Advertisement

Molecular Breeding

, Volume 34, Issue 4, pp 2033–2048 | Cite as

Construction of a genetic linkage map of an interspecific diploid blueberry population and identification of QTL for chilling requirement and cold hardiness

  • Lisa J. Rowland
  • Elizabeth L. Ogden
  • Nahla Bassil
  • Emily J. Buck
  • Susan McCallum
  • Julie Graham
  • Allan Brown
  • Claudia Wiedow
  • A. Malcolm Campbell
  • Kathleen G. Haynes
  • Bryan T. Vinyard
Article

Abstract

A genetic linkage map has been constructed from an interspecific diploid blueberry population [(Vaccinium darrowii Fla4B × Vaccinium corymbosum W85-20) F1#10 × V. corymbosum W85-23] designed to segregate for cold hardiness and chilling requirement. The map is comprised of 12 linkage groups (equivalent to the haploid chromosome number of diploid blueberry) and totals 1,740 cM. Included on the map are 265 markers based on simple sequence repeats, expressed sequence tag-polymerase chain reactions, single nucleotide polymorphisms, and randomly amplified polymorphic DNAs. The estimated map coverage is 89.9 %, and the average distance between markers is 7.2 cM. The mapping population was evaluated for 2 years (2009 and 2010) for mid-winter bud cold hardiness and for 3 years (2011–2013) for chilling requirement under controlled conditions. Broad-sense heritability of both cold hardiness and chilling requirement was quite high under these conditions with values of 0.88 and 0.86, respectively. One quantitative trait locus/loci (QTL) for cold hardiness and one for chilling requirement were identified that were consistent over at least 2 years. A second weaker QTL for chilling requirement was detected in only one of the 3 years.

Keywords

EST-PCR SNP SSR Markers Vaccinium corymbosum Vaccinium darrowii 

Abbreviations

CH

Cold hardiness

CR

Chilling requirement

CR50

Chill units resulting in 50 % floral bud break

EST-PCR

Expressed sequence tag-polymerase chain reaction

H

Broad-sense heritability

HRM

High-resolution melting

IM

Interval mapping

LOD

Logarithm of the odds

LT50

Lethal temperature causing 50 % injury

PM

Permutation test

QTL

Quantitative trait locus/loci

RAPD

Randomly amplified polymorphic DNA

rMQM

Restricted multiple QTL mapping

SNP

Single nucleotide polymorphism

SRA

Sequence read archive

SSR

Simple sequence repeat

Notes

Acknowledgments

The authors gratefully acknowledge all the high school and college students who participated in this project as part of an internship or other training opportunity. We specifically would like to acknowledge the students from the University of Maryland (Brianna Driscoll, Dana Robinson, and Jenny Lindvall), who worked in Dr. Rowland’s lab on the mapping project, and the students from Davidson College (Mark Angel, Erich Baker, Spencer Chadinha, Stewart Dalton, Aaron Deal, Catherine Doyle, Tim Keating, David Lloyd, Austin Mudd, Mike Nuttle, Shamita Punjabi, and Daniel Tuerff), who worked in Dr. Campbell’s class to design SSRs near genes of interest. We would also like to thank Barbara Gilmore, April Nyberg, Elisabeth Alperin, and Jeremy Jones, who were involved in screening the mapping parents for SSR polymorphism. This project was partially funded by USDA-ARS Project 1245-21000-185-00D and USDA-CSREES Specialty Crop Research Initiative Grant 2008-51180-04861 entitled ‘Generating Genomic Tools for Blueberry Improvement.’ Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture or any of the other agencies involved in this research.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11032_2014_161_MOESM1_ESM.xlsx (41 kb)
Supplementary material 1 (XLSX 40 kb)
11032_2014_161_MOESM2_ESM.docx (12 kb)
Supplementary material 2 (DOCX 11 kb)

