Spatiotemporal distribution of the glycoprotein pherophorin II reveals stochastic geometry of the growing ECM of $Volvox~carteri$

TL;DR

This study investigates the spatial organization of the ECM in Volvox carteri by tracking pherophorin II distribution, revealing stochastic geometric patterns that evolve during development, akin to foam structures, and providing insights into extracellular matrix formation.

Contribution

It introduces a novel quantitative analysis of ECM geometry in Volvox carteri, linking molecular localization to stochastic spatial patterns during development.

Findings

ECM compartments exhibit gamma-distributed areas and aspect ratios.

A transition from polygonal to looser packing geometry occurs over time.

Stable eccentricity suggests robust geometric regulation during ECM growth.

Abstract

The evolution of multicellularity involved the transformation of a simple cell wall of unicellular ancestors into a complex, multifunctional extracellular matrix (ECM). A suitable model organism to study the formation and expansion of an ECM during ontogenesis is the multicellular green alga $Volvox~carteri$, which, along with the related volvocine algae, produces a complex, self-organized ECM composed of multiple substructures. These self-assembled ECMs primarily consist of hydroxyproline-rich glycoproteins, a major component of which is pherophorins. To investigate the geometry of the growing ECM, we fused the $yfp$ gene with the gene for pherophorin II (PhII) in $V.~carteri$. Confocal microscopy reveals PhII:YFP localization at key structures within the ECM, including the boundaries of compartments surrounding each somatic cell and the outer surface of the organism. Image analysis during the life cycle allows the stochastic geometry of those growing compartments to be quantified. We find that their areas and aspect ratios exhibit robust gamma distributions and exhibit a transition from a tight polygonal to a looser acircular packing geometry with stable eccentricity over time, evoking parallels and distinctions with the behavior of hydrated foams. These results provide a quantitative benchmark for addressing a general, open question in biology: How do cells produce structures external to themselves in a robust and accurate manner?