The processes of flower initiation in apple
Flowers on apple trees are formed on three types of bud:
- Axillary buds, formed in the basal axils of shoots made in the previous season
- Spur buds formed often in clusters on two-year-old or older wood
- Terminal flower buds, which are formed on the ends of short shoots.
The processes by which these buds are formed are complex. The beginning of floral differentiation is seen as a flattening of the apical dome in a bud which, up to that point, could be considered vegetative.
- Before any visible change in the bud morphology is seen, the meristem of the bud is programmed to form flowers by some, as yet unknown, signal or biochemical stimulus.
- Once the bud transforms from vegetative to floral this process is believed to be irreversible.
- Management or climatic factors occurring after this event may change the quality of the bud but not whether it is floral.
To be sensitive to the inductive stimulus (whatever that may be) and to change to floral type, a bud must be in a certain phase or stage. This is characterised by a critical number of nodes, usually 16-20 (Faust, 1989; Buban and Faust, 1982).
- Additional requirements are a minimum duration (possibly 7 days) of what is known as the plastochron. This is the rate of production of new primordia in the apple bud.
- This plastochron remains very stable throughout long periods of the season, irrespective of climatic conditions.
- However, research at East Malling showed that the length of the plastochron did change, relatively abruptly, during the season and it was usually 5, 7 or 18 days.
- These values are thought to be appropriate for many apple varieties.
- The plastochron is controlled by the younger leaf primordia in the bud, which may themselves be controlled by the foliage.
- It is these changes in plastochron which help to determine whether the buds formed are vegetative or floral.
- A final necessity for buds to become floral is the presence of bracts. For further details see Fulford, (1962); Fulford, (1965b) and Buban and Faust, (1982).
The presence of leaves is a prerequisite for flower bud production and it is believed that increasing numbers of leaves on spurs will increase flower initiation. This effect is probably indirect and operates via its effect on available photosynthates.
The influence of rootstock and/or interstock on flower initiation and development
Rootstocks and interstocks have been shown to have a significant influence on flower initiation and development in apple scions. How they bring about these effects is not fully understood.
- It is hypothesised that rootstocks in some way change the partitioning of assimilates (photosynthates) and minerals, such that the sites of floral initiation (e.g. spurs) become strong sinks and the development of increased numbers and better quality floral buds is a consequence of this.
- Part of this change of assimilate partitioning may be explained by rootstock effects on shoot vigour.
- Dwarfing rootstocks bring about slower rates of extension shoot growth during the summer months, but, more importantly, they bring about an earlier cessation of active shoot extension.
- Once the active extension of shoots has stopped and a terminal resting bud is formed, alternative sinks for assimilates in the tree will become more dominant.
- Assimilates will move much more readily to the sites of floral bud initiation in spurs or to roots once active shoot growth ceases.
This explanation is partially flawed, however, as a few invigorating clonal rootstocks (e.g. M.25) stimulate the initiation of many more floral buds on scions than other rootstocks of similar vigour potential.
- This suggests that rootstocks control floral initiation in the scion directly, as well as indirectly via their effects on shoot growth. How they do this is not understood.
Rootstocks do influence the concentrations and movements of plant hormones (auxins, gibberellins, cytokinins and abscisic acid) within the tree (Soumelidou, et al., 1994; Kamboj, et al., 1997).
- It is likely that these differences are in some way involved in their influence on floral bud initiation in the scion.
Another possibility is that as many rootstocks improve the branching angle of scion trees, making branches more horizontal, this could contribute indirectly to their effects on floral initiation.
Effects of pruning and training techniques on flower initiation and development
Both shoot pruning/training and root pruning/restriction techniques may influence flowering on apple trees.
Shoot pruning and training
- It is well known that shoot bending towards or below the horizontal is very effective in inducing increased numbers and quality of floral buds in apple trees.
- What is less well understood is why shoot bending has this effect. It can be suggested that shoot bending slows down new shoot extension, and because new extension leaves form abundant supplies of gibberellins, the result is to reduce the effect of gibberellins on flower bud inhibition.
- However, shoot bending stimulates improved flowering, even when there is no active shoot growth on a branch, indicating a more complex relationship than may at first be apparent (Tromp, 1972).
