Acknowledgements
T. L. Davenport
5.9 Conceptual Flowering Models
Several conceptual models have been proposed that attempt to explain the physiological basis of mango fl owering. Each model should be viewed as a collection of integrated ideas, which require rigorous testing for validity within the context of the models. A useful model should explain how fl ower- ing and vegetative growth is regulated in all cultivars and races in both humid and dry climates in the tropics and subtropics. It should also be sup- ported by the preponderance of research evidence. The fl owering models are either carbohydrate-regulated or hormone-regulated.
Carbohydrate-regulated fl owering models
Cull (1987, 1991) presented a holistic approach for tree crop research and management to maximize sustainable fruit production. This concept is based
Reproductive Physiology 125
on the axiom of genotype/environment adaptability expressed through the annual phenological cycle and is an alternative to the traditional reductive- based approach to crop research and development. He proposed that pro- ductive cultivars follow ‘normal’ phenological patterns from year to year due to gene expression in specifi c environments. A signifi cant departure from this pattern results in reduced or total crop failure. Annual variations in climatic conditions that alter tree phenology can be countered by strategic applications of nutrients, water, plant growth regulators and canopy manip- ulation. The model does not attempt to explain the intricacies of shoot ini- tiation or induction, but takes a broader approach in detailing temporal relationships between reproductive and vegetative growth that lead to reli- able cropping.
The fundamental principle underlying this model is that yield is the product of photoassimilate (carbohydrate) accumulation and subsequent redistribution during the annual growth cycle. Accumulated photoassimi- lates would drive critical growth events that require higher levels of resources than are available from current photoassimilate supplies. Cultivars that pro- ceed with balanced reproductive, vegetative and rest phases are more likely to have suffi cient carbon resources to meet periods of critical demand and therefore will sustain high yields. The model illustrates fl oral initiation as occurring after a 2- to 3-month rest period during autumn/winter when a critical threshold level of carbohydrate is reached in buds together with a putative fl oral stimulus. Bud break during cool weather results in a high per- centage of fl owering stems (> 90%; Searle et al., 1995) with fruit set and reten- tion suppressing vegetative fl ushing on individual fruiting stems until after they have matured and harvested. Shortly after harvest, vegetative buds are released and a fl ush of growth occurs during the summer, which is followed by a period of strong root growth. The regenerated canopy becomes a source for rebuilding photoassimilate reserves that are stored in the roots, bark and resting stems. In the tropics, growth events are less orderly, and cultivar and management skills are of greater importance. The pre-fl owering rest period is usually achieved by drought as temperatures remain above the critical threshold for shoot growth (15°C) (Whiley et al., 1989). Other practices used with some success to enforce canopy quiescence are girdling and the applica- tion of growth retardants.
The principles of phenological modelling have been advanced into work- ing pheno/physiological models for avocado (Whiley, 1994) and mango (Searle et al., 1995). The advantage of this approach is that the annual pro- gression of growth cycles with associated physiological changes is studied concurrently, adding a further dimension to our understanding of tree growth and development. Information gathered in this way provides opportunities to identify and assess critical yield-limiting events, which in the case of man- goes largely relates to the success or failure of fl owering.
Chacko (1991) proposed a fl owering model driven by assimilate supply and diversion to apical meristems (Fig. 5.6). Environmental conditions, such as water stress, cool temperatures, high evaporative demand, fl ooding, girdling and other events that inhibit vegetative growth result in a shift in
T.L. Davenport126
FLORAL INDUCTION KNO3
(cultivar and location specific)
High
starch MISSING
INCREASED ASSIMILATE supply
to SHOOT APEX
ASSIMILATE DIVERSION from SHOOT APEX
GROWTH STIMULATION
and high gibberellin
Exogenous gibberellin
LINK
?
