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Flowering in ‘Honeycrisp’ Apple Shows That Spurs Are Semiautonomous Organs

Authors:
Mokhles A. Elsysy Department of Horticulture and Landscape Architecture, Purdue University, 625 Agriculture Mall Drive, West Lafayette, IN 47907, USA, and Department of Pomology, College of Agriculture, Assiut University, Assiut 71526, Egypt

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Peter M. Hirst Department of Horticulture and Landscape Architecture, Purdue University, 625 Agriculture Mall Drive, West Lafayette, IN 47907, USA

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Article Category:
Research Article
Online Publication Date:
12 May 2023
Page(s):
108–116
Volume/Issue:
Volume 148: Issue 3
Copyright:
© American Society for Horticultural Science 2023
DOI:
https://doi.org/10.21273/JASHS05281-22
Open Access
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Abstract

Irregular flowering and biennial bearing are challenging in many apple (Malus ×domestica) cultivars such as Honeycrisp. Apple flowering is influenced by many factors including crop load, fruit weight, seed number, and bourse shoot length. However, it is unclear how these factors exert their control. We investigated flowering in ‘Honeycrisp’ and whether flower formation is regulated locally within the spur or if it is under the control of the whole tree system. Treatments consisting of 30 to 240 fruit per tree with one or two fruit per spur were applied, and seed number, fruit weight, bourse shoot length, bourse number, and resulting flower formation measured. In 2013, flowering was affected by fruit number per tree, fruit number per spur and their interaction, and with lower total tree crop loads, spurs bearing two fruit had fewer flowers than those with a single fruit. In 2014, few spurs formed flowers regardless of treatment. In 2013, flowering was unaffected by seed number on single-fruited spurs but flowering inhibition was correlated with fruit weight. In spurs bearing two fruit, flowering was inhibited by higher seed numbers but fruit weight per spur had no effect on flowering. Our data suggest that both whole tree and within-spur characteristics contribute to local flower formation. Therefore, ‘Honeycrisp’ spurs can be considered semiautonomous organs because inhibition of flower formation appears to be related to the depletion of resources both locally within the spurs, and systematically within the whole tree. The main factors associated with flower formation were fruit number per tree, fruit number per spur, bourse shoot length, and bourse number per spur. In contrast to previous reports, our data show that seeds do not play a direct role in regulating flower formation.

Keywords: biennial bearing; bourse shoot length; crop load; fruit number; Malus ×domestica; return bloom; seed number

Flowering is a biologically and commercially important stage of apple (Malus ×domestica) tree development. In apple, flowers are usually formed on short shoots or spurs, and one or more buds in the axils of spur leaves may develop into bourse buds or bourse shoots (Abbott 1960). Flowers form within buds, overwinter, and emerge the following spring. One of the most challenging problems that apple growers face is biennial bearing. Biennial bearing is “the fluctuation in cropping from year-to-year caused by irregular flowering” (Hirst 2017). Despite many years of research, biennial bearing remains a major challenge (Bangerth 2006; Elsysy and Hirst 2017; Jonkers 1979; Singh 1948). Biennial bearing has been studied in apple trees more extensively than in any other tree fruit crop (Monselise and Goldschmidt 1982) and can have major economic consequences for growers, including loss of production, poor fruit quality, and continuity of supply. Field management practices to reduce the severity of biennial bearing are seldom completely successful to ensure regular bearing. Therefore, a more detailed understanding of the key factors that control biennial bearing in apple is necessary. A number of newer, higher value cultivars exhibit high degrees of biennial bearing including Cameo, Fuji, Braeburn, and Honeycrisp (Hirst 2017). ‘Honeycrisp’ apple is one of the highest value apples in the United States market and often exhibits a severe tendency for biennial bearing (Elsysy and Hirst 2017; Elsysy et al. 2019). Thus, ‘Honeycrisp’ is a good candidate cultivar to study biennial bearing.

In a landmark study using a single ‘Spencer Seedless’ tree, Chan and Cain (1967) suggested that seeds were the major source of the inhibitory effect on flower formation. They proposed that this correlative inhibition acts through a hormonal process. Since that time, it has become widely accepted that seed-derived gibberellins inhibit local flower formation in apple. This has been supported by many studies showing that exogenous applications of gibberellins can inhibit flower formation, especially when sprayed 2 weeks after full bloom (Elsysy and Hirst 2019; Marino and Greene 1981; Tromp 1982).

The role of seeds in biennial bearing of apple is established in the literature (Chan and Cain 1967; Dennis and Neilsen 1999; Marino and Greene 1981), but there are reasons to question this hypothesis. For example, although gibberellin (GA4 and GA7) activities have been identified in apple seeds in the early stages of fruit development (Dennis and Nitsch 1966), movement of gibberellins from seeds to bourse buds to inhibit flower formation has not been demonstrated. Furthermore, while studies with parthenocarpic cultivars have pointed to a role of seeds (Chan and Cain 1967; Griggs et al. 1970; Neilsen 1998; Weinbaum et al. 2001), none of the major commercial apple cultivars are parthenocarpic. Thus, caution should be used extrapolating results from parthenocarpic cultivars to commercially important, nonparthenocarpic cultivars (Weinbaum et al. 2001).

Biennial bearing is the result of a complex process, influenced by the interaction of many factors, such as fruiting, growth, and development of both the spur and the whole tree, plant growth regulator activities, and the balance between carbohydrate content and nitrogen content (Singh 1948). Whole tree biennial bearing can also be caused by climatic factors such as freeze damage (Glenn 2016). Branches on the same tree may display contrary behavior, where some flower heavily, whereas others may exhibit sparse or no flowering (Davis 1957; Harley et al. 1942). Furthermore, there are often differences in flowering characteristics among trees within the same orchard (Davis 1957). Previous research has shown that the previous year’s crop in perennial fruit tree species can play a central role in return bloom at the spur level and allowing for resting (nonfruiting) spurs may help to ensure return bloom (Bangerth 2006; Elsysy and Hirst 2017). However, even with an adequate number of resting spurs, some apple cultivars, such as Benoni and Laxton’s Superb, may still experience biennial bearing (Jonkers 1979). Hence, biennial bearing can be general and affect the whole tree, or local and affect branches or even individual spurs on the tree.

