Evolution of an ancient protein function involved in organized multicellularity in animals.

Douglas P Anderson,William Campodonico-Burnett,Arielle Woznica,Kenneth E Prehoda,Nicole King,Victor Hanson-Smith,Joseph W Thornton,Dustin S Whitney,Brian F Volkman

doi:10.7554/elife.10147

Douglas P Anderson, William Campodonico-Burnett + Show 7 more

Open Access

https://doi.org/10.7554/elife.10147

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Abstract

To form and maintain organized tissues, multicellular organisms orient their mitotic spindles relative to neighboring cells. A molecular complex scaffolded by the GK protein-interaction domain (GKPID) mediates spindle orientation in diverse animal taxa by linking microtubule motor proteins to a marker protein on the cell cortex localized by external cues. Here we illuminate how this complex evolved and commandeered control of spindle orientation from a more ancient mechanism. The complex was assembled through a series of molecular exploitation events, one of which - the evolution of GKPID's capacity to bind the cortical marker protein - can be recapitulated by reintroducing a single historical substitution into the reconstructed ancestral GKPID. This change revealed and repurposed an ancient molecular surface that previously had a radically different function. We show how the physical simplicity of this binding interface enabled the evolution of a new protein function now essential to the biological complexity of many animals.

Highlights

The evolution of organized multicellularity is one of the most important and least understood transitions in the history of life (Grosberg and Strathmann, 2007; Maynard Smith and Szathmary, 1995; Bonner, 1998; King, 2004)
GK proteininteraction domain (GKPID) are present in all animal genomes analyzed as well as in their closest unicellular relatives, the choanoflagellates and Filasterea; GKPIDs are absent from the genomes of all sequenced fungi and all other eukaryotic and prokaryotic lineages analyzed
Within the GKPIDs, there are two major clades, one of which contains Discs large (Dlg) and closely related paralogs; the other contains other family members, which are involved in cell adhesion and numerous other processes

Summary

Introduction

The evolution of organized multicellularity is one of the most important and least understood transitions in the history of life (Grosberg and Strathmann, 2007; Maynard Smith and Szathmary, 1995; Bonner, 1998; King, 2004). We reconstructed Anc-GK2PID – the more recent progenitor of all Dlg proteins in the ancestral animal – and found that it too orients the mitotic spindle and binds Pins with even higher affinity, suggesting a subsequent fine-tuning of Pins-binding capacity (Figure 2—figure supplement 1).

Results

Conclusion