Shoot Branching and Plant Architecture

Abstract

Shoot architecture is the spatial arrangement of stems, leaves and reproductive structures in plants. A major component of shoot architecture is the formation of secondary axes of growth (branches). In flowering plants, these originate from meristems located in the axils of leaves. Once initiated, axillary meristems can produce a secondary shoot immediately, or arrest as a dormant bud, resulting in a large degree of architectural plasticity. Long‐distance hormonal signals including auxin, cytokinin and strigolactone allow the outgrowth of buds to be tightly coordinated with the physiological and nutritional status of the plant as a whole. Two major models have been proposed to explain how these hormonal signals are integrated to control shoot branching. Shoot architecture is highly varied among model species, but the core regulatory mechanisms are conserved across the flowering plant group.

Key Concepts

  • Shoot architecture in flowering plants is highly plastic and is produced using repeating modules (phytomers), which can vary in number and type.
  • Production of secondary shoots (branches) is a major component of shoot architecture in flowering plants.
  • Branches are produced by axillary meristems, which form in the axils of leaves.
  • Axillary meristem formation may occur simultaneously with leaf formation, or may be delayed until a later stage.
  • Once initiated, axillary meristems may immediately grow out to form a branch, or can produce a dormant axillary bud.
  • The activity‐dormancy switch in axillary buds is the major control point for shoot branching.
  • Long‐distance hormonal signals control bud outgrowth in response to environmental cues.
  • Two major models have been proposed to explain how these hormonal signals are integrated to control shoot branching.
  • Different species use the same fundamental control mechanisms to produce highly varied shoot architectures.

Keywords: shoot apical meristem; axillary meristem; plant development; auxin; cytokinin; strigolactone

Figure 1. Basic terminology in shoot architecture and the effect of apical auxin on branching. (a) An intact shoot apex (the shoot apical meristem and young leaves) inhibits the growth of subtending buds. (b) Removal of the shoot apex allows growth of subtending buds. (c) Replacement of the shoot apex with lanolin paste containing auxin prevents bud outgrowth.
Figure 2. Axillary meristem specification and development. (a) During the formation of a leaf, auxin is transported into the primordium (red arrows) and then through the primordium into the inner tissue layers, resulting in locally high auxin levels (red shading). (b) As the primordium expands, auxin levels drop in the organ boundary and presumptive axil, leading to expression of boundary genes (including CUC2) and cytokinin (CK) synthesis or signalling. (c) Meristem initiation in the leaf axil may be delayed, in which case expression of LAS prevents differentiation of the axillary tissue. (d) Alternatively, meristem initiation may be immediate, in which case STM expression is maintained the axillary tissue. A few unexpanded leaves are produced, after which bud dormancy may be imposed.
Figure 3. Models of shoot branching control. Red arrows indicate hormone transport and blue arrows indicate regulatory interactions. (a) Second messenger model. Apically derived auxin (IAA) is transported through the stem and oppositely regulates cytokinin (CK) and strigolactone (SL) synthesis at the node. Transport of SL and CK into the bud has opposite effects on BRC1 transcription, which acts as a signal integrator. (b) Canalisation model. Apically derived auxin is transported through the stem by the PIN1 auxin efflux carrier. The amount of auxin in the stem determines its auxin sink strength. Canalised auxin export from buds (auxin sources) is required to establish their outgrowth. This is more difficult to achieve if there is high auxin in the stem, and hence the stem is a weak sink for auxin. SL regulates branching by controlling PIN1 removal from the plasma membrane, affecting stem sink strength and the dynamics of auxin transport canalisation from the bud to the stem. The exact mode of action of CK is unclear, but it could also act by modulating auxin transport.
Figure 4. Canalisation and shoot branching. Blue indicates vascular elements and red indicates auxin sources. (a) Auxin application to the side of a decapitated pea seedlings leads to canalised vein formation between auxin source and sink (the central vascular cylinder). (b) Auxin application to the decapitated apex of the hypocotyl prevents establishment of vascular connectivity between the laterally applied auxin and the primary vasculature. (c) Development of a canalised auxin flow between buds and vasculature in the primary stem is analogous to the experiments shown in (a) and (b). A bud can only connect to the main vasculature if it is a sufficiently strong auxin source.
Figure 5. Shoot branching in model dicot and monocot plant species. The schematic drawing represents axillary meristem activity during plant development in the described model species. The thick black line represents the primary axis, the blue lines represent secondary vegetative axes and the red lines represent specialised inflorescence axes bearing flowers (yellow circles).
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Further Reading

Bennett T, Hines G and Leyser O (2014b) Canalization: what the flux? Trends in Genetics 30: 41–48.

Gallavotti A (2013) The role of auxin in shaping shoot architecture. Journal of Experimental Botany 64: 2593–2608.

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Pautler M, Tanaka W, Hirano HY and Jackson D (2013) Grass meristems I: shoot apical meristem maintenance, axillary meristem determinacy and the floral transition. Plant and Cell Physiology 54: 302–312.

Tanaka W, Pautler M, Jackson D and Hirano HY (2013) Grass meristems II: inflorescence architecture, flower development and meristem fate. Plant and Cell Physiology 54: 313–324.

Teichmann T and Muhr M (2015) Shaping plant architecture. Frontiers in Plant Science 6: 233.

Waldie T, McCulloch H and Leyser O (2014b) Strigolactones and the control of plant development: lessons from shoot branching. Plant Journal 79: 607–622.

Wang Q, Hasson A, Rossmann S and Theres K (2015) Divide et impera: boundaries shape the plant body and initiate new meristems. New Phytologist. DOI: 10.1111/nph.13641.

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Bennett, Tom, Ward, Sally P, and Leyser, Ottoline(May 2016) Shoot Branching and Plant Architecture. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020122.pub2]