Molecular convergence by differential domain acquisition is a hallmark of chromosomal passenger complex evolution

Abstract

The chromosomal passenger complex (CPC) is a heterotetrameric regulator of eukaryotic cell26 division, consisting of an Aurora-type kinase and a scaffold built of INCENP, Borealin and Survivin.27 While most CPC components are conserved across eukaryotes, orthologs of the chromatin reader28 Survivin have previously only been found in animals and fungi, raising the question of how its essential29 role is carried out in other eukaryotes. By characterizing proteins that bind to the Arabidopsis Borealin30 ortholog, we identified BOREALIN RELATED INTERACTOR 1 and 2 (BORI1 and BORI2) as31 redundant Survivin-like proteins in the context of the CPC in plants. Loss of BORI function is lethal32 and a reduced expression of BORIs causes severe developmental defects. Similar to Survivin, we33 find that the BORIs bind to phosphorylated histone H3, relevant for correct CPC association with34 chromatin. However, this interaction is not mediated by a BIR domain as in previously recognized35 Survivin orthologs, but by an FHA domain, a widely conserved phosphate-binding module. We36 propose that the unifying criterion of Survivin-type proteins is a helix that facilitates complex formation37 with the other two scaffold components, and that the addition of a phosphate-binding domain,38 necessary for concentration at the inner centromere, evolved in parallel in different eukaryotic groups.39 Using sensitive similarity searches, we indeed find conservation of this helical domain between40 animals and plants, and identify the missing CPC component in most eukaryotic supergroups.41 Interestingly, we also detect Survivin orthologs without a defined phosphate-binding domain, possibly42 reflecting the situation in the last eukaryotic common ancestor