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WIREs Dev Biol
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Phyllotaxis: from patterns of organogenesis at the meristem to shoot architecture

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The primary architecture of the aerial part of plants is controlled by the shoot apical meristem, a specialized tissue containing a stem cell niche. The iterative generation of new aerial organs, (leaves, lateral inflorescences, and flowers) at the meristem follows regular patterns, called phyllotaxis. Phyllotaxis has long been proposed to self‐organize from the combined action of growth and of inhibitory fields blocking organogenesis in the vicinity of existing organs in the meristem. In this review, we will highlight how a combination of mathematical/computational modeling and experimental biology has demonstrated that the spatiotemporal distribution of the plant hormone auxin controls both organogenesis and the establishment of inhibitory fields. We will discuss recent advances showing that auxin likely acts through a combination of biochemical and mechanical regulatory mechanisms that control not only the pattern of organogenesis in the meristem but also postmeristematic growth, to shape the shoot. WIREs Dev Biol 2016, 5:460–473. doi: 10.1002/wdev.231 This article is categorized under: Establishment of Spatial and Temporal Patterns > Repeating Patterns and Lateral Inhibition Gene Expression and Transcriptional Hierarchies > Quantitative Methods and Models Plant Development > Inflorescence, Flower, and Fruit Development
Meristem organization and phyllotaxis. (a) Meristem functional organization. The meristem is composed of three distinct functional zones: the central zone (CZ) that contains the stem cells, the surrounding peripheral zone (PZ) from which the primordia (P) arise, and the rib zone (RZ) where is found the organizing center establishing the stem cell niche. (b) Common patterns of phyllotaxis. From left to right: whorled (with several organs at each node), opposite‐decussate (with successive pairs of opposite organs at 90°), distichous with a divergence angle of 180° between successive organs, and Fibonacci spiral (with a divergence angle of 137.5° between successive organs). (c) Top view of the inflorescence of Arabidopsis thaliana showing how primordia follow a Fibonacci spiral. (d) Contact parastichies: connecting each organ to its closest neighbors creates clockwise and anticlockwise spirals called contact parastichies. On this example, 13 clockwise contact parastichies (several of them are highlighted in green) and 21 anticlockwise contact parastichies (several of them are highlighted in blue) can be found. Thirteen and 21 are two consecutive numbers of the Fibonacci series. This image was modified from https://www.mathsisfun.com/numbers/nature‐golden‐ratio‐fibonacci.html.
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Permutations in spiral phyllotaxis. As discussed in the main text, two organs that are initiated simultaneously at the meristem can lead either to a normal organ distribution or to a permutation of the order of organs along the stem, depending on which organ is positioned above the other after the development of the internode. (a) A canonical sequence of divergence angles along a stem with a spiral phyllotaxis (left) and the same sequence but with a permutation of organs 3 and 4 (right). (b) A single permutation gives rise to a new angle sequence: 2α, 360‐α, 2α (with α = 137.5°).
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Inhibitory fields and phyllotaxis. Existing primordia (numbered from the youngest, P1, to the oldest, P5) generate inhibitory fields that block organ initiation in their vicinity. In this example (a spiral phyllotaxis), growth moves the existing organs away from the tip of the meristem, thus lowering the inhibition and allowing for the next initiation to occur (i1). This process repeats itself as the plant grows.
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Establishment of Spatial and Temporal Patterns > Repeating Patterns and Lateral Inhibition
Plant Development > Inflorescence, Flower, and Fruit Development
Gene Expression and Transcriptional Hierarchies > Quantitative Methods and Models