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Nuclear and chloroplast microsatellite markers to assess genetic diversity and evolution in hazelnut species, hybrids and cultivars

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Abstract

The US Department of Agriculture, Agricultural Research Service, National Clonal Germplasm Repository in Corvallis, Oregon, preserves more than 800 accessions of hazelnut (Corylus), including C. avellana cultivars and representatives of 10 other recognized shrub and tree species. Characterization and study of genetic diversity in this collection require cross-transferable markers, such as trinucleotide microsatellite or simple sequence repeat (SSR) markers and universal chloroplast SSR markers. We developed new SSR markers and evaluated 114 Corylus accessions representing 11 species and 44 interspecific hybrids. Eight of 23 SSRs generated easy-to-score alleles in all species and seven were highly polymorphic. For those seven, the average heterozygosity was moderate at 0.49, and mean allele number, genetic diversity and polymorphism information index were high at 11.71, 0.79 and 0.76, respectively. The three most polymorphic SSRs were CaC-C008, CaC-C040 and CaC-C118. Neighbor-joining (NJ) clustering and structure analysis agreed with classical taxonomic analysis and supported inclusion of C. maxima within the large polymorphic species, C. avellana. Analysis also indicated that C. californica is a distinct species rather than a botanical variety of C. cornuta. Six universal cpSSRs were polymorphic in Corylus and generated 21 distinct chlorotypes with an average of 3 alleles per locus. Diversity at these cpSSRs was high and ranged from 0.33 to 0.64, with an average of 0.54. Incongruence in NJ topologies between the nuclear and chloroplast markers could be attributed to chloroplast capture related to hybridization during the ancestral diversification of the genus, or to homoplasy. The phylogeographical relationships among the 21 chlorotypes in the 11 Corylus species support Asia as a refugium where several hazelnut lineages survived during glaciation and from which they continued to evolve after dispersal from Asia through the Mediterranean to Europe, and across the Atlantic and/or the Bering land bridge to North America.

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References

  • Arroyo-García R, Ruiz-García L, Bolling L, Ocete R, López MA, Arnold C, Ergul A, Söylemezoğlu G, Uzun HI, Cabello F, Ibáñez J, Aradhya MK, Atanassov A, Atanassov I, Balint S, Cenis JL, Costantini L, Gorislavets S, Grando MS, Klein BY, McGovern PE, Merdinoglu D, Pejic I, Pelsy F, Primikirios N, Risovannaya V, Roubelakis-Angelakis KA, Snoussi H, Sotiri P, Tamhankar S, This P, Troshin L, Malpica JM, Lefort F, Martínez-Zapater JM (2006) Multiple origins of cultivated grapevine (Vitis vinifera L. ssp. sativa) based on chloroplast DNA polymorphisms. Mol Ecol 15:3707–3714

    Article  PubMed  Google Scholar 

  • Bandelt HJ, Foster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  PubMed  CAS  Google Scholar 

  • Bassil NV, Botta R, Mehlenbacher SA (2005a) Microsatellite markers in hazelnut: isolation, characterization and cross-species amplification. J Am Soc Hort Sci 130:543–549

    CAS  Google Scholar 

  • Bassil NV, Botta R, Mehlenbacher SA (2005b) Additional microsatellite markers of the European hazelnut. Acta Hort 686:105–110

    CAS  Google Scholar 

  • Bassil NV, Postman J, Hummer K, Botu M, Sezer A (2009) SSR fingerprinting panel verifies identities of clones in backup hazelnut collection at USDA genebank. Acta Hort 845:95–102

    CAS  Google Scholar 

  • Boccacci P, Botta R (2009) Investigating the origin of hazelnut (Corylus avellana L.) cultivars using chloroplast microsatellites. Genet Resour Crop Evol 56:851–859

    Article  CAS  Google Scholar 

  • Boccacci P, Botta R (2010) Microsatellite variability and genetic structure in hazelnut (Corylus avellana L.) cultivars from different growing regions. Sci Hortic 124:128–133

