A review of photoperiodic flowering research in strawberry (Fragaria spp.)

Critical Reviews in Plant Sciences

Volumn 29, Issue 1, 2010, Pages 1-13

  Stewart, Philip J ^a,b   Folta, Kevin M ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b Driscoll's Strawberry Associates   (United States)

Author keywords

Day neutrality; Flowering; Fragaria; Photoperiod; Strawberry

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; FRAGARIA; FRAGARIA X ANANASSA; ROSACEAE;

EID: 77449139531     PISSN: 07352689     EISSN: 15497836     Source Type: Journal    
DOI: 10.1080/07352680903436259     Document Type: Review

References (122)

1. Ahmadi, H. and Bringhurst, R. S. 1991. Genetics of sex expression in Fragaria species. Am. J. Bot. 78: 504-514.
2. Ahmadi, H., Bringhurst, R. S., and Voth, V. 1990. Modes of inheritance of photoperiodism in Fragaria. J. Am. Soc. Hortl Sci. 115: 146-152.
3. Albani, M. C., Battey, N. H., and Wilkinson, M. J. 2004. The development of issr-derived scar markers around the SEASONAL FLOWERING LOCUS (SFL) in Fragaria vesca. Theor. Appl. Genet. 109: 571-579.
4. Alvarenga, A. A., and Valio, I. F. M. 1989. Influence of temperature and photoperiod on flowering and tuberous root-formation of Pachyrrhizus tuberosus. Ann. Bot. 64: 411-414.
5. Amasino, R. M. 1996. Control of flowering time in plants. Curr. Opin. Genet. Dev. 6: 480-487.
6. An, H., Roussot, C., Suarez-Lopez, P., Corbesier, L., Vincent, C., Pineiro, M., Hepworth, S., Mouradov, A., Justin, S., Turnbull, C., and Coupland, G. 2004. CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131: 3615-3626.
7. Arulsekar, S., Bringhurst, R., and Voth, V. 1981. Inheritance of pgi and lap isozymes in octoploid cultivated strawberries. J. Am. Soc. Hort. Sci. 106: 679-683.
8. Barger, I., Nishizawa, T., Shishido, Y., Kudo, M., Kumakura, R., and Hamamoto, H. 1997. Petiole length, chlorophyll and carbohydrate levels and photosynthetic rates of june-bearing strawberry plants as influenced by red-light irradiation during storage under cool conditions. Sci. Hort. 72: 25-33.
9. Braun, J.W., and Kender, W.J. 1985. Correlative bud inhibition and growth habit of the strawberry as influenced by application of gibberellic-acid, cytokinin, and chilling during short daylength. J. Am. Soc. Hort. Sci. 110: 28-34.
10. Bringhurst, R. S., and Voth, V. 1984. Breeding octoploid strawberries. Iowa State J. Res. 58: 371-381.
11. Bringhurst, R. S., Voth, V., and Van Hook, D. 1960. Relationship of root starch content and chilling history to performance of California strawberries. Proc. Amer. Soc. Hort. Sci. 75: 373-381.
12. Brooks, R. M., and Olmo, H. P. 1997. The Brooks and Olmo Register of New Fruit and Nut Varieties. 3rd Edition. ASHS Press, Alexandria, VA.
13. Brown, T., and Wareing, P. F. 1965a. Genetical control of everbearing habit and 3 other characters in varieties of Fragaria vesca. Euphytica 14: 97-98.
14. Brown, T., and Wareing, P. F. 1965b. Genetical control of flowering and runnering in varieties of Fragaria vesca. Heredity 20: 651-653.
15. Chabot, B. F. 1978. Environmental influences on photosynthensis and growth in fragaria vesca. New Phytol. 80: 87-98.
16. Chailakhyan, M. K. 1936a. New facts in support of the hormonal theory of plant development. C.R. (Dokl.) Acad. Sci. URSS 13: 79-83.
17. Chailakhyan, M. K. 1936b. On the mechanism of the photoperiodic reaction. C.R. (Dokl.) Acad. Sci. URSS 10: 89-93.
18. Clark, J. H. 1937. Inheritance of the so-called everbearing tendency in the strawberry. Proc. Amer. Soc. Hort. Sci. 35: 67-70.
