In all organisms, from eukaryotes to prokaryotes, the chromosome is highly compacted and organized. Chromosome condensation is essential in all cells and ranges from 1,000- to more than 10,000-fold between bacterial and eukaryotic cells. Replication and transcription occur in parallel with chromosome segregation in bacteria. Structural maintenance of chromosome proteins play a key role in chromosome compaction and segregation, their coordination with the cell cycle, and in various other chromosome dynamics, including DNA repair. In spite of their essential nature in almost all organisms, their function at a molecular level is only slowly beginning to emerge.

1.
Autret S, Nair R, Errington J: Genetic analysis of the chromosome segregation protein Spo0J of Bacillus subtilis: evidence for separate domains involved in DNA binding and interactions with Soj protein. Mol Microbiol 2001;41:743-755.
[PubMed]
2.
Bartosik AA, Mierzejewska J, Thomas CM, Jagura-Burdzy G: Parb deficiency in Pseudomonas aeruginosa destabilizes the partner protein ParA and affects a variety of physiological parameters. Microbiology (Reading) 2009;155:1080-1092.
[PubMed]
3.
Bazett-Jones DP, Kimura K, Hirano T: Efficient supercoiling of DNA by a single condensin complex as revealed by electron spectroscopic imaging. Mol Cell 2002;9:1183-1190.
[PubMed]
4.
Biller SJ, Burkholder WF: The Bacillus subtilis SftA (YtpS) and SpoIIIE DNA translocases play distinct roles in growing cells to ensure faithful chromosome partitioning. Mol Microbiol 2009;74:790-809.
[PubMed]
5.
Bouthier de la Tour C, Toueille M, Jolivet E, Nguyen HH, Servant P, Vannier F, Sommer S: The Deinococcus radiodurans SMC protein is dispensable for cell viability yet plays a role in DNA folding. Extremophiles 2009;13:827-837.
[PubMed]
6.
Breier AM, Grossman AD: Whole-genome analysis of the chromosome partitioning and sporulation protein Spo0J (ParB) reveals spreading and origin-distal sites on the Bacillus subtilis chromosome. Mol Microbiol 2007;64:703-718.
[PubMed]
7.
Britton RA, Grossman AD: Synthetic lethal phenotypes caused by mutations affecting chromosome partitioning in Bacillus subtilis. J Bacteriol 1999;181:5860-5864.
[PubMed]
8.
Britton RA, Küster-Schöck E, Auchtung TA, Grossman AD: SOS induction in a subpopulation of structural maintenance of chromosome (Smc) mutant cells in Bacillus subtilis. J Bacteriol 2007;189:4359-4366.
[PubMed]
9.
Britton RA, Lin DC, Grossman AD: Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev 1998;12:1254-1259.
[PubMed]
10.
Broedersz CP, Wang X, Meir Y, Loparo JJ, Rudner DZ, Wingreen NS: Condensation and localization of the partitioning protein ParB on the bacterial chromosome. Proc Natl Acad Sci USA 2014;111:8809-8814.
[PubMed]
11.
Bürmann F, Shin HC, Basquin J, Soh YM, Gimenez-Oya V, Kim YG, Oh BH, Gruber S: An asymmetric SMC-kleisin bridge in prokaryotic condensin. Nat Struct Mol Biol 2013;20:371-379.
[PubMed]
12.
Cobbe N: The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol Biol Evol 2003;21:332-347.
[PubMed]
13.
Cuylen S, Metz J, Haering CH: Condensin structures chromosomal DNA through topological links. Nat Struct Mol Biol 2011;18:894-901.
[PubMed]
14.
Cuylen S, Metz J, Hruby A, Haering CH: Entrapment of chromosomes by condensin rings prevents their breakage during cytokinesis. Dev Cell 2013;27:469-478.
[PubMed]
15.
De Piccoli G, Torres-Rosell J, Aragón L: The unnamed complex: what do we know about Smc5-Smc6? Chromosome Res 2009;17:251-263.
[PubMed]
16.
Dedrick RM, Wildschutte H, McCormick JR: Genetic interactions of smc, ftsK, and parB genes in Streptomyces coelicolor and their developmental genome segregation phenotypes. J Bacteriol 2009;191:320-332.
[PubMed]
17.
