Localized growth drives spongy mesophyll morphogenesis

TL;DR

This study presents a mechanical model explaining how the spongy mesophyll tissue in plant leaves develops its porous structure through localized cell growth and adhesion, maintaining stability and porosity.

Contribution

It introduces a purely mechanical simulation model that reproduces the development of spongy mesophyll microstructure, highlighting physical principles in tissue morphogenesis.

Findings

Model accurately recapitulates leaf tissue microstructure development

Porosity depends on balance of cell growth, adhesion, and stiffness

Mechanical stability is maintained during pore formation

Abstract

The spongy mesophyll is a complex, porous tissue found in plant leaves that enables carbon capture and provides mechanical stability. Unlike many other biological tissues, which remain confluent throughout development, the spongy mesophyll must develop from an initially confluent tissue into a tortuous network of cells with a large proportion of intercellular airspace. How the airspace in the spongy mesophyll develops while the cells remain mechanically stable remains unknown. Here, we used computer simulations of deformable particles to develop a purely mechanical model for the development of the spongy mesophyll tissue. By stipulating that (1) cell perimeter grows only near voids, (2) cells both form and break adhesive bonds, and (3) the tissue pressure remains constant, the computational model was able to recapitulate the developmental trajectory of the microstructure of the spongy mesophyll observed in Arabidopsis thaliana leaves. Robust generation of pore space in the spongy mesophyll requires a balance of cell growth, adhesion, stiffness and tissue pressure to ensure cell networks remain both porous yet mechanically robust. The success of this mechanical model of tissue growth and porosity evolution suggests that simple physical principles can coordinate and drive the development of complex plant tissues like the spongy mesophyll.