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Apical dominance maximizes reproductive strategies in Lilium longiflorum

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Abstract

Axillary meristems are the regenerating insurance of most plant species. They are initiated while the shoot apical meristem (SAM) produces leaves and usually remain inactive until a specific physiological change occurs. This common growth regulation is named "apical dominance". In bulbous plants, axillary meristems initiate storage organs, which usually contain their own apical meristem. In Lilium longiflorum, an ornamental geophyte, the axillary meristems produce the bulbs of the following season. Large bulbs must get cold in order to flower, while small ones can flower without cold exposure under long-day conditions. Our aim was to clarify the foundation of the different flowering pathways regulated by bulb size, in view of the apical dominance mechanism, and identify its horticultural consequences. We monitored the development of L. longiflorum's bulbs produced from axillary meristems under an array of environmental and physiological alterations, including natural conditions and agrotechniques. The growth rate of L. longiflorum bulbs was highly affected by the developmental stage of the SAM, as well as by SAM decapitation and auxin application. Leaf biomass contributed as well to the final bulb size. Cold exposure quantitatively hastened flowering time and induced bud abortion. Bulb size and floral induction pathway (cold exposure or long-day conditions) affected flowering phenotype of the plants. We suggest a model by which apical dominance plays a major role in the reproductive strategy of L. longiflorum by regulating its prospective flowering pathways: either vernalization or photoperiod. This new concept enlightens the benefits of apical dominance for the plant growth-cycle under changing environments and disturbed habitats. Based on these results, we propose a novel horticultural protocol for lily forcing, taking into account the bulb size and the flowering pathway.

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At the reproductive stage, lily plants bear two morphological types of mature leaves, one at the lower and one at the upper part of the stem. At the vegetative stage, all the leaves are similar to each other and to the reproductive plant's lower leaves. This heterophylly has not yet been explored. In this study, we show that it is not a result of the plant's age but rather an outcome of floral induction. The induction appears as an on‐going process, during which the meristem still produces leaves but progressively becomes committed to reproduction. This intermediate period lasts until the ultimate switch to flower primordia occur. The leaves produced during floral induction, termed here as "inductive", appear at the upper part of the stem. Besides their typical higher stomata density, these leaves have a poly‐layered palisade mesophyll, whose cells exhibit a unique morphology and contain more chlorophyll than leaves of vegetative plants. These leaves display higher carbon assimilation, soluble sugars production and chloroplast‐lipid accumulation. Accordingly, genes associated with stomata, chloroplast and photosynthesis are upregulated in these leaves. Our results were obtained when floral induction was achieved either by vernalization or photoperiod signals, ruling out a mere environmental effect. We suggest that lily plants prepares themselves for the high energy‐demanding bloom by producing leaves with enhanced photosynthetic capacity, leading to an increase in soluble sugars. These novel findings introduce an adjacent affinity between photosynthesis and flowering and provide a non‐destructive tool for identifying the plant's developmental stage – vegetative or reproductive. This article is protected by copyright. All rights reserved.
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Lilium longiflorum (Easter lily) vegetative propagation occurs through production of underground bulbs containing an apical and an axillary meristems. In addition, sexual reproduction is achieved by flowering of elongated shoots above the bulb. It is generally accepted that L. longiflorum has an obligatory requirement for vernalization and that long day (LD) regime hastens flowering. However, the effect of bulb size and origin, with respect to axillary or apical meristem on flowering, as well as the interactions between these meristems are largely unknown. The aim of this study was to explore the effect of bulb size, vernalization and photoperiod on L. longiflorum flowering. To this end, we applied vernalization and photoperiod treatments on the different bulb sizes and used a system of constant ambient temperature of 25°C, above vernalization spectrum, to avoid cold-dependent floral induction during plant growth. Vernalization and LD hasten flowering in all bulbs. Large, non-vernalized bulbs invariably remained at a vegetative stage. However, small non-vernalized bulbs flowered under LD conditions. These results demonstrate for the first time that cold exposure is not an obligatory requisite for L. longiflorum flowering, and that an alternative flowering pathway can by-pass vernalization in small bulbs. We suggest that apical dominance interactions determine the distinct flowering pathways of the apical and the axillary meristems. Similar floral induction is achieved in propagation bulblets from scaling. These innovative findings in the field of geophyte floral induction represent valuable applicative knowledge for lily production. This article is protected by copyright. All rights reserved.