    Article  CAS  Google Scholar 

  • Boccacci P, Akkak A, Bassil NV, Mehlenbacher SA, Botta R (2005) Characterization and evaluation of microsatellite loci in european hazelnut (Corylus avellana L.) and their transferability to other Corylus species. Mol Ecol Notes 5:934–937

    Article  CAS  Google Scholar 

  • Boccacci P, Akkak A, Botta R (2006) DNA-typing and genetic relationships among European hazelnut (Corylus avellana L.) cultivars using microsatellite markers. Genome 49:598–611

    Article  PubMed  CAS  Google Scholar 

  • Boccacci P, Botta R, Rovira M (2008) Genetic diversity of hazelnut (Corylus avellana L.) germplasm in northeastern Spain. HortSci 43:667–672

    Google Scholar 

  • Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32:314–331

    PubMed  CAS  Google Scholar 

  • Botta R, Akkak A, Boccacci P (2005) DNA-typing of hazelnut: a universal methodology for describing cultivars and evaluating genetic relatedness. Acta Hort 686:117–124

    CAS  Google Scholar 

  • Chen ZD, Manchester SR, Sun HY (1999) Phylogeny and evolution of the Betulaceae as inferred from DNA sequences, morphology, and paleobotany. Am J Bot 86:1168–1181

    Article  PubMed  CAS  Google Scholar 

  • Crane PR (1989) Early fossil history and evolution of the Betulaceae. In: Crane PR, Blackmore S (eds) Evolution, systematics and fossil history of the Hamamelidae, vol 2, ‘Higher’ Hamame- lidae. Clarendon Press, Oxford, pp 87–116

  • Cronquist A (1981) An integrated system of classification of flowering plants. Columbia University Press, London

    Google Scholar 

  • Cuenca A, Escalante AE, Piñero D (2003) Long-distance colonization, isolation by distance, and historical demography in a relictual Mexican pinyon pine (Pinus nelsonii Shaw) as revealed by paternally inherited genetic markers (cpSSRs) M. Mol Ecol 12:2087–2097

    Article  PubMed  CAS  Google Scholar 

  • De Candolle A (1864) Corylus. In: Prodromus systemnatis naturalis regni vegetabilis, vol 16, part 2. Treuttel & Wurtz, Paris, pp 128–133

  • Erdoğan V, Mehlenbacher SA (2000a) Phylogenetic relationships of Corylus species (Betulaceae) based on nuclear ribosomal DNA ITS region and chloroplast matK gene sequences. Syst Bot 25:727

    Article  Google Scholar 

  • Erdoğan V, Mehlenbacher SA (2000b) Interspecific hybridization in hazelnut. J Am Soc Hort Sci 125(4):489–497

    Google Scholar 

  • Forest F, Bruneau A (2000) Phylogenetic analysis, organization and molecular evolution of the nontranscribed spacer of 5S ribosomal RNA genes in Corylus (Betulaceae). Int J Plant Sci 161:793–806

    Article  CAS  Google Scholar 

  • Forest F, Savolainen V, Chase MW, Lupia R, Bruneau A, Crane PR (2005) Teasing apart molecular- versus fossil-based error estimates when dating phylogenetic trees: a case study in the Birch family (Betulaceae). Syst Bot 30:118–133

    Article  Google Scholar 

  • Gastier JM, Pulido JC, Sunden S, Brody T, Buetow KH, Murray JC, Weber JL, Hudson TJ, Sheffield VC, Duyk GM (1995) Survey of trinucleotide repeats in the human genome: assessment of their utility as genetic markers. Hum Mol Genet 4:1829–1836

    Article  PubMed  CAS  Google Scholar 

  • Ghanbari A, Akkak A, Boccacci P, Talaie A, Vezvaie A, Botta A (2005) Characterization of hazelnut (Corylus avellana L.) cultivars using microsatellite markers. Acta Hort 686:111–115

    CAS  Google Scholar 

  • Gökirmak T, Mehlenbacher SA, Bassil NV (2009) Characterization of European hazelnut (Corylus avellana) cultivars using SSR markers. Genet Resour Crop Evol 56:147–172