Fruiting spurs have a strong demand for carbohydrates (Marqurard 1987), and sucrose has been suggested as the apple flowering signal (Xing et al. 2015). Carbohydrate content, as a vital substrate for flower formation, has often been studied by correlating it with flower intensity, although results have been inconsistent. Recently, we showed that flower formation in ‘Honeycrisp’ was unaffected by spur characteristics associated with increased spur carbohydrate status (Elsysy et al. 2018). Removal of fruit by midsummer was associated with an increase in flower differentiation and starch reserves in citrus (Goldschmidt and Golomb 1982), and flower initiation was directly related to starch level in pistachio (Crane and Nelson 1971). Girdling, a technique that promotes flower formation in crops including apple (Arakawa et al. 1997) and citrus [Citrus sp. (Cohen 1981)], results in accumulation of carbohydrates within girdled branches (Fishler et al. 1983; Furr and Armstrong 1956). Heinicke (1917) suggested that seeds promote the fruit demand for different resources, and these resources could include carbohydrates, plant growth regulators, and/or nutrients. The decline in carbohydrate content within the spur or the whole tree in response to fruiting was reported for several fruit and nut (Davis and Sparks 1974; Grochowska 1973; Jones et al. 1975), but how this depletion of resources is managed in the whole tree vs. the spur is not well understood.

Therefore, the objective of this study was to investigate spur vs. whole tree regulation of flower formation in apple. We hypothesized that apple spurs are semiautonomous organs, and that flower formation is regulated by crosstalk between fruiting spurs and the rest of the tree (i.e., flowering is determined by both spur and whole tree effects).

Materials and Methods

Plant materials.

This experiment was conducted on mature ‘Honeycrisp’ apple trees planted in 2003 and growing on M.7 rootstock at a spacing of 5 m × 3 m, at the Samuel G. Meigs Horticulture Facility of Purdue University in Lafayette, IN, USA (lat. 40.29°N, long. 86.88°W). The soil type was Drummer silty clay loam (fine-silty, mixed, superactive, mesic Typic Endoaquolls) with a pH of 7.2 (Mickelbart et al. 2012). Trees were trained to a vertical axis form and were managed according to standard commercial practices (Midwest Fruit Workers 2012). Crop load was adjusted manually by hand thinning at petal fall. No plant growth regulator materials were applied to the trees. This experiment was conducted on the same set of trees over two consecutive seasons (2013 and 2014). In the year preceding the experiment (2012), a series of severe spring frosts resulted in total fruit loss, which offered a uniform starting point for all trees.

Experimental procedure.

At the time of full bloom, in a block of 100 ‘Honeycrisp’ trees, flower formation was rated visually from 0 to 10 where 0 represented no flowers and 10 represented heavy flowering. We selected 42 trees with a high level of flowering as experimental units both years. At the time of full bloom, six trees were randomly assigned to one of seven treatments, in a completely randomized design. Treatments were as follows: 15, 30, 60, or 120 spurs per tree thinned to two fruit per spur (double-fruited spurs) and 30, 60 or 120 spurs per tree thinned to one fruit per spur (single-fruited spurs) (Table 1). Thinning was carried out at petal-fall where king fruit were retained for single-fruited treatments and king fruit and one lateral fruit retained for two-fruited treatments. Treatments were characterized as very low, low, medium, and high for 30, 60, 120, and 240 fruit per tree, respectively. Selected spurs were spaced at least 15 cm apart to reduce spur-to-spur effects. Trees were thinned manually at petal fall, and only tagged spurs were allowed to develop fruit. All other fruit were removed. Trunk cross-sectional area for each tree was calculated (Table 1). The same thinning treatments were repeated in the same group of trees in 2014.

Table 1.

Treatments as actual number of fruit per tree and number of fruit per spur applied to ‘Honeycrisp’ apple trees in 2013 and 2014.
Table 1.

Measurements.

At commercial harvest time, fruit were harvested, weighed, and seed number per fruit counted. Fruit from all treatments was harvested on the same day. At the end of the growing season, during winter, tagged spurs were harvested, bourse number on each spur counted, bourse shoot lengths measured, and bourse buds were dissected under a microscope (Olympus Corp., Center Valley, PA, USA) to determine flower formation for each bud (Hirst and Ferree 1995). Only those spurs on which fruit persisted until maturity were included in our analyses. Finally, to determine flower formation in resting-spurs, bloom was visually rated in the following spring from 0 to 10, where zero represented no flowers on the tree and 10 represented heavy flowering.

Data Analysis

Effects of fruit number per spur, fruit weight, seed number, bourse shoot length, and total fruit number per tree on fruiting spur flower formation.

Mixed effects logistic regression model for each separate year used fruit number per tree and per spur, fruit weight, seed number, bourse number, and bourse shoot length as predictors of flowering status. Within each year, a separate analysis of the treatments with single-fruited spurs and those with double-fruited spurs was performed. Because there was a significant effect of seed number on flower formation in double-fruited spurs in 2013 single-fruited spurs in 2014, we divided seed number into four about equal categories based on seed number distribution and tested the effect of these categories on flower formation and fruit weight. In 2013, bourse shoot length had a significant effect on flower formation, so we divided bourse shoot length into four approximately equal categories based on the distribution in that year and tested the differences in flower formation among these categories. Odds ratios (ORs) were presented due to the presence of more than one explanatory variable in the logistic regression model.

General vs. local effect on flower formation of fruiting spurs.

The proportion of flower formation for fruiting spurs was used to conduct a comparison of slopes from regression models of treatments with single-fruited spurs with double-fruited spurs, using the equation: y = β0 + β1 x1 + β2 x2 + β3 x1 × x2, where β0 = the intercept of the regression line, x1 = fruit number per tree, x2 = fruit number per spur, β1 = slope for x1, β2 = slope for x2, β3 = slope for x1 × x2, and y = predicted value given specific x.

Effect of treatments on flower formation of resting spurs.

Analysis of variance was used to determine effects of treatments on flower formation of vegetative spurs. Flower formation was visually rated for each tree using a 10-point scale, where 1 represented no flowering and 10 represented heavy flowering.

Effect of year on fruiting spur characteristics.

Analysis of variance was used to determine the effect of year on fruiting spur bourse shoot length, bourse number, fruit weight, and flower formation.

Software.

Analyses were made using the statistical package R (version 3.3.1; R Foundation for Statistical Computing, Vienna, Austria). R used libraries “Lme4” (Bates et al. 2018), “MASS” (Venables and Ripley 2002), and “Vegan” (Oksanen et al. 2016). Comparisons were conducted using Tukey’s Studentized range test P < 0.05 [packet multcomp 1.2–12 (Torsten and Frank 2008)].

Results

General vs. local effects

The actual fruit numbers were lower than target fruit number due to lower than expected fruit set. In 2013, fruit number per spur, fruit number per tree, and their interaction all affected flower formation of fruiting spurs (Fig. 1A). In treatments with single-fruited spurs, flower formation decreased as total fruit number per tree increased (Fig. 1A). For lower (<48 fruit/tree) total tree crop load, treatments with double-fruited spurs had lower flowering than treatments with single-fruited spurs (Fig. 1A). Flower formation inhibition occurred on all spurs with double-fruited spurs in both years (Fig. 1A and B). Despite no crop load in 2012 due to frost and manual adjustment of crop loads in 2013 to low or modest crop load levels, flower formation inhibition occurred in almost all fruiting spurs in 2014, regardless of total fruit number per tree and spur fruit number, bourse number, bourse shoot length, or fruit weight (Fig. 1B).