Dervyn E, Noirot-Gros MF, Mervelet P, McGovern S, Ehrlich SD, Polard P, Noirot P: The bacterial condensin/cohesin-like protein complex acts in DNA repair and regulation of gene expression. Mol Microbiol 2004;51:1629-1640.
[PubMed]
18.
Fennell-Fezzie R, Gradia SD, Akey D, Berger JM: The MukF subunit of Escherichia coli condensin: architecture and functional relationship to kleisins. EMBO J 2005;24:1921-1930.
[PubMed]
19.
Fuentes-Perez ME, Gwynn EJ, Dillingham MS, Moreno-Herrero F: Using DNA as a fiducial marker to study SMC complex interactions with the atomic force microscope. Biophys J 2012;102:839-848.
[PubMed]
20.
Glaser P, Sharpe ME, Raether B, Perego M, Ohlsen K, Errington J: Dynamic, mitotic-like behavior of a bacterial protein required for accurate chromosome partitioning. Genes Dev 1997;11:1160-1168.
[PubMed]
21.
Gómez R, Jordan PW, Viera A, Alsheimer M, Fukuda T, Jessberger R, Llano E, Pendás AM, Handel MA, Suja JA: Dynamic localization of SMC5/6 complex proteins during mammalian meiosis and mitosis suggests functions in distinct chromosome processes. J Cell Sci 2013;126:4239-4252.
[PubMed]
22.
Graham TGW, Wang X, Song D, Etson CM, van Oijen AM, Rudner DZ, Loparo JJ: ParB spreading requires DNA bridging. Genes Dev 2014;28:1228-1238.
[PubMed]
23.
Graumann PL: Bacillus subtilis SMC is required for proper arrangement of the chromosome and for efficient segregation of replication termini but not for bipolar movement of newly duplicated origin regions. J Bacteriol 2000;182:6463-6471.
[PubMed]
24.
Graumann PL, Knust T: Dynamics of the bacterial SMC complex and SMC-like proteins involved in DNA repair. Chromosome Res 2009;17:265-275.
[PubMed]
25.
Graumann PL, Losick R, Strunnikov AV: Subcellular localization of Bacillus subtilis SMC, a protein involved in chromosome condensation and segregation. J Bacteriol 1998;180:5749-5755.
[PubMed]
26.
Gruber S, Arumugam P, Katou Y, Kuglitsch D, Helmhart W, Shirahige K, Nasmyth K: Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell 2006;127:523-537.
[PubMed]
27.
Gruber S, Errington J: Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 2009;137:685-696.
[PubMed]
28.
Gruber S, Haering CH, Nasmyth K: Chromosomal cohesin forms a ring. Cell 2003;112:765-777.
[PubMed]
29.
Gruber S, Veening J-W, Bach J, Blettinger M, Bramkamp M, Errington J: Interlinked sister chromosomes arise in the absence of condensin during fast replication in B. subtilis. Curr Biol 2014;24:293-238.
[PubMed]
30.
Haering CH, Löwe J, Hochwagen A, Nasmyth K: Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 2002;9:773-788.
[PubMed]
31.
Hiraga S, Niki H, Ogura T, Ichinose C, Mori H, Ezaki B, Jaffé A: Chromosome partitioning in Escherichia coli: novel mutants producing anucleate cells. Bacteriol 1989;171:1496-1505.
[PubMed]
32.
Hirano T: At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 2006;7:311-322.
[PubMed]
33.
Hirano M, Anderson DE, Erickson HP, Hirano T: Bimodal activation of SMC ATPase by intra- and inter-molecular interactions. EMBO J 2001;20:3238-3250.
[PubMed]
34.
Hirano M, Hirano T: Hinge-mediated dimerization of SMC protein is essential for its dynamic interaction with DNA. EMBO J 2002a;21:5733-5744.
[PubMed]
35.
Hirano M, Hirano T: Hinge-mediated dimerization of SMC protein is essential for its dynamic interaction with DNA. EMBO J 2002b;21:5733-5744.
[PubMed]
36.
Hirano M, Hirano T: Positive and negative regulation of SMC-DNA interactions by ATP and accessory proteins. EMBO J 2004;23:2664-2673.
[PubMed]
37.
Hirano M, Hirano T: Opening closed arms: long-distance activation of SMC ATPase by hinge-DNA interactions. Mol Cell 2006;21:175-186.
[PubMed]
38.