GROWTH CHECK
Sugar
· Water stress
· Low temperature
· High VPD
· Flooding
· High temperature
· High humidity
· High soil moisture
High nitrogen
High gibberellin
levels
JUVENILITY HEREDITY
Over vigorous cultivars e.g. ‘Kensington’
Dwarf/precocious cultivars e.g. ‘Irwin’
Frequent flushing of roots and shoots
· Stem girdling
· Root pruning
· High reserves
· Efficient assimilate partitioning
· Low reserves
· More wood formation
· Mild nitrogen stress
· Growth retardants
· Inhibitors
FLORAL INHIBITION
Fig. 5.6. Chacko’s Assimilate Supply and Diversion Flowering Model, a carbohydrate-regulated fl owering model (Source: Chacko, 1991).
Reproductive Physiology 127
carbohydrate partitioning and a diversion of soluble assimilates to stem api- ces. The elevated carbohydrate status in buds, together with a fl oral stimulus, results in fl oral induction. Vigorously growing cultivars and juvenile plants have low starch reserves (Whiley et al., 1988, 1989, 1991) and a diversion of soluble assimilates from stem apices results in fl oral inhibition. Conditions that promote vegetative growth, i.e. high temperature and moisture, high gibberellins and N, also lead to fl oral inhibition. Experiments involving chemical girdling of trees are based on this model (Blaikie et al., 1999).
Hormone-regulated fl owering models
Tri-factor Hypothesis of Flowering
Extensive work on movement of the putative fl oral stimulus across grafts from donor to receptor stems (Kulkarni, 1986, 1988b) and the inhibitory infl u- ence of fruit on subsequent fl owering (Kulkarni and Rameshwar, 1989) form the basis of a fl owering model proposed by Kulkarni (1991): the Tri-factor Hypothesis of Flowering in mango (Kulkarni, 2004). This theory (Fig. 5.7) proposes an interactive role for a putative, cyclically produced fl oral stimu- lus in leaves, a fl oral inhibitor in leaves and fruits, and bud activity during the fl oral cycle. During dormancy following a vegetative cycle, genetic and
Flowering promoter synthesized in the leaves in the floral
cycle
Flowering inhibitor and vegetative
promoter synthesized in the leaves and possibly
other organs
Bud activity in synchrony with
the floral cycle
Pure panicles Mixed leafy panicles Vegetative flush Genetic and Environmental Factors
Fig. 5.7. Kulkarni’s Tri-factor Hypothesis of Flowering in mango, a hormone-regulated fl owering model (Source: Kulkarni, 2004).
T.L. Davenport 128
environmental factors determine the level of synthesis of the putative fl oral stimulus. Flowering occurs only if certain correlative factors are present, for example if the receptor bud becomes active. If fruits are or have been recently present on the stem, vegetative growth will result. Presence of the putative fl oral inhibitor in leaves interferes with expression of the fl oral stimulus resulting in vegetative growth. The level of the fl oral stimulus determines the response: high levels give rise to normal panicles, intermediate levels give rise to mixed panicles and low levels result in vegetative growth.
Comprehensive Conceptual Flowering Model
This is a model of fl owering involving the various classes of phytohormones (Davenport, 1992, 1993, 2000, 2003; Davenport and Núñez-Elisea, 1997) (Fig. 5.8) based on many lines of experimental evidence as well as on research of other tropical and subtropical fruit crops with similar phenological cycles (Menzel, 1983; Davenport, 1990, 1992; Menzel et al., 1990; Menzel and Simp- son, 1994; Davenport and Stern, 2005). Focusing on events occurring in indi- vidual buds, it is applicable to monoembryonic and polyembryonic cultivars in the tropics and subtropics and attempts to explain the physiological basis for the annual progression of the phenological cycle.
SHOOT FORMATION. Two distinct events must occur for vegetative or repro- ductive growth to occur in resting apical or lateral buds of mango: (i) the
Mango flowering model
PHOTOASSIMILATES FRUIT
MIXED SHOOT GENERATIVE SHOOT
CHILLING TEMP.
OTHER FACTORS?
WATER STRESS PROMOTER
IN LEAVES INDUCTION
VEGETATIVE SHOOT AUXIN
GIBBERELLINS
SHOOT INITIATION
ROOT INITIATION
ROOTS CYTOKININS
GIRDLING CHILLING TEMP.