    Article  Google Scholar 

  • Gürcan K, Mehlenbacher SA (2010a) Transferability of microsatellite markers in the Betulaceae. J Am Soc Hort Sci 135(2):159–173

    Google Scholar 

  • Gürcan K, Mehlenbacher SA (2010b) Development of microsatellite marker loci for European hazelnut (Corylus avellana L.) from ISSR fragments. Mol Breed 26:551–559

    Article  Google Scholar 

  • Gürcan K, Mehlenbacher SA, Bassil NV, Boccacci P, Akkak A, Botta R (2010a) New microsatellite markers for Corylus avellana from enriched libraries. Tree Genet Gen 6:513–531

    Article  Google Scholar 

  • Gürcan K, Mehlenbacher SA, Erdoğan V (2010b) Genetic diversity in hazelnut cultivars from Black Sea countries assessed using SSR markers. Plant Breed 129:422–434. doi:10.1111/j.1439-0523.2009.01753.x

    Google Scholar 

  • Ishii T, McCouch SR (2000) Microsatellites and microsynteny in the chloroplast genomes of Oryza and eight other Graminae species. Theor Appl Genet 100:1257–1266

    Article  CAS  Google Scholar 

  • Ishii T, Mori N, Ogihara Y (2001) Evaluation of allelic diversity at chloroplast microsatellite loci among common wheat and its ancestral species. Theor Appl Genet 103:896–904

    Article  CAS  Google Scholar 

  • Kasapligil B (1972) A bibliography on Corylus (Betulaceae) with annotations. Annu Rpt Northern Nut Growers Assn 63:107–162

    Google Scholar 

  • Kutil BL, Williams CJ (2001) Triplet repeat microsatellites shared among hard and soft pines. J Heredity 92:327–332

    Article  CAS  Google Scholar 

  • Li PC, Cheng SX (1979) Betulaceae. In: Kuang K-Z, Li P-C (eds) Flora republicae popularis sinicae, vol 21. Science Press, Beijing, pp 44–137 (In Chinese)

  • Liang WJ, Zhang YM (1988) Investigation and study of filbert resources in China. In: Proceedings of the international symposium on horticultural germplasm, Cultivated and Wild. Beijing, China. 5–9 Sept. 1988

  • Liewlaksaneeyanawin C, Ritland CE, El-Kassaby YA, Ritland K (2004) Single-copy, species-transferable microsatellite markers developed from loblolly pine ESTs. Theor Appl Genet 109:361–369

    Article  PubMed  CAS  Google Scholar 

  • Liu K, Muse SV (2005) Powermarker: integrated analysis environment for genetic marker data. Bioinformatics 21:2128–2129

    Article  PubMed  CAS  Google Scholar 

  • Malusà E (1994) Interspecific relationships among Corylus species. Acta Hort 51:335–340

    Google Scholar 

  • Mehlenbacher SA (1991) Hazelnuts (Corylus). Genetic resources of temperate fruit and nut crops. Acta Hort 290:791–836

    Google Scholar 

  • Mehlenbacher SA (2009) Genetic resources for hazelnut: state of the art and future perspectives. Acta Hort 845:33–38

    Google Scholar 

  • Mehlenbacher SA, Brown RN, Nouhra ER, Gökirmak T, Bassil NV, Kubisiak TL (2006) A genetic linkage map for hazelnut (Corylus avellana L.) based on RAPD and SSR markers. Genome 49:122–133

    PubMed  CAS  Google Scholar 

  • Minch E (1997) MICROSAT version 1.5b. Stanford University Medical Center, Stanford, CA. http://hpgl.stanford.edu/projects/microsat/ Accessed 02 January 2012

  • Molnar TJ, Goffreda JC, Funk CR (2005) Developing hazelnuts for the eastern United States. Acta Hort 68:609–617

    Google Scholar 

  • Morgante M, Hanafey M, Powell W (2002) Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat Genet 30:194–200

    Article  PubMed  CAS  Google Scholar 

  • Navascués M, Emerson BC (2005) Chloroplast microsatellites: measures of genetic diversity and the effect of homoplasy. Mol Ecol 14:1333–1341