Ireton K, Grossman AD: A developmental checkpoint couples the initiation of sporulation to DNA replication in Bacillus subtilis. EMBO J 1994;13:1566-1573.
[PubMed]
39.
Ireton K, Gunther NW, Grossman AD: Spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillussubtilis. J Bacteriol 1994;176:5320-5329.
[PubMed]
40.
Kaimer C, Gonzaler-Pastor E, Graumann PL: SpoIIIE and a novel type of DNA translocase, SftA, couple chromosome segregation with cell division in Bacillus subtilis. Mol Microbiol 2009;74:810-825.
[PubMed]
41.
Kamada K, Miyata M, Hirano T: Molecular basis of SMC ATPase activation: role of internal structural changes of the regulatory subcomplex ScpAB. Structure 2013;21:581-594.
[PubMed]
42.
Kidane D, Graumann PL: Intracellular protein and DNA dynamics in competent Bacillus subtilis cells. Cell 2005;122:73-84.
[PubMed]
43.
Kim J-S, Lee S, Kang BS, Kim MH, Lee H-S, Kim K-J: Crystal structure and domain characterization of ScpB from Mycobacterium tuberculosis. Proteins 2008;71:1553-1556.
[PubMed]
44.
Kim JS, Shin DH, Pufan R, Huang C, Yokota H, Kim R, Kim SH: Crystal structure of ScpB from Chlorobium tepidum, a protein involved in chromosome partitioning. Proteins 2006;62:322-328.
[PubMed]
45.
Kimura K, Rybenkov VV, Crisona NJ, Hirano T, Cozzarelli NR: 13s condensin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 1999;98:239-248.
[PubMed]
46.
Kjos M, Veening JW: Tracking of chromosome dynamics in live Streptococcus pneumoniae reveals that transcription promotes chromosome segregation. Mol Microbiol 2014;91:1088-1105.
[PubMed]
47.
Kleine Borgmann LA, Hummel H, Ulbrich MH, Graumann PL: SMC condensation centers in Bacillus subtilis are dynamic structures. J Bacteriol 2013a;195:2136-2145.
[PubMed]
48.
Kleine Borgmann LA, Ries J, Ewers H, Ulbrich MH, Graumann PL: The bacterial SMC complex displays two distinct modes of interaction with the chromosome. Cell Rep 2013b;3:1483-1492.
[PubMed]
49.
Kois A, Swiatek M, Jakimowicz D, Zakrzewska-Czerwinska J: SMC protein-dependent chromosome condensation during aerial hyphal development in Streptomyces. J Bacteriol 2009;191:310-319.
[PubMed]
50.
Krishnamurthy M, Tadesse S, Rothmaier K, Graumann PL: A novel SMC-like protein, SbcE (YhaN), is involved in DNA double-strand break repair and competence in Bacillus subtilis. Nucleic Acids Res 2010;38:455-466.
[PubMed]
51.
Kumar M, Mommer MS, Sourjik V: Mobility of cytoplasmic, membrane, and DNA-binding proteins in Escherichia coli. Biophys J 2010;98:552-559.
[PubMed]
52.
Lammens A, Schele A, Hopfner KP: Structural biochemistry of ATP-driven dimerization and DNA-stimulated activation of SMC ATPases. Curr Biol 2004;14:1778-1782.
[PubMed]
53.
Lasocki K, Bartosik AA, Mierzejewska J, Thomas CM, Jagura-Burdzy G: Deletion of the parA (soj) homologue in Pseudomonas aeruginosa causes ParB instability and affects growth rate, chromosome segregation, and motility. J Bacteriol 2007;189:5762-5772.
[PubMed]
54.
Lee PS, Grossman AD: The chromosome partitioning proteins Soj (ParA) and Spo0J (ParB) contribute to accurate chromosome partitioning, separation of replicated sister origins, and regulation of replication initiation in Bacillussubtilis. Mol Microbiol 2006;60:853-869.
[PubMed]
55.
Lengronne A, Katou Y, Mori S, Yokobayashi S, Kelly GP, Itoh T, Watanabe Y, Shirahige K, Uhlmann F: Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 2004;430:573-578.
[PubMed]
56.
Lin DC, Grossman AD: Identification and characterization of a bacterial chromosome partitioning site. Cell 1998;92:675-685.
[PubMed]
57.
