Consistent fruit production is highly dependent on flowering frequency. Flower formation is related to biennial bearing and continues to be a major challenge for the apple industry and many other fruit tree industries worldwide. Biennial (or alternate) bearing is the “fluctuation of cropping from year to year caused by irregular flowering” (Hirst, 2017). Despite considerable research, the underlying mechanisms of biennial bearing remain largely unknown (Bangerth, 2006, 2009; Hoad, 1978; Jonkers, 1979; Monselise and Goldschmidt, 1982; Singh, 1948; Xing et al., 2015). In apple trees, biennial bearing varies among cultivars and appears to be under both genetic and environmental control (Guitton et al., 2011; Hanke et al., 2007; Monselise and Goldschmidt, 1982). Factors that regulate flower formation in apple trees include leaf area (Davis, 2002; Sahulka, 1967), shoot growth (Luckwill, 1970; Sahulka, 1967), bourse length (Dennis and Neilsen, 1999), crop load (Embree et al., 2007; Meland, 2009), and seed number (Chan and Cain, 1967). It is unclear how these different factors interact to promote or inhibit flower formation in biennial cultivars or why these factors do not have the same effect in annual cultivars. For example, most annual cultivars, such as ‘Gala’ and ‘GoldRush’, tend to flower regularly despite characteristics usually associated with flowering inhibition such as high seed numbers. On the other hand, some biennial cultivars, such as ‘Honeycrisp’ and ‘Golden Delicious’, have moderate seed numbers yet often exhibit biennial bearing. Some researchers have suggested that leaves, fruit, and seeds activate or inhibit flower formation pathways by affecting the endogenous balance of plant growth regulators (Bangerth, 2009; Hanke et al., 2007). A recent study involving quantitative trait loci in apples suggested that biennial bearing is under control of plant growth regulators genes (Guitton et al., 2011).
The transition of apple buds from vegetative to a floral state requires sufficient leaf area around the bud (Sahulka, 1967); however, the role of such leaves in flower formation pathways is not well understood (Grochowska, 1963). Leaves may affect flower formation in several ways. They provide carbohydrates and plant growth regulators, and work as the main receptors for environmental signals. Moreover, transpiring leaves increase the flow of substances transported via the xylem stream. It is well understood that flower induction genes are active in the leaves (Hanke et al., 2007). It is commonly accepted that flower formation occurs in apple trees when shoot growth ceases (Luckwill, 1970). Removal of leaves can reduce flower bud formation (Childers et al., 1995; Fulford, 1960; Harley et al., 1942), and may be a practice to manipulate biennial bearing because partial defoliation in off-years prevents excessive flower formation in on-years (Davis, 1957; Fulford, 1960). In these studies, partial defoliation reduced but did not totally inhibit flower formation. Return bloom was suppressed with whole-tree and partial-tree defoliation in ‘Braeburn’, ‘Golden Delicious’, ‘Ramey York’, and ‘Fuji’ (Davis, 2002), but defoliation effects on flower formation varied among cultivars (Sahulka, 1967). There is a clear relationship between flower formation and defoliation time and severity because inhibition of flower formation declined as defoliation time was delayed (Davis, 1957; Liewelyn, 1968) and as defoliation severity was decreased (Harley et al., 1942; Tustin et al., 1997).
In 1948, Singh suggested that reducing carbohydrate supply by reducing leaf area inhibits flower formation. Although there have been positive correlations between carbohydrate content as an essential substrate for flower formation and flower intensity, results have been variable. It appears that sucrose could be the signal in flower induction (Xing et al., 2015).
Crop load affects flower formation, especially in biennial cultivars. Generally, higher crop loads result in lower return bloom (Meland, 2009). For 40 years, it has been widely accepted that it is the seeds within a fruit that are the major cause of biennial bearing in apple trees (Chan and Cain, 1967). In ‘Honeycrisp’, crop load reduction enhances flower formation (Embree et al., 2007). It is commonly accepted that high crop load inhibits vegetative growth (Singh, 1948), and light crop load promotes vegetative growth (Maggs, 1963). Therefore, there are negative relationships between both crop load and vegetative growth, and flower formation in apple trees.
