A Dynamical Phyllotaxis Model to Determine Floral Organ Number

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.

Author Summary

Why do most eudicot flowers have either four or five petals? This fundamental and attractive problem in botany has been little investigated. Here, we identify the properties responsible for organ-number determination in floral development using mathematical modeling. Earlier experimental and theoretical studies showed that the arrangements of 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. In computer simulations incorporating such initiation inhibition and mutual repulsion, the floral organs spontaneously formed several circles, consistent with the concentric circular arrangement of sepals and petals in eudicot flowers. 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.

Contributors

Stéphane Douady: Role: Editor

Journal

Journal ID (nlm-ta): PLoS Comput Biol

Journal ID (iso-abbrev): PLoS Comput. Biol

Journal ID (publisher-id): plos

Journal ID (pmc): ploscomp

Title: PLoS Computational Biology

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Print): 1553-734X

ISSN (Electronic): 1553-7358

Publication date Collection: May 2015

Publication date (Electronic): 7 May 2015

Volume: 11

Issue: 5

Affiliations

[1 ]Department of Biological Sciences, Osaka University, Toyonaka, Osaka, Japan

[2 ]Japan Society for the Promotion of Science, Tokyo, Japan

University Paris Diderot, FRANCE

Author notes

The authors have declared that no competing interests exist.

Conceived and designed the experiments: MSK KF. Performed the experiments: MSK. Analyzed the data: MSK. Contributed reagents/materials/analysis tools: MSK. Wrote the paper: MSK KF.

[¤]

Current address: Center for Education in Liberal Arts and Sciences, Osaka University, Toyonaka, Osaka, Japan

* E-mail: kitazawa@ 123456bio.sci.osaka-u.ac.jp (MSK); fujimoto@ 123456bio.sci.osaka-u.ac.jp (KF)

Article

Publisher ID: PCOMPBIOL-D-14-01151

DOI: 10.1371/journal.pcbi.1004145

PMC ID: 4423988

PubMed ID: 25950739

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

Page count

Figures: 7, Tables: 0, Pages: 27

Product

Funding

MSK is a JSPS Research Fellow (24.1243). KF is supported by the Osaka University Life Science Young Independent Researcher Support Program through the Special Coordination Program to Disseminate Tenure Tracking System, and Grant-in-Aid for Scientific Research on Innovative Areas (26113511), MEXT. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Categories

Subject: Research Article

Custom metadata

Data Availability All relevant data are within the paper and its Supporting Information files.