Advertisement

Genetic Resources and Crop Evolution

, Volume 64, Issue 3, pp 451–466 | Cite as

Discriminating power of microsatellites in cranberry organelles for taxonomic studies in Vaccinium and Ericaceae

  • Brandon Schlautman
  • Giovanny Covarrubias-Pazaran
  • Diego Fajardo
  • Shawn Steffan
  • Juan Zalapa
Research Article

Abstract

Simple sequence repeats (SSRs) in chloroplast and mitochondrial DNA, which have not been previously developed in the Ericaceae or, more specifically, in the genus Vaccinium, can be powerful tools for determining evolutionary relationships among taxa. In this study, 30 chloroplast, 23 mitochondrial, and 1 mitochondrion-like SSRs were identified in cranberry (V. macrocarpon), and primer-pairs were developed and tested for each locus. Although no polymorphisms were detected for any of the 54 SSR loci in nine diverse cranberry genotypes, all primers were cross-transferable to some extent to a panel of 12 additional Vaccinium taxa and four non-Vaccinium Ericaceae species. A Neighbor-Joining tree of the estimated average squared distances resolved the species by genus and by section within Vaccinium. Similar topologies with increased branch support were observed in Bayesian inference trees constructed from the DNA sequences of six plastid and two mitochondrial SSR loci. Two multiplexing/poolplexing panels of M13 fluorescently labeled primers, which amplify 24 of the 54 markers, were developed and can serve as an efficient, cost-effective means for characterizing the basic molecular phylogeny of Vaccinium. Increased understanding of evolutionary relationships among Vaccinium species should facilitate interspecific hybridization and introgression efforts to improve economically important traits of commercial berry crops.

Keywords

Cross-species amplification Ericaceae Mitochondria Organelle markers Plastid Phylogenetic analysis SSR markers Vaccinium 

Notes

Acknowledgments

1 Corinthians 10:31. The authors thank James Polashock, Jennifer Johnson-Cicalese, and Nicholi Vorsa for their contribution of plant materials and comments on this manuscript. This project was supported by USDA-ARS (Project No. 3655-21220-001-00 provided to J.Z. and S.S.); WI-DATCP (SCBG Project #14-002); National Science Foundation (DBI-1228280); Ocean Spray Cranberries, Inc.; Wisconsin Cranberry Growers Association; Cranberry Institute; B.S. was supported by the Frank B. Koller Cranberry Fellowship Fund for Graduate Students; G.C.-P. was supported by the Consejo Nacional de Ciencia y Tecnología (CONACYT, Mexico).

Author contribution

B.S., D.F., S.S., and J.Z. conceived the research and designed experiments. B.S. and D.F. performed SSR mining and primer design. B.S. and G.C-P. performed fragment analyses and Sanger sequencing. B.S. and D.F. performed phylogenetic analyses. B.S. developed multiplexing/poolplexing panels. D.F. and S.S. assisted in analyzing results and developing discussion points. B.S. and J.Z. wrote the paper and oversaw the study.

Compliance with ethical standards

Conflicts of interest

The authors declare that there are no conflicts of interest.

Supplementary material

10722_2016_371_MOESM1_ESM.pdf (129 kb)
Bayesian inference tree of nine cranberry (V. macrocarpon); three V. oxycoccos; 11 other Vaccinium spp. from sections Cyanococcus, Vitis-idaea, and Batodendron; and 4 other Ericaceae species based on aligned nucelotide sequences with indels and microsatellite differences coded as binary characters and concatenated as a separate partition to the end of the aligned sequence matrix for six chloroplast SSR loci (CP3, CP8, CP12, CP14, CP16, CP17). Branch labels are posterior probabilities (PP) from Bayesian inference followed by bootstrap support (BS) by maximum likelihood (PDF 129 kb)
10722_2016_371_MOESM2_ESM.pdf (129 kb)
Bayesian inference tree of nine cranberry (V. macrocarpon); three V. oxycoccos; 11 other Vaccinium spp. from sections Cyanococcus, Vitis-idaea, and Batodendron; and four other Ericaceae species based on aligned nucelotide sequences with indels and microsatellite differences coded as binary characters and concatenated as a separate partition to the end of the aligned sequence matrix for two mitochondria SSR loci (MT6 and MT24). Branch labels are posterior probabilities (PP) from Bayesian inference followed by bootstrap support (BS) by maximum likelihood (PDF 128 kb)
10722_2016_371_MOESM3_ESM.pdf (117 kb)
Visualization of alleles of 24 chloroplast and mitochondrial SSR loci in the cranberry cultivar ‘Stevens’ amplified in multiplexing/poolplexing panel one (A) and panel two (B) with M13 FAM (Blue), HEX (Green), NED (Black), or PET (Red) labeled primers (PDF 117 kb)
10722_2016_371_MOESM4_ESM.docx (16 kb)
Supplementary material 4 (DOCX 16 kb)
10722_2016_371_MOESM5_ESM.docx (13 kb)
Supplementary material 5 (DOCX 12 kb)

