Diverse evolutionary paths to cell adhesion

Abstract

The morphological and physiological diversity of animals, fungi, plants, and other multicellular organisms stems from the fact that each lineage acquired multicellularity independently during the course of evolution. A prerequisite for the origin of multicellularity in each lineage was the evolution of mechanisms for stable cell-cell adhesion or attachment. Recent advances in genomics and phylogenetics allow comparative studies that provide critical insights into the evolutionary foundations of cell adhesion. Reconstructing the evolution of cell junction proteins in animals and their unicellular relatives exemplifies the roles of co-option and innovation during evolutionary transitions to multicellularity. Comparative studies of volvocine algae reveal specific molecular changes that accompanied the evolution of multicellularity in Volvox. Finally, comparisons between animals and Dictyostelium indicate the extent to which commonalities and differences in the biology of their unicellular ancestors influenced the evolution of adhesive mechanisms in each lineage. Understanding the unicellular ancestry of cell adhesion helps illuminate the basic cell biology of multicellular development in modern organisms.

Multicellularity arose several times in the evolution of eukaryotes (Response to DOI 10.1002/bies.201100187)

“…cell adhesion, communication, and differentiation) found across taxa demonstrate that there are many routes to its evolution [10]. The frequent occurrence of multicellularity is likely due to strong selective pressures favoring multicellularity, few genetic changes necessary to enable the switch, or a combination of these factors [13].…”

“…Despite deep evolutionary divergence [8], many genes crucial to these processes in animals are found in Dictyostelium [9]. The shared processes related to multicellularity have been shown to be similar in structure, function, and underlying molecular machinery [3,4,10,11]. These parallels are surprising because Dictyostelium multicellularity occurs by aggregation of solitary amoebae during one stage of the life cycle, which is fundamentally different from repeated division of a zygote that leads to multicellularity in animals.…”

“…the common ancestor of both organismal groups already possessed many of these characteristics; or convergence, meaning that the two groups arrived at similar methods for evolving multicellularity independently. Multicellularity in different clades is commonly attributed to convergent evolution across eukaryotes [10,12,13]. Convergence is also presumed between animals and Dictyostelium [9].…”

“…In both taxa the multicellular organism is composed of motile cells that must communicate and adhere to one another. In contrast, multicellular plants and algae contain rigid, non-motile cells [10,13]. Based on the striking similarities between metazoan and dictyostelid cell adhesion, Dickinson and colleagues hypothesize that homology is a more likely explanation and that the last common ancestor of dictyostelids and animals was multicellular [7].…”

The cell adhesion molecule DdCAD-1 regulates morphogenesis through differential spatiotemporal expression inDictyostelium discoideum

“…Therefore, individual cells or groups of cells must continuously change their relative positions and mutual adhesiveness during morphogenesis. It has been proposed that proteins involved in cell adhesion, cell-cell signaling and cell differentiation are genetic tool kits for multicellularity (Vogel and Chothia, 2006;King et al, 2007;Abedin and King, 2010).…”