amended ultramafic soil was carried out with three ultramafic (U) and two non-ultramafic (NU) populations of A. serpyllifolium. The leaf ionome was determined by elemental analysis and used as a proxy for serpentine adaptation. A Ni-hyperaccumulating phenotype was estimated from leaf Ni concentrations. Cultured plants were genotyped using Amplified Fragment Length Polymorphism (AFLP) markers. Outlier analysis and regressions of leaf ionome over band distribution were applied to detect markers potentially involved in Ni-hyperaccumulation and serpentine tolerance.

Results

As well as U populations, some plants from NU populations were found to be able to hyperaccumulate Ni in leaves to concentrations exceeding 0.1% (w/w). U populations had a higher Ca/Mg leaf ratio than NU populations, mainly due to Mg exclusion. 374 AFLP markers were amplified and a potential adaptive value was identified in 34 of those markers.

Conclusions

Phenotype regression analyses were found to be more powerful than outlier analyses and indicated that regulation of foliar concentrations of Ni, Ca, Mg and P are the main factors involved in serpentine adaptation. More research is needed in order to resolve the ancestral or recently -evolved nature of Ni-hyperaccumulation.

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References

  • Adamidis GC, Dimitrakopoulos PG, Manolis A, Papageorgiou AC (2014) Genetic diversity and population structure of the serpentine endemic Ni hyperaccumulator Alyssum lesbiacum. Plant Syst Evol 300:2051–2060

    Article  Google Scholar 

  • Álvarez-López V 2016 Plant-microbe-soil interactions and their role in phytotechnologies applied to trace metal-rich soils. PhD Thesis, CSIC-USC, Santiago de Compostela 356 pp.

  • Álvarez-López V, Prieto-Fernández A, Becerra-Castro C, Monterroso C and Kidd P S 2015 Rhizobacterial communities associated with the flora of three serpentine outcrops of the Iberian Peninsula. Plant Soil, 1–20

  • Antao T, Beaumont MA (2011) Mcheza: A workbench to detect selection using dominant markers. Bioinformatics 27:1717–1718

    Article  CAS  PubMed  Google Scholar 

  • Baker AJM (1981) Accumulators and excluders – strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    Article  CAS  Google Scholar 

  • Ball PW, Dudley TR (1993) Alyssum. In: Flora Europaea Vol. I, 2nd edition. Ed. T G Tutin et al. Cambridge University Press, Cambridge, pp 359–369

    Google Scholar 

  • Bani A, Pavlova D, Echevarria G, Mullaj A, Reeves RD, Morel JL, Sulçe S (2010) Nickel hyperaccumulation by the species of Alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Bot Serb 34:3–14

    Google Scholar 

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

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300

    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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Brooks RR (1987) Serpentine and its Vegetation: a Multidisciplinary Approach. Dioscorides Press, Oregon, 454 pp

    Google Scholar 

  • Brooks RR, Shaw S, Asensi Marfil A (1981) Some observations on the ecology, metal uptake and nickel tolerance of Alyssum serpyllifolium subspecies from the Iberian peninsula. Vegetatio 45:183–188

    Article  Google Scholar 

  • Cabello-Conejo M I 2015 Nickel hyperaccumulating plants: strategies to improve phytoextraction and a characterisation of Alyssum endemic to the Iberian Peninsula. PhD Thesis, CSIC-USC, Santiago de Compostela. 204 pp.

  • Cecchi L, Colzi I, Coppi A, Gonnelli C, Selvi F (2013) Diversity and biogeography of Ni hyperaccumulators of Alyssum section Odontarrhena (Brassicaceae) in the central western Mediterranean: evidence from karyology, morphology and DNA sequence data. Bot J Linn Soc 173:269–289

    Article  Google Scholar 

  • Centofanti T, Sayers Z, Cabello-Conejo MI, Kidd PS, Nishizawa NK, Kakei Y, Davis AP, Sicher RC, Chaney RL (2013) Xylem exudate composition and root-to-shoot nickel translocation in Alyssum species. Plant Soil 373:59–75

    Article  CAS  Google Scholar 

  • Coart E, Van Glabeke S, Petit RJ, Van Bockstaele E, Roldan-Ruiz I (2005) Range wide versus local patterns of genetic diversity in hornbeam (Carpinus betulus L.) Conserv Genet 6:259–273

    Article  CAS  Google Scholar 

  • Deng THB, Tang YT, van der Ent A, Sterckeman T, Echevarria G, Morel JL, Qiu RL (2016) Nickel translocation via the phloem in the hyperaccumulator Noccaea caerulescens (Brassicaceae). Plant Soil 404:35–45

    Article  CAS  Google Scholar 

  • Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species' geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17:1170–1188