19. Collins, W. B., and Barker, W. G. 1964. A flowering response of strawberry to continuous light. Can. J. Bot. 42: 1309-1311.
20. Corbesier, L., and Coupland, G. 2006. The quest for florigen: A review of recent progress. J. Exp. Bot. 57: 3395-3403.
21. Dale, A., and Sjulin, T. M. 1990. Few cytoplasms contribute to north-American strawberry cultivars. Hortscience 25: 1341-1342.
22. Darnell, R. L., and Hancock, J. F. 1996. Balancing vegetative and reproductive growth in strawberry. In: M.V. Pritts C. K. C., and T.E. Crocker, ed. Proceedings of the IV North American Strawberry Conference, 1996: 144-150.
23. Darrow, G. 1966. The Strawberry: History Breeding and Physiology. New York: Holt, Rinehart and Winston.
24. Darrow, G. M. 1936. Interrelation of temperature and photoperiodism in the production of fruit-buds and runners in the strawberry. Proc. Amer. Soc. Hort. Sci. 34: 360-363.
25. Darrow, G. M., and Waldo, G. F. 1929. The practical significance of increasing the daily light period of winter for strawberry breeding. Science 69: 496-497.
26. Darrow, G. M., and Waldo, G. F. 1930. Fruit bud formation in the strawberry in spring in the south-eastern states. Science 72: 349-350.
27. Darrow, G. M., and Waldo, G. F. 1934. Responses of strawberry varieties and species to the duration of the daily light period. USDA Tech. Bul. 453.
28. Darrow, G. M., Waldo, G. F., and Schuster, C. E. 1933. Twelve years of straw-berry breeding - a summary of the strawberry breeding work of the United States Department of Agriculture. J. Hered. 24: 391-402.
29. Darrow, G. M., and Waldo, G.F. 1933. Photoperiodism as a cause of the rest period in strawberries. Science 353-354.
30. Dellavecchia, P. T., and Peterson, C. E. 1984. Inheritance of flowering response in cucumber. J. Am. Soc. Hort. Sci. 109: 761-763.
31. Dennis,F.G.,Lipecki,J.,and Kiang,C.L. 1970. Effects of photoperiod and other factors upon flowering and runner development of 3 strawberry cultivars. J. Amer. Soc. Hort. Sci. 95: 750-754.
32. Downs, R. J., and Piringer, A. A. 1955. Differences in photoperiodic responses of everbearing and june-bearing strawberries. Proc. Amer. Soc. Hort. Sci. 66: 234-236.
33. Duchesne, A. 1766. Histoire naturelle du fraisiers. Paris.
34. Durner, E. F., Barden, J. A., Himelrick, D. G., and Poling, E. B. 1984. Photoperiod and temperature effects on flower and runner development in day-neutral, junebearing, and everbearing strawberries. J. Amer. Soc. Hort. Sci. 109: 396-400.
35. Durner, E. F., and Poling, E. B. 1987. Flower bud induction, initiation, differentiation and development in the earliglow strawberry. Scientia Hort. 31: 61-69.
36. Durner, E. F., Poling, E. B., and Albregts, E. A.1987. Early season yield responses of selected strawberry cultivars to photoperiod and chilling in a florida winter production system. J. Amer. Soc. Hort. Sci. 112: 53-56.
37. Faedi, W., Mourgues, F., and Rosati, C. 2002. Strawberry breeding and varieties: Situation and perspectives. Acta Hort., 567: 51-59.
38. Federova, N. J. 1937. Inter-und intragattungshybridisation der erdbeere und ihre bedeuting für die züchtung. Gartenbauwissenschaft, 10: 106-107.
39. Fletcher, S. W. 1917. The Strawberry in North America. New York: Macmillan Co.
40. Folta, K. M., and Childers, K. S. 2008. Light as a growth regulator: Con-trolling plant biology with narrow-bandwidth solid-state lighting systems. Hortscience, 43: 1957-1964.