References

  1. Alfaro ME, Zoller S, Lutzoni F (2003) Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol Biol Evol 20(2):255–266. doi: 10.1093/molbev/msg028 CrossRefPubMedGoogle Scholar
  2. Arroyo-García R, Ruiz-García L, Bolling L, Ocete R, López MA, Arnold C, Ergul A, Söylemezolu 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, Martinez-Zapater JM (2006) Multiple origins of cultivated grapevine (Vitis vinifera L. ssp. sativa) based on chloroplast DNA polymorphisms. Mol Ecol 15(12):3707–3714. doi: 10.1111/j.1365-294X.2006.03049.x CrossRefPubMedGoogle Scholar
  3. Bänfer G, Moog U, Fiala B et al (2006) A chloroplast genealogy of myrmecophytic Macaranga species (Euphorbiaceae) in Southeast Asia reveals hybridization, vicariance and long-distance dispersals. Mol Ecol 15(14):4409–4424. doi: 10.1111/j.1365-294X.2006.03064.x CrossRefPubMedGoogle Scholar
  4. Borchsenius F (2009) FastGap 1.2. Department of Biological Sciences. University of Aarhus, Aarhus, DenmarkGoogle Scholar
  5. Bruederle L, Hugan M, Dignan J, Vorsa N (1996) Genetic variation in natural populations of the large cranberry, Vaccinium macrocarpon Ait. (Ericaceae). Bull Torrey Bot Club 123:41–47CrossRefGoogle Scholar
  6. Camp W (1945) The North American blueberries with notes on other groups of Vacciniaceae. Brittonia 5:203–275. doi: 10.2307/2804880 CrossRefGoogle Scholar
  7. Darrow G, Camp W (1945) Vaccinium hybrids and the development of new horticultural material. Bull Torrey Bot Club 72:1–21CrossRefGoogle Scholar
  8. Dweikat IM, Lyrene PM (1988) Production and viability of unreduced gametes in triploid interspecific blueberry hybrids. Theor Appl Genet 76(4):555–559. doi: 10.1007/BF00260907 CrossRefPubMedGoogle Scholar
  9. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. doi: 10.1093/nar/gkh340 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fajardo D, Morales J, Zhu H, Steffan S, Harbut R, Bassil N, Hummer K, Polashock J, Vorsa N, Zalapa J (2012) Discrimination of American cranberry cultivars and assessment of clonal heterogeneity using microsatellite markers. Plant Mol Biol Report 31(2):1–8Google Scholar
  11. Fajardo D, Senalik D, Ames M, Zhu H, Steffan S, Harbut R, Polashock J, Vorsa N, Gillespie E, Kron K, Zalapa J (2013) Complete plastid genome sequence of Vaccinium macrocarpon: structure, gene content, and rearrangements revealed by next generation sequencing. Tree Genet Genomes 9(2):489–498. doi: 10.1007/s11295-012-0573-9 CrossRefGoogle Scholar
  12. Fajardo D, Schlautman B, Steffan S, Polashock J, Vorsa N, Zalapa J (2014) The American cranberry mitochondrial genome reveals the presence of selenocysteine (tRNA-Sec and SECIS) insertion machinery in land plants. Gene 536(2):336–343. doi: 10.1016/j.gene.2013.11.104 CrossRefPubMedGoogle Scholar
  13. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package). Distributed by the author.” Department of Genome Sciences, University of Washington, Seattle, Version 3Google Scholar
  14. Filiz E (2014) SSRs mining of Brassica species in mitochondrial genomes: bioinformatic approaches. Hortic Environ Biotechnol 54(6):548–553. doi: 10.1007/s13580-013-0026-x CrossRefGoogle Scholar
  15. Georgi L, Herai RH, Vidal R, Carazzolle M, Pereira G, Polashock J, Vorsa N (2011) Cranberry microsatellite marker development from assembled next-generation genomic sequence. Mol Breed 30(1):227–237. doi: 10.1007/s11032-011-9613-7 CrossRefGoogle Scholar
