Abstract
Cranberry (Vaccinium macrocarpon Ait.) breeding is evolving as consumer demand increases for specialty products such as sweetened and dried cranberries. New varieties are needed with not only higher yield and better adaptations to biotic (e.g., fungal fruit rot) and abiotic (e.g., cold tolerance) stressors, but also with increased fruit quality for processing and human nutrition. Cranberry is one of the few species in the genus Vaccinium that is utilized as a crop. However, the genus is composed of many understudied and underused species, such as wild blueberries and cranberries, lingonberries, and deerberries. Many of these species are cross-compatible and possess an array of traits of high agronomical value that may be commercially exploited through intrasectional or intersectional interspecific breeding. In order to provide a toolset for Vaccinium breeders, we tested the cross-transferability of 507 V. macrocarpon simple sequence repeat (SSR) markers on 17 different Vaccinium species. We found 61 SSR markers that consistently amplified and produced scorable bands across all 17 species tested. The ability of the markers to discriminate species based on their genetic relationships was tested for future use in phylogenetics. We genetically discriminated the different species and sections of the genus, providing an insightful look into the genetic relationship of species in this genus. These markers represent a working set of SSRs to use for the development of Vaccinium interspecific hybrids and to allow the development of population genetic studies of poorly understood species.
Similar content being viewed by others
References
Alston JM, Medellín-Azuara J, Saitone TL (2014) Economic impact of the North American cranberry industry. University of California, Davis
Bache SM, Wickham H (2014) magrittr: a forward-pipe operator for R. R Package Version 1:1
Ballington JR (2008) The role of interspecific hybridization in blueberry improvement. XI Int Vaccinium Symp 810:49–60
Ballington JR et al (1990) Germplasm resources available to meet future needs for blueberry cultivar improvement. Fruit Var J 44:54–62
Barbara T, Palma-Silva C, Paggi GM, Bered F, Fray MF, Lexer C (2007) Cross-species transfer of nuclear microsatellite markers: potential and limitations. Mol Ecol 16:3759–3767
Bassil N, Oda A, Hummer KE (2008) Blueberry microsatellite markers identify cranberry cultivars. Acta Hortic 810:181–187
Bian Y, Ballington J, Raja A, Brouver C, Reid R, Burke M, Wang X, Rowland LJ, Bassil N, Brown A (2014) Patterns of simple sequence repeats in cultivated blueberries (Vaccinium section Cyanococcus spp.) and their use in revealing genetic diversity and population structure. Mol Breed 34:675–689
Bidani A, Hummer KE, Rowland LJ, Bassil NV (2016) Development of an efficient DNA test for genetic identity confirmation in blueberry. In: XI international Vaccinium symposium 1180. actahort.org, pp 363–368
Boches P (2005) Microsatellite marker development and molecular characterization in highbush blueberry (Vaccinium corymbosum L.) and Vaccinium species. M.S. Dissertation, Oregon State University, Corvallis, USA
Boches PS, Bassil NV, Rowland LJ (2005) Microsatellite markers for Vaccinium from EST and genomic libraries. Mol Ecol Notes 5:657–660
Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by taq DNA polymerase: primer modifications that facilitate genotyping. Biotechiques 20(6):1004–1010
Bruvo R, Michiels NK, D’Souza TG, Schulenburg H (2004) A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol Ecol 13:2101–2106
