Targeted migration of pherophorin-S indicates extensive extracellular matrix dynamics in Volvox carteri.

Benjamin Von Der Heyde,Armin Hallmann

doi:10.1111/tpj.14901

Abstract

Hydroxyproline-rich glycoproteins (HRGPs) constitute a major group of proteins of the extracellular matrix (ECM). The multicellular green alga Volvox carteri is a suitable model organism in which to study the evolutionary transition to multicellularity, including the basic principles and characteristics of an ECM. In Volvox, the ECM is dominated by a single HRGP family: the pherophorins. Our inventory amounts to 117 pherophorin-related genes in V.carteri. We focused on a pherophorin with an unexpected characteristic: pherophorin-S is a soluble, non-cross-linked ECM protein. Using transformants expressing a YFP-tagged pherophorin-S we observed the synthesis and secretion of pherophorin-S by somatic cells in vivo, and we then traced the protein during its conspicuous migration to the ECM around prehatching juveniles and its localized concentration there. Our results provide insights into how an ECM zone surrounding the progeny is remotely affected by distantly located parental somatic cells. In view of the properties and migration of pherophorin-S, we conclude that pherophorin-S is likely to act as an ECM plasticizer to allow for dynamic ECM remodeling.

Highlights

One of the most important innovations in the history of life has been the evolutionary transition from unicellular to multicellular species, with the division of labor between germline and somatic cells
A recent search for genes that are computationally annotated as pherophorins in the V. carteri genome (v2.1) of Phytozome 12 (Goodstein et al, 2012), resulted in 97 pherophorin genes
Our detailed BLAST searches (Altschul et al, 1990; Johnson et al, 2008; Boratyn et al, 2013) of the V. carteri genome (v2.1) in Phytozome 12 using pherophorins as query sequences revealed a total of 117 pherophorin genes

Summary

Introduction

One of the most important innovations in the history of life has been the evolutionary transition from unicellular to multicellular species, with the division of labor between germline and somatic cells To investigate this evolutionary transition, the spheroidal green alga Volvox carteri and its close relatives have long been seen as suitable model organisms. The surprisingly elaborated ECM of V. carteri consists of many region-specific and anatomically distinct structures arranged in a defined spatial pattern (Kirk et al, 1986; Hallmann, 2003) (Figure 1) These ECM structures are supposed to be modified under physiological, metabolic or developmental control. The cell walls or ECMs of both unicellular volvocine algae, like Chlamydomonas, and multicellular volvocine algae, like Volvox, are known to be assembled mainly from hydroxyproline-rich glycoproteins (HRGPs), which dominate the ECM composition of green algae and represent a main constituent of the ECMs of embryophytic land plants (Miller et al, 1972; Sommer-Knudsen et al, 1998; Sumper and Hallmann, 1998; Hallmann, 2003; Showalter and Basu, 2016)

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