  16. Georgi L, Johnson-Cicalese J, Honig J, Das S, Rajah V, Bhattacharya D, Bassil N, Rowland L, Polashock J, Vorsa N (2013) The first genetic map of the American cranberry: exploration of synteny conservation and quantitative trait loci. Theor Appl Genet. 126(3):673–692. doi: 10.1007/s00122-012-2010-8 CrossRefPubMedGoogle Scholar
  17. Goldstein DB, Linares AR, Cavalli-Sforza LL, Feldman MW (1995) An evaluation of genetic distances for use with microsatellite loci. Genetics 139:463–471PubMedPubMedCentralGoogle Scholar
  18. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi: 10.1093/sysbio/syq010 CrossRefPubMedGoogle Scholar
  19. Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174CrossRefPubMedGoogle Scholar
  20. Iorizzo M, Senalik D, Szklarczyk M, Grzebelus D, Spooner D, Simon P (2012) De novo assembly of the carrot mitochondrial genome using next generation sequencing of whole genomic DNA provides first evidence of DNA transfer into an angiosperm plastid genome. BMC Plant Biol 12(1):61CrossRefPubMedPubMedCentralGoogle Scholar
  21. Islam MS, Studer B, Byrne SL, Farrell JD, Panitz F, Christian Bendixen C, Møller IM, Asp T (2013) The genome and transcriptome of perennial ryegrass mitochondria. BMC Genomics. doi: 10.1186/1471-2164-14-202 PubMedPubMedCentralGoogle Scholar
  22. Jacquemart A (1997) Vaccinium oxycoccos L. (Oxycoccus palustris Pers.) and Vaccinium microcarpum (Turcz. ex Rupr.) Schmalh. (Oxycoccus microcarpus Turcz. ex Rupr.). J Ecol 85:381–396CrossRefGoogle Scholar
  23. Kearse M, Moir R, Wilson A, Havas SS, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kron KA, Judd WS (1990) Phylogenetic relationships within the Rhodoreae (Ericaceae) with specific comments on the placement of Ledum. Syst Bot 15(1):57–68CrossRefGoogle Scholar
  25. Kron KA, Fuller R, Crayn DM, Gadek PA, Quinn CJ (1999) Phylogenetic relationships of epacrids and vaccinioids (Ericaceae s. l.) based on matK sequence data. Plant Syst Evol 218(1/2):55–65. doi: 10.1007/BF01087034 CrossRefGoogle Scholar
  26. Kron KA, Judd WS, Stevens PF, Crayn DM, Anderberg AA, Gadek PA, Quinn CJ, Luteyn JL (2002a) Phylogenetic classification of Ericaceae: molecular and morphological evidence. Bot Rev 68(3):335–423CrossRefGoogle Scholar
  27. Kron KA, Powell EA, Luteyn JL (2002b) Phylogenetic relationships within the blueberry tribe (Vaccinieae, Ericaceae) based on sequence data from MATK and nuclear ribosomal ITS regions, with comments on the placement of Satyria. Am J Bot 89(2):327–336CrossRefPubMedGoogle Scholar
  28. Kuntal H, Sharma V, Daniell H (2012) Microsatellite analysis in organelle genomes of Chlorophyta. Bioinformation 8(6):255–259. doi: 10.6026/97320630008255 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Liu Y, Liu S, Liu D, Wei Y, Liu C, Yang Y, Tao C, Liu W (2014) Exploiting EST databases for the development and characterization of EST-SSR markers in blueberry (Vaccinium) and their cross-species transferability in Vaccinium spp. Sci Hortic 176:319–329. doi: 10.1016/j.scienta.2014.07.026 CrossRefGoogle Scholar
  30. Lyrene PM (2011) First report of Vaccinium arboreum hybrids with cultivated highbush blueberry. HortSci 46(4):563–566Google Scholar
  31. Lyrene P, Vorsa N, Ballington J (2003) Polyploidy and sexual polyploidization in the genus Vaccinium. Euphytica 133(1):27–36CrossRefGoogle Scholar