Fig. 1.
Fig. 1.

Flower formation in ‘Honeycrisp’ apple fruiting spurs for treatments with different fruit number per spur and different fruit number per tree in (A) Summer 2013 and (B) Summer 2014. Slopes describing the response of flowering to different crop loads from trees with single-fruited spurs and those with double-fruited spurs were different (P = 0.018) in 2013 only. Data points represent the mean of six single-tree replicates and standard errors are indicated.

Citation: Journal of the American Society for Horticultural Science 148, 3; 10.21273/JASHS05281-22

Effects of fruit number per spur, fruit weight, seed number, bourse number, and bourse shoot length on fruiting spur flower formation

Fruit number per spur.

In 2013 only, the constant effect of the predictor of flowering (odds) decreased by 72%, with double-fruited spurs compared with single-fruited spurs (OR = 0.28) (Table 2).

Table 2.

Mixed effects logistic regression model of ‘Honeycrisp’ apple in Summer 2013 and 2014. Effect of fruit number per spur, seed number, fruit weight, bourse shoot length, bourse number, and fruit number per tree on fruiting spur flower formation.
Table 2.

Seed number.

Statistical models constructed for 2013 and 2014 treatments showed that overall seed number did not inhibit flowering (Table 2). Statistical models constructed for 2013 treatments with single-fruited and double-fruited spurs categorized separately showed that seed number had an inhibitory effect on flowering, but only of double-fruited spurs (Table 3). When seed number of double-fruited spurs was categorized in 2013, flower formation on spurs with lower seed numbers (5 to 12 seeds per spur) was higher than for those spurs with more seeds. Seed number did not affect spur flower formation for treatments with single-fruited spurs in 2013. Similarly, seed number on double-fruited spurs did not significantly affect fruit weight in 2013 (Fig. 2A), but fruit weight showed a significant effect on spur flower formation in treatments with single-fruited spurs in 2013 (Table 3).

Fig. 2.
Fig. 2.

Effect of seed number per spur on flower formation and fruit weight in ‘Honeycrisp’ apple spurs (A) double-fruited spurs in 2013 and (B) single-fruited spurs in 2014. Seed number was categorized in four categories based on distribution: in 2013, N = 54, 57, 51, and 46 for 5–12, 13–16, 17–19, and >19 seeds, respectively; in 2014, N = 261, 103, 202, and 78 for seed numbers of 0–6, 7, 8–9, and >9 seeds, respectively. Different letters indicate significant differences among means based on Tukey test at P < 0.05.

Citation: Journal of the American Society for Horticultural Science 148, 3; 10.21273/JASHS05281-22

Table 3.

Mixed effects logistic regression model of ‘Honeycrisp’ apple of treatments with single-fruited spurs or double-fruited spurs in Spring 2013. Effects of seed number per spur, fruit weight, bourse shoot length, bourse number and fruit number per tree on fruiting spur flower formation.
Table 3.

Statistical models constructed for 2014 treatments showed that seed number had an inhibitory effect on flowering of spurs bearing a single fruit but had no effect on double-fruited spurs (Table 4). When 2014 treatments with single-fruited spurs were divided into four equal categories based on seed number per spur, flower formation was below 10% for all categories. Flowering was highest in spurs with 0 to 6 seeds and lowest in those with 8 to 9 seeds (Fig. 2B). Seed number did not affect spur flower formation for treatments with double-fruited spurs in 2014.

Table 4.

Mixed effects logistic regression model of ‘Honeycrisp’ apple of treatments with single-fruited spurs or double-fruited spurs in Spring 2014. Effects of seed number per spur, fruit weight, bourse shoot length, bourse number and fruit number per tree on fruiting spur flower formation.
Table 4.

Seed number per spur for both single- and double-fruited spurs showed similar distribution patterns in both years. Treatments with single-fruited spurs showed 0 to 18 and 0 to 13 seeds per spur in 2013 and 2014, respectively. Treatments with double-fruited spurs showed 5 to 27 and 8 to 24 seeds per spur in 2013 and 2014, respectively (Fig. 3).

Fig. 3.
Fig. 3.

Frequency distribution of seed number per spur of ‘Honeycrisp’ apple (A) 2013 and (B) 2014.

Citation: Journal of the American Society for Horticultural Science 148, 3; 10.21273/JASHS05281-22

Bourse number and bourse shoot length.

The pattern of number of bourses per spur was similar in both years of this experiment. In each year, ∼40% of spurs had one bourse, 58% had two bourses, and 2% had three bourses (Fig. 4A and B). Bourse number per spur showed a positive linear relationship to flower formation per spur in 2013 (Table 2), with spur flower formation of 31%, 43%, and 62% for spurs that bore one, two, and three bourses, respectively (Fig. 4A). Bourse shoot length had a significant negative effect on flower formation in 2013 (Table 2), but this was only statistically significant for single-fruited spurs in 2013 (Table 3). Bourse shoots were categorized into four equal groups, based on length in 2013, and bourse shoots longer than 16 cm rarely formed flowers (Fig. 5). In 2014, neither bourse shoot length nor bourse number showed a significant effect on fruiting-spur flower formation (Figs. 4B and 5B, Table 2).

Fig. 4.
Fig. 4.

Proportion of ‘Honeycrisp’ apple spurs with different bourse shoot number, and proportion of flower formation for spurs with different bourse shoot number in (A) Summer 2013 and (B) Summer 2014. Different letters indicate significant differences among means based on Tukey test at P < 0.001.

Citation: Journal of the American Society for Horticultural Science 148, 3; 10.21273/JASHS05281-22

Fig. 5.
Fig. 5.

Effect of bourse shoot length on flower formation in ‘Honeycrisp’ apple. Bourse shoot lengths were placed in four categories based on length distribution: (A) Summer 2013, n = 379, 385, 370, and 370 for bourse shoot lengths of 0.2 to 3.2, 3.21 to 8.5, 8.51 to 16.2, and >16.2 cm, respectively. (B) Summer 2014, n = 136, 79, 16, 3, and 160 for bourse shoot lengths of 0.1 to 1.49, 1.5 to 3.49, 3.5 to 9.54, and >9.54 cm, respectively. Different letters indicate highly significant differences among means based on Tukey’s test at P < 0.001.

Citation: Journal of the American Society for Horticultural Science 148, 3; 10.21273/JASHS05281-22

Effect of crop load treatments on total tree flowering, spur, and fruit

On the basis of visual ratings of whole-tree flowering, fruit number per tree had no effect on resting-spur flower formation in either year of this experiment (Fig. 6A and B).

Fig. 6.
Fig. 6.