Bujor O-C, Ginies C, Popa VI, Dufour C (2018) Phenolic compounds and antioxidant activity of lingonberry (Vaccinium vitis-idaea L.) leaf, stem and fruit at different harvest periods. Food Chem 252:356–365
Česonienė L, Daubaras R, Areškevičiūtė J, Viškelis P (2006) Evaluation of morphological peculiarities, amount of total phenolics and anthocyanins in berries of European Cranberry (Oxycoccus palustris). Baltic For 12:59–63
Česonienė L, Daubaras R, Jasutienė I, Venclovienė J, Miliauskienė I (2011) Evaluation of the biochemical components and chromatic properties of the juice of Vaccinium macrocarpon aiton and Vaccinium oxycoccos L. Plant Foods Hum Nutr 66:238–244
Clark LV, Jasieniuk M (2011) POLYSAT: an R package for polyploid microsatellite analysis. Mol Ecol Resour 11:562–566
Covarrubias-Pazaran G, Diaz-Garcia L, Schlautman B, Deutsch J, Salazar W, Hernandez-Ochoa M, Gryglesk E, Steffan S, Iorizzo M, Polashock J, Zalapa JE, Vorsa N (2016) Exploiting genotyping by sequencing to characterize the genomic structure of the American cranberry through high-density linkage mapping. BMC Genom 17:451
Darrow GM, Camp WH (1945) Vaccinium hybrids and the development of new horticultural material. Bull Torrey Bot Club 72:1–21
Darrow GM, Scott DH, Dermen H (1954) Tetraploid blueberries from hexaploid x diploid species crosses. Proc Am Soc Hortic Sci 63:266–270
Daverdin G, Johnson-Cicalese J, Zalapa J, Vorsa N, Polashock J (2017) Identification and mapping of fruit rot resistance QTL in American cranberry using GBS. Mol Breed 37(3):38
Diaz-Garcia L, Rodriguez-Bonilla L, Rohde J et al (2019) Pacbio sequencing reveals identical organelle genomes between American Cranberry (Vaccinium macrocarpon Ait.) and a wild relative. Genes. https://doi.org/10.3390/genes10040291
Doyle JJ, Doyle JL (1987) CTAB DNA extraction in plants. Phytochem Bull 19:11–15
Draper AD (1977) Tetraploid hybrids from crossed of diploid, tetraploid and hexaploid Vaccinium species. Acta Hort 61:33–37
Dray S, Dufour A-B et al (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
Fajardo D, Morales J, Zhu H, Steffan S, Harbut R, Bassil N, Hummer K, Polashock Vorsa N, Zalapa JE (2013) Discrimination of American Cranberry cultivars and assessment of clonal heterogeneity using microsatellite markers. Plant Mol Biol Rep 31(2):264–271
Fajardo D, Schlautman B, Steffan S, Polashock 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
FAOSTAT (1998) Food and Agriculture Organization of the United Nations. FAOSTAT database
Gallardo R, Zhang Q, Polashock JJ, Rodriguez-Soana C, Vorsa N, Atucha A, Zalapa JE, Iorizzo M (2018) Breeding trait priorities of the cranberry industry in the United States and Canada. HortScience 53(10):1467–1474
Galletta GJ, Ballington JR (1996) Blueberries, cranberries and lingonberries. Fruit Breed 2:107
Georgi L, Herai RH, Vidal R et al (2011) Cranberry microsatellite marker development from assembled next-generation genomic sequence. Mol Breed 30:227–237
Hancock J, Lyrene P, Finn C et al (2008) Blueberries and cranberries. pp 115–150
Hokkanen J, Mattila S, Jaakola L, Pirttilä AM, Tolonen A (2009) Identification of phenolic compounds from lingonberry (Vaccinium vitis-idaea L.), bilberry (Vaccinium myrtillus L.) and hybrid bilberry (Vaccinium x intermedium Ruthe L.) leaves. J Agric Food Chem 57(20):9437–9447
Hosseinzadeh-Colagar A, Haghighatnia MJ, Amiri Z, Mohadjerani M, Tafrihi M (2016) Microsatellite (SSR) amplification by PCR usually led to polymorphic bands: evidence which shows replication slippage occurs in extend or nascent DNA strands. Mol Biol Res Commun 5(3):167–174
Jacquemart AL (1997) Vaccinium Oxycoccos L. (Oxycoccus Palustris Pers.) and Vaccinium Microcarpum (Turcz. ex Rupr.) Schmalh. (Oxycoccus Microcarpus Turcz. ex Rupr.). J Ecol 85:381–396