Research on clones of Red Delicious grown in the USA has shown that summer pruning 30 days after flowering increased spur length and the number, size and area of spur leaves but did not influence flowering spur diameter (Rom and Barritt, 1990).
Root pruning and restriction
In trials conducted at HRI-East Malling, root pruning or root restriction of young apple trees has been shown to increase the abundance of flower production (Webster, et al., 2000).
- However, flowering is not always increased by root pruning, as shown by trials on mature Golden Delicious trees growing in the USA (Schupp et al., 1992)
- These USA trials did report an advancement in the time of flowering following root pruning.
- Root pruning causes reductions in shoot growth, a temporary negative water potential, reduced stomatal conductance, transpiration and photosynthesis.
The effects of defoliation on flower initiation
Removal of spur leaves on temperate fruit trees is known to inhibit flower production for the subsequent season (Huet, 1973).
- This inhibitory effect may be due to the removal of sites for cytokinin synthesis, which is believed to be important in flower initiation (Hoad, 1980; Ramirez and Hoad, 1981).
The importance of spur leaves has implications concerning the use of certain chemicals for flower thinning.
- Use of urea as a flower thinner may result in reduced flower numbers in the subsequent year.
- Urea often thins by damaging the spur leaves surrounding the flowers.
Work on spur types of Red Delicious growing in the USA has shown that reducing the spur leaf area on non-cropping (vegetative) spurs in August caused a reduction in flower number but not flower size in the subsequent season (Rom and Barritt, 1990).
- Reducing leaf area on the fruiting spurs caused a reduction in the growth of the bourse shoot in the subsequent season.
The influence of crop load on flower initiation and development
Attempts to understand how crop load influences flower initiation in apple were made at Long Ashton Research Station in the 1970s (Abbott et al., 1975).
- The results are shown below:
| Treatment No. | Total fruit number/tree 1973 | No. of short shoots/tree (>5cm) 1973 | Length of longest shoot/tree (cm) 1973 | Fruit buds/tree 1974 | |
|---|---|---|---|---|---|
| <60mm | >60mm | ||||
| 1 | 90 | 79 | 6.5 | 46 | 0 |
| 2 | 30 | 89 | 7.6 | 46 | 0.2 |
| 3 | 5 | 86 | 6.9 | 42 | 1.0 |
| 4 | 0 | 50 | 10.1 | 51 | 7.4 |
| 5 | - | - | 12.0 | 85 | 10.3 |
- It can be seen that high fruit numbers on these small trees reduced shoot growth as well as almost completely inhibiting flowering in the subsequent season.
- However, although return bloom was closely correlated with fruit numbers in the previous year, in this experiment no such correlation was found with the development of flowering buds.
- Anatomical observations of buds harvested from branches sampled throughout the season showed bud development at roughly the same rate.
- The first visible flower initiation was not noted until mid-August and buds from all the treatments achieved this at approximately the same time.
- The experiment indicated that fruit number on trees (crop loading) influences the intensity of flower initiation through some mechanism other than rate of bud development.
However, other work at Long Ashton (Abbott, 1984) indicated that cropping on trees extended the ‘plastochron’ (the time taken for each node on bud primoridia to form) from 8 to 19 days from mid-June onwards; i.e. it slowed down bud development.
- Another effect of heavy crop loads is reduced root development.
- If one accepts the hypothesis that root activity associated with nitrogen assimilation is a necessary stimulus to flower initiation, then this could be an added reason for heavy cropping reducing flowering.
- This might also explain why root pruning, which stimulates root growth at the expense of shoot growth, also stimulates flower production.
Timing of the thinning operation can be critical in influencing return bloom on apple trees. This has been shown to be particularly relevant with varieties such as Boskoop where biennial bearing may be a problem in some seasons.
- Thinning at full bloom or up to two weeks after had a very positive effect on return bloom in the subsequent season.
- However, thinning three weeks after bloom was too late and no more flowers were initiated than on the unthinned controls (Tromp, 2000).
- This is perhaps surprising, as the formation of significant amounts of gibberellins by the fruits (which are believed to be a major cause of flower bud inhibition) had not begun during this three-week period.
- Competition for vital assimilates may play an important role in flower bud initiation in this early post-flowering period.