Bloom rating of ‘Honeycrisp’ apple resting spurs of treated trees: (A) Spring 2013 and (B) Spring 2014. Flower formation was assessed as ratings of 1 to 10 of whole-tree flower formation, where 0 = no flowers and 10 = profuse flowering. One-way analysis of variance showed nonsignificant differences among treatments in both years.

Citation: Journal of the American Society for Horticultural Science 148, 3; 10.21273/JASHS05281-22

Comparison of fruiting-spur growth and development between 2013 and 2014 showed significant differences in almost all studied characteristics. In 2014, spurs had lower flower formation, fruit weight, bourse shoot length, and bourse number compared with 2013 (Table 5).

Table 5.

Changes in ‘Honeycrisp’ apple overall tree growth and development parameters across all crop load treatments over 2 years.
Table 5.

Seed number was positively correlated, and year negatively correlated, with fruit weight for spurs bearing both single- and double-fruited spurs (Table 6). In addition, for single-fruited spurs, fruit weight was negatively affected by fruit number per tree but positively related to bourse shoot length and bourse number per spur (Table 6).

Table 6.

Mixed-effects model for the effect of fruit number per tree, seed number, year, bourse shoot length, and bourse number on ‘Honeycrisp’ apple fruit weight in single- and double-fruited spurs.
Table 6.

Discussion

In 1948, Singh suggested that biennial bearing is a result of a complex process, and many factors including fruiting, growth and development of both the spur and the whole tree, plant growth regulator activities, and the balance between carbohydrate content and nitrogen content influence biennial bearing. In this experiment, crop load both within a spur and on a more general whole tree basis were the main drivers of biennial bearing in ‘Honeycrisp’ apple. Moreover, we found that other factors can also contribute to flower formation of ‘Honeycrisp’ fruiting spurs such as bourse shoot length, bourse number, seed number, and fruit weight (Tables 2 and 3). These factors could possibly gain their impact by affecting the availability of different resources, as suggested by Heinicke (1917) and Singh (1948), both within spurs and the whole tree. In Summer 2014, attributes of fruiting-spur growth and development such as fruit weight, vegetative growth, and flower formation were reduced compared with the previous year (Table 5). This year-to-year variation in growth and development accompanied by severe flower formation inhibition is typical of that seen in cultivars prone to biennial bearing, such as Honeycrisp (Hirst 2017).

General vs. local effect on fruiting spur flower formation.

We suggest that fruiting affects the availability of different resources within fruiting spurs (local effect) and within the whole tree (general effect). Such resource availability may affect resources available to support flower formation on fruiting spurs. The effect of fruiting on different resources such carbohydrate, hormones, and nutrients has been previously described (Grochowska 1973; Heinicke 1917; Johnson and Lakso 1986a, 1986b). However, the effect of fruit number per spur on resource availability has not been reported. The increase in fruit number per spur may increase demand for local, within-spur resources and reduce the resources available for fruiting-spur flower formation. Additionally, the increase in total fruit number per tree likely increased demand for general, whole-tree resources, and thereby reduced fruiting-spur flower formation. Given that flowering and fruiting was lost in 2012, our opinion is that there were enough resources in the trees in Summer 2013 to support flower formation of fruiting spurs, and the availability of those resources to support flower formation decreased as total fruit number per tree increased (Table 2). Hence, for single-fruited spurs, inhibition of flower formation increased as fruit number per tree increased. However, for double-fruited spurs, flower formation was inhibited regardless of the total fruit number per tree, due to the much higher within spur demand for resources (Fig. 1A). On the other hand, in Summer 2014, fruiting suppressed flower formation of fruiting spurs regardless of fruit number per tree or per spur (Fig. 1B). It seems possible that there were not enough stored resources in the trees to overcome the inhibiting effect of fruiting. Hence, our data suggest that fruiting was the main trigger for inhibition of flower formation of fruiting spurs in both years, and fruit number per spur plays a major role inhibiting flower formation (Fig. 1A and B).

Effects of bourse number and bourse shoot length.

Our findings about both bourse shoot length and bourse number are novel and have not been previously reported. We found that more than 50% of ‘Honeycrisp’ spurs formed two bourse shoots, and some spurs formed three bourse shoots. Logically, bourse shoot number per spur correlated positively with flower formation because it increases both local resources and number of meristematic buds per spur. However, the increase in bourse number did not result in a proportional increase in flowering. For every bourse added to the spur, flowering increased by ∼30% to 45% (Fig. 4A).

Bourse shoots in ‘Honeycrisp’ reached up to 80 cm long. In Summer 2013, the on-crop year, bourse shoot length showed a negative linear relationship with flower formation. Bourse shoots longer than 16 cm represented 25% and 13% of total measured bourses in 2013 and 2014, respectively and were almost always nonflowering in both years (Fig. 5). The effect of bourse shoot length on flower formation could be related to the excessive production of MdTFL1 (a negative regulator of apple flowering) required for vegetative growth (Flachowsky et al. 2012; Kotoda et al. 2003), the time of bourse shoot growth termination, or the period during which the bourse functions as a source rather than a sink.

Effect of seeds.

It is well understood for different fruit trees that increased seed number enhances sink strength of fruit and correlates positively with fruit weight (Ho 1992; Keulemans et al. 1996). Heinicke (1917) suggested that apple seeds reinforce the demand by fruit for resources such as carbohydrates, plant growth regulators, and nutrients. In the present study, our data suggest that the effect of seeds on flower formation in ‘Honeycrisp’ is tenuous, and any effect may be related to elevated demand for transported resources from the spurs to the fruit, consequently reducing available resources for other physiological process such as flower formation.

Weinbaum (2001) suggested that the effect of seed number on flower formation was exaggerated and further expressed concerns that the results of Chan and Cain (1967) may be overgeneralized to different cultivars and/or crops. Furthermore, beside the fact that both annual and biennial cultivars are seeded, our results suggest that seeds play neither the most critical role nor a direct role in regulating Honeycrisp flower formation for the following reasons: 1) in Summer 2014, flower formation inhibition occurred in almost all fruiting spurs regardless of seed number per spur (Table 2); 2) in Summer 2013, inhibition of local flower formation in fruiting spurs was affected by fruit number per spur, total fruit number per tree, bourse number, and bourse shoot length, and not only fruit/seeds per spur (Tables 2 and 3); 3) in both studied years, we found some spurs that bore fruit with 0 seeds and did not form flowers, and other spurs that bore fruit with more than 20 seeds and formed flowers (Figs. 2 and 3); 4) the theoretical movement of gibberellins from seeds to meristematic buds suggests a positive correlation between bourse shoot length and flower formation (Chan and Cain 1967; Dennis and Neilsen 1999; Neilsen 1998), because as bourse shoot length increases, gibberellins need to move a longer distance from the seeds to the bourse bud. However, in this study bourse shoot length had a negative linear relationship with flower formation, and bourse shoots more than 16 cm rarely formed flowers (Tables 2 and 3, Fig. 5). Others have suggested that at least for ‘Honeycrisp’ apple, seed number was not an inhibiting factor of flower formation (J.A. Flore, personal communication).

