Abstract
Silene latifolia is a model dioecious plant with heteromorphic sex chromosomes. The Y chromosome is the largest in this species. Theoretical models propose an accumulation of repetitive DNA sequences in non-recombining parts of the Y chromosome. In this study, we isolated a BAC7H5 clone preferentially hybridizing to the Y chromosome of S. latifolia. Sequence analysis revealed that this BAC7H5 contains part of the chloroplast genome, indicating that these chloroplast sequences have accumulated on the Y chromosome and also may contribute to its large size. We constructed Y chromosome- and X chromosome-specific libraries and screened them to find Y- and/or X-linked copies of chloroplast sequences. Sequence analysis revealed higher divergence of a non-genic region of the chloroplast sequences located on the Y chromosome while genic regions tested showed only very low (max 0.9%) divergence from their chloroplast homologues.
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J. Buzek H. Koutnikova A. Houben K. Riha B. Janousek J. Siroky S. Grant B. Vyskot (1997) ArticleTitleIsolation and characterization of X chromosome-derived DNA sequences from a dioecious plant Melandrium album Chromosome Res. 5 57–65 Occurrence Handle9088644 Occurrence Handle1:CAS:528:DyaK2sXivVyktr4%3D Occurrence Handle10.1023/A:1011693603279
B. Charlesworth (1991) ArticleTitleThe evolution of sex chromosomes Science 251 1030–1033 Occurrence Handle1998119 Occurrence Handle1:STN:280:By6C2cbptVE%3D Occurrence Handle10.1126/science.1998119
D. Charlesworth D.S. Guttman (1999) The evolution of dioecy and plant sex chromosome systems C.C. Ainsworth (Eds) Sex Determination in Plants BIOS Oxford 25–49
D. Charlesworth (2000) ArticleTitleThe degeneration of Y chromosomes Phil. Trans. R. Soc. Lond. B 355 1563–1572 Occurrence Handle1:CAS:528:DC%2BD3MXkvVymsA%3D%3D Occurrence Handle10.1098/rstb.2000.0717
B. Charlesworth P. Sniegowski W. Stephan (1994) ArticleTitleThe evolutionary dynamics of repetitive DNA in eukaryotes Nature 371 215–220 Occurrence Handle8078581 Occurrence Handle1:CAS:528:DyaK2cXmt1emu7o%3D Occurrence Handle10.1038/371215a0
J. Ellis (1982) ArticleTitleChloroplast genes inside plant mitochondria Nature 299 678–679 Occurrence Handle7121600 Occurrence Handle1:CAS:528:DyaL3sXht1Sns7Y%3D Occurrence Handle10.1038/299678a0
R. Erlandsson J.F. Wilson S. Paabo (2000) ArticleTitleSex chromosomal transposable element accumulation and male-driven substitutional evolution in humans Mol. Biol. Evol. 17 804–812 Occurrence Handle10779541 Occurrence Handle1:CAS:528:DC%2BD3cXjt1Gjtbo%3D
S. Grant A. Houben B. Vyskot J. Siroky W.H. Pan J. Macas H. Saedler (1994) ArticleTitleGenetics of sex determination in flowering plants Dev. Genet. 15 214–230 Occurrence Handle10.1002/dvg.1020150304
R. Hobza M. Lengerova H. Cernohorska J. Rubes B. Vyskot (2004) ArticleTitleFAST-FISH with laser beam microdissected DOP-PCR probe distinguishes the sex chromosomes of Silene latifolia Chromosome Res. 12 245–250 Occurrence Handle15125638 Occurrence Handle1:CAS:528:DC%2BD2cXisVyqurY%3D Occurrence Handle10.1023/B:CHRO.0000021929.97208.1c