41. Folta, K. M., and Davis, T. M. 2006. Strawberry genes and genomics. Crit. Rev. Plant Sci. 25: 399-415.
42. Folta, K. M., and Dhingra, A. 2006. Transformation of strawberry: The basis for translational genomics in Rosaceae. In Vitro Cell.Dev. Biol.- Plant 42: 482-490.
43. Fuller, A. S. 1897. The Small Fruit Culturist. New York: Orange Judd Co.
44. Garner, W. W., and Allard, H. A. 1920. Effect of the relative length of day and night and other factors of the enivornment on growth and reproduction in plants. J. Agric. Res., 18: 553-606.
45. Guttridge, C. G., 1969. Fragaria. In: Evans L. T., ed. The Induction of Flowering. Ithaca, NY: Cornell Univ. Press, 247-267.
46. Hancock, J. F. 1999. Strawberries. New York: CABI Publishing.
47. Hancock, J. F., Callow, P. W., Dale, A., Luby, J. J., Finn, C. E., Hokanson, S. C., and Hummer, K. E. 2001. From the Andes to the Rockies: Native strawberry collection and utilization. Hortscience 36: 221-225.
48. Hancock, J. F., and Luby, J. J. 1993. Genetic-resources at our doorstep - the wild strawberries. Bioscience 43: 141-147.
49. Hancock, J. F., Luby, J. J., Dale, A., Callow, P. W., Serce, S., and El-Shiek, A. 2002. Utilizing wild Fragaria virginiana in strawberry cultivar development: Inheritance of photoperiod sensitivity, fruit size, gender, female fertility and disease resistance. Euphytica 126: 177-184.
50. Harmann, K. K., and Poling, E. B. 1997. The influence of runner order, night temperature, and chilling cycles on the earliness of 'Selva' plug plant fruit production. Acta. Hort. 439: 597-603.
51. Hartmann, H. T. 1947a. The influence of temperature on the photoperiodic response of several strawberry varieties grown under controlled environment conditions. Proc. Amer. Soc. Hort. Sci. 50: 243-245.
52. Hartmann, H. T. 1947b. Some effects of temperature and photoperiod on flower formation and runner production in the strawberry. Plant Physiol. 22: 407-420.
53. Heide, O. M. 1977. Photoperiod and temperature interactions in growth and flowering of strawberry. Physiol. Plant. 40: 21-26.
54. Hildreth, A. C., and Powers, C. L. 1941. The Rocky Mountain strawberry as a source of hardiness. Proc. Amer. Soc. Hort. Sci. 38: 410-412.
55. Hummer, K., and Hancock, J. F. 2009. Strawberry Genomics: Botanical History, Cultivation, Traditional Breeding and New Technologies. In: Folta K. M., and Gardiner S. E., eds. Genetics and Genomics of Rosaceae. New York:Springer, 238-495.
56. Igrashi, I., Monma, S., Fujino, M., Okimura, M., Okitsu, S., Takada, K., and Nii, T. 1994. Breeding of new strawberry varieties "Ever Berry". Bull. Natl. Res. Inst. Veg. Ornam. Plants Tea Jpn. Ser. 9: 69-84.
57. Imaizumi, T., and Kay, S. A. 2006. Photoperiodic control of flowering: Not only by coincidence. Trends Plant Sci. 11: 550-558.
58. Ito, H., and Saito, T. 1962. Studies on the flower formation in the strawberry plants. I. Effects of temperature and photoperiod on the flower formation. Tahoku J. Agric. Res. 13: 191-203.
59. Izawa, T., Takahashi, Y., and Yano, M. 2003. Comparative biology comes into bloom: Genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr. Opin. Plant Biol. 6: 113-120.
60. Izhar, S. 1997. Infra short-day strawberry types. Acta Hort. 439: 155-160.
61. Joshua, D. C., and Thakare, R. G. 1986. A day-neutral mutant in jute. Trop. Agricult. 63: 316-318.
62. Kacszmarska, E., and Hortynski, J. A. 2002. The application of rapd markers for genetic studies on Fragaria x ananassa Duch. (strawberry) with due consideration for permanent flowering. Elec. J. Polish. Agric. Univ. 5: 2.
