Abstract

How organisms determine particular organ numbers is a fundamental key to the development of precise body structures; however, the developmental mechanisms underlying organ-number determination are unclear. In many eudicot plants, the primordia of sepals and petals (the floral organs) first arise sequentially at the edge of a circular, undifferentiated region called the floral meristem, and later transition into a concentric arrangement called a whorl, which includes four or five organs. The properties controlling the transition to whorls comprising particular numbers of organs is little explored. We propose a development-based model of floral organ-number determination, improving upon earlier models of plant phyllotaxis that assumed two developmental processes: the sequential initiation of primordia in the least crowded space around the meristem and the constant growth of the tip of the stem. By introducing mutual repulsion among primordia into the growth process, we numerically and analytically show that the whorled arrangement emerges spontaneously from the sequential initiation of primordia. Moreover, by allowing the strength of the inhibition exerted by each primordium to decrease as the primordium ages, we show that pentamerous whorls, in which the angular and radial positions of the primordia are consistent with those observed in sepal and petal primordia in Silene coeli-rosa, Caryophyllaceae, become the dominant arrangement. The organ number within the outmost whorl, corresponding to the sepals, takes a value of four or five in a much wider parameter space than that in which it takes a value of six or seven. These results suggest that mutual repulsion among primordia during growth and a temporal decrease in the strength of the inhibition during initiation are required for the development of the tetramerous and pentamerous whorls common in eudicots.

Highlights

  • How to determine the numbers of body parts is a fundamental problem for the development of complete body structures in multicellular organisms

  • Each circle tended to contain four or five organs arranged in positions that agreed quantitatively with the organ positions in the pentamerous flower, Silene coeli-rosa, Caryophyllaceae. These results suggest that the temporal decay of initiation inhibition and the mutual repulsion among growing organs determine the particular organ number during eudicot floral development

  • Hofmeister described a hypothesis of pattern formation in 1868 [24], which we summarize in three basic rules: the time periodicity of primordia initiation, the initiation of a primordium at the largest available space at the edge of the meristem, and the relative movement of primordia in a centrifugal direction from the apex due to the growth of the stem tip

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Summary

Author Summary

Why do most eudicot flowers have either four or five petals? This fundamental and attractive problem in botany has been little investigated. Model for Floral Organ Numbers preexisting organs determine where a new organ will arise Expanding upon those studies, we integrated two interactions between floral organs: (1) spatially and temporally decreased inhibition of new organ initiation by preexisting organs, and (2) mutual repulsion among organs such that they are “pushed around” during floral development. Each circle tended to contain four or five organs arranged in positions that agreed quantitatively with the organ positions in the pentamerous flower, Silene coeli-rosa, Caryophyllaceae. These results suggest that the temporal decay of initiation inhibition and the mutual repulsion among growing organs determine the particular organ number during eudicot floral development

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