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Genetic diversity of diploid Japanese strawberry species based on microsatellite markers

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Abstract

The United States Department of Agriculture (USDA)—Agricultural Research Service (ARS)—National Clonal Germplasm Repository (NCGR) in Corvallis, Oregon, is a genebank that preserves strawberry genetic resources. Representatives of two Japanese diploid species, Fragaria iinumae Makino and F. nipponica Makino were collected for conservation by the NCGR during an expedition to Hokkaido, Japan. Fragaria iinumae may be a genome contributor to the cultivated octoploid strawberries. The objective of this study was to evaluate the genetic diversity of these two species by using simple sequence repeat (SSR) markers. Twenty of 82 Fragaria-derived SSRs, polymorphic among and within the two species, were selected for genetic analysis of 137 accessions. Genetic diversity, based on the proportion of shared alleles between the two species, in F. nipponica (0.4542) and F. iinumae (0.1808) was significantly different. Three wild interspecific hybrids were identified from intermediate memberships in the two diploid species groups revealed by using the clustering program, Structure. Principal coordinate analysis followed by non-parametric modal clustering (PCO-MC) grouped accessions into two clusters representing the two diploid species. Further clustering within the species groups generated with the program, STRUCTURAMATM, resulted in seven subclusters in F. iinumae and three in F. nipponica, which may represent breeding populations appropriate for clonal conservation. Long-term preservation of the species populations and the limited number of hybrids on the island is discussed relative to their geographical distribution and the geological history of Hokkaido Island.

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References

  • Abbott RJ, James JK, Milne RI, Gillies ACM (2003) Plant introductions, hybridization and gene flow. Philos Trans R Soc B 358:1123–1132

    Article  CAS  Google Scholar 

  • Ashley MV, Wilk JA, Styan SMN, Craft KJ, Jones KL, Feldheim KA, Lewers KS, Ashman TL (2003) High variability and disomic segregation of microsatellites in the octoploid Fragaria virginiana Mill (Rosaceae). Theor Appl Genet 107:1201–1207

    Article  PubMed  CAS  Google Scholar 

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Evol Syst 16:113–148

    Article  Google Scholar 

  • Bassil NV, Gunn M, Folta KM, Lewers KS (2006a) Microsatellite markers for Fragaria from ‘Strawberry Festival’ expressed sequence tags. Mol Ecol Notes 6:473–476

    Article  CAS  Google Scholar 

  • Bassil NV, Njuguna W, Slovin JP (2006b) EST-SSR markers from Fragaria vesca L. cv. Yellow Wonder. Mol Ecol Notes 6:806–809

    Article  CAS  Google Scholar 

  • Bortiri E, Sang-Hun Oh, Jianguo J, Scott B, Andrew G, Clay W, Megan B, Daniel P, Dan EP (2001) Phylogeny and systematics of Prunus (Rosaceae) as determined by sequence analysis of ITS and the chloroplast trnL-trnF spacer DNA. Syst Bot 26:797–807

    Google Scholar 

  • Bringhurst RS (1990) Cytogenetics and evolution in American Fragaria. HortScience 25:879–881

    Google Scholar 

  • Bringhurst RS, Voth V (1984) Breeding octoploid strawberries. Iowa State J Res 58:371–381

    Google Scholar 

  • Bruneau A, Starr JR, Joly S (2009) Phylogenetic relationships in the genus Rosa: new evidence from chloroplast DNA sequences and an appraisal of current knowledge. Syst Bot 32:366–378

    Article  Google Scholar 

  • Chakraborty R, Jin L (1993) A unified approach to study hypervariable polymorphism: statistical considerations of determining relatedness and population distances. In: Pena SDJ, Chakraborty R, Epplen JT, Jeffreys AJ (eds) DNA fingerprinting: state of the science. Birkhäuser Verlag, Basel, pp 153–175

    Chapter  Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  PubMed  CAS  Google Scholar 

