The Role of the Primary Cell Wall in Plant Morphogenesis

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.

The Cell Wall PAC (Proline-Rich, Arabinogalactan Proteins, Conserved Cysteines) Domain-Proteins Are Conserved in the Green Lineage

“…Altogether, the sequence showing the highest level of identity to bona fide PAC domains was found in C. orbicularis. This is consistent with the assumption that the Coleochaetales could be one of the ancestors of the green lineage [29].…”

Phyllotaxis Turns Over a New Leaf—A New Hypothesis

“…However, in plasmolyzed pollen tubes [7] and root hair tips [29] ( Figure 2), a high density of Hechtian strands correlates rapid tip growth with Hechtian adhesion arguably mediated by AGP57C [25]. This suggests its essential role in transduction of the wall stress vector that initiates oscillations and cytosolic Ca 2+ waves as hypothesized by the Hechtian Oscillator ( Figure 1 [2]. This figure shows stills from the animation in Supplemental Data.…”

“…The Hechtian Oscillator exemplifies the pollen tube paradigm of rapid tip growth in particular [2,7]. The rapidly growing cell wall transmits its stress-strain status via Hechtian adhesion to the plasma membrane.…”

Plant Cell Wall Proteins and Development

“…Eight experimental articles, nine up-to-date review articles, as well as a concept article, have been published. We wish to thank all the authors for their great contribution to this unique collection of articles as well as the International Journal of Molecular Science supporting team.The content of this Special Issue embraces several topics, all of them stressing the roles of cell wall proteins: cell wall proteomics studies on monocot species [7,12]; the role of cell wall proteins during plant development [13][14][15] or in response to environmental stresses [16][17][18][19]; overviews on several cell wall protein families either from green microalgae [20] or from plants, i.e., fasciclin arabinogalactan proteins (FLAs) [21,22], membrane-bound class III peroxidases (Class III Prxs) [23], pectin methylesterases inhibitors [24], DUF642 (Domain of Unknown Function 642) proteins [25], and Proline-rich, Arabinogalactan proteins, conserved Cysteines (PAC) domain-proteins [26]; and the role of fasciclin arabinogalactan proteins (FLAs) in Ca 2+ signaling during plant morphogenesis [27,28].For two decades, cell wall proteomics has become a powerful experimental approach and has revealed the diversity of the cell wall protein families. Arabidopsis thaliana has been the most studied plant species, and almost half of its expected cell wall proteome has been described so far (see WallProtDB, http://www.polebio.lrsv.ups-tlse.fr/WallProtDB/).…”

“…This Special issue was also open to new concepts. Two articles by Lamport et al [27,28] propose new roles for the arabinogalactan protein (AGP) family in root and shoot morphogenesis, as well as in phyllotaxis patterning. Such molecules are actually proteoglycans with a proportion of glycans of up to 90% [39], which are assumed to play roles in signaling.…”