  32. Martínez-Alberola F, Del Campo EM, Lázaro-Gimeno D, Mezquita Claramonte S, Molins A, Mateu Andreas I, Pedrola Monfort J, Casano LM, Barreno E (2013) Balanced gene losses, duplications and intensive rearrangements led to an unusual regularly sized genome in Arbutus unedo chloroplasts. PLoS One: e79685 doi:  10.1371/journal.pone.0079685
  33. Martins WS, Soares Lucas DC, De Souza Neves KF, Bertioli DJ (2009) WebSat: a web software for microsatellite marker development. Bioinformation 3:282–283CrossRefPubMedPubMedCentralGoogle Scholar
  34. Minch E, Ruiz-Linares A, Goldstein DB, Feldman MW, Cavalli-Sforza LL (1998) Microsat2: a computer program for calculating various statistics on microsatellite allele data. Department of Genetics, Stanford University, Stanford, CAGoogle Scholar
  35. Nishikawa T, Vaughan DA, Kadowaki KI (2005) Phylogenetic analysis of Oryza species, based on simple sequence repeats and their flanking nucleotide sequences from the mitochondrial and chloroplast genomes. Theor Appl Genet 110(4):696–705. doi: 10.1007/s00122-004-1895-2 CrossRefPubMedGoogle Scholar
  36. Odell EA, Vander Kloet SP (1991) The utility of stem characters in the classification of Vaccinium L. (Ericaceae). Taxon 40(2):273–283CrossRefGoogle Scholar
  37. Ozyigit II, Dogan I, Filiz E (2015) In silico analysis of simple sequence repeats (SSRs) in chloroplast genomes of Glycine species. Plant Omics 8(1):24–29Google Scholar
  38. Polashock J, Zelzion E, Fajardo D, Zalapa J, Georgi L, Bhattacharya D, Vorsa N (2014) The American cranberry: first insights into the whole genome of a species adapted to bog habitat. BMC Plant Biol 14:165CrossRefPubMedPubMedCentralGoogle Scholar
  39. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256. doi: 10.1093/molbev/msn083 CrossRefPubMedGoogle Scholar
  40. Powell E, Kron K (2002) Hawaiian blueberries and their relatives: a phylogenetic analysis of Vaccinium sections Macropelma, Myrtillus, and Hemimyrtillus (Ericaceae). Syst Bot 27(4):768–779. doi: 10.1043/0363-6445-27.4.768 Google Scholar
  41. Rambaut A (2015) FigTree. http://tree.bio.ed.ac.uk/software/figtree [Accessed 16 Aug 2015]
  42. Ravanko O (1990) The taxonomic value of morphological and cytological characteristics in Oxycoccus (subgenus of Vaccinium, Ericaceae) species in Finland. Ann Bot Fenn 27(3):235–239Google Scholar
  43. Ronquist F, Teslenko M, Der Van, Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542. doi: 10.1093/sysbio/sys029 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Rowland L, Dhanaraj A, Polashock J, Arora R (2003) Utility of blueberry-derived EST-PCR primers in related Ericaceae species. HortScience 38(7):1428–1432Google Scholar
  45. Schlautman B, Covarrubias-Pazaran G, Diaz-Garcia LA, Johnson-Cicalese J, Iorrizo M, Rodriguez-Bonilla L, Bougie TA, Bougie TC, Wiesman E, Steffan S, Polashock J, Vorsa N, Zalapa J (2015a) Development of a high-density cranberry SSR linkage map for comparative genetic analysis and trait detection. Mol Breed 35(8):1–18. doi: 10.1007/s11032-015-0367-5 CrossRefGoogle Scholar
  46. Schlautman B, Fajardo D, Bougie T, Wiesman E, Polashock J, Vorsa N, Steffan S, Zalapa J (2015b) Development and validation of 697 novel polymorphic genomic and EST-SSR markers in the American cranberry (Vaccinium macrocarpon Ait.). Molecules 20:2001–2013. doi: 10.3390/molecules20022001 CrossRefPubMedGoogle Scholar
  47. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18(2):1–2CrossRefGoogle Scholar