    Article  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionay genetics. Columbia University Press, New York

    Google Scholar 

  • Palmé AE, Vendramin GG (2002) Chloroplast DNA variation, postglacial recolonization and hybridization in hazel, Corylus avellana. Mol Ecol 11:1769–1779

    Article  PubMed  Google Scholar 

  • Petit RJ, Aguinagalde I, de Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Müller-Starck G, Demesure-Musch B, Palmé A, Martín JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565

    Article  PubMed  CAS  Google Scholar 

  • Pigg KB, Manchester SR, Wehr WC (2003) Corylus, Carpinus, and Palaeocarpinus (Betulaceae) from the middle Eocene Klondike Mountain and Allenby Formations of northwestern North America. Int J Plant Sci 164:807–822

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Provan J, Powell W, Hollingsworth PH (2001) Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends Ecol Evol 16:142–147

    Article  PubMed  Google Scholar 

  • Rajora OP, Rahman MH, Dayanandan S, Mosseler A (2001) Isolation, characterization, inheritance and linkage of microsatellite DNA markers in white spruce (Picea glauca) and their usefulness in other spruce species. Mol Gen Genet 264:871–882

    Article  PubMed  CAS  Google Scholar 

  • Rovira M (1997) Genetic variability among hazelnut (C. avellana L.) cultivars. Acta Hort 445:45–50

    Google Scholar 

  • Sathuvalli SR, Mehlenbacher SA (2011) Characterization of American hazelnut (Corylus americana) accessions and Corylus americana × Corylus avellana hybrids using microsatellite markers. Genet Resour Crop Evol. doi:10.1007/s10722-011-9743-0

    Google Scholar 

  • Schneider C (1916) Betulaceae. In: ed., Sargent CS (ed) Plantae wilsonianae: an enumeration of the woody plants collected in western China for the Arnold Arboretum of Harvard University during the years 1907, 1908, and 1910, vol. 2. Publications of the Arnold Arboretum, no. 4, pp 423–508

  • Scotti I, Magni F, Fink R, Powell W, Binnelli G, Hedley PE (2000) Microsatellite repeats are not randomly distributed within Norway spruce (Picea abies L.) expressed sequences. Genome 43:41–46

    PubMed  CAS  Google Scholar 

  • Sheffield VC, Weber JL, Buetow KH, Murray JC, Even DA, Wiles K, Gastier JM, Pulido JC, Yandava C, Sunden SL et al (1995) A collection of tri- and tetra-nucleotide repeat markers used to generate high quality, high resolution human genome-wide linkage maps. Hum Mol Genet 4:1837–1844

    Article  PubMed  CAS  Google Scholar 

  • Shepherd M, Cross M, Maguire TL, Dieters MJ, Williams CG, Henry RJ (2002) Transpecific microsatellites for hard pines. Theor Appl Genet 104:819–827

    Article  PubMed  CAS  Google Scholar 

  • Slate GL (1947) Some results with filbert breeding at Geneva, New York. Annu Rep North Nut Grow Assoc 38:94–100

    Google Scholar 

  • Stàgel A, Portis E, Toppino L, Rotino GL, Lanteri S (2008) Gene-based microsatellite development for mapping and phylogeny studies in eggplant. BMC Genomics 9:357–370

    Article  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. doi:10.1093/molbev/msr121

    Google Scholar 

  • Terrab A, Paun O, Talavera S, Tremetsberger K, Arista MF, Stuessy TF (2006) Genetic diversity and population structure in natural populations of Moroccan Atlas cedar (Cedrus atlantica, Pinaceae) determined with cpSSR markers. Am J Bot 93(9):1274–1280

    Article  PubMed  CAS  Google Scholar 

  • Testolin R, Cipriani G (2010) Molecular markers for germplasm identification and characterization. Acta Hort 859:59–72

    CAS  Google Scholar 

  • The Plant List (2010) Version 1. Published on the Internet; http://www.theplantlist.org/. Accessed April 23, 2012

