Ubiquity and Origins of Structural Maintenance of Chromosomes (SMC) Proteins in Eukaryotes

Anderson DE, Losada A, Erickson HP, Hirano T. 2002. Condensin and

cohesin display different arm conformations with characteristic hinge

angles. J Cell Biol. 156(3):419–424.

Andrews EA, et al. 2005. Nse2, a component of the Smc5-6 complex, Is a

SUMO ligase required for the response to DNA damage. Mol Cell Biol.

25(1):185–196.

n L. 2018. The Smc5/6 complex: new and old functions

Arago

of the enigmatic long-distance relative. Annu Rev Genet.

52(1):89–107.

Bergsten J. 2005. A review of long-branch attraction. Hoboken (NJ): Wiley

Online Library.

Birkenbihl RP, Subramani S. 1995. The rad21 gene product of

Schizosaccharomyces pombe is a nuclear, cell cycle-regulated phosphoprotein. J Biol Chem. 270(13):7703–7711.

Britton RA, Lin DC, Grossman AD. 1998. Characterization of a prokaryotic

SMC protein involved in chromosome partitioning. Genes Dev.

12(9):1254–1259.

Camacho C, et al. 2009. BLASTþ: architecture and applications. BMC

Bioinform. 10(1):421.

Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. 2009. trimAl: a tool for

automated alignment trimming in large-scale phylogenetic analyses.

Bioinformatics 25(15):1972–1973.

Carramolino L, et al. 1997. SA-1, a nuclear protein encoded by one member of a novel gene family: molecular cloning and detection in hemopoietic organs. Gene 195(2):151–159.

Chen S, Zhou Y, Chen Y, Gu J. 2018. fastp: an ultra-fast all-in-one FASTQ

preprocessor. Bioinformatics 34(17):i884–i890.

16

Cobbe N, Heck MM. 2000. Review: SMCs in the world of chromosome

biology— from prokaryotes to higher eukaryotes. J Struct Biol. 129(2–

3):123–143.

Cobbe N, Heck MM. 2004. The evolution of SMC proteins: phylogenetic

analysis and structural implications. Mol Biol Evol. 21(2):332–347.

Diaz M, Pecinka A. 2018. Scaffolding for repair: understanding molecular

functions of the SMC5/6 complex. Genes 9(1):36.

Fousteri MI, Lehmann AR. 2000. A novel SMC protein complex in

Schizosaccharomyces pombe contains the Rad18 DNA repair protein.

EMBO J. 19(7):1691–1702.

Fu L, Niu B, Zhu Z, Wu S, Li W. 2012. CD-HIT: accelerated for clustering the

next-generation sequencing data. Bioinformatics 28(23):3150–3152.

Fujioka Y, Kimata Y, Nomaguchi K, Watanabe K, Kohno K. 2002.

Identification of a novel non-structural maintenance of chromosomes

(SMC) component of the SMC5-SMC6 complex involved in DNA repair. J Biol Chem. 277(24):21585–21591.

Funayama T, et al. 1999. Identification and disruption analysis of the recN

gene in the extremely radioresistant bacterium Deinococcus radiodurans. Mutat Res. 435(2):151–161.

Gao F, et al. 2016. The All-data-based evolutionary hypothesis of ciliated

protists with a revised classification of the phylum Ciliophora

(Eukaryota, Alveolata). Sci Rep. 6(1):24874.

Gluenz E, Sharma R, Carrington M, Gull K. 2008. Functional characterization of cohesin subunit SCC1 in Trypanosoma brucei and dissection

of mutant phenotypes in two life cycle stages. Mol Microbiol.

69(3):666–680.

Grabherr MG, et al. 2011. Full-length transcriptome assembly from RNASeq data without a reference genome. Nat Biotechnol.

29(7):644–652.

Haering CH, Farcas A, Arumugam P, Metson J, Nasmyth K. 2008. The

cohesin ring concatenates sister DNA molecules. Nature

454(7202):297–301.

Hirano T, Mitchison TJ. 1994. A heterodimeric coiled-coil protein required

for mitotic chromosome condensation in vitro. Cell 79(3):449–458.

Hirano T, Kobayashi R, Hirano M. 1997. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a

Xenopus homolog of the Drosophila barren protein. Cell

89(4):511–521.

Hu B, et al. 2005. Qri2/Nse4, a component of the essential Smc5/6 DNA

repair complex. Mol Microbiol. 55(6):1735–1750.

Ishiguro K. 2019. The cohesin complex in mammalian meiosis. Genes Cells

24(1):6–30.

Janouskovec J, et al. 2019. Apicomplexan-like parasites are polyphyletic

and widely but selectively dependent on cryptic plastid organelles.

eLife 8:e49662.

Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol

Evol. 30(4):772–780.

Lartillot N, Lepage T, Blanquart S. 2009. PhyloBayes 3: a Bayesian software

package for phylogenetic reconstruction and molecular dating.

Bioinformatics 25(17):2286–2288.

Lax G, et al. 2018. Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes. Nature 564(7736):410–414.

Lehmann AR, et al. 1995. The rad18 gene of Schizosaccharomyces pombe

defines a new subgroup of the SMC superfamily involved in DNA

repair. Mol Cell Biol. 15(12):7067–7080.

