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

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.