  • Cipriani G, Testolin R (2004) Isolation and characterization of microsatellite loci in Fragaria. Mol Ecol Notes 4:366–368

    Article  CAS  Google Scholar 

  • Darwin CH (1877) The various contrivances by which British and foreign orchids are fertilized by insects, 2nd edn. D Appleton and company, New York

    Google Scholar 

  • Davis TM, DiMeglio LM (2004) Identification of putative diploid genome donors to the octoploid cultivated strawberry, Fragaria ×ananassa. Plant and Animal Genome XII. San Diego, CA, January 10–14. (poster #603)

  • Davis TM, DiMeglio LM, Yang R, Styan SMN, Lewers KS (2006) Assessment of SSR marker transfer from the cultivated strawberry to diploid strawberry species: functionality, linkage group assignment, and use in diversity analysis. J Am Soc Hortic Sci 131:506–512

    CAS  Google Scholar 

  • Davis TM, Shields ME, Reinhard AE, Reavey PA, Lin J, Zhang H, Mahoney LL (2010) Chloroplast DNA inheritance, ancestry, and sequencing in Fragaria. Acta Hortic 859:221–228

    CAS  Google Scholar 

  • Folta KM, Davis TM (2006) Strawberry genes and genomics. Crit Rev Plant Sci 25:399–415

    Article  CAS  Google Scholar 

  • Fukunaga K, Hill J, Vigouroux Y, Matsuoka Y, Sanchez J, Liu K, Buckler ES, Doebley J (2005) Genetic diversity and population structure of teosinte. Genetics 169:22241–22254

    Article  Google Scholar 

  • Gil-Ariza DJ, Amaya I, Botella MA, Blanco JM, Caballero JL, Lopez-Aranda JM, Valpuesta V, Sanchez-Sevilla JF (2006) EST-derived polymorphic microsatellites from cultivated strawberry (Fragaria ×ananassa) are useful for diversity studies and varietal identification among Fragaria species. Mol Ecol Notes 6:1195–1197

    Article  CAS  Google Scholar 

  • Govan C, Simpson D, Johnson A, Tobutt K, Sargent D (2008) A reliable multiplexed microsatellite set for genotyping Fragaria and its use in a survey of 60 F. ×ananassa cultivars. Mol Breed 22:649–661

    Article  CAS  Google Scholar 

  • Gupta PK, Varshney RK (2000) The development and use of microsatellite markers for genetic analysis and plant breeding with emphasis on bread wheat. Euphytica 113:163–185

    Article  CAS  Google Scholar 

  • Hadonou AM, Sargent D, Wilson F, James CM, Simpson DW (2004) Development of microsatellite markers in Fragaria, their use in genetic diversity analysis, and their potential for genetic linkage mapping. Genome 47:429–438

    Article  PubMed  CAS  Google Scholar 

  • Hancock JF (1999) Strawberries. CABI Publishing, Oxford

    Google Scholar 

  • Harrison RE, Luby JJ, Furnier GR (1997) Chloroplast DNA restriction fragment variation among strawberry (Fragaria spp.) taxa. J Am Soc Hortic Sci 122:63–68

    Google Scholar 

  • Harrison RE, Luby JJ, Furnier GR, Hancock JF, Cooley D (1998) Variation for susceptibility to crown rot and powdery mildew in wild strawberry from North America. Acta Hortic 484:43–48

    Google Scholar 

  • Huelsenbeck JP, Andolfatto P (2007) Inference of population structure under a Dirichlet process model. Genetics 175:1787–1802

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hummer KE, Davis T, Iketani H, Imanishi H (2006) American-Japanese expedition to Hokkaido to collect berry crops in 2004. HortScience 41:993

    Google Scholar 

  • Hummer K, Nathewet P, Yanagi T (2009) Decaploidy in Fragaria iturupensis Staudt (Rosaceae). Am J Bot 96:713–716