An apple fruiting spur produces two different types of leaves, spur leaves (SL) and bourse leaves (BL). SL grow directly from the spur, and BL grow from subsequent vegetative growth on the spur called the bourse shoot (Fig. 1). If the flower formation signals are perceived in the terminal meristem of the bourse shoot, floral buds will be formed for the following year’s crop (Abbott, 1960).
It remains unclear whether the requirement for leaf area in close proximity to the potential flowering bud is similar in annual vs. biennial cultivars. Therefore, we investigated differences in the regulation of flower formation between two Malus cultivars, ‘Honeycrisp’, a biennial cultivar, and ‘Gala’, an annual cultivar. The effect of spur defoliation and fruiting treatments, and their interaction, on local flower formation were evaluated. We hypothesized that in response to these treatments, the cultivars would have different patterns of flower formation from year to year. Such information would help clarify the roles of SL and BL, and the presence of fruit, on flower promotion and inhibition signals within the spur.
Bangerth, F. 2009 Floral induction in mature, perennial angiosperm fruit trees: Similarities and discrepancies with annual/biennial plants and the involvement of plant hormones Sci. Hort. 122 153 163
Childers, N.F., Morris, J.R. & Sibbett, G.S. 1995 Modern fruit science. 10th ed. Horticultural Publ., Gainsville, FL
Davis, D.E. 2002 Inhibition of flower bud initiation and development in apple by defoliation, gibberellic acid and crop load manipulation. Virginia Polytechnic Inst. State Univ., PhD Diss
Dennis, F.G. & Neilsen, J.C. 1999 Physiological factors affecting biennial bearing in tree fruit: The role of seeds in apple HortTechnology 9 317 322
Embree, C.G., Myra, M.T.D., Nichols, D.S. & Wright, A.H. 2007 Effect of blossom density and crop load on growth, fruit quality, and return bloom in ‘Honeycrisp’ apple HortScience 42 1622 1625
Grochowska, M.J. 1963 Studies on natural growth regulators in apple trees in relation to biennial bearing Bul. Acad. Pol. Sci. Biol. 12 379 383
Guitton, B., Kelner, J., Velasco, R., Gardiner, S. & Chagné, D. 2011 Genetic control of biennial bearing in apple J. Expt. Bot. 63 131 149
Hanke, M.V., Flachowsky, H., Peil, A. & Hättasch, C. 2007 No flower no fruit-genetic potentials to trigger flowering in fruit trees Genes Genomes and Genomics Journal 1 1 20
Harley, C.P., Magness, J.R., Masure, M.P., Fletcher, L.A. & Degman, E.S. 1942 Investigations on the cause and control of biennial bearing of apples USDA Tech. Bul. 792 1 58
Hirst, P.M. 2017 Advances in understanding flowering and pollination in apple trees. In: K. Evans (ed.). Achieving sustainable cultivation of apples. Burleigh Dodds Sci. Publ., Cambridge, UK
Hirst, P.M. & Ferree, D.C. 1995 Rootstock effects on the flowering of ‘Delicious’ apple. I. Bud development J. Amer. Soc. Hort. Sci. 120 1010 1017
Liewelyn, F.W.M. 1968 The effect of partial defoliation in different times in the season on fruit drop and shoot growth in Lord Lambourne apple trees J. Hort. Sci. 43 519 526
Luckwill, L.C. 1970 The control of growth and fruitfulness of apple trees, p. 237–254. In: Physiology of tree crops. Academic Press, New York, NY
Meland, M. 2009 Effects of different crop loads and thinning times on yield, fruit quality, and return bloom in Malus ×domestica Borkh. ‘Elstar’ J. Hort. Sci. Biotechnol. 84 117 121
Tustin, D.S., Stanley, C.J. & Adams, H.M. 1997 Physiological and phenological responses of apple trees to artificial reduction of the growth period from harvest to leaf fall Acta Hort. 451 383 392
Xing, L.B., Zhang, D., Li, Y.M., Shen, Y.W., Zhao, C.P., Ma, J.J., An, N. & Han, M.Y. 2015 Transcription profiles reveal sugar and hormone signaling pathways mediating flower induction in apple (Malus domestica Borkh.) Plant Cell Physiol. 56 10 2052 2068