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Functional centromeres in soybean include two distinct tandem repeats and a retrotransposon

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Abstract

The centromere as a kinetochore assembly site is fundamental to the partitioning of genetic material during cell division. In order to determine the functional centromeres of soybean, we characterized the soybean centromere-specific histone H3 (GmCENH3) protein and developed an antibody against the N-terminal end. Using this antibody, we cloned centromere-associated DNA sequences by chromatin immunoprecipitation. Our analyses indicate that soybean centromeres are composed of two distinct satellite repeats (GmCent-1 and GmCent-4) and retrotransposon-related sequences (GmCR). The possible allopolyploid origin of the soybean genome is discussed in view of the centromeric satellite sequences present.

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Abbreviations

CENH3:

Centromere-specific histone H3

EST:

Expressed sequence tag

RACE:

Rapid amplification of cDNA ends

PHEMES:

PIPES (piperazine-1,4-bis (2-ethanesulfonic acid)), HEPES (4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid), EGTA (ethylene glycol tetraacetic acid), MgCl2, sorbitol

PBS:

Phosphate-buffered saline

ChIP:

Chromatin immunoprecipitation

DAPI:

4,6-Diamino-2-phenylindole

References

  • Ansari HA, Ellison NW, Griffiths AG, Williams WM (2004) A lineage-specific centromeric satellite sequence in the genus Trifolium. Chromosome Res 12:357–367

    Article  PubMed  CAS  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218

    Article  CAS  Google Scholar 

  • Bao W, Zhang W, Yang Q et al (2006) Diversity of centromeric repeats in two closely related wild rice species, Oryza officinalis and Oryza rhizomatis. Mol Genet Genomics 275:421–430

    Article  PubMed  CAS  Google Scholar 

  • Black BE, Foltz DR, Chakravarthy S, Luger K, Woods VL, Cleveland DW (2004) Structural determinants for generating centromeric chromatin. Nature 430:578–582

    Article  PubMed  CAS  Google Scholar 

  • Cheeseman IM, Desai A (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9:33–46

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JL, Rauscher JT, Brown AHD (2004) Evolution of the perennial soybean polyploid complex (Glycine subgenus Glycine): a study of contrasts. Biol J Linn Soc 82:583–597

    Article  Google Scholar 

  • Gill N, Findley S, Walling JG et al (2009) Molecular and chromosomal evidence for allopolyploidy in soybean. Plant Physiol 151:1167–1174

    Article  PubMed  CAS  Google Scholar 

  • Gindullis F, Desel C, Galasso I, Schmidt T (2001) The large-scale organization of the centromeric region in Beta species. Genome Res 11:253–265

    Article  PubMed  CAS  Google Scholar 

  • Hall AE, Keith KC, Hall SE, Copenhaver GP, Preuss D (2004) The rapidly evolving field of plant centromeres. Curr Opin Plant Biol 7:108–114

    Article  PubMed  CAS  Google Scholar 

  • Han Y, Wang G, Liu Z et al (2010) Divergence in centromere structure distinguishes related genomes in Coix lacryma-jobi and its wild relative. Chromosoma 119:89–98

    Article  PubMed  CAS  Google Scholar 

  • Henikoff S, Ahmad K, Platero JS, van Steensel B (2000) Heterochromatic deposition of centromeric histone H3-like proteins. Proc Natl Acad Sci USA 97:716–721

    Article  PubMed  CAS  Google Scholar 

  • Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102

    Article  PubMed  CAS  Google Scholar 

  • Hirsch CD, Wu Y, Yan H, Jiang J (2009) Lineage-specific adaptive evolution of the centromeric protein CENH3 in diploid and allotetraploid Oryza species. Mol Biol Evol 26:2877–2885

    Article  PubMed  CAS  Google Scholar 

  • Houben A, Schroeder-Reiter E, Nagaki K et al (2007) CENH3 interacts with the centromeric retrotransposon cereba and GC-rich satellites and locates to centromeric substructures in barley. Chromosoma 116:275–283

    Article  PubMed  CAS  Google Scholar 

  • Jiang J, Gill BS, Wang GL, Ronald PC, Ward DC (1995) Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc Natl Acad Sci USA 92:4487–4491

    Article  PubMed  CAS  Google Scholar 

  • Jiang J, Birchler JA, Parrott WA, Dawe RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8:570–575

    Article  PubMed  CAS  Google Scholar 

  • Kamm A, Galasso I, Schmidt T, Heslop-Harrison JS (1995) Analysis of a repetitive DNA family from Arabidopsis arenosa and relationships between Arabidopsis species. Plant Mol Biol 27:853–862