STORAGE CARBOHYDRATES PRUNING
DEFOLIATION NITRATE SPRAY ETHYLENE
FREQUENT VEGETATIVE
GROWTH
AUXIN GIBBERELLINS A3
Ax
GA1 GA3
GAx
Fig. 5.8. Davenport’s Comprehensive Conceptual Hormone-regulated Flowering Model (Source: Davenport and Núñez-Elisea, 1997; Davenport, 2000). Single lines indicate promotive impact. Double lines indicate inhibitory impact.
Reproductive Physiology 129
bud(s) must be initiated to grow (shoot initiation); and (ii) at the time of ini- tiation, shoot development (i.e. vegetative, mixed, or generative) is deter- mined (induction). Although conditions for fl oral induction may be present prior to shoot initiation, determination of that inductive condition in buds is not made until initiation occurs. Initiation and induction events are regulated by different signals and each may be manipulated by different stimuli.
Removing the apical whorl of leaves or tip pruning physiologically mature stems stimulates shoot initiation in apical or lateral buds, respectively. If containerized plants are maintained in warm temperatures (30°C day/25°C night) following initiation, vegetative shoot growth is induced. If they are kept under cool conditions (18°C day/10°C night), initiating shoots are induced to be generative. In either of the two temperature regimes without pruning, they do not initiate shoots until the natural fl ushing event occurs much later. They become vegetative or reproductive according to the tem- perature at the time of shoot initiation. If transferred from cool to warm tem- peratures before shoot initiation, new shoot growth is induced to be vegetative.
Induction is therefore determined at the time of shoot initiation, and plants rapidly lose their fl oral inductive potential when removed from the cool envi- ronment. Determination of shoot type can be reversed during morphogenesis by transferring containerized trees from warm-to-cool or cool-to-warm con- ditions (Batten and McConchie, 1995; Núñez-Elisea et al., 1996).
INITIATION CYCLE. The cyclic initiation of vegetative or reproductive shoots is common to all mango cultivars. Developing vegetative shoots are rich sources of auxins and gibberellins, which may be inhibitors in an internal cycle that regulates shoot initiation. Auxins are actively transported basipe- tally to roots from production sites in stems (Goldsmith, 1968; Cane and Wilkins, 1970; Wilkins and Cane, 1970; Goldsmith and Ray, 1973), and they stimulate adventitious root growth in mango and other crops (Hassig, 1974;
Wightman et al., 1980; Sadhu and Bose, 1988; Rajan and Ram, 1989; Núñez- Elisea et al., 1992). Elevated auxin synthesis in periodically fl ushing shoots is likely to form a concentrated pulse of auxin, which inhibits recurring bud break and moves basipetally to the roots. This pulse of elevated auxin may stimulate initiation of new root fl ushes following each vegetative fl ush.
Alteration of root and shoot growth occurs in mango (Krishnamurthi et al., 1960; Cull, 1987, 1991; Parisot, 1988) and other tropical and subtropical trees (Bevington and Castle, 1986; Williamson and Coston, 1989; Ploetz et al., 1991, 1993). Timing of the root fl ush may depend on the distance from stems to roots, the physiological condition of the transport path, and environmental conditions (i.e. temperature or water relations).
New roots that develop following growth stimulation are a primary source of cytokinins (Davies, 1995). Cytokinins are transported passively to stems via the xylem sap in all plants and are active in bud break (Went, 1943;
Kende and Sitton, 1967; Sitton et al., 1967; Itai et al., 1973; Haberer and Kieber, 2002). Cytokinins stimulate shoot initiation in mango (Chen, 1985; Núñez- Elisea et al., 1990) and other plants (Oslund and Davenport, 1987; Belding and Young, 1989; Williamson and Coston, 1989; Davenport, 1990; Davies, 1995;
T.L. Davenport 130
Henny, 1995). Auxin inhibits shoot initiation (Davies, 1995) and confers api- cal dominance by preventing axillary bud break. Leaf-produced auxin and petiolar auxin transport capacity declines as leaves age (Davenport et al., 1980). Auxin and cytokinins may therefore be involved in the periodic cycle of bud break.
