Phyllotaxis Turns Over a New Leaf-A New Hypothesis.

Derek T A Lamport,Marcia J Kieliszewski,Li Tan,Michael Held

doi:10.3390/ijms21031145

Derek T A Lamport, Marcia J Kieliszewski + Show 2 more

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https://doi.org/10.3390/ijms21031145

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Abstract

Phyllotaxis describes the periodic arrangement of plant organs most conspicuously floral. Oscillators generally underlie periodic phenomena. A hypothetical algorithm generates phyllotaxis regulated by the Hechtian growth oscillator of the stem apical meristem (SAM) protoderm. The oscillator integrates biochemical and mechanical force that regulate morphogenetic gradients of three ionic species, auxin, protons and Ca2+. Hechtian adhesion between cell wall and plasma membrane transduces wall stress that opens Ca2+ channels and reorients auxin efflux “PIN” proteins; they control the auxin-activated proton pump that dissociates Ca2+ bound by periplasmic arabinogalactan proteins (AGP-Ca2+) hence the source of cytosolic Ca2+ waves that activate exocytosis of wall precursors, AGPs and PIN proteins essential for morphogenesis. This novel approach identifies the critical determinants of an algorithm that generates phyllotaxis spiral and Fibonaccian symmetry: these determinants in order of their relative contribution are: (1) size of the apical meristem and the AGP-Ca2+ capacitor; (2) proton pump activity; (3) auxin efflux proteins; (4) Ca2+ channel activity; (5) Hechtian adhesion that mediates the cell wall stress vector. Arguably, AGPs and the AGP-Ca2+ capacitor plays a decisive role in phyllotaxis periodicity and its evolutionary origins.

Highlights

Agnes Arber [1] in “The Natural Philosophy of Plant Form” comprehensively described the development of plant morphology from the ancient philosophers—Plato, Aristotle and Theophrastus—to the more recent Cambridge botanical tradition that extends from William Turner, Nehemiah Grew and “Robin” Hill to the present
Arber [1] presented “The mechanism of plant morphology” and an insightful approach to the pivotal role of the cell wall and the stress–strain of cell expansion that results in “form conditioned by pressure” where “even a minor [cell wall] alteration may be associated with striking changes in the external form.”
Discussion of the Hechtian Oscillator vis-a-vis the role of the primary cell wall in plant morphogenesis [2] suggests extrapolating the oscillator to phyllotaxis based on the premise that presence of the oscillator components implies the presence of a functional Hechtian Oscillator

Summary

Introduction

Agnes Arber [1] in “The Natural Philosophy of Plant Form” comprehensively described the development of plant morphology from the ancient philosophers—Plato, Aristotle and Theophrastus—to the more recent Cambridge botanical tradition that extends from William Turner, Nehemiah Grew and “Robin” Hill to the present. Plant morphogenesis involves periodicity strikingly displayed by the pattern of leaves and floral organs [5] that often appear as Fibonacci spirals typified by whorls of 3, 5, 8, 13, 21 and 34 petals [6] Such periodicity depends on an underlying oscillator such as the recently formulated Hechtian growth oscillator [2,7] that involves auxin-driven Ca2+ release from arabinogalactan proteins (AGPs) of the cell surface; this hypothesis accounts for the origin of oscillations in molecular detail absent from previous models of tip growth [8]. Further transmission of a biochemical signal to the cytoplasm involves stretch-activated proton and Ca2+ ion fluxes of the plasma membrane generated by the Hechtian growth oscillator [7]. Regulation of Ca2+ homeostasis is the major function of the proton pump rather than the regulation of wall pH

Transduction of the Stress Vector through the Protoderm

10. Evolutionary Origin of Angiosperm Phyllotaxis