John ME (1992) An efficient method for isolation of RNA and DNA from plants containing polyphenolics. Nucleic Acids Res 20:2381
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405
Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281
Kron KA, Judd WS, Stevens PF, Crayn AA, Anderberg PA, Gadek PA, Quinn CJ, Luteyn JL (2002) Phylogenetic classification of ericaceae: molecular and morphological evidence. Bot Rev 68(3):335–423
Liu Y-C, Liu S, Liu DC, Wei YX, Liu C, Yang YM, Tao CG, Liu WS (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
Luby JJ, Ballington JR, Draper AD, Kazimierz P, Austin ME (1991) Blueberries and cranberries (Vaccinium). Genet Resour Temp Fruit Nut Crops 290:393–458
Mahy G, Bruederle LP, Connors B, Hofwegen Van, Vorsa N (2000) Allozyme evidence for genetic autopolyploidy and high genetic diversity in tetraploid cranberry, Vaccinium oxycoccos (Ericaceae). Am J Bot 87:1882–1889
McCallum S, Graham J, Jorgensen L, Rowland LJ, Bassil NV, Hancock JF, Wheeler EJ, Vining K, Poland JA, Olmstead JW, Buck E (2016) Construction of a SNP and SSR linkage map in autotetraploid blueberry using genotyping by sequencing. Mol Breed 36(4):41
Ortiz R, Vorsa N, Bruederle LP, Laverty T (1992) Occurrence of unreduced pollen in diploid blueberry species Vaccinium sect. Cyanococcus. Theor Appl Genet 85:55–60
Paradis E (2010) pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26:419–420
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
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
Polashock J, Zelzion E, Fajardo D, Zalapa JE, 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(1):165
R Core Team (2018) R: A language and environment for statistical computing. R Found Stat Comput, Vienna
Rowland LJ, Ogden EL, Bassil N, Buck EJ, McCallum S, Graham J, Brown A, Wiedow C, Campbell AM, Haynes KG, Vinyard BT (2014) Construction of a genetic linkage map of an interspecific diploid blueberry population and identification of QTL for chilling requirement and cold hardiness. Mol Breed 34(4):2033–2048
Schlautman B (2016) Accelerating Domestication and Genetic Gain in the American Cranberry (Vaccinium Macrocarpon Ait.): New Genetic and Genomic Resources for the Cranberry Breeders’ Toolbox. Ph.D. thesis University of Wisconsin-Madison
Schlautman B, Fajardo D, Bougie T, Wiesman E, Vorsa N, Steffan S, Zalapa J (2015) Development and validation of 697 novel polymorphic genomic and EST-SSR markers in the American cranberry (Vaccinium macrocarpon Ait). Molecules 20(2):2001–2013
Schlautman B, Covarrubias-Pazaran G, Diaz-Garcia L, Iorizzo M, Polashock J, Grygleski E, Vorsa N, Zalapa J (2017a) Construction of a high-density American cranberry (Vaccinium macrocarpon Ait.) composite map using genotyping-by-sequencing for multi-pedigree linkage mapping. G3: Genes Genomes Genet 7:1177–1189
Schlautman B, Covarrubias-Pazaran G, Fajardo D, Steffan S, Zalapa J (2017b) Discriminating power of microsatellites in cranberry organelles for taxonomic studies in Vaccinium and Ericaceae. Genet Resour Crop Evol 64(3):451–466
Schlautman B, Diaz-Garcia L, Covarrubias-Pazaran G, Schlautman N, Vorsa N, Polashock J, Ogden EL, Brown A, Lin YC, Bassil N, Buck EJ (2018) Comparative genetic mapping reveals synteny and collinearity between the American cranberry and diploid blueberry genomes. Mol Breed 38(1):9
Schuelke M (2002) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18(2):233
Scott LJ, Shepherd M, Henry RJ (2003) Characterization of highly conserved microsatellite loci in Araucaria cunninghamii and related species. Plant Syst Evol 236:115–123