Climatic effects on flower initiation and development
The main climatic effects on flower initiation and development are as follows:
- Climatic effects on flower initiation in the season prior to flowering.
- Climatic effects on winter dormancy.
- Climatic effects on pre-budburst flower quality.
Climatic effects on flower initiation in the season prior to flowering
In research conducted many years ago at Long Ashton Research Station, the effects of different day/night temperatures on flower development were assessed (Abbott and Bull, 1973a).
- Trees of Cox’s Orange Pippin, which were subjected to temperatures of 9oC during the day and 5oC during the night during August to December, reached full bloom at the beginning of April in a glasshouse.
- However, only 23% of the buds were floral and the buds were of what was described as of ‘young’ type.
- The fruitlets on these trees dropped steadily and at harvest only a few ‘king’ fruits remained.
- In contrast, trees retained at 17oC during the days and 13oC during the nights from August to December were slow to break bud in the spring and did not flower until the end of April (three weeks later than the trees subjected to cool autumns).
- With these trees, 70% of the buds were floral and the clusters were typically of the ‘old’ type.
- Fruit drop was less on these trees and concentrated mainly in the June drop period, but the fruits formed were slightly flattened with short stalks.
- The best yielding trees were those subjected to 13oC during the day and 9oC during the night between August and December.
- It is interesting to note that these temperatures were closest to those normally experienced in the orchard.
In research conducted by the same Long Ashton team, the influence of temperatures between the end of April and mid-October on flower initiation of Cox was also studied (Abbott and Bull, 1973b).
- Cox trees subjected to day temperatures of 13.5oC and night temperatures of 7.5oC developed necrotic spots on the primary (spur) leaves which were similar to ‘Cox Spot’ and the new unfolding leaves showed symptoms similar to zinc deficiency.
- Flower numbers in the subsequent spring were average for this treatment but the flowers were variable in their time of opening.
- Other characteristics of this treatment were large spur leaves, a high rate of flower abortion, long bourse or cluster axes, and short flower stalks.
- This all suggests that bud development was slow and flower initiation was late on these trees. The fruits formed were mostly kings.
- Trees subjected to daily fluctuations of 13.5oC and 7.5oC developed bourse shoots, which grew out, and then rosetted and formed short shoots a few cm long.
- This second flush occurred too late for flower buds to develop properly within these spurs and flower numbers were low in the subsequent spring.
- Trees maintained in temperatures of 21.5oC day and 15.5oC night produced ‘old’ type flower clusters with small spur leaves and uniform flowers with long stalks and short bourse shoots.
- Unfortunately, the blossoming abundance on these trees was very variable being inversely related to the fruit numbers/tree carried in the previous summer.
The general conclusion is that higher than average summer temperatures improve flower initiation on apple trees grown in the UK.
- This is thought to be due to the temperatures inducing flower initiation early in the season, allowing more time in the season for successful development of flowers.
- However, care must be taken when trying to use increased temperature to stimulate flowering.
- Trees experiencing high temperatures under glass or polythene structures usually show reduced flower initiation and development.
- This is caused by the stimulation of competitive extension shoot growth and bourse shoot flushing, as well as the lower light levels under protective structures.
Research conducted in Canada has shown that high temperatures (30oC or higher) in June during flower initiation have a deleterious effect on flowering in the subsequent season, as do temperatures over 26oC in August during flower development (Caprio and Quamme, 1999).
- Such high temperatures are unlikely to be a limit on flower initiation in the UK climate.
Climatic effects on winter dormancy
- Apple trees of most scion varieties are believed to require an accumulation of approximately 1000 hours of temperatures of less than 8oC but higher than freezing in order to satisfy their winter chilling (dormancy) requirement.
- Temperatures of above 12oC are thought to result in a loss of some of the accumulated chilling units.
- Many of the ornamental Malus species require several hundred hours less chilling units.