    Article  PubMed  CAS  Google Scholar 

  • Kawabe A, Nasuda S (2005) Structure and genomic organization of centromeric repeats in Arabidopsis species. Mol Genet Genomics 272:593–602

    Article  PubMed  CAS  Google Scholar 

  • Kolchinsky A, Gresshoff PM (1995) A major satellite DNA of soybean is a 92-base pairs tandem repeat. Theor Appl Genet 90:621–626

    Article  CAS  Google Scholar 

  • Kulikova O, Geurts R, Lamine M et al (2004) Satellite repeats in the functional centromere and pericentromeric heterochromatin of Medicago truncatula. Chromosoma 113:276–283

    Article  PubMed  CAS  Google Scholar 

  • Laten HM, Havecker ER, Farmer LM, Voytas DF (2003) SIRE1, an endogenous retrovirus family from Glycine max, is highly homogeneous and evolutionarily young. Mol Biol Evol 20:1222–1230

    Article  PubMed  CAS  Google Scholar 

  • Lee JS, Verma DP (1984) Structure and chromosomal arrangement of leghemoglobin genes in kidney bean suggest divergence in soybean leghemoglobin gene loci following tetraploidization. EMBO J 3:2745–2752

    PubMed  CAS  Google Scholar 

  • Lee HR, Zhang W, Langdon T et al (2005) Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species. Proc Natl Acad Sci USA 102:11793–11798

    Article  PubMed  CAS  Google Scholar 

  • Lin JY, Jacobus BH, SanMiguel P et al (2005) Pericentromeric regions of soybean (Glycine max L. Merr.) chromosomes consist of retroelements and tandemly repeated DNA and are structurally and evolutionarily labile. Genetics 170:1221–1230

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Yue W, Li D et al (2008) Structure and dynamics of retrotransposons at wheat centromeres and pericentromeres. Chromosoma 117:445–456

    Article  PubMed  CAS  Google Scholar 

  • Ma J, Wing RA, Bennetzen JL, Jackson SA (2007) Plant centromere organization: a dynamic structure with conserved functions. Trends Genet 23:134–139

    Article  PubMed  CAS  Google Scholar 

  • Malik HS, Henikoff S (2003) Phylogenomics of the nucleosome. Nat Struct Biol 10:882–891

    Article  PubMed  CAS  Google Scholar 

  • Meraldi P, McAinsh AD, Rheinbay E, Sorger PK (2006) Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol 7:R23

    Article  PubMed  CAS  Google Scholar 

  • Morgante M, Jurman I, Shi L, Zhu T, Keim P, Rafalski JA (1997) The STR120 satellite DNA of soybean: organization, evolution and chromosomal specificity. Chromosome Res 5:363–373

    Article  PubMed  CAS  Google Scholar 

  • Nagaki K, Murata M (2005) Characterization of CENH3 and centromere-associated DNA sequences in sugarcane. Chromosome Res 13:195–203

    Article  PubMed  CAS  Google Scholar 

  • Nagaki K, Talbert PB, Zhong CX, Dawe RK, Henikoff S, Jiang J (2003) Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics 163:1221–1225

    PubMed  CAS  Google Scholar 

  • Nagaki K, Cheng Z, Ouyang S et al (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36:138–145

    Article  PubMed  CAS  Google Scholar 

  • Nagaki K, Kashihara K, Murata M (2005) Visualization of diffuse centromeres with centromere-specific histone H3 in the holocentric plant Luzula nivea. Plant Cell 17:1886–1893

    Article  PubMed  CAS  Google Scholar 

  • Nagaki K, Kashihara K, Murata M (2009) A centromeric DNA sequence colocalized with a centromere-specific histone H3 in tobacco. Chromosoma 118:249–257

    Article  PubMed  CAS  Google Scholar 

  • Palmer DK, O'Day K, Trong HL, Charbonneau H, Margolis RL (1991) Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone. Proc Natl Acad Sci USA 88:3734–3738

    Article  PubMed  CAS  Google Scholar 

  • Pedrosa A, Sandal N, Stougaard J, Schweizer D, Bachmair A (2002) Chromosomal map of the model legume Lotus japonicus. Genetics 161:1661–1672

    PubMed  CAS  Google Scholar 

  • Pontes O, Neves N, Silva M et al (2004) Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome. Proc Natl Acad Sci USA 101:18240–18245

    Article  PubMed  CAS  Google Scholar 

  • Santaguida S, Musacchio A (2009) The life and miracles of kinetochores. EMBO J 28:2511–2531

    Article  PubMed  CAS  Google Scholar 

  • Shibata F, Murata M (2004) Differential localization of the centromere-specific proteins in the major centromeric satellite of Arabidopsis thaliana. J Cell Sci 117:2963–2970

