, Volume 235, Issue 6, pp 1123–1139 | Cite as

Flower and early fruit development in a diploid strawberry, Fragaria vesca

  • Courtney A. Hollender
  • Aviva C. Geretz
  • Janet P. SlovinEmail author
  • Zhongchi LiuEmail author
Original Article


The diploid woodland strawberry, Fragaria vesca, is being recognized as a model for the more complex octoploid commercial strawberry, Fragaria × ananassa. F. vesca exhibits a short seed to seed cycle, can be easily transformed by Agrobacteria, and a draft genome sequence has been published. These features, together with its similar flower structure, potentially make F. vesca a good model for studying the flower development of other members of the Rosaceae family, which contains many economically important fruit trees and ornamental plants. To propel F. vesca’s role in genetic and genomic research and to facilitate the study of its reproductive development, we have investigated in detail F. vesca flower and early fruit development using a seventh generation inbred diploid line, Yellow Wonder 5AF7. We present here standardized developmental staging and detailed descriptions of morphological changes associated with flower and early fruit development based on images of hand dissected flowers, histological sections, and scanning electron microscopy. In situ hybridization with the F. vesca AGAMOUS homolog, FvAG, showed expression in young stamen and carpel primordia. This work lays the essential groundwork and standardization for future molecular, genetic, and genomic studies of F. vesca.


Woodland strawberry Carpel development Anther development Embryo development AGAMOUS Developmental staging 





Yellow Wonder 5AF7

H4 × 4

Hawaii 4 × 4


Scanning electron micrograph



We would like to thank Tim Maugel of the Laboratory for Biological Ultrastructure, University of Maryland, College Park for assistance with SEM, and Heven Sze for use of her microscope. We are also grateful to anonymous reviewers and the editor for helpful suggestions to improve the manuscript. This work was supported by NSF grant MCB0923913 to Z.L. and J.S., the Hokensen graduate fellowship to CH, USDA CRIS project #1275-21000-185-00D and Maryland MAES Hatch Project (MD-CBMG-0525).

Supplementary material

425_2011_1562_MOESM1_ESM.pdf (1.2 mb)
Supplementary material 1 (PDF 1.19 mb)
425_2011_1562_MOESM2_ESM.pdf (2.6 mb)
Supplementary material 2 (PDF 2.60 mb)


