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Keywords:

  • allometry;
  • apple (Malus domestica);
  • flowering pattern;
  • fruit and shoot size;
  • parent branch;
  • reproductive shoot;
  • return-bloom;
  • vegetative shoot

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • • 
    In apple (Malus domestica), the size of a shoot and the vegetative or reproductive fate of the terminal bud on that shoot are considered to be related phenomena but with contrasted results depending on studies. Our hypothesis was that these relationships would be partly cultivar-dependent.
  • • 
    Over a 3-yr period, the size relationships between shoots and fruit on two architecturally contrasted apple cultivars were assessed. For shoots, flowering frequency (dependent variable) was related to subtending shoot size (independent variable).
  • • 
    Linear correlations were adjusted for size relationships between contiguous shoots in the same year (inflorescence vs bourse-shoot), and between years with differences in slopes and intercepts between the two cultivars. The relationships between the size of a shoot and flowering frequency differed between the two cultivars, with high flowering whatever shoot size vs parabolic relationships between the two variables, respectively.
  • • 
    It is concluded that the relationships between shoot size and fate are cultivar-dependent. It is speculated that the flowering pattern not only depends on the property of the shoot alone, but also on the structural proportions of the parent branch and branching density.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The growth and flowering habit of the whole plant results from a network of growth correlations, or allometric relationships, between plant parts, either closely related, such as length and width of a leaf, or spatially and/or temporally distinct, such as shoot and root growth (Champagnat, 1974; Pieters, 1974; Niklas & Enquist, 2002). These relationships have been addressed through two complementary themes.

The first is the quantitative relationship between the size (i.e. weight, length, number of subunits such as leaves) of organs whose development can be concomitant (e.g. follicule and seeds) or dephased in its morphological expression (e.g. in temperate climate, shoot growth during a growing season and terminal flowering during the spring of the next growing season). The correlations are usually positive and a common interpretation is that they reflect the functional requirements (e.g. mechanical support, vascular supply) for scaling. Studies have been carried out on either vegetative (Barcellos de Souza et al., 1986; Niklas, 1993; Brouat et al., 1998) or reproductive (Midgley et al., 1991; Goldschmidt & Koch, 1996) features. Other studies have documented the size relationships between vegetative and reproductive features (Midgley & Bond, 1989; Niklas, 1993; Vaughton, 1993; Lauri et al., 1996).

The second theme is that the size of a shoot may partly determine the vegetative or reproductive fate of the shoot that develops in terminal position. The positive effects of leaf area on flowering are well documented in trees and annual plants (Harley et al., 1942; Huet, 1972; Hempel et al., 2000). In apple, the number of leaves or length of a shoot, at least within certain limits, increases the frequency of flowering in terminal position on this shoot (Chan & Cain, 1967; Neilsen & Dennis, 2000). These results are in agreement with the documented relationship between the length of the flowering shoot and the tendency to have an alternate compared with a regular flowering pattern on individual shoots: cultivars with a high proportion of short fruiting shoots (spur type) usually have a strong alternate bearing tendency, whereas cultivars with longer shoots (tip-bearing type) are able to flower annually (Looney & Lane, 1984; Lauri & Lespinasse, 1993; Davenport, 2000). However, other results suggest an inverse relationship between shoot growth vigor and flowering (Forshey & Elfving, 1989; Zhu et al., 1997). Therefore, it is likely that shoot length or number of leaves alone is not sufficient to determine the fate of the terminal bud. It has been proposed that seeds counteract leaf area positive effects on flowering via either the production of an inhibitor or the competition for a flowering promoter (Chan & Cain, 1967; Hoad, 1984; Dennis & Neilsen, 1999). A simple hormonal mechanism is, however, still controversial (Barlow, 1994) and the importance of nutritional factors, for example the role of seeds in increasing fruit sink strength, is also stressed (Weinbaum et al., 2001).

Our hypothesis was that the differences observed in the relationships between shoot size and fate would be partly cultivar dependent. We chose the apple as model because the relationships between vegetative growth and flowering as a function of cultivar are well documented in this species (Lauri et al., 1995). In apple, the inflorescence or bourse is made up, in acropetal sequence, of a vegetative part (transitional and foliage leaves) followed by a terminal determinate flower cluster (Pratt, 1988). A relay-axis, the bourse-shoot, may develop at the axil of one or more foliage leaves of the inflorescence. Each bourse-shoot and its bearing inflorescence will be hereafter referred to as a reproductive shoot. The role of the entire reproductive shoot in carbohydrate support for fruit development is documented (Abbott, 1960). In some cases there is no bourse-shoot development leading to the death of that branch (extinction phenomenon; Lauri et al., 1995). Flowering is lateral on long shoots (i.e. with long internodes; as a rule of thumb, 5 cm; Wünsche et al., 2000) and terminal on long and short shoots. In any given position within the tree architecture, a branch is made up of a sequence of vegetative and/or reproductive annual shoots. If all consecutive terminal buds of the branch are vegetative, the sequence determines a strictly monopodial growth, that is the branch results from the growth of a single meristem. If not, the sequence determines a partial or total sympodial growth, that is the branch results from the growth of more than one meristem (Lauri et al., 1995). In this paper the emphasis will be on the size and fate relationships between contiguous organs (vegetative or reproductive shoot, fruit) through either apical (i.e. monopodial) growth, or subterminal branching (i.e. sympodial growth) process (Godin & Caraglio, 1998), in the same year and across three consecutive years. We assumed that the shoot was an autonomous entity and that this level of analysis was relevant to analyze size and fate relationships. The study was carried out to answer the three following questions: first, what are the size relationships between contiguous organs in the same year (i.e. between inflorescence and bourse-shoot, and between reproductive shoot and fruit) and between years (i.e. shoot size relationships between two consecutive years)? Second, how does the size of a shoot affect the fate of the shoot it gives rise to in the following year? And third, are these relationships cultivar-dependent?

