Tissue-wide integration of mechanical cues promotes effective auxin patterning

João R D Ramos,Karen Alim,Alexis Maizel

doi:10.1140/epjp/s13360-021-01204-6

Abstract

New plant organs form by local accumulation of auxin, which is transported by PIN proteins that localize following mechanical stresses. As auxin itself modifies tissue mechanics, a feedback loop between tissue mechanics and auxin patterning unfolds—yet the impact of tissue-wide mechanical coupling on auxin pattern emergence remains unclear. Here, we use a model composed of a vertex model for plant tissue mechanics and a compartment model for auxin transport to explore the collective mechanical response of the tissue to auxin patterns and how it feeds back onto auxin transport. We compare a model accounting for a tissue-wide mechanical integration to a model that regards cells as mechanically isolated. We show that tissue-wide mechanical coupling not only leads to more focused auxin spots via stress redistribution, but that it also mitigates the disruption to patterning when considering noise in the mechanical properties of each cell of the tissue. We find that this mechanism predicts that a local turgor increase correlates with auxin concentration, and yet auxin spots can exist regardless of the exact local turgor distribution.

Highlights

Formation of organs entails an effective coordination of local cell growth typically initiated by patterns of one or more morphogenic factors
Plants organ formation is interesting from a physical perspective due to the strong mechanical coupling between plant cells, and the fact that growth is driven by changes in the mechanical properties of the cell wall and internal pressure [1,2,3,4,5]
2 Methods In order to investigate the interaction between auxin cell wall softening and collective tissue mechanics, we use a vertex model to describe the mechanical behaviour of the tissue and a compartment model to express auxin concentration and transport between adjacent cells

Summary

Introduction

Formation of organs entails an effective coordination of local cell growth typically initiated by patterns of one or more morphogenic factors. Understanding how these patterns of morphogenic agents robustly emerge is fundamental for predicting organ morphogenesis. Evidence indicates that the morphogenic factors such as the plant hormone auxin change the mechanics of the tissue [6,7], with implications for the shaping of organs [8,9]. The phytohormone auxin, Indole-3-Acetic Acid, is the key morphogenic agent in plants.

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Conclusion