  1. Anderson H, Guttridge C (1982) Strawberry truss morphology and the fate of high-order flower buds. Crop Res (Hort Res) 22:105–122Google Scholar
  2. Archbold DD, Dennis FG (1984) Quantification of free ABA and free and conjugated IAA in strawberry achene and receptacle tissue during fruit development. J Am Soc Hortic Sci 109:330–335Google Scholar
  3. Archbold D, Dennis F (1985) Strawberry receptacle growth and endogenous IAA content as affected by growth regulator application and achene removal. J Am Soc Hortic Sci 110:816–820Google Scholar
  4. Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20PubMedGoogle Scholar
  5. Buzgo M, Soltis D, Soltis P, Ma H (2004) Towards a comprehensive integration of morphological and genetic studies of floral development. Trends Plant Sci 9:164–173PubMedCrossRefGoogle Scholar
  6. Castillejo C, De la Fuente JI, Iannetta P, Botella MA, Valpuesta V (2004) Pectin esterase gene family in strawberry fruit: study of FaPE1, a ripening-specific isoform. J Exp Bot 55:909–918PubMedCrossRefGoogle Scholar
  7. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37PubMedCrossRefGoogle Scholar
  8. Darrow G (1966) The Strawberry: history breeding and physiology. Holt, Rinehart and Winston, New YorkGoogle Scholar
  9. Davis T, Yu H (1997) A linkage map of the diploid strawberry, Fragaria vesca. J Hered 88:215–221CrossRefGoogle Scholar
  10. Deng C, Davis TM (2001) Molecular identification of the yellow fruit color (c) locus in diploid strawberry: a candidate gene approach. Theor Appl Genet 103:316–322CrossRefGoogle Scholar
  11. Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991–1002PubMedCrossRefGoogle Scholar
  12. Dubois A, Raymond O, Maene M, Baudino S, Langlade NB, Boltz V, Vergne P, Bendahmane M (2010) Tinkering with the C-function: a molecular frame for the selection of double flowers in cultivated roses. PLoS One 5:e9288PubMedCrossRefGoogle Scholar
  13. Durner EF, Poling EB (1988) Strawberry developmental responses to photoperiod and temperature: a review. Adv Strawb Prod 7:6–14Google Scholar
  14. Fait A, Hanhineva K, Beleggia R, Dai N (2008) Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development. Plant Physiol 148:730–750Google Scholar
  15. Folta KM, Dhingra A (2007) Transformation of strawberry: the basis for translational genomics in Rosaceae. In Vitro Cell Dev Biol Plant 42:482–490Google Scholar
  16. Galletta GJ, Himelrick DG (1990) Small Fruit Crop Management. Prentice Hall, Engelwood CliffsGoogle Scholar
  17. Giovannoni J (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol 52:725–749PubMedCrossRefGoogle Scholar
  18. Hancock JF (1999) Strawberries. CABI Publishing, New YorkGoogle Scholar
  19. Hartmann HT (1947) Some effects of temperature and photoperiod on flower formation and runner production in the strawberry. Plant Physiol 22:407–420PubMedCrossRefGoogle Scholar
  20. Hummer KE, Hancock JF (2009) Strawberry genomics: botanical history, cultivation, traditional breeding, and new technologies. In: Folta K, Gardiner SE (eds) Genetics and genomics of Rosaceae, plant genetics and genomic: crops and models 6. Springer Science + Business Media, LLCGoogle Scholar
  21. Hytönen T, Elomaa P, Moritz T, Junttila O (2009) Gibberellin mediates daylength-controlled differentiation of vegetative meristems in strawberry (Fragaria x ananassa Duch). BMC Plant Biol 9:18PubMedCrossRefGoogle Scholar
  22. Jensen WA (1962) Botanical Histochemistry. W.H Freeman, San FranciscoGoogle Scholar
  23. Kania W (1973) Entwicklungsgeschichtliche Untersuchungen an Rasaceenbluten. Bot Jb Syst 93:175–246Google Scholar
  24. Krizek BA, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6:688–698PubMedCrossRefGoogle Scholar
  25. Kronenberg H (1959) Poor fruit setting in strawberries. I. Euphytica 8:47–57CrossRefGoogle Scholar
  26. Liu CM, Meinke DW (1998) The titan mutants of Arabidopsis are disrupted in mitosis and cell cycle control during seed development. Plant J 16:21–31PubMedCrossRefGoogle Scholar
  27. Liu Z, Franks RG, Klink VP (2000) Regulation of gynoecium marginal tissue formation by LEUNIG and AINTEGUMENTA. Plant Cell 12:1879–1892PubMedCrossRefGoogle Scholar
  28. Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69PubMedCrossRefGoogle Scholar
  29. Mouhu K, Hytönen T, Folta K, Rantanen M, Paulin L, Auvinen P, Elomaa P (2009) Identification of flowering genes in strawberry, a perennial SD plant. BMC Plant Biol 9:122PubMedCrossRefGoogle Scholar
  30. Nitsch JP (1950) Growth and morphogenesis of the strawberry as related to auxin. Am J Bot 37:211–215CrossRefGoogle Scholar
  31. Oosumi T, Gruszewski H, Blischak L, Baxter A, Wadl P, Shuman J, Veilleux RE, Shulaev V (2006) High-efficiency transformation of the diploid strawberry (Fragaria vesca) for functional genomics. Planta 223:1219–1230PubMedCrossRefGoogle Scholar
  32. Perkins-Veazie PM (1995) Growth and ripening of strawberry fruit. Hortic Rev 17:267–297Google Scholar