References

  1. Arora R, Rowland LJ, Lehman JS, Lim CC, Panta GR, Vorsa N (2000) Genetic analysis of freezing tolerance in blueberry (Vaccinium section Cyanococcus). Theor Appl Genet 100:690–696Google Scholar
  2. Arora R, Rowland LJ, Ogden EL, Dhanaraj AL, Marian CO, Ehlenfeldt MK, Vinyard B (2004) Dehardening kinetics, bud development, and dehydrin metabolism in blueberry (Vaccinium spp.) cultivars during deacclimation at constant, warm temperatures. J Am Soc Hortic Sci 129:667–674Google Scholar
  3. Avia K, Pilet-Nayel M-L, Bahrman N, Baranger A, Delbreil B, Fontaine V, Hamon C, Hanocq E, Niarquin M, Sellier H, Vuylsteker C, Prosperi J-M, Lejeune-Henaut I (2013) Genetic variability and QTL mapping of freezing tolerance and related traits in Medicago truncatula. Theor Appl Genet 126:2353–2366PubMedGoogle Scholar
  4. Basu A, Du M, Leyva MJ, Sanchez K, Betts NM, Wu M, Aston CE, Lyons TJ (2010) Blueberries decrease cardiovascular risk factors in obese men and women with metabolic syndrome. J Nutr 140:1582–1587PubMedCentralPubMedGoogle Scholar
  5. Bielenberg DG, Wang Y, Fan S, Reighard GL, Scorza R, Abbott AG (2004) A deletion affecting several gene candidates is present in the evergrowing peach mutant. J Hered 95:436–444PubMedGoogle Scholar
  6. Bielenberg DG, Wang Y, Li Z, Zhebentyayeva T, Fan S, Reighard GL, Scorza R, Abbott AG (2008) Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet Genomes 4:495–507Google Scholar
  7. Boches P, Bassil NV, Rowland LJ (2006) Genetic diversity in the highbush blueberry Vaccinium corymbosum L. evaluated with microsatellite markers. J Am Soc Hortic Sci 131:674–686Google Scholar
  8. Bushakra JM, Stephens MJ, Atmadjaja AN, Lewers KS, Symonds VV, Udall JA, Chagne D, Buck EJ, Gardiner SE (2012) Construction of black (Rubus occidentalis) and red (R. idaeus) raspberry linkage maps and their comparison to the genomes of strawberry, apple, and peach. Theor Appl Genet 125:311–327PubMedGoogle Scholar
  9. Cao K, Wang L, Zhu G, Fang W, Chen C, Luo J (2012) Genetic diversity, linkage disequilibrium, and association mapping analyses of peach (Prunus persica) landraces in China. Tree Genet Genomes 8:975–990Google Scholar
  10. Celton JM, Martinez S, Jammes MJ, Bechti A, Salvi S, Legave JM, Costes E (2011) Deciphering the genetic determinism of bud phenology in apple progenies: a new insight into chilling and heat requirement effects on flowering dates and positional candidate genes. N Phytol 192:378–392Google Scholar
  11. Chagne D, Gasic K, Crowhurst RN, Han Y, Bassett HC, Bowatte DR, Lawrence TJ, Rikkerink EHA, Gardiner SE, Korban SS (2008) Development of a set of SNP markers present in expressed genes of the apple. Genomics 92:353–358PubMedGoogle Scholar
  12. Chakravarti A, Lasher LK, Reefer JE (1991) A maximum likelihood method for estimating genome length using genetic linkage data. Genetics 128:175–182PubMedCentralPubMedGoogle Scholar
  13. Cho E, Seddon JM, Rosner B, Willett WC, Hankinson SE (2004) Prospective study of intake of fruits, vegetables, vitamins and carotenoids and risk of age-related maculopathy. Arch Ophthalmol 122:883–892PubMedGoogle Scholar
  14. De Vicente MC, Tanksley S (1993) QTL analysis of transgressive segregation in an interspecific tomato cross. Genetics 134:585–596Google Scholar
  15. Dhanaraj AL, Slovin JP, Rowland LJ (2004) Analysis of gene expression associated with cold acclimation in blueberry floral buds using expressed sequence tags. Plant Sci 166:863–872Google Scholar
  16. Dhanaraj AL, Alkharouf NW, Beard HS, Chouikha IB, Matthews BF, Wei H, Arora R, Rowland LJ (2007) Major differences observed in transcript profiles of blueberry during cold acclimation under field and cold room conditions. Planta 225:735–751PubMedGoogle Scholar
  17. Eckert AJ, Bower AD, Wegrzyn JL, Pande B, Jermstad KD, Krutovsky KV, Clair JBS, Neale DB (2009a) Association genetics of coastal Douglas fir (Pseudotsuga menziesu var. menziesii, Pinaceae). I. Cold-hardiness related traits. Genetics 182:1289–1302PubMedCentralPubMedGoogle Scholar