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Cultivars and study sites

Two cultivars issued from the INRA (Institut National de la Recherche Agronomique) breeding program, were chosen for their contrasting growth and flowering habit (Lauri & Lespinasse, 2001). The cultivar ‘Pitchounette’, formerly known as the advanced selection X.3318 (Lauri & Lespinasse, 2001), has a strong tendency to alternate vegetative and reproductive shoots from one year to the next on the same branch. It is characterized by upright growth and develops strong water sprouts in response to natural or artificial bending. The cultivar Belchard ‘Chantecler’, hereafter referred to as ‘Chantecler’, has a regular pattern of flowering. It has a wider intrinsic branch angle than ‘Pitchounette’, with no substantial branch renewal in response to bending.

Branch analysis was carried out in the INRA experimental field of Toulenne near Bordeaux, South-West of France (44°33′-N, 0°16′-W). Forty-five trees per cultivar, grafted onto Malling 9 (M.9) rootstock, were planted in 1993 in two adjacent rows, a cultivar per row, with planting distances of 5 m between the rows and 2 m between trees within the row. The trees were trained as small solaxe trees (Lespinasse, 1996) to facilitate observations, with the scaffold branches maintained in a horizontal position along a wire at a height of c. 2.2 m. This system allowed secondary branches, that is branches directly attached to the scaffold branches, to develop freely on each side of the row. These secondary branches, hereafter referred to as parent branches bore the studied shoots (Fig. 1). The branches were not subjected to any bending or pruning treatment during the 3-yr trial. Chemical fruit thinning was performed and supplemented by hand-thinning at the end of the physiological drop (end of May) to leave one fruit per inflorescence.

image

Figure 1. Scheme of a 4-yr-old apple (Malus domestica) branch with the parent branch developed in year Y bearing shoots in lateral and terminal position. Each consecutive shoot growth increment was categorized by year of development (first, second and third year after parent branch growth; Y1, Y2 and Y3, respectively), and fate (shoot type: vegetative, V; reproductive, R). Data were collected on each new annual growth increment for size (for shoot and fruit) and fate in Y1 and Y2, and for fate only in Y3.

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Data collection

At the end of the spring of 1995 (year Y), 50 growing parent branches during their first year of growth, of approximately the same length and orientation, were selected for each cultivar. The following year (year Y1), all growing shoots that developed in lateral and terminal positions on the parent branch were classified into one of the following two shoot types: vegetative (V) and reproductive (R). Shoot size was assessed by counting foliage leaves, that is those that were more than 3 cm long, rather than measuring metric length or volume, for the following two reasons: first it gives a more reliable and discriminating measure of growth for short shoots, and second it relies more on the developmental stage of the shoot (Sachs, 1999). In the following, leaves will then refer to foliage leaves only. The number of leaves of the inflorescence, and of bourse-shoot and vegetative shoot was determined at flowering, and at the end of the growing season, respectively. At harvest, around mid-September for ‘Pitchounette’ and the beginning of October for ‘Chantecler’, individual fruits were collected. Fruit size was assessed by measuring maximal fruit transverse diameter.

The following year (year Y2) each previously described shoot resumed its growth through either apical growth or branching process, and was reclassified into one of the shoot type categories, based upon the fate of the terminal bud that year. Similar data as in year Y1 were collected on each shoot. Lateral branching on these shoots was not considered. During the following spring (year Y3), the new growth increment was again recorded and classified into one of the shoot type categories. No size data were collected in the third year (Fig. 1).

Data analysis

Statistical analyses were done considering the number of leaves of the subtending shoot as the independent variable and the variables characterizing the supported organ, that is number of leaves, fruit diameter and flowering rate (ratio of the number of reproductive shoots to the total number of shoots in that year), as dependent variables. For each number of leaves of the subtending shoot, these dependent variables contained either a series of observed values (for the number of leaves and fruit diameter) or a proportion (for the flowering rate). As a rule of thumb, only classes of leaves of the subtending shoot with five and more values of the dependent variable were considered.