Studies conducted in New York State in the USA in the early 1990s (Hauagge and Cummins, 1991) showed the following chilling unit requirements. The values are means of three years data:
| Cultivar name | Mean chilling unit requirements (hours) |
|---|---|
| Anna | 218 |
| Delicious | 1093 |
| Elstar | 1027 |
| Empire | 1079 |
| Fuji | 1077 |
| Gala | 1064 |
| Golden Delicious | 1050 |
| Granny Smith | 1049 |
| Idared | 1017 |
| Prima | 1072 |
In the 1970s, USA researchers developed a chilling unit model (Richardson et al., 1975) for use on peaches and several attempts have been made to use this model with other temperate fruit crops including apple (Shaltout and Unrath, 1983).
- Information more specific to UK conditions was first presented by Landsberg, (1974) and Williams et al., (1979).
- The chilling requirement is primarily needed to the buds themselves (Samish, 1954) but studies in the USA also indicated that for effective bud break in the spring the tree roots also need to be chilled (Young, 1988).
Once the dormancy requirement has been satisfied, the buds are capable of developing into flowers or vegetative shoots if subjected to suitable ‘forcing’ (>15oC) temperatures.
Climatic effects pre-budburst on flower quality
It is generally accepted that once the chilling unit requirement has been satisfied and dormancy broken, buds will develop through to flowering if subjected to what are known as forcing temperatures.
- Buds develop at any temperatures over about 10oC, but development is speeded up by higher temperatures.
- The time taken for the flowers to break bud is variable depending upon the scion variety, the bud type and how well the dormancy requirement has been satisfied.
- Temperatures that are unseasonably high during February, March and April (average maxima of 10oC or above) can have a negative influence on flower quality.
- The possible reasons for this effect and its implications are described in the previous section.
The influence of water supply to the tree on flower initiation
In experiments conducted in Germany under very controlled environments and water supply, it was shown that when water supply was reduced to 50% or 25% of the trees estimated needs, the numbers of flower clusters and flowers per tree were reduced (Sritharan and Lenz, 1988).
- However, shoot growth was also greatly reduced and when estimates were made of flowering or fruit set per metre shoot length, the drought treatments caused increases in flowering.
- Unless drought is very severe, it is unlikely to influence the efficiency of flower bud production or flower bud quality.
Effects of tree mineral nutrition on flower initiation and development
The evidence for mineral supply having a significant influence on flower initiation is only strong when considering nitrogenous fertilisers.
- Applications of high rates of nitrogenous fertilisers, together with sufficient water to facilitate their uptake by the tree, will increase the rate and duration of active shoot growth.
- This in turn will delay the initiation and development of floral buds.
- One apparent anomaly is that whilst nitrogen is antagonistic to flowering, as stated above, root growth and associated nitrogen assimilation is thought to be vital for flower initiation (Abbott, 1984).
- This might be explained by the fact that nitrogen applications whilst extension shoot growth is still active are indeed antagonistic to flower initiation, whereas nitrogen applications after termination of shoot growth often improve flower quality.
For many years there was a theory that flower bud initiation was dependent upon the establishment of a critical ratio between the amounts of carbohydrates and the amounts of nitrogen present; the so-called C/N ratio.
- When the ratio is high in favour of carbohydrates then flower bud initiation was thought to occur. However, this theory has now been largely discounted.
The evidence for other elements having a strong effect on flower initiation is poor.
- Indeed, in experiments conducted in controlled environment conditions, scientists at Long Ashton Research Station found no significant effect of mineral supply on flower initiation on Cox.
- However, these experiments were conducted under glass, where temperatures were higher and light levels lower than those experienced in the orchard.
- Subsequent trials at Long Ashton indicated that flower initiation was favourably influenced by an optimal balance of high light, cool temperatures and good nutrition.
Effects of natural and applied plant hormones on flower initiation and development
Apple trees produce several chemicals, often called endogenous hormones, which are important in signalling within the tree and in stimulating many vital processes associated with growth and cropping.
- Some of these natural hormones, especially the gibberellins, but also auxins and cytokinins, have been implicated in the control of initiation and development of flowers on the apple tree.
Alternatively, chemicals that inhibit plant processes may be used in flower initiation. These are mostly plant growth retardants, which inhibit the tree’s production of gibberellins. The most important of these are:
- Paclobutrazol e.g.Cultar
- Calcium Prohexadione e.g. Regalis
Gibberellins
It has been known for many years that gibberellins have an important influence on the formation of reproductive organs in apples and many other seed plants (Pharis and King, 1985).