In conclusion, we suggest that ‘Honeycrisp’ spurs are semiautonomous organs because spur characteristics such as fruit weight, fruit number, bourse number, and bourse weight affect flower formation on fruiting spurs under the influence of the year and the total fruit number per tree. Moreover, inhibition of flower formation may be related to the depletion of resources both within the spurs and within the whole tree. Seeds do not play a direct or critical role inhibiting flower formation; however, they likely increase the demand of the fruit for different resources. We report that ∼50% of ‘Honeycrisp’ spurs bear more than one bourse shoot, and bourse shoots longer than 16 cm rarely form flowers. Studying differences in flower formation pathways among annual and biennial cultivars using different fruit number per tree and per spur could pave the way to further explain the irregularity in flower formation of biennial cultivars and explain the complicated networks involved in apple flower formation.

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    • Search Google Scholar
    • Export Citation

  • Elsysy MA & Hirst PM. 2019 Molecular basis of flower formation in apple caused by defoliation and gibberellins J Am Soc Hortic Sci. 144 414 419 https://doi.org/10.21273/jashs04760-19

    • Search Google Scholar
    • Export Citation

  • Elsysy MA, Serra S, Schwallier P, Musacchi S & Einhorn T. 2019 Net enclosure of ‘Honeycrisp’ and ‘Gala’ apple trees at different bloom stages affects fruit set and alters seed production Agronomy (Basel). 9 478 https://doi.org/10.3390/agronomy9090478

    • Search Google Scholar
    • Export Citation

  • Flachowsky H, Szankowski I, Waidmann S, Peil A, Tränkner C & Hanke MV. 2012 The MdTFL1 gene of apple (Malus × domestica Borkh.) reduces vegetative growth and generation time Tree Physiol. 32 1288 1301 https://doi.org/10.1093/treephys/tps080

    • Search Google Scholar
    • Export Citation

  • Fishler M, Goldschmidt EE & Monselise SP. 1983 Leaf area and fruit size in girdled grapefruit branches J Am Soc Hortic Sci. 108 218 221 https://doi.org/10.21273/jashs.108.2.218

    • Search Google Scholar
    • Export Citation

  • Furr JR & Armstrong WW. 1956 Flower induction in ‘Marsh’ grapefruit in the Coachella Valley, California Proc Am Soc Hortic Sci. 67 176 182

  • Glenn DM. 2016 Dry matter partitioning and photosynthetic response to biennial bearing and freeze damage in ‘Empire’ apple Scientia Hortic. 210 1 5 https://doi.org/10.1016/j.scienta.2016.06.042

    • Search Google Scholar
    • Export Citation

  • Goldschmidt EE & Golomb A. 1982 The carbohydrate balance of alternate-bearing citrus trees and the significance of reserves for flowering and fruiting J Am Soc Hortic Sci. 107 206 208 https://doi.org/10.21273/jashs.107.2.206

    • Search Google Scholar
    • Export Citation

  • Griggs WH, Martin GC & Iwakiri BT. 1970 The effect of seedless versus seeded fruit development on flower bud formation in pear J Am Soc Hortic Sci. 95 243 248 https://doi.org/10.21273/jashs.95.2.243

    • Search Google Scholar
    • Export Citation

  • Grochowska MJ. 1973 Comparative studies on physiological and morphological features of bearing and non-bearing spurs of the apple tree, I. Changes in starch content during growth HortScience. 48 347 356 https://doi.org/10.1080/00221589.1973.11514537

    • Search Google Scholar
    • Export Citation

  • Harley CP, Magness JR, Maure MP, Fletcher LA & Degman ES. 1942 Investigations on the cause and control of biennial bearing of apple trees US Dept Agric Tech Bull 792 https://doi.org/10.22004/ag.econ.169095

    • Search Google Scholar
    • Export Citation

  • Heinicke AJ. 1917 Factors influencing the abscission of flowers and partially developed fruits of the apple (Pyrus malus L.). Cornell Univ Agric Exp Sta Bull. 393 https://doi.org/10.5962/bhl.title.36986

    • Search Google Scholar
    • Export Citation

  • Hirst PM. 2017 Advances in understanding flowering and pollination in apple trees Evans K Achieving sustainable cultivation of apples. Burleigh Dodds Sci. Publ. Cambridge, UK https://doi.org/10.19103/as.2016.0017.04

    • Search Google Scholar
    • Export Citation

  • Hirst PM & Ferree DC. 1995 Rootstock effects on the flowering of ‘Delicious’ apple. I. Bud development J Am Soc Hortic Sci. 120 1010 1017 https://doi.org/10.21273/jashs.120.6.1010

    • Search Google Scholar
    • Export Citation

  • Ho LC. 1992 Fruit growth and sink strength Marshall C & Grace J Fruit and seed production: Aspects of development, environmental physiology and ecology. Cambridge Univ Press Cambridge, UK https://doi.org/10.1017/cbo9780511752322.007

    • Search Google Scholar
    • Export Citation

  • Johnson RS & Lakso AN. 1986a Carbon balance model of a growing apple shoot: I. Development of the model J Am Soc Hortic Sci. 111 160 164 https://doi.org/10.21273/jashs.111.2.160

    • Search Google Scholar
    • Export Citation

  • Johnson RS & Lakso AN. 1986b Carbon balance model of a growing apple shoot: II. Simulated effects of light and temperature on long and short shoots J Am Soc Hortic Sci. 111 164 169 https://doi.org/10.21273/jashs.111.2.164

    • Search Google Scholar
    • Export Citation

  • Jones WW, Embleton TW & Coggins CW Jr 1975 Starch content of roots of ‘Kinnow’ mandarin trees bearing fruits in alternate years HortScience. 10 514 https://doi.org/10.21273/hortsci.10.5.514

    • Search Google Scholar
    • Export Citation

  • Jonkers H. 1979 Biennial bearing in apple and pear—Literature survey Scientia Hortic. 11 303 317 https://doi.org/10.1016/0304-4238(79)90015-3

    • Search Google Scholar
    • Export Citation

  • Keulemans J, Brusselle A, Eyssen R, Vercammen J & van Daele G. 1996 Fruit weight in apple as influenced by seed number and pollinizer Acta Hortic. 423 201 210 https://doi.org/10.17660/actahortic.1996.423.26

    • Search Google Scholar
    • Export Citation

  • Kotoda N, Wada M, Masuda T & Soejima J. 2003 The break-through in the reduction of juvenile phase in apple using transgenic approaches Acta Hortic. 625 337 343 https://doi.org/10.17660/actahortic.2003.625.40