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While sexual regeneration of plants after disturbance is relatively well understood, vegetative regeneration has attracted some attention only recently. Its role along environmental gradients and across biomes is poorly known and standard methods for assessment are not yet established. We review current knowledge about the role of bud banks in vegetative regeneration and the diversity of their modes of functioning. The similarities and differences between bud banks and seed banks are illustrated, focusing on dormancy, dispersability, seasonal dynamics, longevity and storage of carbohydrates. We try to formulate some principles that unify bud bank functioning across habitats and growth forms: (1) the bud banks consist of all buds which may be used for vegetative regeneration, including those formed adventitiously only after injury; (2) vertical distribution of buds reflects avoidance of disturbance; (3) seasonal changes in the bud bank make vegetative regeneration sensitive to timing of disturbance; and (4) ability to form adventitious buds provides a potential for vegetative regeneration from roots, stumps and leaves. Based on these principles, a simple classification of bud banks is presented similar to the classification of seed banks. Bud bank traits are considered in relation to severity, timing and frequency of disturbance. These include vertical distribution and seasonal fluctuations in the number of buds. Methods for quantitative assessment of bud numbers and resprouting capacity are reviewed, and a new approach based on indirect bud counts is proposed. The suggested concept of bud banks may be widely used in studies focusing on plant functional traits in relation to disturbance regimes at the levels of plant individuals, populations and communities. Its further development may incorporate adjustments for areas with non-seasonal climate and refinements for some growth forms, such as epiphytes.
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The genus Lilium is widely used in the flower industry for the production of cut flower stems and potted plants; it is also well known as a garden plant. The wide utilization is also due to the good propagation aptitude, both gamic and agamic, that these species display. Lily seeds display two ways of germination: epigeal seeds germinate immediately after sowing and the cotyledon emerges from the ground, in hypogeal seeds the bulb develops first, remaining underground, and only afterwards the true leaf emerges from the ground. This germination is usually controlled by dormancy which breaks only after the seed has been exposed to cold/warm treatments. Vegetative propagation is facilitated by the high regeneration potential shown by all plant tissues. It is possible to propagate lilies vegetatively in three ways: by using bulbils from the stem, from bulblets around the stem base and from scales. The last method gives the largest quantity of new plants. Vegetative propagation is also possible by hormonal stimulation of tissues to undergo differentiation of shoot or bulbs. Furthermore, bulbous plants, like lilies, have proven to be ideal for tissue culture, as their regeneration potential is usually high. The compact structure of the shoot makes them easy to handle in both solid and liquid cultures. Nowadays, lilies are one of the most important bulbous crops produced in tissue culture also on industrial scale. Combining the benefits of mass production and fast regeneration of uniform plant material in tissue culture is a necessity for the future breeding and culture of lilies. However, to make tissue culture a commercially relevant production system, protocols need to be improved evaluating automation through the more suitable bioreactor type.
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Lilium longiflorum Thunb. `Nellie White' plants grown under 1300 μmol·m ⁻² ·s ⁻¹ maximum photosynthetic photon flux (PPF) in a greenhouse deliberately were completely defoliated when the oldest flower bud was 2, 4, or 7 cm long. Plants were then placed in growth chambers in darkness or in the light (250 μmol·m ⁻² ·s ⁻¹ PPF, 10 hours) with 25C air, along with intact plants as controls; all were harvested at the completion of flowering. Defoliation at the 2- and 4-cm bud stages resulted in complete flower abortion, with or without light. Plants defoliated at the 7-cm stage and kept in light had 60% of the flower buds develop to anthesis but depleted more scale reserves. Those defoliated at the 7-cm stage and kept in darkness had complete flower abortion; however, bulb weights remained similar to those of the intact plants kept in the light.
