Mathematical model studies of the comprehensive generation of major and minor phyllotactic patterns in plants with a predominant focus on orixate phyllotaxis

PLoS Comput Biol. 2019 Jun 6;15(6):e1007044. doi: 10.1371/journal.pcbi.1007044. eCollection 2019 Jun.

Abstract

Plant leaves are arranged around the stem in a beautiful geometry that is called phyllotaxis. In the majority of plants, phyllotaxis exhibits a distichous, Fibonacci spiral, decussate, or tricussate pattern. To explain the regularity and limited variety of phyllotactic patterns, many theoretical models have been proposed, mostly based on the notion that a repulsive interaction between leaf primordia determines the position of primordium initiation. Among them, particularly notable are the two models of Douady and Couder (alternate-specific form, DC1; more generalized form, DC2), the key assumptions of which are that each leaf primordium emits a constant power that inhibits new primordium formation and that this inhibitory effect decreases with distance. It was previously demonstrated by computer simulations that any major type of phyllotaxis can occur as a self-organizing stable pattern in the framework of DC models. However, several phyllotactic types remain unaddressed. An interesting example is orixate phyllotaxis, which has a tetrastichous alternate pattern with periodic repetition of a sequence of different divergence angles: 180°, 90°, -180°, and -90°. Although the term orixate phyllotaxis was derived from Orixa japonica, this type is observed in several distant taxa, suggesting that it may reflect some aspects of a common mechanism of phyllotactic patterning. Here we examined DC models regarding the ability to produce orixate phyllotaxis and found that model expansion via the introduction of primordial age-dependent changes of the inhibitory power is absolutely necessary for the establishment of orixate phyllotaxis. The orixate patterns generated by the expanded version of DC2 (EDC2) were shown to share morphological details with real orixate phyllotaxis. Furthermore, the simulation results obtained using EDC2 fitted better the natural distribution of phyllotactic patterns than did those obtained using the previous models. Our findings imply that changing the inhibitory power is generally an important component of the phyllotactic patterning mechanism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Computational Biology
  • Computer Simulation*
  • Models, Biological*
  • Plant Development / physiology
  • Plant Leaves* / anatomy & histology
  • Plant Leaves* / growth & development
  • Plant Stems* / anatomy & histology
  • Plant Stems* / growth & development
  • Rutaceae* / anatomy & histology
  • Rutaceae* / growth & development

Grants and funding

This work was supported in part by a Research Fellowship for Young Scientists (No. 18J12309 to TY) and by a Grant-in-Aid for Scientific Research on Innovative Areas (No. 16H01248 to HF) from the Japan Society for the Promotion of Science. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.