The Role of the Primary Cell Wall in Plant Morphogenesis.

Derek Lamport,Li Tan,Marcia Kieliszewski,Michael Held

doi:10.3390/ijms19092674

Abstract

Morphogenesis remains a riddle, wrapped in a mystery, inside an enigma. It remains a formidable problem viewed from many different perspectives of morphology, genetics, and computational modelling. We propose a biochemical reductionist approach that shows how both internal and external physical forces contribute to plant morphogenesis via mechanical stress–strain transduction from the primary cell wall tethered to the plasma membrane by a specific arabinogalactan protein (AGP). The resulting stress vector, with direction defined by Hechtian adhesion sites, has a magnitude of a few piconewtons amplified by a hypothetical Hechtian growth oscillator. This paradigm shift involves stress-activated plasma membrane Ca2+ channels and auxin-activated H+-ATPase. The proton pump dissociates periplasmic AGP-glycomodules that bind Ca2+. Thus, as the immediate source of cytosolic Ca2+, an AGP-Ca2+ capacitor directs the vectorial exocytosis of cell wall precursors and auxin efflux (PIN) proteins. In toto, these components comprise the Hechtian oscillator and also the gravisensor. Thus, interdependent auxin and Ca2+ morphogen gradients account for the predominance of AGPs. The size and location of a cell surface AGP-Ca2+ capacitor is essential to differentiation and explains AGP correlation with all stages of morphogenetic patterning from embryogenesis to root and shoot. Finally, the evolutionary origins of the Hechtian oscillator in the unicellular Chlorophycean algae reflect the ubiquitous role of chemiosmotic proton pumps that preceded DNA at the dawn of life.

Highlights

“If questions are to be asked about life processes, how can one fail to enquire into what is perhaps the most striking feature of life, morphogenesis? Morphogenesis is the end product of cell differentiation
We propose a biochemical reductionist approach that shows how both internal and external physical forces contribute to plant morphogenesis via mechanical stress–strain transduction from the primary cell wall tethered to the plasma membrane by a specific arabinogalactan protein (AGP)
Turing invoked Graham’s law of diffusion to infer the existence of morphogen gradients and the drift to equilibria analogous to an electronic oscillator, an idea that we recently developed as the Hechtian growth oscillator [6]

Summary

Introduction

“If questions are to be asked about life processes, how can one fail to enquire into what is perhaps the most striking feature of life, morphogenesis? Morphogenesis is the end product of cell differentiation. The role of AGPs emerged as an essential component of the Hechtian oscillator when we correlated tip-focussed cytosolic Ca2+ and tip-localised AGPs with Hechtian adhesion and rapid tip growth of pollen tubes [6] We extrapolate these recent results to morphogenesis and propose two new avenues: Firstly, we propose the avenue of cell walls and mechanoperception involving Hechtian transduction as described in detail here but not considered by Turing; secondly, we propose postulated chemical morphogen gradients [2] identified here as auxin and Ca2+. Computer-generated models, generally favour a genetic perspective with an emphasis on signalling cascades They ignore two “unknown unknown” missing pieces of the morphogenetic puzzle, identified here as Hechtian mechanotransduction and the AGP-Ca2+ capacitor

Cell Wall Mechanotransduction

Embryogenesis

The Evolution of Morphogenesis