    Article  PubMed  CAS  Google Scholar 

  • Shoemaker RC, Polzin K, Labate J et al (1996) Genome duplication in soybean (Glycine subgenus soja). Genetics 144:329–338

    PubMed  CAS  Google Scholar 

  • Shoemaker RC, Schlueter J, Doyle JJ (2006) Paleopolyploidy and gene duplication in soybean and other legumes. Curr Opin Plant Biol 9:104–109

    Article  PubMed  CAS  Google Scholar 

  • Singh RJ, Hymowitz T (1988) The genomic relationship between Glycine max (L.) Merr. and G. soja Sieb. and Zucc. as revealed by pachytene chromosome analysis. Theor Appl Genet 76:705–711

    Article  Google Scholar 

  • Straub SC, Pfeil BE, Doyle JJ (2006) Testing the polyploid past of soybean using a low-copy nuclear gene—is Glycine (Fabaceae: Papilionoideae) an auto- or allopolyploid? Mol Phylogenet Evol 39:580–584

    Article  PubMed  CAS  Google Scholar 

  • Sullivan KF, Hechenberger M, Masri K (1994) Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J Cell Biol 127:581–592

    Article  PubMed  CAS  Google Scholar 

  • Sullivan BA, Blower MD, Karpen GH (2001) Determining centromere identity: cyclical stories and forking paths. Nat Rev Genet 2:584–596

    Article  PubMed  CAS  Google Scholar 

  • Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S (2002) Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14:1053–1066

    Article  PubMed  CAS  Google Scholar 

  • Vahedian M, Shi L, Zhu T, Okimoto R, Danna K, Keim P (1995) Genomic organization and evolution of the soybean SB92 satellite sequence. Plant Mol Biol 29:857–862

    Article  PubMed  CAS  Google Scholar 

  • Wawrzynski A, Ashfield T, Chen NW et al (2008) Replication of nonautonomous retroelements in soybean appears to be both recent and common. Plant Physiol 148:1760–1771

    Article  PubMed  CAS  Google Scholar 

  • Wright DA, Voytas DF (2002) Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res 12:122–131

    Article  PubMed  CAS  Google Scholar 

  • Yano ST, Panbehi B, Das A, Laten HM (2005) Diaspora, a large family of Ty3-gypsy retrotransposons in Glycine max, is an envelope-less member of an endogenous plant retrovirus lineage. BMC Evol Biol 5:30

    Article  PubMed  CAS  Google Scholar 

  • Zhong CX, Marshall JB, Topp C et al (2002) Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14:2825–2836

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. Jiri Macas for the help in sequence analysis. This work was supported by the Fellowship Program of the Japan Society for the Promotion of Science (JSPS) to ALT and KN.

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Correspondence to Ahmet L. Tek or Kiyotaka Nagaki.

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Responsible Editor: Herbert Macgregor.

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Fig. S1

Alignment of CentGm-1 family with sequences derived from the ChIP analysis. Five complete 92-bp monomers and six partial sequences extracted from clones G48, G56, G61, G71, and G87 are aligned with the two representative CentGm-1 (accession no.) and -2 (accession no.) sequences. The nucleotide position is marked at the beginning and end of the sequence for each monomer. Conserved and diverged regions with thick and thin lines, respectively, are shown below (GIF 101 kb)

High resolution image (TIFF 1375 kb)

Fig. S2

Sequence alignment of CentGm-4 sequences. For illustration purposes, the G30 sequence is divided into two fragments: 5′ (G30-b) and 3′ (G30-a) ends and are boxed with thick and thin lines, respectively. A 153-bp fragment (G92-b, 700–852 bp) of the G92 clone is marked with dotted lines. Sequence positions are shown for each clone at the first and last nucleotides (GIF 136 kb)

High resolution image (TIFF 3373 kb)

Fig. S3

Multiple sequence alignment of gag-pol regions derived from G92-a and four retrotransposons (accession nos. FJ197991, FJ197992, FJ197994, and FJ197995). A single frameshift is corrected at position 13846 in FJ197992. Similarities are shaded in black for 100%, dark gray for 80–99%, light gray for 60–79%, and white for less than 60% (GIF 118 kb)

High resolution image (TIFF 1594 kb)

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Tek, A.L., Kashihara, K., Murata, M. et al. Functional centromeres in soybean include two distinct tandem repeats and a retrotransposon. Chromosome Res 18, 337–347 (2010). https://doi.org/10.1007/s10577-010-9119-x

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  • DOI: https://doi.org/10.1007/s10577-010-9119-x

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