  18. Eckert AJ, Wegrzyn JL, Pande B, Jermstad KD, Lee JM, Liechty JD, Tearse BR, Krutovsky KV, Neale DB (2009b) Multilocus patterns of nucleotide diversity and divergence reveal positive selection at candidate genes related to cold hardiness in coastal Douglas fir (Pseudotsuga menziesu var. menziesii). Genetics 183:289–298PubMedCentralPubMedGoogle Scholar
  19. Fan S, Bielenberg DG, Zhebentyayeva TN, Reighard GL, Okie WR, Holland D, Abbott AG (2010) Mapping quantitative trait loci associated with chilling requirement, heat requirement and bloom date in peach (Prunus persica). N Phytol 185:917–930Google Scholar
  20. Fear CD, Lauer FI, Luby JJ, Stucker RL, Stushnoff C (1985) Genetic components of variance for winter injury, fall growth cessation, and off-season flowering in blueberry progenies. J Am Soc Hortic Sci 110:262–266Google Scholar
  21. Fisk SP, Cuesta-Marcos A, Cistue L, Russell J, Smith KP, Baenziger S, Bedo Z, Corey A, Filichkin T, Karsai I, Waugh R, Hayes PM (2013) FR-H3: a new QTL to assist in the development of fall-sown barley with superior low temperature tolerance. Theor Appl Genet 126:335–347PubMedGoogle Scholar
  22. Flinn CL, Ashworth EN (1994) Blueberry flower hardiness is not estimated by differential thermal analysis. J Am Soc Hortic Sci 119:295–298Google Scholar
  23. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690PubMedCentralPubMedGoogle Scholar
  24. Francia E, Rizza F, Cattivelli L, Stanca AM, Galiba G, Toth B, Hayes PM, Skinner JS, Pecchioni N (2004) Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) × ‘Tremois’ (spring) barley map. Theor Appl Genet 108:670–680PubMedGoogle Scholar
  25. Francia E, Barabaschi D, Tondelli A, Laido G, Rizza F, Stanca AM, Busconi M, Fogher C, Stockinger EJ, Pecchioni N (2007) Fine mapping of a HvCBF gene cluster at the frost resistance locus Fr-H2 in barley. Theor Appl Genet 115:1083–1091PubMedGoogle Scholar
  26. Galiba G, Quarrie SA, Sutka J, Morgounov A, Snape JW (1995) RFLP mapping of vernalization (Vrn1) and frost resistance (Fr1) on chromosome 5A of wheat. Theor Appl Genet 90:1174–1179PubMedGoogle Scholar
  27. Galletta GJ, Ballington JR (1996) Blueberries, cranberries and lingonberries. In: Janick J, Moore JN (eds) Fruit breeding. Vine and small fruit crops, vol II. Wiley, New York, pp 1–107Google Scholar
  28. Georgi L, Johnson-Cicalese J, Honig J, Das SP, Rajah VD, Bhattacharya D, Bassil N, Rowland LJ, Polashock J, Vorsa N (2013) The first genetic map of the American cranberry: exploration of synteny conservation and quantitative trait loci. Theor Appl Genet 126:673–692PubMedGoogle Scholar
  29. Holland JB, Nyquist WE, Cervantes-Martinez CT (2003) Estimating and interpreting heritability for plant breeding: an update. Plant Breed Rev 22:9–112Google Scholar
  30. Holliday JA, Ritland K, Aitken SN (2010) Widespread, ecologically relevant genetic markers developed from association mapping of climate-related traits in Sitka spruce (Picea sitchensis). N Phytol 188:501–514Google Scholar
  31. Howe GT, Saruul P, Davis J, Chen THH (2000) Quantitative genetics of bud phenology, frost damage, and winter survival in an F2 family of hybrid poplars. Theor Appl Genet 101:632–642Google Scholar
  32. Howe GT, Aitken SN, Neale DB, Jermstad KD, Wheeler NC, Chen THH (2003) From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Can J Bot 81:1247–1266Google Scholar
  33. Jaakola L, Maatta K, Pirttila AM, Torronen R, Karenlampi S, Hohtola A (2002) Expression of genes involved in anthocyanin biosynthesis in relation to anthocyanin, proanthocyanidin, and flavonol levels during bilberry fruit development. Plant Phys 130:729–739Google Scholar
  34. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106PubMedGoogle Scholar
  35. Jermstad KD, Bassoni DL, Wheeler NC, Anekonda TS, Aitken SN, Adams WT, Neale DB (2001) Mapping of quantitative loci controlling adaptive traits in coastal Douglas-fir. II. Spring and fall cold-hardiness. Theor Appl Genet 102:1152–1158Google Scholar