    Article  PubMed  Google Scholar 

  • Iwasaki T, Adachi K, Moriya T, Miyamachi H, Matsushima T, Miyashita K, Takeda T, Taira T, Yamada T, Ohtake K (2004) Upper and middle crustal deformation of an arc–arc collision across Hokkaido, Japan, inferred from seismic refraction/wide-angle reflection experiments. Tectonophysics 388:59–73

    Article  Google Scholar 

  • James CM, Wilson F, Hadonou AM, Tobutt KR (2003) Isolation and characterization of polymorphic microsatellites in diploid strawberry (Fragaria vesca L.) for mapping, diversity studies and clone identification. Mol Ecol Notes 3:171–173

    Article  CAS  Google Scholar 

  • Lawrence FJ, Galletta GJ, Scott DH (1990) Strawberry breeding work of the United States Department of Agriculture. HortScience 25:895–896

    Google Scholar 

  • Lewers KS, Styan SMN, Hokanson SC, Bassil NV (2005) Strawberry GenBank-derived and genomic simple sequence repeat (SSR) markers and their utility with strawberry, blackberry, and red and black raspberry. J Am Soc Hortic Sci 130:102–115

    CAS  Google Scholar 

  • Liu K, Muse S (2004) Powermarker: new genetic data analysis software. Version 3.0. 10 October 2005. http://www.powermarker.net

  • Luby J, Hancock J, Dale A, Serce S (2008) Reconstructing Fragaria ×ananassa utilizing wild F. virginiana and F. chiloensis: inheritance of winter injury, photoperiod sensitivity, fruit size, female fertility and disease resistance in hybrid progenies. Euphytica 163:57–65

    Article  Google Scholar 

  • Mahoney LL, Quimby ML, Shields ME, Davis TM (2010) Mitochondrial DNA transmission, ancestry, and sequences in Fragaria. Acta Hortic 859:301–308

    CAS  Google Scholar 

  • Milne RI, Abbott RJ, Wolff K, Chamberlain DF (1999) Hybridization among sympatric species of rhododendron (Ericaceae) in Turkey: morphological and molecular evidence. Am J Bot 86:1776–1785

    Article  PubMed  CAS  Google Scholar 

  • Monfort A, Vilanova S, Davis TM, Arús P (2006) A new set of polymorphic simple sequence repeat (SSR) markers from a wild strawberry (Fragaria vesca) are transferable to other diploid Fragaria species and to Fragaria ×ananassa. Mol Ecol Notes 6:197–200

    Article  CAS  Google Scholar 

  • Murfett J, Strabala T, Zurek D, Mou B, Beecher B, McClure B (1996) S RNase and interspecific pollen-rejection pathways contribute to unilateral incompatibility between self-incompatible and self-compatible species. Plant Cell 8:943–958

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Naruhashi N, Iwata T (1988) Taxonomic re-evaluation of Fragaria nipponica Makino and allied species. J Phytologia taxon 36:59–64

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Oda Y (2002) Photosynthetic characteristics and geographical distribution of diploid Fragaria species native in Japan. Acta Hortic 567:38–384

    Google Scholar 

  • Potter D, Luby JJ, Harrison RE (2000) Phylogenetic relationships among species of Fragaria (Rosaceae) inferred from non-coding nuclear and chloroplast DNA sequences. Syst. Bot 25:337–348

    Article  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Reeves PA, Richards CM (2007) Distinguishing terminal monophyletic groups from reticulate taxa: Performance of phenetic, tree-based, and network procedures. Syst Biol 56:302–320

    Article  PubMed  Google Scholar 

  • Rousseau-Gueutin M, Gaston A, Aïnouche A, Aïnouche ML, Olbricht K, Staudt G, Richard L, Denoyes-Rothan B (2009) Tracking the evolutionary history of polyploidy in Fragaria L. (strawberry): new insights from phylogenetic analyses of low-copy nuclear genes. Mol Phylogenet Evol 51:515–530