  48. Smith TW, Walinga C, Wang S, Kron P, Suda J, Zalapa J (2015) Evaluating the relationship between diploid and tetraploid Vaccinium oxycoccos L. (Ericaceae) in eastern Canada. Botany 93(10):623–636. doi: 10.1139/cjb-2014-0223 CrossRefGoogle Scholar
  49. Suda J, Lysák MA (2001) A taxonomic study of the Vaccinium sect. Oxycoccus (Hill) W.D.J. Koch (Ericaceae) in the Czech Republic and adjacent territories. Folia Geobot 36(3):303–320. doi: 10.1007/BF02803183 CrossRefGoogle Scholar
  50. Tomar RSS, Deshmukh RK, Naik KB, Tomar SMS (2014) Development of chloroplast-specific microsatellite markers for molecular characterization of alloplasmic lines and phylogenetic analysis in wheat. Plant Breed 133(1):12–18. doi: 10.1111/pbr.12116 CrossRefGoogle Scholar
  51. Trehane J (2004) Blueberries, Cranberries, and other Vacciniums. Timber Press, PortlandGoogle Scholar
  52. Vander Kloet SP (1983a) The taxonomy of Vaccinium section Oxycoccus. Rhodora 85(841):1–43. doi: 10.1002/0470011815.b2a13070 Google Scholar
  53. Vander Kloet SP (1983b) The taxonomy of Vaccinium section Cyanococcus: a summation. Can J Bot 61(1):256–266CrossRefGoogle Scholar
  54. Vander Kloet SP (1988) The genus Vaccinium in North America. Canadian Government Publishing Centre, OttawaGoogle Scholar
  55. Vander Kloet SP, Avery TS (2010) Vaccinium on the edge. Edinburgh J Bot 67:7–24CrossRefGoogle Scholar
  56. Von Cräutlein M, Korpelainen H, Helander M, Väre H, Saikkonen K (2014) Development and characterization of chloroplast microsatellite markers in a fine-leaved fescue, Festuca rubra (Poaceae). Appl Plant Sci. doi: 10.3732/apps.1400094 Google Scholar
  57. Wang Q, Zhang Y, Fang Z, Liu Y, Yang L, Zhuang M (2012) Chloroplast and mitochondrial SSR help to distinguish allo-cytoplasmic male sterile types in cabbage (Brassica oleracea L. var. capitata). Mol Breed 30(2):709–716. doi: 10.1007/s11032-011-9656-9 CrossRefGoogle Scholar
  58. Wheeler GL, Dorman HE, Buchanan A, Challagundla L, Wallace LE (2014) A review of the prevalence, utility, and caveats of using chloroplast simple sequence repeats for studies of plant biology. Appl Plant Sci. doi: 10.3732/apps.1400059 PubMedPubMedCentralGoogle Scholar
  59. Woloszynska M (2009) Heteroplasmy and stoichiometric complexity of plant mitochondria genomes—though this be madness, there’s method in’t. Exp Bot 61:657–671. doi: 10.1093/jxb/erp361 CrossRefGoogle Scholar
  60. Zalapa JE, Bougie TC, Bougie TA, Schlautman BJ, Wiesman E, Guzman A, Fajardo DA, Steffan S, Smith T (2015) Clonal diversity and genetic differentiation revealed by SSR markers in wild Vaccinium macrocarpon and Vaccinium oxycoccos. Ann Appl Biol 166(2):196–207. doi: 10.1111/aab.12173 CrossRefGoogle Scholar
  61. Zhu H, Senalik D, McCown BH, Zeldin EL, Speers J, Hyman J, Bassil N, Hummer K, Simon PW, Zalapa JE (2012) Mining and validation of pyrosequenced simple sequence repeats (SSRs) from American cranberry (Vaccinium macrocarpon Ait.). Theor Appl Genet 124(1):87–96. doi: 10.1007/s00122-011-1689-2 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2016

Authors and Affiliations

  • Brandon Schlautman
    • 1
    • 2
  • Giovanny Covarrubias-Pazaran
    • 1
  • Diego Fajardo
    • 3
  • Shawn Steffan
    • 2
  • Juan Zalapa
    • 1
    • 2
  1. 1.Department of HorticultureUniversity of WisconsinMadisonUSA
  2. 2.USDA-ARS, Vegetable Crops Research UnitUniversity of WisconsinMadisonUSA
  3. 3.National Center for Genome ResourcesSanta FeUSA

Personalised recommendations