  • Thompson MM, Lagerstedt HB, Mehlenbacher SA (1996) Hazelnuts. In: Janick J, Moore JN (eds) Fruit breeding: nuts, vol 3. Wiley, New York, pp 125–184

    Google Scholar 

  • Tozaki T, Inoue S, Mashima S, Ohta M, Miura N, Tomita M (2000) Sequence analysis of trinucleotide repeat microsatellites from an enrichment library of the equine genome. Genome 43:354–365

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Weber JL, Zhong G, Tanksley SD (1994) Survey of plant short tandem DNA repeats. Theor Appl Genet 88:1–6

    CAS  Google Scholar 

  • Weising K, Gardner R (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42:9–19

    Article  PubMed  CAS  Google Scholar 

  • Wendel JF, Doyle JJ (1998) Phylogenetic incongruence: window into genome history and molecular evolution. In: Soltis D, Soltis P, Doyle J (eds) Molecular systematics of plants, 2nd edn. Chapman & Hall, New York

    Google Scholar 

  • Whitcher IN, Wen J (2001) Phylogeny and biogeography of Corylus (Betulaceae): inference from ITS sequences. Syst Bot 26:283–298

    Google Scholar 

  • Yoo K-O, Wen J (2002) Phylogeny and biogeography of Carpinus and subfamily Coryloideae (Betulaceae). Int J Plant Sci 163:641–650

    Article  Google Scholar 

  • Yoo K-O, Wen J (2007) Phylogeny of Carpinus and subfamily Coryloideae (Betulaceae) based on chloroplast and nuclear ribosomal sequence data. Plant Syst Evol 267:25–35

    Article  Google Scholar 

  • Young ET, Sloan JS, Van Riper K (2000) Trinucleotide repeats are clustered in regulatory genes in Saccaromyces cerevisae. Genetics 154:1053–1068

    PubMed  CAS  Google Scholar 

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Acknowledgments

We acknowledge Barbara Gilmore, Christine Neou-Anderson, and April Nyberg for technical assistance in microsatellite marker separation. Funding for this study was provided by the USDA-ARS CRIS 5358-21000-033-00D, a USDA-ARS National Plant Germplasm System Evaluation Grant, and by the Fondazione Cassa di Risparmio di Torino (Italy).

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Authors and Affiliations

  1. United States Department of Agriculture (USDA), Agricultural Research Service (ARS), National Clonal Germplasm Repository (NCGR), 33447 Peoria Road, Corvallis, OR, 97333, USA

    Nahla Bassil & Joseph Postman

  2. Plant Virology Institute, National Research Council (IVV-CNR), UOS of Grugliasco, Via Leonardo da Vinci, 44, 10095, Grugliasco, TO, Italy

    Paolo Boccacci

  3. Dipartimento di Colture Arboree, Università degli Studi di Torino, Via Leonardo da Vinci, 44, 10095, Grugliasco, TO, Italy

    Roberto Botta

  4. Department of Horticulture, Oregon State University, Agricultural and Life Sciences Bldg., 4017, Corvallis, OR, 97331, USA

    Shawn Mehlenbacher

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  1. Nahla Bassil
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Correspondence to Nahla Bassil.

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10722_2012_9857_MOESM1_ESM.xlsx

Supplementary Table 1. Amplification and polymorphism of twenty-three SSRs developed from a trinucleotide-enriched library (GAA) of hazelnut. Amplification success and polymorphism are indicated with a ‘+’ while failure and monomorphism are indicated by ‘-‘. ‘D’ refers to discarded primer pairs for that species due to poor amplification in tested representatives of that species. Also listed are the SSR motif, primer sequences, expected size, optimum annealing temperature, linkage group location, and citation where available. (XLSX 25 kb)

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Bassil, N., Boccacci, P., Botta, R. et al. Nuclear and chloroplast microsatellite markers to assess genetic diversity and evolution in hazelnut species, hybrids and cultivars. Genet Resour Crop Evol 60, 543–568 (2013). https://doi.org/10.1007/s10722-012-9857-z

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