In the grasses, stem internode elongation is suppressed during the vegetative phase and the shoot apex, enclosed by the sheath and young leaves, remains close to the base of the plant near the soil surface.
During this phase tillers basal branches are formed and the tillering phase normally overlaps with the vegetative phase Figure 2B. Once the shoot apex transitions to flowering phase, internodes begin to elongate and the tillering phase ends McMaster, A more direct link between the inhibition of bud outgrowth by a growing stem has been identified in the tiller inhibition tin mutant of wheat Kebrom et al. In tin , early cessation of tillering is associated with precocious internode elongation.
In summary, there is ample evidence that supports the indirect theory that a growing stem inhibits bud outgrowth. Stem growth and shoot branching in eudicots and monocots. A In eudicots such as pea, stem internodes elongate during the vegetative phase and shoot branching is inhibited. However, pea plants develop branches indicated by blue arrows from lower nodes adiacent to shortened internodes. B In monocots such as wheat, internodes do not elongate during the vegetative phase and tillers basal branches, indicated by blue arrows develop from the shortened internodes at the base of the shoot.
C When grown at high density enriched with shade signals from neighbor plants, internodes of monocots such as sorghum elongate and bud outgrowth is suppressed. When the density is reduced internode elongation is suppressed and branches indicated by blue arrows develop. The indirect theory of apical dominance proposed by Snow and others in the s did not detail how auxin induced stem growth might inhibit bud outgrowth.
Recent discoveries on the role of sugars in shoot branching in wheat, pea, sorghum, Arabidopsis, chrysanthemum, Rosa species, grapevine, and poplar provide new insights into the indirect theory of apical dominance Kebrom et al.
The inhibition of bud outgrowth in the tin mutant wheat is associated with precocious stem internode elongation and reduced sugar level in the buds Kebrom et al. In pea, the sugar level in a dormant bud increases when the bud is stimulated to grow by decapitation that removes a growing shoot tip, which is a strong sink for sugars Mason et al. In addition, dormant buds in intact pea plants grow when directly fed with sucrose providing conclusive evidence for the significance of sugars for bud outgrowth Mason et al.
Bud dormancy in the phytochrome B mutant sorghum phyB-1 is associated with an increase in plant height and up-regulation of genes marker for sucrose deprivation in the buds Kebrom and Mullet, Therefore, inhibition of bud outgrowth in the tin mutant wheat, pea and phyB-1 sorghum is associated with enhanced growth of the main shoot and reduced sugar level in the dormant buds.
Defoliation experiments in sorghum demonstrate that a small reduction in photosynthetic leaf area inhibits bud outgrowth while a more sever defoliation inhibits the growth of other sink organs including newly formed leaves in the main shoot Kebrom and Mullet, In the presence of strong sink organs such as a growing stem and limited sugar production in the main shoot, buds may become dormant. Therefore, the indirect theory of apical dominance can now be further elucidated as auxin-induced stem growth indirectly inhibits buds by depriving sugars necessary for their growth.
Apical dominance refers to the inhibition of bud outgrowth by the shoot apex. The dormancy versus outgrowth fates of axillary buds, and thus shoot branching is also controlled by other intrinsic and environmental factors besides auxin that act within or outside the bud Leyser, ; Janssen et al. A significant increase or decrease in plant height is commonly noticed in shoot branching mutants when the site of action of a gene is outside the bud.
For example, strigolactones are synthesized primarily in the root, and almost all highly branched strigolactone biosynthesis mutants in diverse species are dwarf Beveridge, ; Stirnberg et al. The reduction in plant height in strigolactone mutants is not due to enhanced lateral branching de Saint Germain et al. Since strigolactones promote internode elongation de Saint Germain et al.
In contrast, plant height and branching can be uncoupled when the site of action of the gene is in the bud. For example, the loss of function teosinte branched1 tb1 mutant of maize branch profusely while the height of the main shoot is not significantly different from the wild type Guan et al. Mutation in the tb1 ortholog brc1 gene in Arabidopsis is non-pleiotropic and specifically increases shoot branching Aguilar-Martinez et al.