    Article  PubMed  CAS  Google Scholar 

  • Sargent DJ, Hadonou M, Simpson DW (2003) Development and characterization of polymorphic microsatellite markers from Fragaria viridis, a wild diploid strawberry. Mol Ecol Notes 3:550–552

    Article  CAS  Google Scholar 

  • Sargent DJ, Clark J, Simpson DW, Tobutt KR, Arús P, Monfort A, Vilanova S, Denoyes-Rothan B, Rousseau M, Folta KM, Bassil NV, Battey NH (2006) An enhanced microsatellite map of diploid Fragaria. Theor Appl Genet 112:1349–1359

    Article  PubMed  CAS  Google Scholar 

  • Sargent D, Fernandéz-Fernandéz F, Ruiz-Roja J, Sutherland B, Passey A, Whitehouse A, Simpson D (2009) A genetic linkage map of the cultivated strawberry (Fragaria ×ananassa) and its comparison to the diploid Fragaria reference map. Mol Breed 24:293–303

    Article  CAS  Google Scholar 

  • Sjulin T, Dale A (1987) Genetic diversity of North American strawberry cultivars. J Am Soc Hortic Sci 112:375–385

    Google Scholar 

  • Smedmark JEE, Eriksson T (2009) Phylogenetic relationships of Geum (Rosaceae) and relatives inferred from the nrITS and trnL-trnF regions. Syst Bot 27:303–317

    Google Scholar 

  • Staudt G (1989) The species of Fragaria, their taxonomy and geographical distribution. Acta Hortic 567:24–31

    Google Scholar 

  • Staudt G (1999) Systematics and geographic distribution of the american strawberry species. Taxonomic studies in the genus Fragaria (Rosaceae: Potentilleae). Publications in Botany 81. University of California Press, Berkeley

    Google Scholar 

  • Staudt G (2005) Notes on Asiatic Fragaria species: IV. Fragaria iinumae. Bot Jahrb Sys 126:163–175

    Article  Google Scholar 

  • Staudt G (2006) Himalayan species of Fragaria (Rosaceae). Bot Jahrb Sys 126:483–508

    Article  Google Scholar 

  • Staudt G (2009) Strawberry biogeography, genetics and systematics. Acta Hortic 842:71–84

    Google Scholar 

  • Staudt G, Dickoré WB (2001) Notes on Asiatic Fragaria species: Fragaria pentaphylla Losinsk. and Fragaria tibetica spec. nov. Bot Jahrb Sys 123:341–354

    Google Scholar 

  • Staudt G, Olbricht K (2008) Notes on Asiatic Fragaria species V: F. nipponica and F. iturupensis. Bot Jahrb Sys 127:317–341

    Article  Google Scholar 

  • Wattier R, Engel CR, Saumitou-Laprade P, Valero M (1998) Short allele dominance as a source of heterozygote deficiency at microsatellite loci: experimental evidence at the dinucleotide locus Gv1CT in Gracilaria gracilis (Rhodophyta). Mol Ecol 7:1569–1573

    Article  CAS  Google Scholar 

  • Wigginton JE, Cutler DJ, Abecasis GR (2005) A note on exact tests of Hardy-Weinberg Equilibrium. Am J Hum Genet 76:887–893

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yang J, Pak JH (2006) Phylogeny of Korean Rubus (Rosaceae) based on its (nrDNA) and trnL/F intergenic region (cpDNA). J Plant Biol 49:44–54

    Article  CAS  Google Scholar 

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Correspondence to Wambui Njuguna.

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Njuguna, W., Hummer, K.E., Richards, C.M. et al. Genetic diversity of diploid Japanese strawberry species based on microsatellite markers. Genet Resour Crop Evol 58, 1187–1198 (2011). https://doi.org/10.1007/s10722-010-9652-7

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