  36. Jermstad KD, Bassoni DL, Jech KS, Ritchie GA, Wheeler NC, Neale DB (2003) Mapping of quantitative loci controlling adaptive traits in coastal Douglas Fir. III. Quantitative trait loci-by-environment interactions. Genetics 165:1489–1506PubMedCentralPubMedGoogle Scholar
  37. Jimenez S, Li Z, Reighard GL, Bielenberg DG (2010) Identification of genes associated with growth cessation and bud dormancy entrance using a dormancy-incapable tree mutant. BMC Plant Biol 10:25PubMedCentralPubMedGoogle Scholar
  38. Kalt W, Joseph JA, Shukitt-Hale B (2007) Blueberries and human health. A review of the current research. J Am Pomol Soc 61:151–160Google Scholar
  39. Knapp SJ, Stroup WW, Ross WM (1985) Exact confidence intervals for heritability on a progeny mean basis. Crop Sci 25:192–194Google Scholar
  40. Knox AK, Dhillon T, Cheng H, Tondelli A, Pecchioni N, Stockinger EJ (2010) CBF gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals. Theor Appl Genet 121:21–35PubMedGoogle Scholar
  41. Krebs SL, Hancock JF (1988) The consequences of inbreeding on fertility in Vaccinium corymbosum L. J Am Soc Hortic Sci 113:914–918Google Scholar
  42. Leida C, Romeu JF, Garcia-Brunton J, Rios G, Badenes ML (2012) Gene expression analysis of chilling requirements for flower bud break in peach. Plant Breed 131:329–334Google Scholar
  43. Lewers KS, Crane EH, Bronson CR, Schupp JM, Keim P, Shoemaker RC (1999) Detection of linked QTL for soybean brown stem rot resistance in ‘BSR 101’ as expressed in a growth chamber environment. Mol Breed 5:33–42Google Scholar
  44. Li Z, Reighard GL, Abbott AG, Bielenberg DG (2009) Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J Exp Bot 60:3521–3530PubMedCentralPubMedGoogle Scholar
  45. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406PubMedCentralPubMedGoogle Scholar
  46. Manly BFJ (1997) Randomization, bootstrap and Monte Carlo methods in biology, 2nd edn. Chapman & Hall, LondonGoogle Scholar
  47. Montgomery J, Wittwer CT, Palais R, Zhou L (2007) Simultaneous mutation scanning and genotyping by high-resolution DNA melting analysis. Nat Protoc 2:59–66PubMedGoogle Scholar
  48. Naik D, Dhanaraj AL, Arora R, Rowland LJ (2007) Identification of genes associated with cold acclimation in blueberry (Vaccinium corymbosum L.) using a subtractive hybridization approach. Plant Sci 173:213–222Google Scholar
  49. Polashock JJ, Arora R, Peng Y, Naik D, Rowland LJ (2010) Functional identification of a C-repeat binding factor transcriptional activator from blueberry associated with cold acclimation and freezing tolerance. J Am Soc Hortic Sci 135:40–48Google Scholar
  50. Prior RL, Cao GH, Martin A, Sofic E, McEwen J, O’Brien C, Lischner N, Ehlenfeldt M, Kalt W, Krewer G, Mainland CM (1998) Antioxidant capacity as influenced by total phenolic and anthocyanin content, maturity, and variety of Vaccinium species. J Agric Food Chem 46:2686–2693Google Scholar
  51. Qu L, Hancock JF (1997) Randomly amplified polymorphic DNA- (RAPD-) based genetic linkage map of blueberry derived from an interspecific cross between diploid Vaccinium darrowii and tetraploid V. corymbosum. J Am Soc Hortic Sci 122:69–73Google Scholar
  52. Quero-Garcia J, Le Dantec L, Fodor A, Reignier A, Capdevilla G, Joly J, Tauzin Y, Fouilhaux L, Dirlewanger E (2010) QTL detection for fruit quality and phenological characters in sweet cherry. In: 5th international rosaceae genomics conference, Stellenbosch, South AfricaGoogle Scholar
  53. Reed GH, Wittwer CT (2004) Sensitivity and specificity of single-nucleotide polymorphism scanning by high-resolution melting analysis. Clin Chem 50:1748–1754PubMedGoogle Scholar
  54. Rowland LJ, Levi A (1994) RAPD-based genetic linkage map of blueberry derived from a cross between diploid species (Vaccinium darrowi × V. elliottii). Theor Appl Genet 87:863–868PubMedGoogle Scholar