For R shoots with a developed bourse-shoot, the sum of the number of leaves of the inflorescence and of the associated bourse-shoot was calculated. If more than one bourse-shoot developed on a same inflorescence, each bourse-shoot was considered separately along with its bearing bourse. Up to 15% and 47% of bourse-shoots on the same inflorescence, for ‘Chantecler’ and ‘Pitchounette’, respectively, were grouped, usually by two (data not shown). The relationships between the number of leaves and fruit diameter in the same year were examined for fruitful reproductive shoots with only one bourse-shoot.

Three types of analysis were performed. The first one concerns a multiple mean comparison between cultivars and years of shoot development of the mean values of the number of leaves of R shoot components (inflorescence, bourse shoot, whole R shoot), and of the proportion of inflorescences with no leaves and fruit-set (proportion of inflorescences with at least one fruit over total number of inflorescences). The Newman-Keuls test was used to compare the mean numbers of leaves. A Kruskal–Wallis test adapted to nonnormally distributed data was used when comparing proportions of inflorescences with no leaves or fruit-set.

Then the relationship between dependent variables and the number of leaves of the subtending shoot was studied. To this aim, the second type of analysis was conducted considering characteristics of the supported organs, either the number of leaves of shoot in the following year or fruit diameter in the same year, as dependent variables. The relationship, either in the same year or from one year to another, was investigated. In each case, to have an idea of the joint evolution tendency of variables, a linear adjustment was made through the points. When appropriate (relationships between number of leaves of shoot in Y1 and number of leaves of shoot in Y2, Fig. 4) we also tried a parabolic adjustment and tested the quadratic term for significance. However, whatever the result we keep through the linear model a global view on the general joint evolution. Let us note here that estimated regression lines and correlations were calculated using the whole set of points but for simplicity only means and standard deviations for each class are indicated on the plot. In this linear modeling, differences in slopes and intercepts were tested from one year of shoot development to another, or from one cultivar to another, or finally from one transition type to another. For this, a covariance analysis was used considering the independent variable (number of leaves of the inflorescence, Fig. 2 and Table 1; number of leaves of shoot in Y1, Fig. 4 and Table 2) as a covariate and either year of shoot development or cultivar or transition type as a factor (R software, version 1.6.1; http://www.r-project.org). In this setting, testing for the effect of interaction between covariate and factor or for the effect of factor is equivalent to testing for differences in slopes and intercepts, respectively.

image

Figure 4. Relationships between the number of leaves of R or V shoots in Y1 and the number of leaves of R or V shoots in Y2, for apple (Malus domestica) (a) ‘Chantecler’ and (b) ‘Pitchounette’. Each symbol (± SD) represents the mean of at least five shoots. Regression line equations: ‘Chantecler’‘R to R’: y = 0.997x + 4.562, R2 = 0.526; ‘Chantecler’‘V to R’: y = 1.385x + 2.005, R2 = 0.635. ‘Pitchounette’‘R to R’: y = 0.633x + 11.147, R2 = 0.138; ‘Pitchounette’‘V to R’: y = 0.656x + 10.424, R2 = 0.392; ‘Pitchounette’‘V to V’: y = 0.750x + 3.745, R2 = 0.617; ‘Pitchounette’‘R to V’: y = 0.185x + 18.613, R2 = 0.003.

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image

Figure 2. Relationships between the number of leaves of the inflorescence and the number of leaves of the associated bourse-shoot in Y1 and Y2, for apple (Malus domestica) ‘Chantecler’ and ‘Pitchounette’. Each symbol (± SD) represents the mean of at least five shoots. Regression line equations: ‘Chantecler’ Y1: y = 2.561x + 1.879, R2 = 0.352; ‘Chantecler’ Y2: y = 2.548x + 1.809, R2 = 0.528. ‘Pitchounette’ Y1: y = 0.980x + 0.375, R2 = 0.010; ‘Pitchounette’ Y2: y = 2.382x −5.552, R2 = 0.144.

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Table 1.  Tests for homogeneity of slopes of the number of leaves of the bourse-shoot with the number of leaves of the inflorescence as the covariate and year of shoot development (Y1, Y2) as the factor, for apple (Malus domestica) ‘Chantecler’ and ‘Pitchounette’ (see Fig. 2)
CultivarFP
  • 1

    Model with identical slopes.

  • 2

    Model with different slopes.

‘Chantecler’
Differences between slopes 0.0030.957
Differences between intercepts1 0.0390.844
‘Pitchounette’
Differences between slopes11.1570.037
Differences between intercepts2 4.3890.001
Table 2.  Tests for homogeneity of slopes of (a) the number of leaves of all shoots in Y2 with the number of leaves of the shoot which developed in the previous year, Y1, as the covariate and the apple (Malus domestica) cultivar (‘Chantecler’, ‘Pitchounette’) as the factor, and (b) the number of leaves of the shoot (R or V) in Y2 with the number of leaves of the shoot which developed in the previous year (Y1) as the covariate and the transition (‘R to R’, ‘R to V’, ‘V to R’ and ‘V to V’) as the factor, for ‘Chantecler’ and ‘Pitchounette’ (see Fig. 4)
ComparisonsFP
  • 1

    Model with identical slopes.