- Applications of gibberellins in spray treatments have been shown to induce parthenocarpy and improve fruit set in apples (Goldwin, 1981) and also to inhibit flowering (Hoad, 1984).
- Strong competing shoot growth or excessive numbers of fruits inhibit flowering on apple trees and it can be speculated that gibberellins, formed either in the fruit seeds or in the shoot tips, are the signal hormone responsible for this effect.
Research in Holland showed that both GA3 and GA7 strongly inhibit flowering whilst GA4 has no inhibitory effect on flowering (Tromp, 1982).
- Indeed, research conducted in Canada suggests that GA4 sometimes promotes flowering in apple (Looney et al., 1985).
- Work in Germany has supported these findings to some extent. It has shown that, whilst gibberellic acid (GA3) is very inhibitory, GA4+7 has very little inhibitory effect upon flower initiation (Prang et al., 1997).
- This work also showed that there was a peak in endogenous (natural) levels of gibberellins (200-450 pg/fruit) in the trees of apple scion varieties at approximately 4-6 weeks after full bloom.
- This timing is known to be critical for flower bud initiation.
- The problem with this hypothesis, that gibberellins are responsible for inhibiting flowering in apples, is that both biennial varieties, such as Elstar, and non-biennial varieties, such as Golden Delicious, appeared to export approximately the same amounts of gibberellins.
The beneficial effects of GA4 on flowering, reported by Looney et al., (1985) are not consistent.
- In research conducted in the USA (Greene, 1993b), GA4 has stimulated and increased, as well as reduced, flowering in Golden and Red Delicious trees.
- Nevertheless, even when GA4 induced negative effects on flowering these effects were less severe than those induced by GA7 at the same concentration.
Auxins
Recent studies in Germany (Callejas and Bangerth, 1997) have suggested that the downward (basipetal) transport of the auxin IAA in the apple shoot could play a role in flower initiation.
- This hypothesis is based on observations that showed that applications of gibberellins to apple shoots (which are known to suppress flower initiation) increased the amounts of IAA diffusing down from the tips, during the critical stage for flower initiation.
- Also, seed number in fruits is known to influence flowering.
- The high numbers of fruits, and hence seeds, produced on biennial bearing varieties in their ‘on’ year is thought to be a major cause of the reduction in flowering in the subsequent ‘off’ year.
- The German work showed that increased seed numbers in fruits were associated with increased auxin transport from the fruits towards the spurs and the sites of potential flower initiation.
Cytokinins
Leaves, as well as fruits, have been shown to be the sites of manufacture by the plant of cytokinins.
- The observation that removal of spur leaves from apple trees inhibited flowering in the subsequent season led some researchers to hypothesise that this reduction in flowering was due to the associated reduction in cytokinin supply to the spurs.
- Research by Hoad (1980) lent credence to this hypothesis.
- In this work and in that of Ramirez and Hoad, (1978) it was shown that the inhibitory effect of spur leaf removal on flower initiation could be reversed by local applications of cytokinins to the spurs.
In research conducted by McLaughlin and Greene (1984) the authors suggested that the main influence of cytokinins on flower initiation was in overcoming the negative influence of diffusing gibberellins.
- Applications of the cytokinin benzyl adenine (BA) to fruiting shoots increased the numbers of flowering spurs in the subsequent season whilst similar applications to non-flowering shoots did not.
- The same research showed that BA applications increased the numbers of flowers per spur on both fruiting and non fruitling limbs and the effect seemed to be one of stimulating lateral flower bud formation.
- The effect of BA thinning sprays on return bloom of apples is thought to be entirely due to the effect of the sprays on fruit, or more importantly seed numbers (Greene and Autio, 1994b).
Other cytokinins used for thinning apples, such as CPPU and thidiazuron do not promote return bloom, suggesting that, in comparison with BA, they have some direct negative influence on flower initiation (Greene, 1993).
Paclobutrazol (PP333 or Cultar)
Trials at East Malling in the 1980s showed that apple trees treated with paclobutrazol frequently formed more flower buds/tree and many more flower buds/metre shoot length than untreated trees.
- It is thought that this effect is stimulated by paclobutrazol’s effect in reducing internode length and shoot length and the partitioning of additional assimilates into the formation of flower buds.