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Temperature is one of the most important factors that directly affect the possibility and the rate of flower differentiation in many geophytes such as Lilium. In this experiment, different day and night temperatures were used to determine the required day and night temperature for flower bud development in Lilium hansonii. After low temperature exposure for breaking bulb dormancy, the bulbs were planted in pots, and placed in designated growth chambers each with a specific temperature. The plants were exposed to different temperatures for 30 days, and 15 days after planting sample plants were collected in each treatment for observation of flower bud development using the scanning electron microscope (SEM). Responses of plant height, number of leaves, and stem diameter were also measured as affected by difference between day and night temperature (DIF) and average daily temperature (ADT). The results showed that average daily temperature and high day temperature had a direct effect on the quality, quantity, and time required for flower bud development. They also affected the stem elongation, number of leaves, and stem diameter. Higher ADT and DT (25°C) promoted stem elongation and increased leaf unfolding rate (LUR), but with less number of leaves produced. As ADT and DT increased, stem diameter decreases. In lower ADT and DT (15°C) treatment, greater stem diameter and higher number of flower buds (2–7 buds) were produced. Higher ADT and DT promoted early flower bud initiation, but lower number of flower buds with higher possibilities of flower bud abortion, while lower ADT and DT showed slower flower bud initiation and development with higher flower bud formation.
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The genus Lilium is important as potted plants or cut flowers for horticultural trade and for gardens. However, most of the extensive research on the growth and flowering of this genus was conducted with L. longiflorum Thunb. (Easter lily) forcing large bulbs grown in the field for at least one or two years. Dormancy had to be broken to induce flowering by cold treatment which was given to mature bulbs (vernalization). It would be desirable if the bulb production phase could be bypassed to shorten the total production time, ideally by manipulating the temperature during the bulb programming phase (vernalization methods) and the early greenhouse forcing phase (from potting to flower bud initiation). Information on the physiology of bulb development, controlled flowering, and timing for the Easter, and to certain extent for the Asiatic hybrid lily is readily available. However, information on LA, L. longiflorum × Oriental (LO), and Oriental × Trumpet (OT) hybrid lilies, is not available. The objective of this article is to review factors that control flower numbers and speed of flowering, and to present outlines for producing quality plants of L. longiflorum, L. ×elegans, and LA hybrids, starting from seeds, stem bulbils, and tissue cultured plants, respectively, in a year. Detailed information on the production of L. ×elegans starting from stem bulbils is presented. Cut flowers of Asiatic hybrid ‘Beni no Mai’ with 2 to 3 flowers and strong 60 cm stems were produced in less than a year when mature bulbils, weighing about 400 mg harvested 40 to 50 days after flowering, are treated with a sequential temperature treatment (SEQ CD) 14 to 20 days each at 5°C-15°C-5°C. This production period can be divided into plug production phase from potting the treated bulbils shoot emergence lasting about 200 to 230 days and the second phase from shoot emergence to flowering requiring 90 to 100 days. The increase in the number of flowers could result from the increased shoot apex size and not from the changes in soluble and cell wall neutral sugars.
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InRosa hybridaL. cv. Ruidriko ‘Vivaldi’®, the effect of position on growth and development potentials of axillary buds was investigated by single internode cuttings excised along the floral stem and its bearing shoot. The experiments were carried out in both glasshouses and in a phytotron. The study firstly concerned the development of the primary shoot from the onset of bud growth until anthesis. The primary shoot was then bent horizontally to promote the growth of the two most proximal secondary buds, the collateral buds, already differentiated inside the primary bud. They gave rise to basal shoots. In the basipetal direction, the axillary buds along the floral stem exhibited both an increase in the lag time before bud growth and a decrease in bud growth percentage, demonstrating the existence of a physiological basipetal gradient of inhibition intrinsic to the buds or due to short range correlations. The same basipetal gradient of inhibition was observed along the floral stem and its bearing shoot, demonstrating that the age of the bud was not a major factor in determining the rate of bud growth. After bending the primary shoot, the percentage of collateral bud growth was also affected by the cutting position. The more proximal the cutting, the lower the sprouting ability of collateral buds. The growth potential of these buds appeared to be already determined inside the main bud before cutting excision.