  • 2

    Model with different slopes.

(a) ‘Chantecler’ vs ‘Pitchounette’– all transitions between Y1 and Y2
Differences between slopes 62.5184.169 × 10−15
Differences between intercepts2 18.1682.109 × 10−5
(b) Cultivar/Type of transition between Y1 and Y2
‘Chantecler’
‘R to R’–‘V to R’
Differences between slopes  6.2860.013
Differences between intercepts2  1.9620.162
‘Pitchounette‘
‘R to R’–‘V to R’
Differences between slopes  0.0620.804
Differences between intercepts1  0.8050.370
‘R to R’–‘V to V’
Differences between slopes  1.0830.299
Differences between intercepts1 60.7646.374 × 10−14
‘R to R’–‘R to V’
Differences between slopes  1.8040.180
Differences between intercepts1  8.4410.004
‘V to R’–‘R to V’
Differences between slopes  3.9560.047
Differences between intercepts2 16.0526.488 × 10−5
‘V to R’–‘V to V’
Differences between slopes  2.6190.106
Differences between intercepts1104.6702.200 × 10−16
‘R to V’–‘V to V’
Differences between slopes  3.8010.052
Differences between intercepts1 81.4112.200 × 10−16

Eventually the third type of analysis consisted of studying the relationship between dependent and independent variables considering the percentage of flowering as a dependent variable. In this case a quadratic adjustment was made and a comparison of maximum location, that is number of leaves at maximum frequency of flowering, and maximum value, that is maximum frequency of flowering, between curves, was tested. To compare maximum location between two curves, a deviance F-test between embedded models was set up, defining as submodel the model with constraint of maximum located at the same place. As for comparisons of maximum values, the standard error of the difference was calculated based on the covariance matrix of the model parameters and a Z-test was then used.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

R shoot component characteristics and size relationships within a same year

‘Chantecler’ had a significantly higher number of inflorescences with no leaves, a lower number of leaves on inflorescence, and a lower fruit-set in both Y1 and Y2 compared with ‘Pitchounette’ (Table 3). The number of bourse-shoot leaves was higher in Y1 compared with Y2 on ‘Chantecler’, whereas the reverse was true for ‘Pitchounette’ (Table 3). As a whole, R shoots had more leaves on ‘Pitchounette’ compared with ‘Chantecler’. There was a positive relationship between the number of leaves of the inflorescence and of the associated bourse-shoot in Y1 and Y2 of ‘Chantecler’ (Fig. 2). Although weaker and possibly nul (Y1), the same trend was observed for ‘Pitchounette’ (Fig. 2). For each cultivar, comparison of slopes and intercepts in models for the number of leaves of the bourse-shoot with the number of leaves of the inflorescence as the covariate and year of shoot development as the factor, is presented in Table 1. For ‘Chantecler’, there were no significant differences in intercepts and slopes for the relationships between the two variables in Y1 and Y2. For ‘Pitchounette’, the linear correlation was weaker in Y1 than in Y2 (Fig. 2), with significant differences between slopes and intercepts of the 2 yr of shoot development.

Table 3.  Number of leaves of inflorescence (inflorescences with at least one leaf), bourse-shoot, and R shoot (per reproductive shoot, mean ± SD), and proportion of inflorescences with no leaves, and fruit-set (per branch, mean ± SD) in Y1 and Y2, for apple (Malus domestica) ‘Chantecler’ and ‘Pitchounette’
Cultivar and Year of shoot developmentNumber of leavesInflorescences with no leaves2Fruit-set2
NR1InflorescenceBourse-shootTotal R shoot
  • 1

    Number of reproductive shoots.

  • 2

    On a parent branch basis (45–50 branches depending on cultivar and year of shoot development).

  • 3

    Within a column, means with the same letter are not significantly different; multiple mean comparison by Newman-Keuls (for numbers) or Kruskal–Wallis (for proportions) test (P < 0.05).