Lindow JC, Britton RA, Grossman AD: Structural maintenance of chromosomes protein of Bacillus subtilis affects supercoiling in vivo. J Bacteriol 2002a;184:5317-5322.
[PubMed]
58.
Lindow JC, Kuwano M, Moriya S, Grossman AD: Subcellular localization of the Bacillus subtilis structural maintenance of chromosomes (SMC) protein. Mol Microbiol 2002b;46:997-1009.
[PubMed]
59.
Löwe J, Cordell SC, van den Ent F: Crystal structure of the SMC head domain: an ABC ATPase with 900 residues antiparallel coiled-coil inserted. J Mol Biol 2001;306:25-35.
[PubMed]
60.
Mascarenhas J, Soppa J, Strunnikov AV, Graumann PL: Cell cycle-dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein. EMBO J 2002;21:3108-3118.
[PubMed]
61.
Mascarenhas J, Volkov AV, Rinn C, Schiener J, Guckenberger R, Graumann PL: Dynamic assembly, localization and proteolysis of the Bacillus subtilis SMC complex. BMC Cell Biol 2005;6:28.
[PubMed]
62.
Melby TE, Ciampaglio CN, Briscoe G, Erickson HP: The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J Cell Biol 1998;142:1595-1604.
[PubMed]
63.
Minnen A, Attaiech L, Thon M, Gruber S, Veening JW: SMC is recruited to oriC by ParB and promotes chromosome segregation in Streptococcus pneumoniae. Mol Microbiol 2011;81:676-688.
[PubMed]
64.
Mohl DA, Easter J, Gober JW: The chromosome partitioning protein, ParB, is required for cytokinesis in Caulobacter crescentus. Mol Microbiol 2001;42:741-755.
[PubMed]
65.
Moriya S, Tsujikawa E, Hassan AK, Asai K, Kodama T, Ogasawara N: A Bacillus subtilis gene-encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition. Mol Microbiol 1998;29:179-187.
[PubMed]
66.
Murray H, Errington J: Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 2008;135:74-84.
[PubMed]
67.
Murray H, Ferreira H, Errington J: The bacterial chromosome segregation protein Spo0J spreads along DNA from pars nucleation sites. Mol Microbiol 2006;61:1352-1361.
[PubMed]
68.
Nasmyth K, Haering CH: The structure and function of SMC and kleisin complexes. Annu Rev Biochem 2005;74:595-648.
[PubMed]
69.
Niki H, Imamura R, Kitaoka M, Yamanaka K, Ogura T, Hiraga S: E. coli MukB protein involved in chromosome partition forms a homodimer with a rod-and-hinge structure having DNA binding and ATP/GTP binding activities. EMBO J 1992;11:5101-5109.
[PubMed]
70.
Niki H, Jaffé A, Imamura R, Ogura T, Hiraga S: The new gene MukB codes for a 177 kD protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J 1991;10:183-193.
[PubMed]
71.
Petrushenko ZM, She W, Rybenkov VV: A new family of bacterial condensins. Mol Microbiol 2011;81:881-896.
[PubMed]
72.
Rybenkov VV: Maintenance of chromosome structure in Pseudomonas aeruginosa. FEMS Microbiol Lett 2014;356:154-165.
[PubMed]
73.
Sanchez H, Alonso JC: Bacillus subtilis RecN binds and protects 3′-single-stranded DNA extensions in the presence of ATP. Nucleic Acids Res 2005;33:2343-2350.
[PubMed]
74.
Sawitzke JA, Austin S: Suppression of chromosome segregation defects of Escherichia coli muk mutants by mutations in topoisomerase I. Proc Natl Acad Sci USA 2000;97:1671-1676.
[PubMed]
75.
Schleiffer A, Kaitna S, Maurer-Stroh S, Glotzer M, Nasmyth K, Eisenhaber F: Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners. Mol Cell 2003;11:571-575.
[PubMed]
76.
Scholefield G, Veening J-W, Murray H: DnaA and ORC: more than DNA replication initiators. Trends Cell Biol 2011;21:188-194.
[PubMed]
77.
Schwartz MA, Shapiro L: An SMC ATPase mutant disrupts chromosome segregation in Caulobacter. Mol Microbiol 2011;82:1359-1374.
[PubMed]
78.
Sherratt DJ, Arciszewska LK, Crozat E, Graham JE, Grainge I: The Escherichia coli DNA translocase FtsK. Biochem Soc Trans 2010;38:395-398.