    • Search Google Scholar
    • Export Citation

  • Marino F & Greene DW. 1981 Involvement of the gibberellins in the biennial bearing of ‘Early McIntosh’ apples J Am Soc Hortic Sci. 106 593 596 https://doi.org/10.21273/jashs.106.5.593

    • Search Google Scholar
    • Export Citation

  • Marqurard RD. 1987 Influence of leaf to fruit ratio on nut quality, shoot carbohydrates, and photosynthesis of pecan HortScience. 22 256 257 https://doi.org/10.21273/hortsci.22.2.256

    • Search Google Scholar
    • Export Citation

  • Mickelbart MV, Gosney MJ, Camberato J & Stanton KM. 2012 Soil pH effects on growth and foliar nutrient concentrations of Spiraea alba Du Roi and Spiraea tomentosa L HortScience. 47 902 906 https://doi.org/10.21273/HORTSCI.47.7.902

    • Search Google Scholar
    • Export Citation

  • Midwest Fruit Workers 2012 Midwest tree fruit spray guide 2012–2013 Purdue Ext Publ ID-168.

  • Monselise SP & Goldschmidt EE. 1982 Alternate bearing in fruit trees Hortic Rev. 4 128 173 https://doi.org/10.1002/9781118060773.ch5

  • Neilsen JC. 1998 Effects of fruit, seed and shoot development on flower induction in apple PhD Diss Michigan State Univ East Lansing, MI, USA https://doi.org/doi:10.25335/M5222R91R

    • Search Google Scholar
    • Export Citation

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL & Wagner H. 2016 Vegan: Community ecology package R package R Foundation for Statistical Computing Vienna, Austria

    • Search Google Scholar
    • Export Citation

  • Singh LB. 1948 Studies in biennial bearing II. A review of the literature J Hortic Sci. 24 45 65 https://doi.org/10.1080/00221589.1948.11513680

    • Search Google Scholar
    • Export Citation

  • Torsten HB & Frank PW. 2008 Simultaneous inference in general parametric models Biometrical J. 50 346 363 https://doi.org/10.1002/bimj.200810425

  • Tromp J. 1982 Flower bud formation in apple as influenced by various gibberellins HortScience. 57 277 282 https://doi.org/10.1080/00221589.1982.11515053

    • Search Google Scholar
    • Export Citation

  • Venables WN & Ripley BD. 2002 Modern applied statistics with S 4th ed. Springer New York, NY, USA

  • Weinbaum SA, DeJong TM & Maki J. 2001 Reassessment of seed influence on return bloom and fruit growth in ‘Bartlett’ pear HortScience. 36 295 297 https://doi.org/10.21273/hortsci.36.2.295

    • Search Google Scholar
    • Export Citation

  • Xing LB, Zhang D, Li YM, Shen YW, Zhao CP, Ma JJ, An N & Han MY. 2015 Transcription profiles reveal sugar and hormone signaling pathways mediating flower induction in apple (Malus domestica Borkh.) Plant Cell Physiol. 56 2052 2068 https://doi.org/10.1093/pcp/pcv124

    • Search Google Scholar
    • Export Citation
Received:
22 Nov 2022
|
Accepted:
17 Mar 2023
|
Published online:
12 May 2023
|
Published-print:
01 May 2023
Received:
22 Nov 2022
|
Accepted:
17 Mar 2023
|
Published online:
12 May 2023
|
Published-print:
01 May 2023
  • Fig. 1.
    View in gallery
    Fig. 1.

    Flower formation in ‘Honeycrisp’ apple fruiting spurs for treatments with different fruit number per spur and different fruit number per tree in (A) Summer 2013 and (B) Summer 2014. Slopes describing the response of flowering to different crop loads from trees with single-fruited spurs and those with double-fruited spurs were different (P = 0.018) in 2013 only. Data points represent the mean of six single-tree replicates and standard errors are indicated.

  • Fig. 2.
    View in gallery
    Fig. 2.

    Effect of seed number per spur on flower formation and fruit weight in ‘Honeycrisp’ apple spurs (A) double-fruited spurs in 2013 and (B) single-fruited spurs in 2014. Seed number was categorized in four categories based on distribution: in 2013, N = 54, 57, 51, and 46 for 5–12, 13–16, 17–19, and >19 seeds, respectively; in 2014, N = 261, 103, 202, and 78 for seed numbers of 0–6, 7, 8–9, and >9 seeds, respectively. Different letters indicate significant differences among means based on Tukey test at P < 0.05.

  • Fig. 3.
    View in gallery
    Fig. 3.

    Frequency distribution of seed number per spur of ‘Honeycrisp’ apple (A) 2013 and (B) 2014.

  • Fig. 4.
    View in gallery
    Fig. 4.

    Proportion of ‘Honeycrisp’ apple spurs with different bourse shoot number, and proportion of flower formation for spurs with different bourse shoot number in (A) Summer 2013 and (B) Summer 2014. Different letters indicate significant differences among means based on Tukey test at P < 0.001.

  • Fig. 5.
    View in gallery
    Fig. 5.

    Effect of bourse shoot length on flower formation in ‘Honeycrisp’ apple. Bourse shoot lengths were placed in four categories based on length distribution: (A) Summer 2013, n = 379, 385, 370, and 370 for bourse shoot lengths of 0.2 to 3.2, 3.21 to 8.5, 8.51 to 16.2, and >16.2 cm, respectively. (B) Summer 2014, n = 136, 79, 16, 3, and 160 for bourse shoot lengths of 0.1 to 1.49, 1.5 to 3.49, 3.5 to 9.54, and >9.54 cm, respectively. Different letters indicate highly significant differences among means based on Tukey’s test at P < 0.001.

  • Fig. 6.
    View in gallery
    Fig. 6.

    Bloom rating of ‘Honeycrisp’ apple resting spurs of treated trees: (A) Spring 2013 and (B) Spring 2014. Flower formation was assessed as ratings of 1 to 10 of whole-tree flower formation, where 0 = no flowers and 10 = profuse flowering. One-way analysis of variance showed nonsignificant differences among treatments in both years.

Fig. 1.

Flower formation in ‘Honeycrisp’ apple fruiting spurs for treatments with different fruit number per spur and different fruit number per tree in (A) Summer 2013 and (B) Summer 2014. Slopes describing the response of flowering to different crop loads from trees with single-fruited spurs and those with double-fruited spurs were different (P = 0.018) in 2013 only. Data points represent the mean of six single-tree replicates and standard errors are indicated.
Fig. 2.