  55. Rowland LJ, Lehman JS, Levi A, Ogden EL, Panta GR (1998) Genetic control of chilling requirement in blueberry. In: Cline WO, Ballington JR (eds) Proceedings of the 8th North American Blueberry Research and extension worker’s conference, North Carolina State University, Raleigh, NC, USA, pp 258–267Google Scholar
  56. Rowland LJ, Ogden EL, Arora R, Lim C-C, Lehman JS, Levi A, Panta GR (1999) Use of blueberry to study genetic control of chilling requirement and cold hardiness in woody perennials. HortScience 34:1185–1191Google Scholar
  57. Rowland LJ, Mehra S, Dhanaraj A, Ogden EL, Arora R (2003a) Identification of molecular markers associated with cold tolerance in blueberry. Acta Hortic 625:59–69Google Scholar
  58. Rowland LJ, Mehra S, Dhanaraj AL, Ogden EL, Slovin JP, Ehlenfeldt MK (2003b) Development of EST-PCR markers for DNA fingerprinting and genetic relationship studies in blueberry (Vaccinium, section Cyanococcus). J Am Soc Hortic Sci 128:682–690Google Scholar
  59. Rowland LJ, Ogden EL, Ehlenfeldt MK, Vinyard B (2005) Cold hardiness, deacclimation kinetics, and bud development among 12 diverse blueberry genotypes under field conditions. J Am Soc Hortic Sci 130:508–514Google Scholar
  60. Rowland LJ, Hancock JF, Bassil NV (2011) Blueberry. In: Folta K, Kole C (eds) Genetics, genomics and breeding of berries. Science, Enfield, pp 1–40Google Scholar
  61. Rowland LJ, Alkharouf N, Darwish O, Ogden EL, Polashock JJ, Bassil NV, Main D (2012) Generation and analysis of blueberry transcriptome sequences from leaves, developing fruit, and flower buds from cold acclimation through deacclimation. BMC Plant Biol 12:46. doi: 10.1186/1471-2229-12-46 PubMedCentralPubMedGoogle Scholar
  62. Sanchez-Perez R, Dicenta F, Martinez-Gomez P (2012) Inheritance of chilling and heat requirements for flowering in almond and QTL analysis. Tree Genet Genomes 8:379–389Google Scholar
  63. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234PubMedGoogle Scholar
  64. Spiers JM (1978) Effect of stage of bud development on cold injury in rabbiteye blueberry. J Am Soc Hortic Sci 103:452–455Google Scholar
  65. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040PubMedCentralPubMedGoogle Scholar
  66. Tayeh N, Bahrman N, Devaux R, Bluteau A, Prosperi J-M, Delbreil B, Lejeune-Henaut I (2013) A high-density genetic map of the Medicago truncatula major freezing tolerance QTL on chromosome 6 reveals colinearity with a QTL related to freezing damage on Pisum sativum linkage group VI. Mol Breed 32:279–289Google Scholar
  67. Tsarouhas V, Gullberg U, Lagercrantz U (2004) Mapping of quantitative trait loci (QTLs) affecting autumn freezing resistance and phenology in Salix. Theor Appl Genet 108:1335–1342PubMedGoogle Scholar
  68. Van Ooijen JW (2004) MapQTL® 5: software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma B.V., WageningenGoogle Scholar
  69. Van Ooijen JW (2006) JoinMap® 4: software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V., WageningenGoogle Scholar
  70. Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211PubMedGoogle Scholar
  71. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedGoogle Scholar
  72. Wang Y, Georgi LL, Reighard GL, Scorza R, Abbott AG (2002) Genetic mapping of the evergrowing gene in peach [Prunus persica (L.) Batsch]. J Hered 93:352–358PubMedGoogle Scholar
  73. Weber CA, Moore G, Deng Z, Gmitter FG Jr (2003) Mapping freeze tolerance quantitative trait loci in a Citrus grandis × Poncirus trifoliata F1 pseudo-testcross using molecular markers. J Am Soc Hortic Sci 128:508–514Google Scholar
  74. Wheeler NC, Jermstad KD, Krutovsky K, Aitken SN, Howe GT, Krakowski J, Neale DB (2005) Mapping of quantitative trait loci controlling adaptive traits in coastal Douglas-fir. IV. Cold-hardiness QTL verification and candidate gene mapping. Mol Breed 15:145–156Google Scholar
  75. Wittwer CT, Reed GH, Gundry CN, Vandersteen JG, Pryor RJ (2003) High-resolution genotyping by amplicon melting analysis using LCGreen. Clin Chem 49:853–860PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2014

