Regulatory Mechanisms of Phyllotaxy

Abstract

Hypotheses to explain phyllotaxy – the regular positioning of leaves on stems – were first proposed in the nineteenth century. Recently, polarized transport of the photohormone auxin was found to have a key role in generating phyllotaxy patterns that is consistent with classical models. How auxin might interact with other patterning mechanism to regulate phyllotaxy is currently unclear.

Keywords: phyllotaxy; phyllotaxis; auxin; leaf development

Figure 1.

Phyllotaxy patterns. Common phyllotaxy patterns include (a) distichous, shown here in the monocot Tradescantia sillamontana, (b) spiral, shown in Arabidopsis thaliana and (c) decussate in the snapdragon, Antirrhinum majus. The helix formed in spiral phyllotaxy (arrows) can be either left‐ of right‐handed. The two Arabidopsis plants showing opposite spirals are genetically identical, suggesting that the handedness is determined by a random process. (d) Flowers of Antirrhinum majus, like the majority of derived angiosperms, have floral organs in whorls. Here a whorl of five green sepals is followed by a whorl of five, partially united red petals. In more basal angiosperms, such as water lilies (Nymphaea species), a variable number of petals and stamens are produced in a spiral phyllotaxy pattern. (e) Phyllotaxy often changes predictably during development. This A. majus plant initially produced leaves in a decussate pattern, changing to spiral phyllotaxy before flowering. (f)The arrangement of leaves can be modified by environment. Here in a horizontally growing branch of Lonicera, leaves are produced in decussate phyllotaxy at the shoot apex (bottom), but are subsequently reoriented by twisting of the stem and bending of their petioles to give the appearance of opposite pairs of leaves in two files. (g) Changes in phyllotaxy patterns can be maintained. Here this juvenile Antirrhinum plant initially produced two leaves at each node and subsequently switched to the production of three leaves per node. This pattern was maintained until the transition to spiral phyllotaxy on flowering.

Figure 2.

Spiral phyllotaxy and the Fibonacci series. The scales of this pine cone – seen from its apex – show spiral phyllotaxy. Each scale is in contact with two neighbours above it, forming two sets of contact helices – five right‐handed (blue) and eight left‐handed (red). These numbers are adjacent members of the Fibonacci series. Although complex, this phyllotaxy pattern has the common property of organs being positioned in the gaps above previously formed organs.

Figure 3.

The inhibitor‐field model of phyllotaxy. (a) In this shoot apical meristem, viewed from above, existing leaf primordia, labelled P1–P5 in order of increasing age, are proposed to produce an inhibitor of leaf initiation, which is shown as a gradient of inhibitor surrounding each primordium. The next primordium (I1) will then initiate where inhibitor is at its lowest level. Subsequent growth of the meristem will result in the level of inhibition reaching a minimum at position I2, from which the next primordium will form. The central zone of the meristem (CZ) is not competent to form primordia. (b) The inhibitor‐field model of phyllotaxy was supported by surgical experiments. Here, a cut (black line) was made to isolate a newly formed primordium (P1) from the meristem of Lupin. The positions at which the next two leaf primordia would normally form are shown as I1 and I2 in the left‐hand figure. The cut does not affect the position of I1, which was presumably determined by this stage, but causes I2 to form a primordium nearer to P1, consistent with the cut having blocked movement of the inhibitor from P1 to the meristem. Redrawn from Snow and Snow, .

Figure 4.

The polar auxin transport model of phyllotaxy. Auxin is transported to the shoot apex by asymmetrically localized PIN1 protein (blue), mainly in the outermost cell layer, L1. Higher levels of auxin cause an increase in PIN1 abundance and its reorientation towards the future tip of the leaf primordium, increasing auxin flow (red arrows) into the primordium. Increased auxin triggers leaf fate and PIN is expressed in internal cells of the primordium where it is oriented to move auxin down into the stem. This depletes auxin around the primordium and prevents new primordia forming in this region.

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References

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Further Reading

Carro N, Peaucelle A, Laufs P and Traas J (2006) Cell differentiation and organ initiation at the shoot apical meristem. Plant Molecular Biology 60: 811–826.

Fleming AJ (2005) Formation of primordia and phyllotaxy. Current Opinions in Plant Biology 8: 53–58.

Paciorek T and Friml J (2006) Auxin signalling. Journal of Cell Science 119: 1199–1202.

Reinhardt D (2005) Regulation of phyllotaxis. International Journal of Developmental Biology 49: 539–546.

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How to Cite close
Hudson, Andrew(Apr 2007) Regulatory Mechanisms of Phyllotaxy. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020118]