  33. Perkins-Veazie PM, Huber DJ, Brecht JK (1995) Characterization of ethylene production in developing strawberry fruit. Plant Growth Regul 17:33–39Google Scholar
  34. Qin Y, Teixeira da Silva JA, Zhang L, Zhang S (2008) Transgenic strawberry: state of the art for improved traits. Biotechnol Adv 26:219–232PubMedCrossRefGoogle Scholar
  35. Reganold J, Andrews P, Reeve J, Carpenter-Boggs L, Schadt C, Alldredge JR, Ross C, Davies N, Zhou J (2010) Fruit and soil quality of organic and conventional strawberry agroecosystems. PLoS One 5(9):e12346. doi: 10.1371/journal.pone.0012346
  36. Rosin F, Aharoni A, Salentijn E, Schaart J (2003) Expression patterns of a putative homolog of AGAMOUS, STAG1, from strawberry. Plant Sci 165:959–968Google Scholar
  37. Rousseau-Gueutin M, Lerceteau-Köhler E, Barrot L, Sargent DJ, Monfort A, Simpson D, Arús P, Guérin G, Denoyes-Rothan B (2008) Comparative genetic mapping between octoploid and diploid Fragaria species reveals a high level of colinearity between their genomes and the essential disomic behavior of the cultivated octoploid strawberry. Genetics 179:2045–2060PubMedCrossRefGoogle Scholar
  38. Sanders PM, Bui AQ, Weterings K, Mcintire KN, Hsu Y, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322CrossRefGoogle Scholar
  39. Sargent DJ, Davis T, Simpson D (2009) Strawberry (Fragaria spp.) structural genomics. In: Folta K, Gardiner SE (eds) Genetics and genomics of Rosaceae, plant genetics and genomics: crops and models 6. Springer Science + Business Media, New YorkGoogle Scholar
  40. Schwab W, Schaart J, Rosati C (2009) Functional molecular biology research in Fragaria. In: Folta K, Gardiner SE (eds) Genetics and genomics of Rosaceae, plant genetics and genomics: crops and models 6. Springer Science + Business Media LLC, New YorkGoogle Scholar
  41. Serçe S, Hancock JF (2005) The temperature and photoperiod regulation of flowering and runnering in the strawberries, Fragaria chiloensis, F. virginiana, and F. × ananassa. Sci Hortic 103:167–177CrossRefGoogle Scholar
  42. Shulaev V, Korban SS, Sosinski B, Abbott A, Aldwinckle HS, Folta KM, Iezzoni A, Main D, Arús P, Dandekar AM, Lewers K, Brown SK, Davis TM, Gardiner SE, Potter D, Veilleux RE (2008) Multiple models for Rosaceae genomics. Plant Physiol 147:985–1003PubMedCrossRefGoogle Scholar
  43. Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, Jaiswal P, Mockaitis K, Liston A, Mane SP, Burns P, Davis TM, Slovin JP, Bassil N, Hellens RP, Evans C, Harkins T, Kodira C, Desany B, Crasta OR, Jensen RV, Allan AC, Michael TP, Setubal JC, Celton JM, Rees DJ, Williams KP, Holt SH, Ruiz Rojas JJ, Chatterjee M, Liu B, Silva H, Meisel L, Adato A, Filichkin SA, Troggio M, Viola R, Ashman TL, Wang H, Dharmawardhana P, Elser J, Raja R, Priest HD, Bryant DW, Fox SE, Givan SA, Wilhelm LJ, Naithani S, Christoffels A, Salama DY, Carter J, Lopez Girona E, Zdepski A, Wang W, Kerstetter RA, Schwab W, Korban SS, Davik J, Monfort A, Denoyes-Rothan B, Arus P, Mittler R, Flinn B, Aharoni A, Bennetzen JL, Salzberg SL, Dickerman AW, Velasco R, Borodovsky M, Veilleux RE, Folta KM (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116PubMedCrossRefGoogle Scholar
  44. Slovin J, Michael T (2011) Strawberry. Part 3 structural and functional genomics. In: Folta K, Kole C (eds) Genetics, genomics and breeding of berries. Science Publishers, Enfield, pp 162–193CrossRefGoogle Scholar
  45. Slovin J, Rabinowicz PD (2007) Fragaria vesca, a useful tool for Rosaceae genomics. In: Takeda F (ed) 6th North American Strawberry Symposium. American Society for Horticultural Science, Ventura, pp 112–117Google Scholar
  46. Slovin JP, Schmitt K, Folta KM (2009) An inbred line of the diploid strawberry Fragaria vesca f. semperflorens for genomic and molecular genetic studies in the Rosaceae. Plant Methods 5:15PubMedCrossRefGoogle Scholar
  47. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767PubMedCrossRefGoogle Scholar
  48. Stangeland B, Salehian Z (2002) An improved clearing method for GUS assay in Arabidopsis endosperm and seeds. Plant Mol Biol Report 20:107–114CrossRefGoogle Scholar
  49. Taiz L, Zeiger E (2006) Ethylene: the gaseous hormone. Plant Physiology. Sinauer Associates, Inc., Sunderland, pp 571–591Google Scholar
  50. Trainotti L, Pavanello A, Casadoro G (2005) Different ethylene receptors show an increased expression during the ripening of strawberries: does such an increment imply a role for ethylene in the ripening of these non-climacteric fruits? J Exp Bot 56:2037–2046PubMedCrossRefGoogle Scholar
  51. Weberling F (1989) Morphology of flowers and inflorescences. Cambridge University Press, CambridgeGoogle Scholar
  52. Williamson SC, Yu H, Davis TM (1995) Shikamate dehydrogenase allozymes: inheritance and close linkage to fruit color in the diploid strawberry. J Hered 86:74–76Google Scholar
  53. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Cell Biology and Molecular GeneticsUniversity of Maryland, College ParkCollege ParkUSA
  2. 2.Genetic Improvement of Fruit and Vegetables Laboratory, USDA/ARSBeltsvilleUSA

Personalised recommendations