Authors and Affiliations

  • Lisa J. Rowland
    • 1
  • Elizabeth L. Ogden
    • 1
  • Nahla Bassil
    • 2
  • Emily J. Buck
    • 3
  • Susan McCallum
    • 4
  • Julie Graham
    • 4
  • Allan Brown
    • 5
  • Claudia Wiedow
    • 3
  • A. Malcolm Campbell
    • 6
  • Kathleen G. Haynes
    • 1
  • Bryan T. Vinyard
    • 7
  1. 1.Genetic Improvement of Fruits and Vegetables Laboratory, Henry A. Wallace Beltsville Agricultural Research Center-WestUnited States Department of Agriculture, Agricultural Research ServiceBeltsvilleUSA
  2. 2.National Clonal Germplasm RepositoryUnited States Department of Agriculture, Agricultural Research ServiceCorvallisUSA
  3. 3.The New Zealand Institute for Plant and Food Research LtdPalmerston NorthNew Zealand
  4. 4.Department of GeneticsJames Hutton InstituteDundeeScotland, UK
  5. 5.Department of Horticultural Science, Plants for Human Health InstituteNorth Carolina State UniversityKannapolisUSA
  6. 6.Department of BiologyDavidson CollegeDavidsonUSA
  7. 7.Henry A. Wallace Beltsville Agricultural Research Center-West, Biometrical Consulting ServiceUnited States Department of Agriculture, Agricultural Research ServiceBeltsvilleUSA

Personalised recommendations