Effect of seed number per spur on flower formation and fruit weight in ‘Honeycrisp’ apple spurs (A) double-fruited spurs in 2013 and (B) single-fruited spurs in 2014. Seed number was categorized in four categories based on distribution: in 2013, N = 54, 57, 51, and 46 for 5–12, 13–16, 17–19, and >19 seeds, respectively; in 2014, N = 261, 103, 202, and 78 for seed numbers of 0–6, 7, 8–9, and >9 seeds, respectively. Different letters indicate significant differences among means based on Tukey test at P < 0.05.
Fig. 3.

Frequency distribution of seed number per spur of ‘Honeycrisp’ apple (A) 2013 and (B) 2014.
Fig. 4.

Proportion of ‘Honeycrisp’ apple spurs with different bourse shoot number, and proportion of flower formation for spurs with different bourse shoot number in (A) Summer 2013 and (B) Summer 2014. Different letters indicate significant differences among means based on Tukey test at P < 0.001.
Fig. 5.

Effect of bourse shoot length on flower formation in ‘Honeycrisp’ apple. Bourse shoot lengths were placed in four categories based on length distribution: (A) Summer 2013, n = 379, 385, 370, and 370 for bourse shoot lengths of 0.2 to 3.2, 3.21 to 8.5, 8.51 to 16.2, and >16.2 cm, respectively. (B) Summer 2014, n = 136, 79, 16, 3, and 160 for bourse shoot lengths of 0.1 to 1.49, 1.5 to 3.49, 3.5 to 9.54, and >9.54 cm, respectively. Different letters indicate highly significant differences among means based on Tukey’s test at P < 0.001.
Fig. 6.

Bloom rating of ‘Honeycrisp’ apple resting spurs of treated trees: (A) Spring 2013 and (B) Spring 2014. Flower formation was assessed as ratings of 1 to 10 of whole-tree flower formation, where 0 = no flowers and 10 = profuse flowering. One-way analysis of variance showed nonsignificant differences among treatments in both years.

  • Abbott DL. 1960 The bourse shoot as a factor in the growth of apple trees Ann Appl Biol. 48 434 438 https://doi.org/10.1111/j.1744-7348.1960.tb03546.x

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  • Arakawa O, Kanno K, Kanetsuka A & Shiozaki Y. 1997 Effects of girdling and bark inversion on tree growth and fruit quality of apple Acta Hortic. 451 579 585 https://doi.org/10.17660/ActaHortic.1997.451.67

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  • Bangerth F. 2006 Flower induction in perennial fruit trees: Still an enigma? Acta Hortic. 727 177 195 https://doi.org/10.17660/actahortic.2006.727.20

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  • Bates D, Kliegl R, Vasishth S & Baayen RH. 2018 Parsimonious mixed models arXiv 1506 https://doi.org/10.48550/arXiv.1506.04967

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  • Davis JT & Sparks D. 1974 Assimilation and translocation patterns of carbon 14 in the shoot of fruiting pecan trees Carya illinoensis Koch J Am Soc Hortic Sci. 99 468 480 https://doi.org/10.21273/jashs.99.5.468

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  • Davis LD. 1957 Flowering and alternate bearing Proc Am Soc Hortic Sci. 70 545 556

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  • Dennis FG Jr & Neilsen JC. 1999 Physiological factors affecting biennial bearing in tree fruit: The role of seeds in apple HortTechnology. 9 317 322 https://doi.org/10.21273/horttech.9.3.317

    • Search Google Scholar
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  • Elsysy MA & Hirst PM. 2017 The role of spur leaves, bourse leaves, and fruit on local flower formation in apple: An approach to understanding biennial bearing HortScience. 52 1229 1232 https://doi.org/10.21273/hortsci12136-17

    • Search Google Scholar
    • Export Citation

  • Elsysy MA, Mickelbart MV & Hirst PM. 2018 Effect of fruiting and biennial bearing potential on spur quality and leaf gas exchange in apple J Am Soc Hortic Sci. 144 31 37 https://doi.org/10.21273/jashs04524-18

    • Search Google Scholar
    • Export Citation

  • Elsysy MA & Hirst PM. 2019 Molecular basis of flower formation in apple caused by defoliation and gibberellins J Am Soc Hortic Sci. 144 414 419 https://doi.org/10.21273/jashs04760-19

    • Search Google Scholar
    • Export Citation

  • Elsysy MA, Serra S, Schwallier P, Musacchi S & Einhorn T. 2019 Net enclosure of ‘Honeycrisp’ and ‘Gala’ apple trees at different bloom stages affects fruit set and alters seed production Agronomy (Basel). 9 478 https://doi.org/10.3390/agronomy9090478

    • Search Google Scholar
    • Export Citation

  • Flachowsky H, Szankowski I, Waidmann S, Peil A, Tränkner C & Hanke MV. 2012 The MdTFL1 gene of apple (Malus × domestica Borkh.) reduces vegetative growth and generation time Tree Physiol. 32 1288 1301 https://doi.org/10.1093/treephys/tps080

    • Search Google Scholar
    • Export Citation

  • Fishler M, Goldschmidt EE & Monselise SP. 1983 Leaf area and fruit size in girdled grapefruit branches J Am Soc Hortic Sci. 108 218 221 https://doi.org/10.21273/jashs.108.2.218

    • Search Google Scholar
    • Export Citation

  • Furr JR & Armstrong WW. 1956 Flower induction in ‘Marsh’ grapefruit in the Coachella Valley, California Proc Am Soc Hortic Sci. 67 176 182

  • Glenn DM. 2016 Dry matter partitioning and photosynthetic response to biennial bearing and freeze damage in ‘Empire’ apple Scientia Hortic. 210 1 5 https://doi.org/10.1016/j.scienta.2016.06.042

    • Search Google Scholar
    • Export Citation

  • Goldschmidt EE & Golomb A. 1982 The carbohydrate balance of alternate-bearing citrus trees and the significance of reserves for flowering and fruiting J Am Soc Hortic Sci. 107 206 208 https://doi.org/10.21273/jashs.107.2.206

    • Search Google Scholar
    • Export Citation

  • Griggs WH, Martin GC & Iwakiri BT. 1970 The effect of seedless versus seeded fruit development on flower bud formation in pear J Am Soc Hortic Sci. 95 243 248 https://doi.org/10.21273/jashs.95.2.243

    • Search Google Scholar
    • Export Citation

  • Grochowska MJ. 1973 Comparative studies on physiological and morphological features of bearing and non-bearing spurs of the apple tree, I. Changes in starch content during growth HortScience. 48 347 356 https://doi.org/10.1080/00221589.1973.11514537

    • Search Google Scholar
    • Export Citation

  • Harley CP, Magness JR, Maure MP, Fletcher LA & Degman ES. 1942 Investigations on the cause and control of biennial bearing of apple trees US Dept Agric Tech Bull 792 https://doi.org/10.22004/ag.econ.169095