[PubMed]
79.
Soppa J: Prokaryotic structural maintenance of chromosomes (SMC) proteins: distribution, phylogeny, and comparison with MukBs and additional prokaryotic and eukaryotic coiled-coil proteins. Gene 2001;278:253-264.
[PubMed]
80.
Soppa J, Kobayashi K, Noirot-Gros MF, Oesterhelt D, Ehrlich SD, Dervyn E, Ogasawara N, Moriya S: Discovery of two novel families of proteins that are proposed to interact with prokaryotic SMC proteins, and characterization of the Bacillus subtilis family members ScpA and ScpB. Mol Microbiol 2002;45:59-71.
[PubMed]
81.
Strunnikov AV, Larionov VL, Koshland D: Smc1: an essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous protein family. J Cell Biol 1993;123:1635-1648.
[PubMed]
82.
Sullivan NL, Marquis KA, Rudner DZ: Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 2009;137:697-707.
[PubMed]
83.
Tadesse S, Mascarenhas J, Kosters B, Hasilik A, Graumann PL: Genetic interaction of the SMC complex with topoisomerase IV in Bacillus subtilis. Microbiology 2005;151:3729-3737.
[PubMed]
84.
Torres-Rosell J, Machin F, Farmer S, Jarmuz A, Eydmann T, Dalgaard JZ, Aragon L: SMC5 and SMC6 genes are required for the segregation of repetitive chromosome regions. Nat Cell Biol 2005;7:412-419.
[PubMed]
85.
Uhlmann F, Lottspeich F, Nasmyth K: Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 1999;400:37-42.
[PubMed]
86.
Vecchiarelli AG, Mizuuchi K, Funnell BE: Surfing biological surfaces: exploiting the nucleoid for partition and transport in bacteria. Mol Microbiol 2012;86:513-523.
[PubMed]
87.
Verver DE, Langedijk NSM, Jordan PW, Repping S, Hamer G: The SMC5/6 complex is involved in crucial processes during human spermatogenesis. Biol Reprod 2014;91:22.
[PubMed]
88.
Verver DE, van Pelt AMM, Repping S, Hamer G: Role for rodent SMC6 in pericentromeric heterochromatin domains during spermatogonial differentiation and meiosis. Cell Death Dis 2013;4:e749.
[PubMed]
89.
Volkov A, Mascarenhas J, Andrei-Selmer C, Ulrich HD, Graumann PL: A prokaryotic condensin/cohesin-like complex can actively compact chromosomes from a single position on the nucleoid and binds to DNA as a ring-like structure. Mol Cell Biol 2003;23:5638-5650.
[PubMed]
90.
Wang X, Tang OW, Riley EP, Rudner DZ: The SMC condensin complex is required for origin segregation in Bacillus subtilis. Curr Biol 2014;24:287-292.
[PubMed]
91.
Woo JS, Lim JH, Shin HC, Suh MK, Ku B, Lee KH, Joo K, Robinson H, Lee J, Park SY, Ha NC, Oh BH: Structural studies of a bacterial condensin complex reveal ATP-dependent disruption of intersubunit interactions. Cell 2009;136:85-96.
[PubMed]
92.
Wood AJ, Severson AF, Meyer BJ: Condensin and cohesin complexity: the expanding repertoire of functions. Nat Rev Genet 2010;11:391-404.
[PubMed]
93.
Yamazoe M, Onogi T, Sunako Y, Niki H, Yamanaka K, Ichimura T, Hiraga S: Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli. EMBO J 1999;18:5873-5884.
[PubMed]
94.
Yoshimura SH, Hizume K, Murakami A, Sutani T, Takeyasu K, Yanagida M: Condensin architecture and interaction with DNA: regulatory non-SMC subunits bind to the head of SMC heterodimer. Curr Biol 2002;12:508-513.
[PubMed]
95.
Yu W, Herbert S, Graumann PL, Gotz F: Contribution of SMC (structural maintenance of chromosomes) and SpoIIIE to chromosome segregation in Staphylococci. J Bacteriol 2010;192:4067-4073.
[PubMed]
96.
Yu XC, Weihe EK, Margolin W: Role of the C terminus of FtsK in Escherichia coli chromosome segregation. J Bacteriol 1998;180:6424-6428.
[PubMed]
You do not currently have access to this content.