    Article  CAS  PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flynn TA (2012) Evolution of nickel hyperaccumulation in Alyssum L. D.Phil. thesis. University of Oxford, Oxford, 232 pp

    Google Scholar 

  • Galardi F, Mengoni A, Pucci S, Barletti L, Massi L, Barzanti R, Gabbrielli R, Gonnelli C (2007) Intra-specific differences in mineral element composition in the Ni-hyperaccumulator Alyssum bertolonii: a survey of populations in nature. Environ Exp Bot 60:50–56

    Article  CAS  Google Scholar 

  • Gao J, Sun L, Yang X, Liu JX (2013) Transcriptomic analysis of cadmium stress response in the heavy metal hyperaccumulator Sedum alfredii Hance. PLoS One 8(6):e64643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gerth A, Merten D, Baumbach H (2011) Verbreitung, Vergesellschaftung und genetische Populationsdifferenzierung des Berg-Steinkrautes (Alyssum montanum L.) auf Schwermetallstandorten im östlichen Harzvorland. Hercynia 44:73–92

    Google Scholar 

  • Ghasemi R, Ghaderian SM (2009) Responses of two populations of an Iranian nickel-hyperaccumulating serpentine plant, Alyssum inflatum Nyar., to substrate Ca/Mg quotient and nickel. Environ Exp Bot 67:260–268

    Article  CAS  Google Scholar 

  • Halimaa P, Blande D, Aarts MGM, Tuomainen M, Tervahauta A, Kärenlampi S (2014) Comparative transcriptome analysis of the metal hyperaccumulator Noccaea caerulescens. Front Plant Sci 5:213. doi:10.3389/fpls.2014.00213

    Article  PubMed  PubMed Central  Google Scholar 

  • Herrera CM, Bazaga P (2009) Quantifying the genetic component of phenotypic variation in unpedigreed wild plants: tailoring genomic scan for within-population use. Mol Ecol 18:2602–2614

    Article  CAS  PubMed  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 

  • Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508

    CAS  PubMed  Google Scholar 

  • Kazakou E, Adamidis GC, Baker AJM, Reeves RD, Godino M, Dimitrakopoulos PG (2010) Species adaptation in serpentine soils in Lesbos Island (Greece): metal hyperaccumulation and tolerance. Plant Soil 332:369–385

    Article  CAS  Google Scholar 

  • Kidd P S, Cabello-Conejo M I, Monterroso C, Becerra-Castro C, Álvarez-López V, Acea M J and Prieto-Fernández A 2011 Nickel bioaccumulation in different populations of Alyssum pintodasilvae and Alyssum malacitanum: Application in phytoextraction. XI ICOBTE Conference.

    Google Scholar 

  • Kidd PS, Mench M, Álvarez-López V, Bert V, Dimitriou I, Friesl-Hanl W, Herzig R, Janssen JO, Kolbas A, Müller I, Neu S, Renella G, Ruttens A, Vangronsveld J, Puschenreiter M (2015) Agronomic practices for improving gentle remediation of trace element-contaminated soils. Int J Theor Phys 17:1005–1037

    CAS  Google Scholar 

  • Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534

    Article  PubMed  Google Scholar 

  • Kruckeberg A R 2002 The influences of lithology on plant life. In Geology and Plant Life: The Effects of Landforms and Rock Type on Plants pp. 160–181. Seattle/London: Univ. Wash. Press. 362 pp.

    Google Scholar 

  • Küpfer P, Nieto-Feliner G (1993) Alyssum. In: Flora Iberica Vol. IV. Ed. S Castroviejo et al. Real Jardín Botánico. CSIC, Madrid, pp 167–184

    Google Scholar 

  • Lex A, Gehlenborg N, Strobelt H, Vuillemot R, Pfister H (2014) UpSet: Visualization of Intersecting Sets. IEEE Trans Vis Comput Graph 20:1983–1992

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13

    Article  CAS  Google Scholar 

  • Mengoni A, Cecchi L, Gonnelli C (2012) Nickel hyperaccumulating plants and Alyssum bertolonii: model systems for studying biogeochemical interactions in serpentine soils. In: Bio-Geo Interactions in Metal-Contaminated Soils. Soil Biology 31. Ed. E Kothe and A Varma. Springer, Berlin, pp 279–296

    Chapter  Google Scholar 

  • Merlot S, Hannibal L, Martins S, Martinelli L, Amir H, Lebrun M, Thomine S (2014) The metal transporter PgIREG1 from the hyperaccumulator Psychotria gabriellae is a candidate gene for nickel tolerance and accumulation. J Exp Bot 65:1551–1564

    Article  CAS  PubMed  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 

  • Morrison RS, Brooks RR, Reeves RD (1980) Nickel uptake by Alyssum species. Plant Sci Lett 17:451–457