    • Search Google Scholar
    • Export Citation

  • Heinicke AJ. 1917 Factors influencing the abscission of flowers and partially developed fruits of the apple (Pyrus malus L.). Cornell Univ Agric Exp Sta Bull. 393 https://doi.org/10.5962/bhl.title.36986

    • Search Google Scholar
    • Export Citation

  • Hirst PM. 2017 Advances in understanding flowering and pollination in apple trees Evans K Achieving sustainable cultivation of apples. Burleigh Dodds Sci. Publ. Cambridge, UK https://doi.org/10.19103/as.2016.0017.04

    • Search Google Scholar
    • Export Citation

  • Hirst PM & Ferree DC. 1995 Rootstock effects on the flowering of ‘Delicious’ apple. I. Bud development J Am Soc Hortic Sci. 120 1010 1017 https://doi.org/10.21273/jashs.120.6.1010

    • Search Google Scholar
    • Export Citation

  • Ho LC. 1992 Fruit growth and sink strength Marshall C & Grace J Fruit and seed production: Aspects of development, environmental physiology and ecology. Cambridge Univ Press Cambridge, UK https://doi.org/10.1017/cbo9780511752322.007

    • Search Google Scholar
    • Export Citation

  • Johnson RS & Lakso AN. 1986a Carbon balance model of a growing apple shoot: I. Development of the model J Am Soc Hortic Sci. 111 160 164 https://doi.org/10.21273/jashs.111.2.160

    • Search Google Scholar
    • Export Citation

  • Johnson RS & Lakso AN. 1986b Carbon balance model of a growing apple shoot: II. Simulated effects of light and temperature on long and short shoots J Am Soc Hortic Sci. 111 164 169 https://doi.org/10.21273/jashs.111.2.164

    • Search Google Scholar
    • Export Citation

  • Jones WW, Embleton TW & Coggins CW Jr 1975 Starch content of roots of ‘Kinnow’ mandarin trees bearing fruits in alternate years HortScience. 10 514 https://doi.org/10.21273/hortsci.10.5.514

    • Search Google Scholar
    • Export Citation

  • Jonkers H. 1979 Biennial bearing in apple and pear—Literature survey Scientia Hortic. 11 303 317 https://doi.org/10.1016/0304-4238(79)90015-3

    • Search Google Scholar
    • Export Citation

  • Keulemans J, Brusselle A, Eyssen R, Vercammen J & van Daele G. 1996 Fruit weight in apple as influenced by seed number and pollinizer Acta Hortic. 423 201 210 https://doi.org/10.17660/actahortic.1996.423.26

    • Search Google Scholar
    • Export Citation

  • Kotoda N, Wada M, Masuda T & Soejima J. 2003 The break-through in the reduction of juvenile phase in apple using transgenic approaches Acta Hortic. 625 337 343 https://doi.org/10.17660/actahortic.2003.625.40

    • Search Google Scholar
    • Export Citation

  • Marino F & Greene DW. 1981 Involvement of the gibberellins in the biennial bearing of ‘Early McIntosh’ apples J Am Soc Hortic Sci. 106 593 596 https://doi.org/10.21273/jashs.106.5.593

    • Search Google Scholar
    • Export Citation

  • Marqurard RD. 1987 Influence of leaf to fruit ratio on nut quality, shoot carbohydrates, and photosynthesis of pecan HortScience. 22 256 257 https://doi.org/10.21273/hortsci.22.2.256

    • Search Google Scholar
    • Export Citation

  • Mickelbart MV, Gosney MJ, Camberato J & Stanton KM. 2012 Soil pH effects on growth and foliar nutrient concentrations of Spiraea alba Du Roi and Spiraea tomentosa L HortScience. 47 902 906 https://doi.org/10.21273/HORTSCI.47.7.902

    • Search Google Scholar
    • Export Citation

  • Midwest Fruit Workers 2012 Midwest tree fruit spray guide 2012–2013 Purdue Ext Publ ID-168.

  • Monselise SP & Goldschmidt EE. 1982 Alternate bearing in fruit trees Hortic Rev. 4 128 173 https://doi.org/10.1002/9781118060773.ch5

  • Neilsen JC. 1998 Effects of fruit, seed and shoot development on flower induction in apple PhD Diss Michigan State Univ East Lansing, MI, USA https://doi.org/doi:10.25335/M5222R91R

    • Search Google Scholar
    • Export Citation

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL & Wagner H. 2016 Vegan: Community ecology package R package R Foundation for Statistical Computing Vienna, Austria

    • Search Google Scholar
    • Export Citation

  • Singh LB. 1948 Studies in biennial bearing II. A review of the literature J Hortic Sci. 24 45 65 https://doi.org/10.1080/00221589.1948.11513680

    • Search Google Scholar
    • Export Citation

  • Torsten HB & Frank PW. 2008 Simultaneous inference in general parametric models Biometrical J. 50 346 363 https://doi.org/10.1002/bimj.200810425

  • Tromp J. 1982 Flower bud formation in apple as influenced by various gibberellins HortScience. 57 277 282 https://doi.org/10.1080/00221589.1982.11515053

    • Search Google Scholar
    • Export Citation

  • Venables WN & Ripley BD. 2002 Modern applied statistics with S 4th ed. Springer New York, NY, USA

  • Weinbaum SA, DeJong TM & Maki J. 2001 Reassessment of seed influence on return bloom and fruit growth in ‘Bartlett’ pear HortScience. 36 295 297 https://doi.org/10.21273/hortsci.36.2.295

    • Search Google Scholar
    • Export Citation

  • Xing LB, Zhang D, Li YM, Shen YW, Zhao CP, Ma JJ, An N & Han MY. 2015 Transcription profiles reveal sugar and hormone signaling pathways mediating flower induction in apple (Malus domestica Borkh.) Plant Cell Physiol. 56 2052 2068 https://doi.org/10.1093/pcp/pcv124

    • Search Google Scholar
    • Export Citation
Mokhles A. Elsysy Department of Horticulture and Landscape Architecture, Purdue University, 625 Agriculture Mall Drive, West Lafayette, IN 47907, USA, and Department of Pomology, College of Agriculture, Assiut University, Assiut 71526, Egypt

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Peter M. Hirst Department of Horticulture and Landscape Architecture, Purdue University, 625 Agriculture Mall Drive, West Lafayette, IN 47907, USA

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Contributor Notes

We thank Bruce Craig and Rongrong Zhang from the Purdue Statistical Consulting Service for their advice on statistical design and analysis. M.A.E. thanks lab mates Khalil Jahed, Jacob Franzen, Biying Shi, Fatemeh Sheibani, Seval Taskin, and Bofan Xie for their help during different phases of this experiment.

P.M.H. is the corresponding author. E-mail: hirst@purdue.edu.

Received:
22 Nov 2022
|
Accepted:
17 Mar 2023
|
Published online:
12 May 2023
|
Published-print:
01 May 2023
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