Sharp RH, Darrow GM (1959) Breeding blueberries for the Florida climate. Proc Florida State Hortic Soc 72:308–311
Smith TW, Walinga C, Wang S, Kron P, Suda J, Zalapa J (2015) Evaluating the relationship between diploid and tetraploid Vaccinium oxycoccos (Ericaceae) in eastern Canada. Botany 93(10):623–636
Song G-Q, Hancock JF (2011) Vaccinium. In: Wild crop relatives: genomic and breeding resources: Temperate Fruit
Suda J (2003) Sympatric occurrences of various cytotypes of Vaccinium sect. Oxycoccus (Ericaceae). Nord J Bot 22:593–601
Suda J, Lysák MA (2001) A taxonomic study of the Vaccinium sect. Oxycoccus (Hill) WDJ Kock (Ericaceae) in the Czech Republic and adjacent territories. Folia Geobot 36:303–320
Vander Kloet SP (1983) The taxonomy of Vaccinium oxycoccus. Rhodora 85:1–43
Vander Kloet SP (1988) The genus Vaccinium in North America. Agriculture Canada
Vander Kloet SP, Dickinson TA (1999) The taxonomy of Vaccinium section Myrtillus (Ericaceae). Brittonia 51:231–254
Vorsa N (1996) On a wing: the genetics and taxonomy of Vaccinium species from a pollination perspective. VI Int Symp Vaccinium Cult 446:59–66
Vorsa N, Johnson-Cicalese J (2012) American Cranberry. In: Fruit breeding. Springer US, Boston, MA, 191–223
Vorsa N, Polashock J (2005) Alteration of anthocyanin glycosylation in cranberry through interspecific hybridization. J Am Soc Hortic Sci 130(5):711–715
Vorsa N, Johnson-Cicalese J, Polashock J (2009) A blueberry cranberry hybrid derived from a Vaccinium darrowii x (V. macrocarpon x V. oxycoccos) intersectional cross. IX Int Vaccinium Symp 810:187–190
Zalapa JE, Cuevas H, Zhu H, Steffan S et al (2012) Using next-generation sequencing approaches to isolate simple sequence repeat (SSR) loci in the plant sciences. Am J Bot 99(2):193–208
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
Zhu H, Senalik D, McCown BH, Zeldin EL, Speers J, Bassil N et al (2012) Mining and validation of pyrosequenced simple sequence repeats (SSRs) from American cranberry (Vaccinium macrocarpon Ait.). Theor Appl Genet 124:87–96
Acknowledgements
We are grateful to Drs. Jennifer Johnson-Cicalese and Nicholi Vorsa from Rutgers, The State University of New Jersey, and the Philip E. Marucci Center for Blueberry and Cranberry, Chatsworth NJ and Dr. Kim Hummer and staff of the United States Department of Agriculture National Clonal Germplasm Repository at Corvallis, OR for the samples supplied for this research. We thank UW-Madison and the Cranberry Genetics and Genomics Lab members for their contributions, especially Walter Salazar and Giovanny Eduardo Covarrubias Pazaran. We also thank the anonymous reviewers who helped enhance the quality of this paper. JZ would like to express his gratitude through Ps 136:1.
Funding
This project was supported by USDA-ARS (Project No. 5090-21220-004-00-D provided to JZ); WI-DATCP (SCBG Project #14-002); Ocean Spray Cranberries, Inc.; Wisconsin Cranberry Growers Association; Cranberry Institute. LRB was supported in part by the UW Madison SciMed GRS.
Author information
Authors and Affiliations
Contributions
LRB and JZ design the study; JZ provided plant material; LRB performed the experiment; LRB DM and JR analyzed the data; LRB and JZ wrote the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rodriguez-Bonilla, L., Rohde, J., Matusinec, D. et al. Cross-transferability analysis of SSR markers developed from the American Cranberry (Vaccinium macrocarpon Ait.) to other Vaccinium species of agricultural importance. Genet Resour Crop Evol 66, 1713–1725 (2019). https://doi.org/10.1007/s10722-019-00826-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10722-019-00826-1