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It is suggested that evolution in plants may be associated with the emergence of three primary strategies, each of which may be identified by reference to a number of characteristics including morphological features, resource allocation, phenology, and response to stress. The competitive strategy prevails in productive, relatively undisturbed vegetation, the stress-tolerant strategy is associated with continuously unproductive conditions, and the ruderal strategy is characteristic of severely disturbed but potentially productive habitats. A triangular model based upon the three strategies may be reconciled with the theory of r- and K-selection, provides an insight into the processes of vegetation succession and dominance, and appears to be capable of extension to fungi and to animals.
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Summary • Changes in the physical state of cellular water and its interrelations with carbohydrate metabolism were studied during preplanting storage of tulip bulbs (Tulipa gesneriana‘Apeldoorn’). • Magnetic resonance imaging, light and scanning electron microscopy and high-performance anion exchange chromatography with pulsed amperometric detection were used to follow time-dependent changes during bulb storage at 17 or 20°C (nonchilled) or 4°C (chilled). • No visible differences in scale structure and central bud development were observed microscopically between chilled and nonchilled bulbs. However, the scales of the chilled bulbs exhibited higher water content, faster starch degradation and increased concentrations of sucrose and ethanol-soluble fructan. Quantitative measurements of magnetization transfer (MT) indicated a smaller fraction of a solid or a restricted-mobility proton pool in the scales of the chilled bulbs. By contrast, the MT effect was significantly higher in the central bud of the chilled than in the nonchilled bulbs. • Degradation of storage polysaccharides to low-molecular-weight sugar molecules during release from dormancy could be accompanied by local release of water molecules tightly bound to the polysaccharide granules into the bulk water, or by an influx of free water molecules due to increased osmotic potential caused by the raised sugar concentration, or by a combination of both effects.
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Flower growth and opening are commonplace events, but physiologically intricate and inadequately explained. In this review, we have brought together and evaluated information on this subject to focus attention on the dynamic facets of flower development. In particular, the physiological basis of flower bud dormancy, nature of cleistogamy, mechanism of flower bud growth and turgor maintenance and role of stamens in corolla growth have been examined. The regulation of flower movements and opening by temperature and light, and circadian rhythms in flower opening have been discussed, along with a consideration of the role of the petal epidermis in light perception. It is emphasized that studies on flower physiology need to be intensified in view of the lacunae in our basic knowledge as well as to provide a sound basis for improving yields of both agricultural and horticultural crops.
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Plants are able to tolerate tissue loss through vigorous branching which is often triggered by release from apical dominance and activation of lateral meristems. However, damage-induced branching might not be a mere physiological outcome of released apical dominance, but an adaptive response to environmental signals, such as damage timing and intensity. Here, branching responses to both factors were examined in the annual plant Medicago truncatula. Branching patterns and allocation to reproductive traits were examined in response to variable clipping intensities and timings in M. truncatula plants from two populations that vary in the onset of reproduction. Phenotypic selection analysis was used to evaluate the strength and direction of selection on branching under the damage treatments. Plants of both populations exhibited an ontogenetic shift in tolerance mechanisms: while early damage induced greater meristem activation, late damage elicited investment in late-determined traits, including mean pod and seed biomass, and supported greater germination rates. Severe damage mostly elicited simultaneous development of multiple-order lateral branches, but this response was limited to early damage. Selection analyses revealed positive directional selection on branching in plants under early- compared with late- or no-damage treatments. The results demonstrate that damage-induced meristem activation is an adaptive response that could be modified according to the plant's developmental stage, severity of tissue loss and their interaction, stressing the importance of considering these effects when studying plastic responses to apical damage.