    Article  CAS  Google Scholar 

  • Mota JF, Medina-Cazorla JM, Navarro FB, Pérez-García FJ, Pérez-Latorre A, Sánchez-Gómez P, Torres JA, Benavente A, Blanca G, Gil C, Lorite J, Merlo ME (2008) Dolomite flora of the Baetic ranges glades (South Spain). Flora 203:359–375

    Article  Google Scholar 

  • Nkrumah PN, Baker AJM, Chaney RL, Erskine PD, Echevarria G, Morel JL, van der Ent A (2016) Current status and challenges in developing nickel phytomining: an agronomic perspective. Plant Soil 406:55–69

    Article  CAS  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  CAS  PubMed  Google Scholar 

  • O’Dell RE, James JJ, Richards JH (2006) Congeneric serpentine and nonserpentine shrubs differ more in leaf Ca: Mg than in tolerance of low N, low P, or heavy metals. Plant Soil 280:49–64

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217:8–17

    Article  PubMed  Google Scholar 

  • Quintela-Sabarís C, Ribeiro MM, Poncet B, Costa R, Castro-Fernández D, Fraga MI (2012) 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

    Article  Google Scholar 

  • Sobczyk MK, Smith JAC, Pollard AJ, Filatov DA (2017) Evolution of nickel hyperaccumulation and serpentine adaptation in the Alyssum serpyllifolium species complex. Heredity 118:31–41

    Article  CAS  PubMed  Google Scholar 

  • Spaniel S, Marhold K, Filova B, Zozomova-Lihova J (2011a) Genetic and morphological variation in the diploid-polyploid Alyssum montanum in Central Europe: taxonomic and evolutionary considerations. Plant Syst Evol 294:1–25

    Article  Google Scholar 

  • Spaniel S, Marhold K, Passlacqua NG, Zozomova-Lihova J (2011b) Intricate variation patterns in the diploid-polyploid complex of Alyssum montanum-A. repens (Brassicaceae) in the Apennine Peninsula: evidence for long-term persistence and diversification. Am J Bot 98:1887–1904

    Article  PubMed  Google Scholar 

  • Spaniel S, Marhold K, Thiv M, Zozomova-Lihova J (2012) A new circumscription of Alyssum montanum ssp. montanum and A. montanum ssp. gmelinii (Brassicaceae) in Central Europe: molecular and morphological evidence. Bot J Linn Soc 169:378–402

    Article  Google Scholar 

  • Strasburg JL, Sherman NA, Wright KM, Moyle LC, Willis JH, Rieseberg LH (2012) What can patterns of differentiation across plant genomes tell us about adaptation and speciation? Philos Trans R Soc B 367:364–373

    Article  Google Scholar 

  • Turner TL, Bourne EC, Von Wettberg EJ, Hu TT, Nuzhdin SV (2010) Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nat Genet 42:260–264

    Article  CAS  PubMed  Google Scholar 

  • van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334

    Article  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

    Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was funded by the FACCE Surplus project Agronickel (ID71). CQS was awarded a Research Grant from the Deputación da Coruña, and a Postdoctoral contract financed by the French National Research Agency through the national program “Investissements d’avenir” with the reference ANR-10-LABX-21-01 / LABEX RESSOURCES21.

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Authors and Affiliations

  1. Consejo Superior de Investigaciones Científicas (CSIC), Instituto de Investigacións Agrobiolóxicas de Galiza (IIAG), 15706, Santiago de Compostela, Spain

    Celestino Quintela-Sabarís & Petra S. Kidd

  2. INRA, Laboratoire Sols et Environnement, UMR 1120, F-54518, Vandœuvre-lès-Nancy, France

    Celestino Quintela-Sabarís

  3. Laboratoire Sols et Environnement (UMR 1120 LSE), Ensaia - 2 avenue de la Forêt de Haye, TSA 40602, 54518, Vandoeuvre-lès-Nancy, France

    Celestino Quintela-Sabarís

  4. BIOGECO, UMR INRA 1202, Université de Bordeaux, allée G. St Hilaire, CS50023, F-33615, Pessac, France

    Lilian Marchand

  5. Department of Plant Sciences, University of Oxford, Oxford, OX1 3RB, UK

    J. Andrew C. Smith

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  1. Celestino Quintela-Sabarís
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  2. Lilian Marchand
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  3. J. Andrew C. Smith
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  4. Petra S. Kidd
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Correspondence to Celestino Quintela-Sabarís.

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Responsible Editor: Antony Van der Ent.

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Quintela-Sabarís, C., Marchand, L., Smith, J.C. et al. Using AFLP genome scanning to explore serpentine adaptation and nickel hyperaccumulation in Alyssum serpyllifolium . Plant Soil 416, 391–408 (2017). https://doi.org/10.1007/s11104-017-3224-y

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