A critical balance of these two phytohormones, possibly modulated by GA3, may regulate shoot initiation. During a rest period, the inhibitory action of auxin transported to buds decreases with time; whereas, cytokinin lev- els in buds increase (Chen, 1987). When a critical cytokinin/auxin ratio is achieved, the buds are stimulated to grow, thereby resetting the cycle with initiation of new shoots. The interaction of auxin and cytokinin to control bud break in plants is a concept that is supported by molecular studies (see review by Nordstrom et al., 2004). Moreover, initiation of shoot growth occurs following pruning, defoliation or the application of thidiazuron (Núñez- Elisea et al., 1990). Vigorous cultivars (Whiley et al., 1989) and young, small trees under vegetatively promotive conditions fl ush frequently with only short periods of rest; however, this cycle slows with age. Old centennial trees fl ush infrequently (N. Golez, personal communication, the Philippines, 1989).
Foliar or soil-applied NO3− stimulates initiation of reproductive shoots only if applied after resting stems have attained an age to overcome any veg- etatively inductive infl uence. In contrast, high N in soils leads to high N lev- els in leaves resulting in frequent vegetative fl ushes. The mechanism whereby NO3− stimulates shoot initiation is unknown.
Seeds are rich sources of auxin and gibberellins, which contribute to the strong inhibition of bud break commonly observed on fruit-bearing mango stems. The longer that fruit are attached to stems, the longer the postharvest inhibition may last in the stem (Kulkarni and Rameshwar, 1989; Kulkarni, 1991).
Water stress inhibits shoot initiation by its direct impact on cell division and elongation possibly by interfering with translocation of cytokinins from roots. There is little evidence that water stress is directly involved in induc- tive processes. During water stress, roots continue to grow and produce cyto- kinins (Itai and Vaadia, 1965; Itai et al., 1968; Wu et al., 1994). Reduced xylem fl ux due to limited soil hydration, and transpiration due to increased sto- matal resistance during water stress may reduce the amount of cytokinins reaching stems. After rewatering, the increased levels of cytokinins in roots may translocate to and accumulate in buds. Auxin synthesis and transport from leaves are reduced during water stress (Davenport et al., 1980) and may require several days for correction after rewatering. This rapid shift in the cytokinin/auxin ratio of buds may explain the shooting response that occurs soon after relief of water stress. GA3 may act with auxin to inhibit shoot ini- tiation (Davenport et al., 2001b). Early fl owering in plants treated with PBZ may be a response to lowered gibberellin levels, thus lowering the level of initiation inhibitor.
This model could explain why sectors of tree canopies fl ush in the trop- ics. Mango trees fl ush often and synchronously throughout the canopy when they are young. With advancing age, the frequency of fl ushing is reduced
Reproductive Physiology 131
and synchrony is lost, resulting in sporadic fl ushes of vegetative or reproduc- tive growth in sections of the canopy. As the distance between stems and roots increases, the time required for transport of the putative pulses of ele- vated auxin levels to roots, formed during a vegetative fl ush, is increased.
Groups of stems exhibiting simultaneous fl ushing ultimately connect to a common branch. Dye trace studies indicate that water transport remains in strict phylotaxic alignment from secondary roots to the canopy, even in large trees (T.L. Davenport, unpublished results, Florida, 1991). Unless disturbed by girdling or by pruning of branches or roots, specifi c branches in the can- opy communicate only with those roots in phylotaxic alignment with them.
The hormone transport time may vary among sections of the canopy as the tree grows. This generates individual initiation cycles in sections of the can- opy that are separately maintained unless resynchronized with the rest of the tree following a canopy-wide environmental trigger.
Synchronization of growth throughout trees occurs following exposure to low temperature, water stress, light pruning of the entire tree and any condition that would increase the postulated cytokinin/auxin ratio in buds throughout the canopy. An increased ratio may occur by inhibiting auxin transport from leaves to buds, or increasing cytokinin translocation from roots to stems. Winter in the subtropics would reduce auxin transport;
whereas, water stress in the tropics may impact the availability of cytokinins from roots and auxin from leaves. The intensity of the initiation response (i.e.
synchronization of fl ushes in the canopy) may be regulated by decreased auxin transport at low temperatures, the base level of which may be deter- mined by the age of individual stems. Passage of a strong, extended cold front during subtropical winters produces synchronized fl owering. Milder winters with weak cold fronts result in asynchronous fl owering in sections of trees. The oldest sectors of canopies fl ower fi rst, followed by sectors bearing sequentially younger fl ushes in subsequent cold fronts. Vegetative fl ushes occur when night temperatures are > 18°C for signifi cant periods between cold fronts.