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Apical dominance is the control exerted by the shoot apex over lateral bud outgrowth. The concepts and terminology associated with apical dominance as used by various plant scientists sometimes differ, which may lead to significant misconceptions. Apical dominance and its release may be divided into four developmental stages: (I) lateral bud formation, (II) imposition of inhibition on lateral bud growth, (III) release of apical dominance following decapitation, and (IV) branch shoot development. Particular emphasis is given to discriminating between Stage III, which is accompanied by initial bud outgrowth during the first few hours of release and may be promoted by cytokinin and inhibited by auxin, and Stage IV, which is accompanied by subsequent bud outgrowth occurring days or weeks after decapitation and which may be promoted by auxin and gibberellin. The importance of not interpreting data measured in Stage IV on the basis of conditions and processes occurring in Stage III is discussed as well as the correlation between degree of branching and endogenous auxin content, branching mutants, the quantification of apical dominance in various species (including Arabidopsis ), and apical control in trees.
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In three experiments (twoin-vivo, onein-vitro), an attempt was made to separate the possible effects of age and position of axillary buds of chrysanthemum on bud outgrowth and the subsequent quality of cuttings. In thein-vivoexperiments, bud age and bud position were not significant factors in bud outgrowth and subsequent quality of cuttings. Nevertheless, most outgrowth parameters showed slightly higher values for the lower positioned buds and the time needed to produce a cutting tended to decrease with the age of the axillary bud. In thein-vitroexperiment, the relationship between age and the various parameters showed an optimum.
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The relative growth rate (Rw) of daughter bulbs of the tulip cultivar Rose Copland was remarkably constant during the spring period of growth in four seasons at two sites. The Q10 of Rw was 2.2, and the long period of constant Rw is attributed to compensation of a fall with age by increasing temperatures in the spring. Final bulb weight differed among four cultivars because of differences in Rw and in initial daughter bulb weights. Partial defoliation reduced Rw roughly in proportion to the leaf area removed, and removal of mother bulb scales resulted in reduced leaf area, fewer daughter bulbs, and a lower daughter bulb Rw. Heat-treatment of mother bulbs before planting (blindstoken) killed the flower within the bulb, inactivated the apical dominance exerted by the flower, and resulted in a higher initial daughter-bulb weight at the start of the spring period of exponential growth. The Rw of heat-treated and control daughter bulbs were not different, neither were the leaf areas, so it is assumed that final daughter-bulb weights were higher following treatment because of increased sink strength. The economic implications of these findings are discussed.
Article
Evidence from pea rms1, Arabidopsis max4 and petunia dad1 mutant studies suggest an unidentified carotenoid-derived/plastid-produced branching inhibitor which moves acropetally from the roots to the shoots and interacts with auxin in the control of apical dominance. Since the plant hormone, abscisic acid (ABA), known to inhibit some growth processes, is also carotenoid derived/plastid produced, and because there has been indirect evidence for its involvement with branching, a re-examination of the role of ABA in apical dominance is timely. Even though it has been determined that ABA probably is not the second messenger for auxin in apical dominance and is not the above-mentioned unidentified branching inhibitor, the similarity of their derivation suggests possible relationships and/or interactions. The classic Thimann-Skoog auxin replacement test for apical dominance with auxin [0.5 % naphthalene acetic acid (NAA)] applied both apically and basally was combined in similar treatments with 1 % ABA in Ipomoea nil (Japanese Morning Glory), Solanum lycopersicum (Better Boy tomato) and Helianthus annuus (Mammoth Grey-striped Sunflower). Auxin, apically applied to the cut stem surface of decapitated shoots, strongly restored apical dominance in all three species, whereas the similar treatment with ABA did not. However, when ABA was applied basally, i.e. below the lateral bud of interest, there was a significant moderate repression of its outgrowth in Ipomoea and Solanum. There was also some additive repression when apical auxin and basal ABA treatments were combined in Ipomoea. The finding that basally applied ABA is able partially to restore apical dominance via acropetal transport up the shoot suggests possible interactions between ABA, auxin and the unidentified carotenoid-derived branching inhibitor that justify further investigation.
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