‘Chantecler’
 Y1 3733.0 ± 1.9 d39.7 ± 8.6 a312.7 ± 9.9 b30.37 ± 0.20 a30.21 ± 0.16 b3
 Y2 4484.9 ± 2.3 c5.0 ± 2.3 c10.0 ± 4.7 c0.10 ± 0.09 b0.34 ± 0.21 b
‘Pitchounette’
 Y1 3635.4 ± 1.8 b7.0 ± 6.0 b12.4 ± 6.7 b0.01 ± 0.03 c0.71 ± 0.36 a
 Y216077.1 ± 1.4 a9.0 ± 7.9 a16.2 ± 8.6 a0.00 ± 0.00 c0.83 ± 0.16 a

Fruit diameter was lower for ‘Pitchounette’ (maximum values of 68 mm and 77 mm in Y1 and Y2, respectively) than for ‘Chantecler’ (maximum values of 72 mm and 89 mm for Y1 and Y2, respectively), with lower fruit diameter in Y1 compared with Y2 (Fig. 3). For both cultivars, the number of leaves of fruitful R shoots was lower in Y1 than in Y2 (up to 12 leaves in Y1 compared with 35 leaves in Y2, Fig. 3).Considering separately the 2 yr of shoot development, there was no or only a weak correlation between the number of leaves of R shoot and fruit diameter. However, notably on ‘Chantecler’, combining data from Y1 and Y2 and thus extending the range of variation of both variables, would show a positive relationship between the number of leaves of R shoot and fruit diameter due to the year of shoot development (Fig. 3).

image

Figure 3. Relationships between the number of leaves of the fruitful R shoot and fruit diameter in Y1 and Y2, for apple (Malus domestica) ‘Chantecler’ and ‘Pitchounette’. Each symbol (± SD) represents the mean of at least five fruits. Regression line equations: ‘Chantecler’ Y1: y = 0.599x + 66.655, R2 = 0.062; ‘Chantecler’ Y2: y = 0.369x + 75.332, R2 = 0.032. ‘Pitchounette’ Y1: y = 0.812x + 57.717, R2 = 0.157; ‘Pitchounette’ Y2: y = −0.124x + 76.519, R2 = 0.029.

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Size relationships between shoots in Y1 and Y2

There was a positive relationship in both cultivars, between the number of leaves of a shoot in Y1 and the number of leaves of the shoot that developed from it in Y2 (Fig. 4). Due to the specific flowering pattern of the cultivars, leading to insufficient sample sizes in certain cases (e.g. almost no transition to V shoots for ‘Chantecler’), not all transitions between shoot types could be explored. As a general trend, considering all transitions from Y1 to Y2, ‘Chantecler’ had a significantly higher slope and lower intercept compared with ‘Pitchounette’ (P < 10−4, Table 2a). For ‘Chantecler’ (Fig. 4a), regressions for ‘R to R’ and ‘V to R’ transitions were not significantly different for intercepts but were significantly different for slopes (P = 0.013, Table 2b). There was a clear trend towards a parabolic relationship for both transitions (P = 2.16 × 10−11 and P = 3.85 × 10−3 for ‘R to R’ and ‘V to R’, respectively; data not shown) with no increase in the number of leaves of the shoot in Y2 above 18 leaves or above 26 leaves, for V and R shoots in Y1, respectively. For ‘Pitchounette’ (Fig. 4b), regressions were not significantly different for slopes for all transitions except a weak difference was found between ‘V to R’ and ‘R to V’ (P = 0.047, Table 2b). All transitions had significantly different intercepts except between ‘R to R’ and ‘V to R’ (P < 0.370, Table 2b). Linear adjustment offered a better model for three (P = 0.357, P = 0.168, P = 0.423 for ‘R to R’, ‘V to V’ and ‘R to V’, respectively; data not shown) over four (P = 0.016 for ‘V to R’; data not shown) transitions.

Shoot size and bud fate in terminal position

The relationships between the number of leaves per shoot and the fate of the terminal bud showed contrasting patterns depending on the cultivar and shoot type (Fig. 5). For ‘Chantecler’ the percentage of flowering was high in Y1, Y2 and Y3, that is 90% on average (data not shown) and the number of leaves on shoots had only a little influence on the fate of the shoot in the following year (Fig. 5a). Whereas flowering frequency in Y2 was high for V shoots in Y1, whatever the number of leaves, two contrasting patterns were observed for R shoots. For R shoots in Y1, flowering frequency in Y2 increased up to six leaves reaching c. 100%. For R shoots in Y2, increasing the number of leaves tended to decrease flowering frequency in Y3 with higher variability. In both cases adjusting a quadratic function would not be appropriate. For ‘Pitchounette’, there was a significant effect of the number of leaves per shoot on the fate of the terminal bud (Fig. 5b). The relationships were well adjusted by quadratic functions for three out of four relationships – R shoot in Y1 and Y2, and V shoot in Y2 – with a positive followed by a negative effect on flowering of the number of leaves on the subtending shoot. Although not well fitted by a quadratic function, V shoot in Y1 would show a similar trend with an increasing flowering frequency with an increasing number of leaves up to four leaves, followed by a decreasing flowering frequency with higher variability for a higher number of leaves. There was no flowering in Y3 for R shoots in Y2 with fewer than eight leaves, whereas flowering in Y3 was observed on V shoots in Y2 with two leaves, and for R shoots in Y1 with four leaves. For transitions where the number of leaves significantly influenced flowering in the following year, the highest maximum flowering frequency was reached for R shoots in Y1 and Y2 (c. 0.9; Table 4a), but was associated with a significantly higher number of leaves in Y2 compared with Y1 (27 vs 19; Table 4a). V shoots in Y2 had a similar maximum frequency of flowering and associated number of leaves than R shoot in Y1 (0.82 vs. 0.90, Table 4a) but had significantly lower values of both variables than R shoot in Y2 (Table 4a).

