Tri-factor Hypothesis of Flowering
Extensive work on movement of the putative floral stimulus across grafts from donor to receptor stems (Kulkarni, 1986, 1988b) and the inhibitory influence of fruit on subsequent flowering (Kulkarni and Rameshwar, 1989) form the basis of a flowering 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 floral stimulus in leaves, a floral inhibitor in leaves and fruits, and bud activity during the floral cycle. During dormancy following a vegetative cycle, genetic and
Mixed leafy panicles
Fig. 5.7. Kulkarni's Tri-factor Hypothesis of Flowering in mango, a hormone-regulated flowering model (Source: Kulkarni, 2004).
Mango flowering model
Mango flowering model
environmental factors determine the level of synthesis of the putative floral 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 floral inhibitor in leaves interferes with expression of the floral stimulus resulting in vegetative growth. The level of the floral 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.
This is a model of flowering involving the various classes of phytohormones (Davenport, 1992, 1993, 2000, 2003; Davenport and Nunez-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 Simpson, 1994; Davenport and Stern, 2005). Focusing on events occurring in individual 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 reproductive growth to occur in resting apical or lateral buds of mango: (i) the bud(s) must be initiated to grow (shoot initiation); and (ii) at the time of initiation, shoot development (i.e. vegetative, mixed, or generative) is determined (induction). Although conditions for floral 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 flushing event occurs much later. They become vegetative or reproductive according to the temperature at the time of shoot initiation. If transferred from cool to warm temperatures 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 floral inductive potential when removed from the cool environment. Determination of shoot type can be reversed during morphogenesis by transferring containerized trees from warm-to-cool or cool-to-warm conditions (Batten and McConchie, 1995; Nunez-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; Nunez-Elisea et al., 1992). Elevated auxin synthesis in periodically flushing 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 flushes following each vegetative flush. 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 flush 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; Nunez-Elisea et al., 1990) and other plants (Oslund and Davenport, 1987; Belding and Young, 1989; Williamson and Coston, 1989; Davenport, 1990; Davies, 1995;
Henny, 1995). Auxin inhibits shoot initiation (Davies, 1995) and confers apical 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 levels 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 (Nunez-Elisea et al., 1990). Vigorous cultivars (Whiley et al., 1989) and young, small trees under vegetatively promotive conditions flush frequently with only short periods of rest; however, this cycle slows with age. Old centennial trees flush 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 influence. In contrast, high N in soils leads to high N levels in leaves resulting in frequent vegetative flushes. 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 inductive 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 flux 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 initiation (Davenport et al., 2001b). Early flowering 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 flush in the tropics. Mango trees flush often and synchronously throughout the canopy when they are young. With advancing age, the frequency of flushing is reduced and synchrony is lost, resulting in sporadic flushes of vegetative or reproductive growth in sections of the canopy. As the distance between stems and roots increases, the time required for transport of the putative pulses of elevated auxin levels to roots, formed during a vegetative flush, is increased. Groups of stems exhibiting simultaneous flushing 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, specific branches in the canopy 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 canopy 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 flushes in the canopy) may be regulated by decreased auxin transport at low temperatures, the base level of which may be determined by the age of individual stems. Passage of a strong, extended cold front during subtropical winters produces synchronized flowering. Milder winters with weak cold fronts result in asynchronous flowering in sections of trees. The oldest sectors of canopies flower first, followed by sectors bearing sequentially younger flushes in subsequent cold fronts. Vegetative flushes occur when night temperatures are > 18°C for significant 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 vegetative 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, flowering 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 sufficiently aged so that the ratio of the basal level of resident FP to decreasing VP increases to a critical threshold to provide floral induction when shoots are initiated. This could explain how flowering on non-synchronized 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 conditions, indicating the marginally floral-inductive ratios present under these conditions. In contrast, flowering in younger stems having higher levels of VP is observed only when initiation occurs in cool, floral-inductive temperatures. More flowering 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 flowering responses in tropical and subtropical cultivars and why a cultivar grown in an environment different from that in which it was selected is less productive. Cultivars selected in the subtropics usually flower as well in the low-latitude tropics as those selected in the tropics. Cool temperatures in the subtropics sometimes cause earlier flowering in tropical cultivars than those selected in the sub-tropics. Kulkarni (1991) demonstrated that several multi-flowering cultivars can induce flowering in receptor graft plants and cause a range of the flowering response of the receivers to donors. Some cultivars may produce higher base levels of putative FP than others. These are the same cultivars that readily flower under warm temperatures and flower early during cool winter months. The Comprehensive Conceptual Flowering Model suggests that flowering can occur at any time in any cultivar regardless of origin so long as stems are sufficiently 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 identified, the VP may be a gibberellin. Triazoles and other plant growth retardants that inhibit gibberellin synthesis, promote strong and out-of-season flowering under conditions that would normally be marginally or non-floral inductive.
photoassimilates. Photoassimilates produced by leaves provide carbohydrates 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 flow 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 number of fruit-bearing branches. Substantial delays in subsequent vegetative flushes until close to the normal flowering period impact the flowering ability of young shoots. This may explain the occurrence of chronic alternate bearing in some cultivars.
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