Furthermore, although cytokinins promote bud outgrowth when applied directly to the bud, buds in cytokinin deficient Arabidopsis plants grow in response to decapitation Muller et al. Therefore, it appears that factors that control shoot branching by acting outside the bud override those that act within the bud and induce or inhibit bud outgrowth.
As yet there is no known signal from the main shoot that is transmitted to the bud and controls its activity. However, sugar supply from the main shoot to the bud would be indispensable for bud outgrowth; the sucrose might also serve as a signaling molecule promoting bud outgrowth Rabot et al.
Since an increase in plant height in response to environmental and intrinsic factors in diverse species is associated with a reduction in shoot branching, and dwarfism is associated with enhanced shoot branching, it is likely that shoot branching is determined mainly by source—sink status of the main shoot. The plant source—sink relationship is a very complex process that depends on many factors including photosynthetic leaf area and efficiency, size and position of competing sinks, plant hormone dynamics and growth stage of the plant, and availability of nutrients such as nitrogen, light, and water Lemoine et al.
For example, a small reduction in photosynthetic leaf area due to disease or herbivory could result in the inhibition of bud outgrowth in particular during the early stage of plant growth and development Kebrom and Mullet, It is also possible that plants with relatively small photosynthetic leaf area at early stages of development such as Arabidopsis may not be able to develop branches during the vegetative stage. In sorghum, stem internodes are formed during the vegetative phase and elongate in response to high planting density or shade signals Kebrom et al.
As shown in Figure 2C , the length of internodes in a sorghum plant increased and reduced by alternating high and low plant density, respectively, and branches developed from buds adjacent to shortened internodes.
In pea that displays strong apical dominance branches can still develop from buds in the lower nodes Boyer et al. In maize, the length of internodes is negatively correlated to the number and size of ears that develop from axillary buds Xu et al. Therefore, the size of internodes adjacent to the buds determines the sink strength of the internodes for sucrose utilization and storage, and indirectly regulates availability of sugars to the buds.
However, a plant may grow taller and develop more branches when it synthesizes photoassimlates in excess. A concomitant reduction in plant height and shoot branching could also occur under poor growing condition.
For example, Arabidopsis plants grown in low nitrogen are shorter and developed fewer branches than those grown at higher nitrogen de Jong et al. In addition, mutations that reduce the overall growth of a plant might reduce both plant height and shoot branching.
In fact, some of the plants reported as shoot branching mutants could be defective in the growth and development of the main shoot. For example, the reduced tillering tin wheat mutant is defective in the timing of development of internodes Kebrom et al.
Therefore, it appears that the tremendous variation in the number of branches and their position observed within and between species of annual plants could be in part due to variations in source—sink status of the main or parent shoots indirectly affecting the dormancy versus outgrowth fates of axillary buds. It is well established that during apical dominance auxin from the shoot apex inhibits bud outgrowth indirectly without entering into buds.
The two current theories of apical dominance, auxin transport canalization, and second messenger, describe processes in the main shoot in response to auxin from the shoot apex, including an increase in the level of strigolactones and a decrease in the level of cytokinins, leading to enhanced stem growth and formation of vascular tissues. Therefore, apically derived-auxin stimulates the growth of stem internodes in the main shoot and internode growth, which is a strong sink, inhibits buds indirectly by depriving sugars necessary for their growth Figure 3.
Intrinsic and environmental factors besides auxin that promote the growth and development of new sink organs including stem internodes and reproductive organs could also inhibit shoot branching indirectly by limiting sugars available for bud outgrowth. On the other hand, dwarfism in the absence of either auxin or strigolactones might stimulate shoot branching by making excess sugars available for growing buds. Therefore, shoot branching might be an unintended consequence of source—sink relationships and result from an overflow of sugars to axillary buds that cannot be utilized by the main shoot.
While bud outgrowth depends on sugar supply from the main shoot, subsequent growth of the developing branch depends on an ample supply of nutrients and water from the roots.
Nutrients are also one of the major factors determining the source—sink status, and thus indirectly regulate shoot branching. A model for the inhibition of bud outgrowth by a growing stem.