INDUCTION SWITCH. Floral or vegetative induction is possibly governed by the interactive ratio of a FP that is up-regulated in low temperatures to an age- regulated VP in leaves at the time of shoot initiation. High FP:VP ratios would be conducive to induction of generative shoots, low ratios conducive to veg- etative shoots and an intermediate ratio of the two would be conducive to mixed shoots. Regardless of the endogenous levels of the two components perceived in buds at the time of initiation, fl owering and vegetative growth responses can best be explained by the ratio of the two.
Although the putative FP seems to be up-regulated during leaf exposure to cool temperatures (< 18°C), there appears to be a basal level present at all times in leaves exposed to higher temperatures. Flowering of mango occurs in low-latitude tropics lacking cool night temperatures when stems become suffi ciently aged so that the ratio of the basal level of resident FP to decreas- ing VP increases to a critical threshold to provide fl oral induction when shoots are initiated. This could explain how fl owering on non-synchronized
T.L. Davenport 132
branches may occur at any time of the year in trees growing in low-latitude tropics. High proportions of mixed shoots are commonly found in these con- ditions, indicating the marginally fl oral-inductive ratios present under these conditions. In contrast, fl owering in younger stems having higher levels of VP is observed only when initiation occurs in cool, fl oral-inductive tempera- tures. More fl owering occurs throughout the canopy when stems are exposed to cool temperatures, attributable to the higher ratio of up-regulated FP to resident VP.
Genetic differences in base levels of the putative FP and/or VP or the receptors of these components could explain the range in fl owering responses in tropical and subtropical cultivars and why a cultivar grown in an environ- ment different from that in which it was selected is less productive. Cultivars selected in the subtropics usually fl ower as well in the low-latitude tropics as those selected in the tropics. Cool temperatures in the subtropics sometimes cause earlier fl owering in tropical cultivars than those selected in the sub- tropics. Kulkarni (1991) demonstrated that several multi-fl owering cultivars can induce fl owering in receptor graft plants and cause a range of the fl ower- ing response of the receivers to donors. Some cultivars may produce higher base levels of putative FP than others. These are the same cultivars that read- ily fl ower under warm temperatures and fl ower early during cool winter months. The Comprehensive Conceptual Flowering Model suggests that fl owering can occur at any time in any cultivar regardless of origin so long as stems are suffi ciently old to reduce the VP level to below the critical FP/VP ratio when initiation occurs.
Although the putative FP, perhaps a product of an ortholog of the Arabi- dopsis FT gene, has not been identifi ed, the VP may be a gibberellin. Triazoles and other plant growth retardants that inhibit gibberellin synthesis, promote strong and out-of-season fl owering under conditions that would normally be marginally or non-fl oral inductive.
PHOTOASSIMILATES. Photoassimilates produced by leaves provide carbohy- drates essential for development of roots and other plant organs, including fruit. They are either used immediately by the nearest sinks (Finazzo et al., 1994) or are stored in locations throughout the tree to be used when demand for carbon resources exceeds the existing photosynthetic supply (Whiley et al., 1988, 1989, 1991). A direct role for carbohydrates in shoot initiation or induction is not part of this model, although they facilitate mass fl ow in phloem from leaves to passively carry the FP to buds.
ALTERNATE BEARING. High levels of auxin and gibberellins produced in seeds possibly inhibit shoot initiation on fruit-bearing stems for weeks or months following fruit removal. Rapid production of new shoots following light pruning of fruit-bearing stems after harvest indicates that residual levels of auxin and gibberellins linger only in the rachis and last intercalary unit. If fruit are not set on the lingering rachis, there is less inhibition. Heavy fruit set in 1 year impacts the timing of subsequent shoot initiation on the large num- ber of fruit-bearing branches. Substantial delays in subsequent vegetative