image

Figure 5. Relationships between the number of leaves of R or V shoot in Y1 or Y2 and flowering frequency in terminal position on that shoot in Y2 and Y3, respectively, for apple (Malus domestica) (a) ‘Chantecler’ and (b) ‘Pitchounette’. Each symbol represents flowering frequency on at least five shoots. For ‘Chantecler’, not enough data for V in Y2; no regression curve fitted for all relationships. For ‘Pitchounette’, regression curve equations: R shoot in Y1: y = −0.002x2 + 0.092x + 0.029, R2 = 0.654; R shoot in Y2: y = −0.003x2 + 0.150x –1.102, R2 = 0.872; V shoot in Y2: y = −0.002x2 + 0.082x–0.003, R2 = 0.678. No regression curve fitted for V shoot in Y1.

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Table 4.  ‘Pitchounette’. Summary of the comparisons between the maximum flowering frequency, and the number of leaves at maximum flowering frequency, for the parabolic relationships between (a) the number of leaves of R or V shoot and flowering frequency on two consecutive years, and (b) the number of leaves of R or V shoots in Y1 and flowering frequency in Y3 (see Figs 5 and 6)
Relationship /Shoot typeMaximum flowering frequencyTest ZPNumber of leavesTest FP
(a) Nb of leaves in Y1 and fate in Y2
 R in Y10.899  18.9  
Nb of leaves in Y2 and fate in Y3
 R in Y20.931  27.1  
 V in Y20.824  20.2  
Comparisons:
 R in Y1–R in Y2 0.6990.242  7.2770.009
 R in Y1–V in Y2 1.4290.076  0.4680.498
 R in Y2–V in Y2 2.4090.008 13.9930.001
(b) Nb of leaves in Y1 and fate in Y3
 R in Y10.882  14.0  
 V in Y10.891  27.1  
Comparison:
 R in Y1–V in Y1 0.1640.435  4.2290.046

As for the relationships between consecutive years, Y1 and Y2, the relationships between the number of leaves of shoots in Y1 and flowering frequency of the same branch in Y3, irrespective of shoot type in Y2, showed contrasted patterns between the two cultivars (Fig. 6). Due to high flowering in Y3, there was no consistent relationship for ‘Chantecler’. For ‘Pitchounette’, there was a parabolic relationship between these two variables for both R and V shoots. Flowering in Y3 could be observed on R shoots, and to a lesser extent on V shoots, with no leaves in Y1. There was no significant difference between the two shoot types in Y1 in the maximal value of flowering frequency in Y3 (c. 0.9; Table 4b), with only a small difference (P = 0.046) in the corresponding number of leaves of the shoot in Y1 (14–27 leaves; Table 4b).

image

Figure 6. Relationships between the number of leaves of R or V shoot in Y1 and flowering frequency on the same branch in Y3, for apple (Malus domestica) ‘Chantecler’ and ‘Pitchounette’. Each symbol represents flowering frequency on at least five shoots. ‘Chantecler’: no regression curves fitted for all relationships. ‘Pitchounette’, regression curve equations: R shoot: y = −0.003x2 + 0.087x+ 0.274, R2 = 0.758; V shoot: y = −0.001x2+ 0.065x + 0.014, R2 = 0.848.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Size relationships between contiguous organs in the same year

The apple inflorescence – leaves and flowers – and the 2–5 proximal leaves of the bourse-shoot(s) are preformed in the over-wintering bud (Bijhouwer, 1924; Pratt, 1988). Therefore, the bourse-shoot is almost totally neo-formed during the growing season. Since the bourse-shoot is borne by the inflorescence and develops after inflorescence expands (Abbott, 1960; Lauri & Térouanne, 1995), our results strongly suggest a causal and positive relationship, both spatial and temporal, between the size of the preformed inflorescence and that of the bourse-shoot that develops from it. This finding is in agreement with previous results from other species, about the positive relationships between the size of the preformed bud, or the number of preformed appendages, and the size of the neoformed shoot which develops from it (Kozlowski, 1973; Powell, 1991; Greene & Autio, 1994).