A The growth of stem intemodes in auxin or strigolactone deficient mutant plants or plants grown at high light intensity or low planting density is suppressed. A short intemode is not strong sink for sucrose. Therefore, excess sucrose exported from photosynthetic leaves to the stem overflow into axillary buds and induces bud outgrowth.
B Intrinsic factors such as auxin and strigolactones and environmental factors such as shade promote stem intemode elongation in the main shoot. Elongated intemode, which is a strong sink, inhibits bud outgrowth indirectly by limiting sugar supply to axillary bud. The plant source—sink relations is regulated by intrinsic and environmental factors making shoot branching a complex trait that cannot be predicted easily without considering the growth and developmental status of the whole plant and prevailing environmental conditions.
Reappraisal of the source—sink status in shoot branching mutants and wild-types and systematic study of the effect of source—sink status of the main shoot on dormancy and outgrowth of axillary buds might advance our knowledge of the physiological basis of apical dominance and shoot branching in plants. Future studies should accurately determine the sink or source status of an organ being manipulated.
For example, the cotyledons in pea contribute to seed germination. The nutrient reserve and biomass of the cotyledons are exhausted within the first 10 days after sowing, during which the plant transitions from heterotrophic to autotrophic growth Hanley et al.
Experiments involving cotyledon removal or defoliation of young newly formed or old non-photosynthetic leaves assuming that they are source of nutrients or photoassimilates might lead to incorrect conclusions. Besides their role in shoot branching, sugars are also important in many other aspects of plant growth and development including phase transitions from juvenile to adult and from vegetative to flowering Wahl et al.
Therefore, when investigating plant growth and development, sugar demand and supply should be taken into consideration. The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The author thanks Dr. Aguilar-Martinez, J. Plant Cell 19, — Albacete, A. Hormonal and metabolic regulation of source-sink relations under salinity and drought: from plant survival to crop yield stability. Barbier, F. Sucrose is an early modulator of the key hormonal mechanisms controlling bud outgrowth in Rosa hybrida.
Beveridge, C. Long-distance signalling and a mutational analysis of branching in pea. Plant Growth Regul. Pea has its tendrils in branching discoveries spanning a century from auxin to strigolactones. Plant Physiol. Booker, J. Auxin acts in xylem-associated or medullary cells to mediate apical dominance. Plant Cell 15, — Boyer, F. Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching.
Cline, M. Exogenous auxin effects on lateral bud outgrowth in decapitated shoots. Auxin and strigolactone signaling are required for modulation of Arabidopsis shoot branching by nitrogen supply.
Strigolactones stimulate internode elongation independently of gibberellins. Auxin-mediated plant architectural changes in response to shade and high temperature. Deng, W. The tomato SlIAA15 is involved in trichome formation and axillary shoot development. New Phytol. Dierck, R. Response to strigolactone treatment in chrysanthemum axillary buds is influenced by auxin transport inhibition and sucrose availability. Acta Physiol. Domagalska, M. Signal integration in the control of shoot branching.
Cell Biol. Ferguson, B. Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Finlayson, S. Phytochrome regulation of branching in Arabidopsis.
Franklin, K. Phytochromes and shade-avoidance responses in plants. Guan, J. Diverse roles of strigolactone signaling in maize architecture and the uncoupling of a branching-specific subnetwork.
Hall, S. Correlative inhibition of lateral bud growth in Phaseolus vulgaris L. Planta , — Hanley, M. Early plant growth: identifying the end point of the seedling phase. Hosokawa, Z. Apical dominance control in ipomoea-nil - the influence of the shoot apex, leaves and stem. Ishikawa, S. Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol. Janssen, B. Regulation of axillary shoot development.
Plant Biol. Kebrom, T. Plants were treated with 0. For each experimental variant stem segment samples were collected from 10 plants. In all stem segment variants samples were incubated in a dioxane-based liquid scintillator cocktail overnight. Six hours after decapitation, 0. How to cite this article : Balla, J. Auxin flow-mediated competition between axillary buds to restore apical dominance.
Rameau, C. Multiple pathways regulate shoot branching. Plant Sci. Article Google Scholar. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science , — Polar PIN localization directs auxin flow in plants. Science , Swarup, R. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Gene Dev. Thimann, K. On the inhibition of bud development and other functions of growth substance in Vicia faba.