Losada A, Hirano M, Hirano T. 1998. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev.

12(13):1986–1997.

Lo¨we J, Cordell SC, van den Ent F. 2001. Crystal structure of the SMC head

domain: an ABC ATPase with 900 residues antiparallel coiled-coil. J

Mol Biol. 306(1):25–35.

Melby TE, Ciampaglio CN, Briscoe G, Erickson HP. 1998. The symmetrical

structure of structural maintenance of chromosomes (SMC) and MukB

Genome Biol. Evol. 13(12) https://doi.org/10.1093/gbe/evab256 Advance Access publication 19 November 2021

Downloaded from https://academic.oup.com/gbe/article/13/12/evab256/6432042 by UNIV OF TSUKUBA user on 13 December 2021

We aligned 126 amino acid sequences belonging to the

kleisin superfamily (i.e., 39 Rad21/Scc1, 33 CAP-H, 26 Nse4,

12 archaeal ScpA, and 16 bacterial ScpA sequences) as described above. After the exclusion of ambiguously aligned

positions (see above), the alignment was subjected to the

ML analysis with the LG þ C þ I model. UFBP support values

were calculated from 1,000 replicates.

GBE

Evolutoin of SMC Proteins in Eukaryotes

Shimodaira H. 2002. An approximately unbiased test of phylogenetic tree

selection. Syst Biol. 51(3):492–508.

Soppa J. 2001. Prokaryotic structural maintenance of chromosomes (SMC)

proteins: distribution, phylogeny, and comparison with MukBs and

additional prokaryotic and eukaryotic coiled-coil proteins. Gene

278(1–2):253–264.

Susko E, Roger AJ. 2007. On reduced amino acid alphabets for phylogenetic inference. Mol Biol Evol. 24(9):2139–2150.

Sutani T, Yanagida M. 1997. DNA renaturation activity of the SMC complex

implicated

in

chromosome

condensation.

Nature

388(6644):798–801.

Takemata N, Samson RY, Bell SD. 2019. Physical and functional compartmentalization of archaeal chromosomes. Cell 179(1):165–179.

 th A, et al. 1999. Yeast cohesin complex requires a conserved protein,

To

Eco1p(Ctf7), to establish cohesion between sister chromatids during

DNA replication. Genes Dev. 13(3):320–333.

}si GJ, Embley TM. 2020.

Williams TA, Cox CJ, Foster PG, Szo¨llo

Phylogenomics provides robust support for a two-domains tree of

life. Nat Ecol Evol. 4(1):138–147.

Yazaki E, et al. 2017. Global Kinetoplastea phylogeny inferred from a

large-scale multigene alignment including parasitic species for better

understanding transitions from a free-living to a parasitic lifestyle.

Genes Genet Syst. 92(1):35–42.

Zaremba-Niedzwiedzka K, et al. 2017. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541(7637):353–358.

Associate editor: Sandra Baldauf

Genome Biol. Evol. 13(12) https://doi.org/10.1093/gbe/evab256 Advance Access publication 19 November 2021

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Downloaded from https://academic.oup.com/gbe/article/13/12/evab256/6432042 by UNIV OF TSUKUBA user on 13 December 2021

proteins: long, antiparallel coiled coils, folded at a flexible hinge. J Cell

Biol. 142(6):1595–1604.

Nguyen L, Schmidt HA, von Haeseler A, Minh BQ. 2015. IQ-TREE: a fast

and effective stochastic algorithm for estimating maximum-likelihood

phylogenies. Mol Biol Evol. 32(1):268–274.

Niki H, Jaffe A, Imamura R, Ogura T, Hiraga S. 1991. The new gene mukB

codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J. 10(1):183–193.

Palecek JJ, Gruber S. 2015. Kite proteins: a superfamily of SMC/Kleisin

partners conserved across Bacteria, Archaea, and Eukaryotes.

Structure 23(12):2183–2190.

Palou R, et al. 2018. Condensin ATPase motifs contribute differentially to

the maintenance of chromosome morphology and genome stability.

PLoS Biol. 16(6):e2003980.

Pebernard S, McDonald WH, Pavlova Y, Yates JR, Boddy MN. 2004. Nse1,

Nse2, and a novel subunit of the Smc5-Smc6 complex, Nse3, play a

crucial role in meiosis. MBoC 15(11):4866–4876.

Pebernard S, Wohlschlegel J, McDonald WH, Yates JR, Boddy MN. 2006.

The Nse5-Nse6 dimer mediates DNA repair roles of the Smc5-Smc6

complex. Mol Cell Biol. 26(5):1617–1630.

Sarai C, et al. 2020. Dinoflagellates with relic endosymbiont nuclei as

models for elucidating organellogenesis. Proc Natl Acad Sci USA.

117(10):5364–5375.

Sayers EW, et al. 2020. Database resources of the national center for

biotechnology information. Nucleic Acids Res. 48(D1):D9–D16.

Schleiffer A, et al. 2003. Kleisins: a superfamily of bacterial and eukaryotic

SMC protein partners. Mol Cell. 11(3):571–575.

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