Ubiquity and evolution of structural maintenance of chromosomes (SMC) proteins in eukaryotes

Structural maintenance of chromosomes (SMC) protein complexes are common
in Bacteria, Archaea, and Eukaryota. SMC proteins, together with the
proteins related to SMC (SMC-related proteins), constitute a superfamily
of ATPases. Bacteria/Archaea and Eukaryotes are distinctive from one
another in terms of the repertory of SMC proteins. A single type of SMC
protein is dimerized in the bacterial and archaeal complexes, whereas
eukaryotes possess six distinct SMC subfamilies (SMC1-6), constituting
three heterodimeric complexes, namely cohesin, condensin, and SMC5/6
complex. Thus, to bridge the homodimeric SMC complexes in Bacteria and
Archaea to the heterodimeric SMC complexes in Eukaryota, we need to invoke
multiple duplications of an SMC gene followed by functional divergence.
However, to our knowledge, the evolution of the SMC proteins in Eukaryota
had not been examined for more than a decade. In this study, we reexamined
the ubiquity of SMC1-6 in phylogenetically diverse eukaryotes that cover
the major eukaryotic taxonomic groups recognized to date and provide two
novel insights into the SMC evolution in eukaryotes. First, multiple
secondary losses of SMC5 and SMC6 occurred in the eukaryotic evolution.
Second, the SMC proteins constituting cohesin and condensin (i.e.,
SMC1-4), and SMC5 and SMC6 were derived from closely related but distinct
ancestral proteins. Based on the above-mentioned findings, we discuss how
SMC1-6 have diverged from the archaeal homologs.