Fruit size is a characteristic of the cultivar and is affected by the year of development of the fruitful shoot in relation to the age of the parent branch, with fruit in a lateral position in Y1, that is the year following the growth of the parent branch, being smaller than fruit that developed in Y2 and Y3 (Lespinasse, 1970; Volz et al., 1994; Lauri & Lespinasse, 2001). Our results, which included fruit in terminal position in Y1 but in small proportion (0.20 and 0.11 for ‘Chantecler’ and ‘Pitchounette’, respectively; data not shown), confirmed these effects, and showed that year of development of the shoot also affected the size relationships between R shoot and fruit. In Y1, fruit developed preferentially on R shoots with < 12 leaves (Fig. 3) representing 65% and 84% of all fruitful R shoots in Y1 for ‘Chantecler’ and ‘Pitchounette’, respectively (data not shown), whereas larger R shoots existed in Y1 (up to 36 leaves; Fig. 4a,b). In Y2 however, the same scheme was not observed, and large R shoots with up to 35 leaves were fruitful (Fig. 3).

Considering the R shoot as a subunit with its own morphological and physiological characteristics, these contrasting patterns might be interpreted in terms of source–sink relationships (Watson & Casper, 1984; Minchin & Thorpe, 1996). At the branch level, although an acrotonic gradient exists along the annual shoot (Simons & Chu, 1967; Costes, 2003), lateral inflorescences in Y1 usually have fewer leaves and flowers of smaller size, smaller flower receptacles, and weaker vascular connections (May, 1970; Dennis, 1986; Volz et al., 1994) compared with inflorescences that developed in Y2 and Y3. As a consequence, an inflorescence in Y1, especially in lateral position, has a lower ‘sink strength’ (Dennis, 1986; Marcelis, 1996) than an inflorescence in Y2. It is then more dependent on other sources of assimilates than an inflorescence in Y2 or Y3 with respect to fruit-set and early fruit growth (Lauri et al., 1996; Lauri & Térouanne, 1999). The relationships between fruit-set and fruit growth, and the bearing R shoot, are usually split into two main phases: early in the season, inflorescence leaves are primary sources of photosynthates for flowers and fruitlets while the growing bourse-shoot may be concurrent at that time; later in the season bourse-shoot leaves strongly contribute to fruit growth, final fruit size and calcium content (Abbott, 1960; Quinlan & Preston, 1971; Ferree & Palmer, 1982; Volz et al., 1994). Reciprocally, fruit sink stimulates photosynthesis of adjacent leaves (Hansen, 1977). These interactions would lead to a positive relationship between the size of the whole R shoot and fruit size. Our results, notably on ‘Chantecler’, would follow this scheme when combining fruitful R shoots in Y1 and Y2 but not if we consider each year independently (Fig. 3). However, the tendency to lower fruit-set (Table 3), although not statistically significant in this study but well documented in literature (Dennis, 1986; Lauri et al., 1996), as well as the lower fruit size and number of leaves on fruitful R shoots in Y1, (Fig. 3) suggested that, compared with R shoots on Y2, stronger competitions exist within the R shoot in Y1, that is between the bourse-shoot and the inflorescence (flowers and fruitlets), and also between adjacent shoots on the parent branch. In Y2, inflorescences have a higher number of leaves, with possibly less competition with the adjacent bourse-shoot, and also between shoots on the parent branch. In Y2, R shoots are then more autonomous for fruit-set (Table 3) and fruit growth.

Shoot size relationships between two consecutive years and fate of the terminal bud

As previously stated, there is a positive relationship between the size of a shoot in a given year and the size of the shoot it gives rise to in the following year (Powell, 1991; Barlow, 1994). According to Alaoui-Sosséet al. (1994) on Quercus robur, and Goldschmidt & Koch (1996) on Citrus, the previous growth cycle provides assimilates – from either reserves and/or current photosynthates according to the species – to the new developing growth increment. The present findings on the size relationships between these two consecutive years of shoot growth support these previous results and it has been shown here that each cultivar had a specific pattern of size relationships, that is higher slope and lower intercept for ‘Chantecler’ compared with ‘Pitchounette’. On ‘Chantecler’ the parabolic adjustment is better for the two transitions leading to a decrease in Y2 of the size of the longer shoots in Y1. On ‘Pitchounette’ the trend was linear for three out of four transitions leading to shorter shoots in Y2 compared with Y1 for long shoots. Both cultivars thus exhibited a tendency towards a decrease in shoot size in Y2 compared with Y1, illustrating two expressions of the phenomenon of ageing, that is reduction in the annual growth increment (Wareing, 1970; Poethig, 1990; Costes et al., 2003).

These results suggest that growth correlations, once established in Y1, may lead to a self-organization process (Nozeran et al., 1971; Champagnat, 1974), which tends to maintain the growth potential of the underlying shoot developed in the previous year. This 3-yr study showed that the development of a shoot on the parent branch is a highly integrated process where the number of primordia in the preformed bud in Y1 strongly determined shoot (Fig. 2), and to a lesser extent, fruit (Fig. 3) size in the same year and in the following year (Fig. 4). This chain of consecutive and possibly causally related events complement previous results on apple, on the positive relationship between the size of a shoot and the size of the inflorescence in terminal position (Lauri et al., 1996). According to recent results (H. Cochard et al., unpublished) on Fagus sylvatica, hydraulic conductance in an annual growth has a strong influence on the number of preformed organs in the terminal bud, and the length of the shoot in the following year. These findings would suggest that timing and intensity of vascular connections of the bud in Y1 can have a dramatic effect on shoot development in the following years. Since hydraulic properties of a shoot depend on thickness and more generally on the allometric relationships between length and diameter (Kervella et al., 1994), which is related to leaf area (Barcellos de Souza et al., 1986; Bond & Midgley, 1988; Brouat et al., 1998), it is likely that the structural proportion of the 1-yr-old parent branch would give additional information on the initial developmental phases of the terminal or the lateral shoot.