Hall, S. Correlative inhibition of lateral bud growth in Phaseolus vulgaris L. Planta , — Balla, J. Involvement of auxin and cytokinins in initiation of growth of isolated pea buds. Plant Growth Regul. Prusinkiewicz, P. Control of bud activation by an auxin transport switch. USA , — Crawford, S. Strigolactones enhance competition between shoot branches by dampening auxin transport.
Development , — Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth. Plant J. Shinohara, N. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol. Sachs, T. The control of patterned differentiation of vascular tissues.
Stafstrom, J. Dormancy-associated gene expression in pea axillary buds. Aquilar-Martinez, J. Plant Cell 19, — Goldsmith, M. The polar transport of auxin. Plant Physiol. Peterson, C. Lateral bud growth on excised stem segments: effect of the stem. Morris, S. Auxin dynamics after decapitation are not correlated with the initial growth of axillary buds.
Ferguson, B. Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Renton, M. Models of long-distance transport: how is carrier-dependent auxin transport regulated in the stem? New Phytol. Mason, M. Sugar demand, not auxin, is the initial regulator of apical dominance. Brewer, P. Strigolactone inhibition of branching independent of polar auxin transport. Rayle, D. The acid growth theory of auxin-induced cell elongation is alive and well.
Yamagami, M. Two distinct signaling pathways participate in auxin-induced swelling of pea epidermal protoplasts. Dhonukshe, P. Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Morgan, D. Nature, , — Auxin efflux carrier activity and auxin accumulation regulate cell division and polarity in tobacco cells. Planta, , — Yoneyama, K. Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites.
Sorefan, K. Genes Dev 17, — Bainbridge, K. Hormonally controlled expression of the Arabidopsis MAX4 shoot branching regulatory gene. Bangerth, F. Response of cytokinin concentration in the xylem exudate of bean Phaseolus vulgaris L. Kim, J. Google Scholar.
Do phytotropins inhibit auxin efflux by impairing vesicle traffic? Borkovec, V. Plant Growth Reg. Robinson, J. Differential effects of brefeldin A and cycloheximide on the activity of auxin efflux carriers in Cucurbita pepo L. Geldner, N. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature , — Die, J. Evaluation of candidate reference genes for expression studies in Pisum sativum under different experimental conditions. Paciorek, T. Immunocytochemical technique for protein localization in sections of plant tissues.
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Advanced search. Skip to main content Thank you for visiting nature. Download PDF. Subjects Plant development Plant physiology. Abstract Apical dominance is one of the fundamental developmental phenomena in plant biology, which determines the overall architecture of aerial plant parts. Introduction It is widely accepted that genetic determination and variable responses to different environmental conditions are responsible for the wide range of plant body forms. Results Axillary buds released from dormancy compete for dominance in pea Garden pea, among plant species, has well pronounced apical dominance.
Figure 1. Axillary buds released from dormancy compete for dominance in pea. Full size image. Figure 2. Auxin pool in decapitated stem delays release of buds from dormancy.
Figure 3. PAT Interruption in the primary stem releases buds from dormancy. Figure 4. Interruption of PAT between buds releases lower bud from dormancy. Figure 5. Inhibition of PAT from the upper bud releases lower bud from dormancy.
Discussion In plants with strong apical dominance, the shoot apex supplies the primary stem with auxin, and inhibits outgrowth of axillary buds. Methods Plant material, growth conditions, inhibitors and hormonal treatment Pea plants Pisum sativum L. Polar auxin transport capacity assay Plants were treated with 0. Additional Information How to cite this article : Balla, J. References Rameau, C. Article Google Scholar Swarup, R. Article Google Scholar Stafstrom, J.
Article Google Scholar Goldsmith, M. Article Google Scholar Morris, S. Article Google Scholar Yoneyama, K. Article Google Scholar Borkovec, V. View author publications. Ethics declarations Competing interests The authors declare no competing financial interests. Electronic supplementary material. Supplementary Information. Rights and permissions This work is licensed under a Creative Commons Attribution 4.
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