63. Klebs, G. 1913. Uber das verhaltnis der aussenwelt zur entwicklung der pflanzen. Sitzungsber. Heidelb. Akad. Wiss. Math. Naturwiss. Kl. Ser., 5: 1-47.
64. Knott, J. E. 1934. Effect of localized photoperiod on spinach. Proc. Am. Soc. Hort. Sci. 31: 152-154.
65. Kotecha, A. K., Yermanos, D. M., and Shropshire, F. M. 1975. Flowering in cultivars of sesame (Sesamum indicum) differing in photoperiodic sensitivity. Econ. Bot. 29: 185-191.
66. Kotoda, N., Iwanami, H., Takahashi, S., and Abe, K. 2006. Antisense expression of mdTFL1, a TFL1-like gene, reduces the juvenile phase in apple. J. Amer. Soc. Hort. Sci. 131: 74-81.
67. Kotoda, N., and Wada, M. 2005. MdTFL1, a TFL1-like gene of apple, retards the transition from the vegetative to reproductive phase in transgenic arabidopsis. Plant Sci. 168: 95-104.
68. Kotoda, N., Wada, M., Komori, S., Kidou, S., Abe, K., Masuda, T., and Soejima, J. 2000. Expression pattern of homologues of floral meristem identity genes LEAFY and AP1 during flower development in apple. J. Amer. Soc. Hort. Sci. 125: 398-403.
69. Kotoda, N., Wada, M., Kusaba, S., Kano-Murakami, Y., Masuda, T., and Soe-jima, J. 2002. Overexpression of mdMADS5, an APETALA1-like gene of apple, causes early flowering in transgenic arabidopsis. Plant Sci. 162: 679-687.
70. Lemiere, P., Hadley, P., Darby, J., and Battey, N. H. 1996. The effect of temperature and photoperiod on the rate of flower initiation and the onset of dormancy in the strawberry (Fragaria x ananassa Duch). J. Hort. Sci. 71: 361-371.
71. Leshem, Y., and Koller, D. 1964. The control of flowering in the strawberry Fragaria ananassa Duch. I. Interaction of positional and environmental effects. Ann. Bot. 112: 569-578.
72. Lewis, C. F., and Richmond, T. R. 1957. The genetics of flowering response in cotton.1. Fruiting behavior of Gossypium hirsutum var Marie Galante in a cross with a variety of cultivated American upland cotton. Genetics, 42: 499-509.
73. Lewis, C. F., and Richmond, T. R. 1960. The genetics of flowering response in cotton.2. Inheritance of flowering response in a Gossypium barbadense cross. Genetics, 45: 79-85.
74. Macoun, W. T. 1924. Report of the dominion horticulturist- Ottawa, Canada for 1923.
75. Manakasem, Y., and Goodwin, P. B. 2001. Responses of dayneutral and junebearing strawberries to temperature and daylength. J. Hort. Sci. Biotech. 76: 629-635.
76. Mangelsdorf, A. J., and East, E. M. 1927. Studies on the genetics of Fragaria. Genetics 12: 307-339.
77. Maystrenko, O. I., and Aliev, E. B. 1986. Chromosomal location of genes for photoperiodic response in a winter common wheat variety Skorospelka-35 slightly sensitive to short daylight. Cereal Res. Comm. 14: 41-47.
78. Millar, A. J. 2003. Suite of photoreceptors entrains the plant circadian clock. J. Biol. Rhythms 18: 217-226.
79. Monma, S., Okitsu, S., and Takada, K. 1990. Inheritance of the everbearing habit in strawberry. Bull. Natl. Res. Inst. Veg. Ornam. Plants Tea Jpn. Ser. 1.
80. Moore, J. N., and Hough, L. F. 1962. Relationships between auxin levels, time of floral induction and vegetative growth of the strawberry. Proc. Amer. Soc. Hort. Sci. 81: 255-264.