In our results, the relationship between shoot size and fate of the terminal bud was clearly cultivar dependent. The ‘in-built tendency’ for spurs to alternate (Browning, 1985; Davenport, 2000) was not verified here, even though the two cultivars exhibited contrasting patterns of flowering. On ‘Chantecler’ return-bloom, that is the transition from R shoot in one year to R shoot in the following year, was high with no substantial relation to shoot size. On ‘Pitchounette’ return-bloom was clearly dependent on shoot size, and in Y2 was even higher than transition from V (Fig. 5b). This is in agreement with the findings of some authors (Feucht, 1976; Weinbaum et al., 2001) that the relationships between shoot size and terminal flowering may be influenced by genotypic characteristics. Here, shoot size was assessed by counting foliage leaves and thus did not include scales and transition leaves. From the results obtained for R and V shoots in Y1, on ‘Chantecler’ and ‘Pitchounette’, respectively, we hypothesized that the typical parabolic, that is an increase followed by a decrease, relationship observed for three out of four transitions for ‘Pitchounette’, might be a common scheme of the relationships between shoot size in the first year and terminal flowering in the following year (Fig. 5) or 2 yr later (Fig. 6). According to this hypothesis, the left portion of a theoretical curve, which would include scales and transitional leaves, may be hidden for certain cultivars if only foliage leaves are considered (Fig. 7). On ‘Chantecler’, with high flowering in Y1, Y2 and Y3, an increase in flowering frequency is likely to occur on shoots with only transition leaves (V shoots in Y1) or with a few foliage leaves (R shoots in Y1), and in all cases reaches maximum values with the very first foliage leaves (Fig. 5a). On ‘Pitchounette’, transition to flowering is more dependent on the previous year shoot type and size, and year of development in relation to parent branch age (see difference between V shoots in Y1 and Y2; Fig. 5b). For the latter cultivar, the relationship between transition to flowering and number of leaves is in accordance with the statement of Feucht (1961) that flowering frequency is the highest in terminal position on shoots 1–15 cm long. The possibility to forecast the fate of the terminal bud up to 3 yr would suggest that, without extrinsic manipulation, the shoot enters as soon as shoot inception in Y1 on the parent branch, a predetermined behavior.

image

Figure 7. Theoretical curves of the relationships between the number of appendages of an apple shoot and flowering frequency in terminal position.

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Finally, the two contrasted habits of ‘Chantecler’ and ‘Pitchounette’ suggested that, on a between-cultivar basis, shoot size and terminal flowering were partly autonomous phenomena. Indeed, the ability to flower in terminal position on long shoots, including strong erect water-sprouts, is variable depending on cultivar and has been proposed as an easy-to-use discriminating feature between apple cultivars (Lauri, 2002). From our results, it can be concluded that the analysis of the flowering pattern of a cultivar should not only focus on the relationships between shoot length, or leaf number and area as is usually done, but should integrate other variables at both shoot and parent branch levels. Lespinasse & Delort (1993) showed on a range of cultivars that bourse volume is positively related to return-bloom, suggesting that the location of stored assimilates close to the terminal bud of the bourse-shoot is of primordial importance for inflorescence and fruit development in the following year. At the branch level, (Lauri et al., 1995; Lauri et al., 1997) showed that the extinction phenomenon that reduces branching density between Y1 and Y2 of regular bearing apple cultivars may be causally related to the high return-bloom ability of the remaining shoots. Hence, the hypothesis of the autonomy of the shoot with regard to the relationship between shoot size and fate of the terminal bud is not an absolute rule (Lauri & Térouanne, 1999; Sprugel, 2002) and varies with cultivar and position in tree architecture. On ‘Pitchounette’, shoot size in Y1 may determine fate in both Y2 and Y3. On ‘Chantecler’, with high extinction between Y1 and Y2, and high flowering in all years (Lauri & Lespinasse, 2001), whole parent branch features are likely to strongly determine the flowering pattern.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We gratefully acknowledge Jean-Marie Lespinasse for his contribution to the setting-up and the field management of this experiment, and helpful discussions. We also thank Francis Delort, Lydie Fouilhaux and Gilbert Garcia for their help in collecting and typing field data. We are grateful to Frank Dennis and an anonymous referee for useful comments on the manuscript, and to Annik Lacombe for improving the English.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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