81. National Climatic Data Center. 2001. Available online at: http://www.ncd. noaa.gov/oa/ncdc.html
82. Nicoll, M. F., and Galletta, G. J. 1987. Variation in growth and flowering habits of junebearing and everbearing strawberries. J. Amer. Soc. Hort. Sci. 112: 872-880.
83. Ourecky,D.K.,and Slate,G.L.1967. Behavior of the everbearing characteristics in strawberries. Proc. Amer. Soc. Hort. Sci. 91: 236-248.
84. Paran, I., and Michelmore, R. W. 1993. Development of reliable pcr-based markers linked to downy mildew resistance genes in lettuce. Theo. Appl. Genet. 85: 985-993.
85. Piringer, A. A., and Scott, D. H. 1964. Interrelation of photoperiod, chilling, and flower-cluster and runner production by strawberries. Proc. Amer. Soc. Hort. Sci. 84: 295-301.
86. Powers, L. 1954. Inheritance of period of blooming in progenies of strawberries. Proc. Amer. Soc. Hort. Sci. 64: 293-298.
87. Rédei, G. P. 1962. Supervital mutants of Aarabidopsis. Genetics 47: 443-460.
88. Richardson, C. 1914. A preliminary note on the genetics of Fragaria. J. Genet. 3: 171-177.
89. Ross, J. J., and Murfet, I. C.1985. Flowering and branching in Lathyrus odoratus -Environmental and genetic-effects. Ann. Bot. 55: 715-726.
90. Sakin, M., Hancock, J. F., and Luby, J. J. 1997. Identifying new sources of genes that determine cyclic flowering in rocky mountain populations of Fragaria virginiana ssp glauca Staudt. J. Amer. Soc. Hort. Sci. 122: 205-210.
91. Salisbury, F. B., and Ross, C. W. 1992. Plant Physiology. Belmont, CA: Wadsworth Publishing Co.
92. Salome, P. A., and Mcclung, C. R. 2005. What makes the Arabidopsis clock tick on time? A review on entrainment. Plant, Cell Environ. 28: 21-38.
93. Samach, A., Onouchi, H., Gold, S. E., Ditta, G. S., Schwarz-Sommer, Z., Yanof-sky, M. F., and Coupland, G. 2000. Distinct roles of constans target genes in reproductive development of arabidopsis. Science 288: 1613-1616.
94. Scott, D. H., and Lawrence, F. J. 1975. Strawberries. In: And J. J., and Moore J. N., eds. Advances in Fruit Breeding. West Lafayette, IN, USA: Purdue University Press.
95. Serçe, S., and Hancock J.F. 2003. Assessment of day-neutrality scoring methods in strawberry families grown in greenhouse and field environments. Turk. J. Agric. For. 27: 191-198.
96. Serce, S., and Hancock, J. F. 2005a. Inheritance of day-neutrality in octoploid species of Fragaria. J. Amer. Soc. Hort. Sci. 130: 580-584.
97. Serce, S., and Hancock, J. F. 2005b. The temperature and photoperiod regulation of flowering and runnering in the strawberries, Fragaria chiloensis, F. virginiana, and F. x ananassa. Scientia Hor. 103: 167-177.
98. Shaw, D. V., and Famula, T. R. 2005. Complex segregation analysis of day-neutrality in domestic strawberry (Fragaria xananassa Duch.). Euphytica, 145: 331-338.
99. Shulaev, V., Korban, S. S., Sosinski, B., Abbott, A. G., Aldwinckle, H. S., Folta, K. M., Iezzoni, A., Main, D., Arus, P., Dandekar, A. M., Lewers, K., Brown, S. K., Davis, T. M., Gardiner, S. E., Potter, D., and Veilleux, R. E. 2008. Multiple models for rosaceae genomics. Plant Physiol 147: 985-1003.
100. Simpson, G. G. 2003. Evolution of flowering in response to day length: Flipping the constans switch. Bioessays 25: 829-832.
101. Sironval, C., and El Tannir-Lomba, J. 1960. Vitamin E and flowering of Fragaria vesca Var. semperflorens Duch. Nature 185: 855-856.
102. Sjulin, T. M., and Dale, A. 1987. Genetic diversity of North-American straw-berry cultivars. J. Amer. Soc. Hort. Sci. 112: 375-385.
103. Sonsteby, A. 1997. Short-day period and temperature interactions on growth and flowering in strawberry. Acta Hort. 439: 609-616.
104. Spalding, E. P., and Folta, K. M. 2005. Illuminating topics in plant photobiology. Plant, Cell Environ. 28: 39-53.
105. Stewart, P. J., Winslow, A. R., and Folta, K. M. 2007. An initial characterization of fragaria CONSTANS mRNA levels in short-day and day-neutral cultivars. Proceedings of the 2007 Proceedings of the North American Strawberry Symposium, 2007: 100-104.
106. Stutte, G. W. 2009. Light-emitting diodes for manipulating the phytochrome apparatus. Hortscience. 231-234.
107. Suarez-Lopez, P., Wheatley, K., Robson, F., Onouchi, H., Valverde, F., and Coupland, G. 2001. Constans mediates between the circadian clock and the control of flowering in arabidopsis. Nature. 410: 1116-1120.
108. Sudds, R. N. 1928. Fruit-bud formation in the strawberry. Penn. Agri. Expt. Sta. Bul. 230.
109. Sugimoto, T., Tamaki, K., Matsumoto, J., Yamamoto, Y., Shiwaku, K., and Watanabe, K. 2005. Detection of rapd markers linked to the everbearing gene in japanese cultivated strawberry. Plant Breeding. 124: 498-501.
110. Sung, S. K., Yu, G. H., and An, G. 1999. Characterization of mdMADS2, a member of the squamosa subfamily of genes, in apple. Plant Physiol. 120: 969-978.
111. Takeda, F., Glenn, D. M., and Stutte, G. 2008. Light quality affects flowering in short-day 'strawberry festival' strawberry. Hortscience. 43: 1146-1146.
112. Thomas, B., and Vince-Prue, D. 1984. Juvenility, photoperiodsm, and vernal-ization. In: Wilkins M. B., ed. Advanced Plant Physiology. London: Pitman, 408-439.
113. Thompson, P. A., and Guttridge, C. G., 1960. The role of leaves as inhibitors of flower induction in strawberry. Ann. Bot. 24: 482-490.
114. Tournois, J. 1912. Influence de la lumiere sur la floraison du houblon japonais et du chanvre. C.R. Hebd. Seances Acad.Sci., 155: 297-300.
115. Valverde, F., Mouradov, A., Soppe, W., Ravenscroft, D., Samach, A., and Coup-land, G. 2004. Photoreceptor regulation of constans protein in photoperiodic flowering. Science. 303: 1003-1006.
116. Vince-Prue, D., and Guttridge, C. G. 1973. Floral initiation in strawberry: Spectral evidence for the regulation of flowering by long-day inhibition. Planta. 110: 165-172.
117. Wada, M., Cao, Q. F., Kotoda, N., Soejima, J., and Masuda, T. 2002. Apple has two orthologues of FLORICAULA/LEAFY involved in flowering. Plant Mol. Biol. 49: 567-577.
118. Wyatt, J. E. 1985. Inheritance of photoperiod sensitivity, hirsute seed, and albinism in okra. J. Amer. Soc. Hort. Sci. 110: 74-78.
119. Yanagi, T., Yachi, T., Okuda, N., and Okamoto, K. 2006. Light quality of continuous illuminating at night to induce floral initiation of Fragaria chiloensis Chi-24-1. Scientia Hort. 109: 309-314.
120. Yano, M., Katayose, Y., Ashikari, M., Yamanouchi, U., Monna, L., Fuse, T., Baba, T., Yamamoto, K., Umehara, Y., Nagamura, Y., and Sasaki, T. 2000. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell. 12: 2473-2484.
121. Yao, J.-L., Dong, Y.-H., and Morris, B. A. M. 2001. Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc. Nat. Acad. Sci. 98: 1306-1311.
122. Yarnell, S. H. 1931. Genetic and cytological studies on Fragaria. Genetics. 16: 422-454.