N. Junakovic A. Terrinoni C. Di Franco C. Vieira C. Loevenbruck (1998) ArticleTitleAccumulation of transposable elements in the heterochromatin and on the Y chromosome of Drosophila simulans and Drosophila melanogaster J. Mol. Evol. 46 661–668 Occurrence Handle9608048 Occurrence Handle1:CAS:528:DyaK1cXjslOgurk%3D Occurrence Handle10.1007/PL00006346
T. Kiss M. Kiss F. Solymosy (1989) ArticleTitleNucleotide-sequence of a 25 S ribosomal-RNA gene from tomato Nucleic Acids Res. 17 796–796 Occurrence Handle2915931 Occurrence Handle1:CAS:528:DyaL1MXlvVymsb0%3D
B.T. Lahn D.C. Page (1999) ArticleTitleRetroposition of autosomal mRNA yielded testis-specific gene family on human Y chromosome Nature Genet. 21 429–433 Occurrence Handle10192397 Occurrence Handle1:CAS:528:DyaK1MXitFKrsLs%3D Occurrence Handle10.1038/7771
M. Lengerova R.C. Moore S.R. Grant B. Vyskot (2003) ArticleTitleThe sex chromosomes of Silene latifolia revisited and revised Genetics 165 935–938 Occurrence Handle14573500
M. Lengerova E. Kejnovsky R. Hobza J. Macas S.R. Grant B. Vyskot (2004) ArticleTitleMulticolor FISH mapping of the dioecious model plant, Silene latifolia Theor. Appl. Genet. 108 1193–1199 Occurrence Handle14727034 Occurrence Handle1:CAS:528:DC%2BD2cXjtlOru7c%3D Occurrence Handle10.1007/s00122-003-1568-6
R. Lewin (1984) ArticleTitleNo genome barriers to promiscuous DNA Science 224 970–971 Occurrence Handle10.1126/science.224.4652.970
X. Lin S. Kaul S. Rounsley et al. (1999) ArticleTitleSequence analysis of chromosome 2 of the plant Arabidopsis thaliana Nature 402 761–768 Occurrence Handle10617197 Occurrence Handle1:STN:280:DC%2BD3c%2FotlCrtQ%3D%3D Occurrence Handle10.1038/45471
Z. Liu P.H. Moore H. Ma C.M. Ackerman M. Ragiba Q.Y. Yu H.M. Pearl M.S. Kim J.W. Charlton J.I. Stiles F.T. Zee A.H. Paterson R. Ming (2004) ArticleTitleA primitive Y chromosome in papaya marks incipient sex chromosome evolution Nature 427 348–352 Occurrence Handle14737167 Occurrence Handle1:CAS:528:DC%2BD2cXltFCgsA%3D%3D Occurrence Handle10.1038/nature02228
W. Martin R.G. Herrmann (1998) ArticleTitleGene transfer from organelles to the nucleus: How much, what happens, and why Plant Physiol. 118 9–17 Occurrence Handle9733521 Occurrence Handle1:CAS:528:DyaK1cXmtV2msLs%3D Occurrence Handle10.1104/pp.118.1.9
S. Matsunaga E. Isono E. Kejnovsky B. Vyskot J. Dolezel S. Kawano D. Charlesworth (2003) ArticleTitleDuplicative transfer of a MADS box gene to a plant Y chromosome Mol. Biol. Evol. 20 1062–1069 Occurrence Handle12716981 Occurrence Handle1:CAS:528:DC%2BD3sXltlenu7o%3D Occurrence Handle10.1093/molbev/msg114
S. Okada T. Sone M. Fujisawa S. Nakayama M. Takenaka K. Ishizaki K. Kono Y. Shimizu-Ueda T. Hanajiri K.T. Yamato H. Fukuzawa A. Brennicke K. Ohyama (2001) ArticleTitleThe Y chromosome in the liverwort Marchantia polymorpha has accumulated unique repeat sequences harboring a male-specific gene Proc. Natl. Acad. Sci. USA 98 9454–9459 Occurrence Handle11481501 Occurrence Handle1:CAS:528:DC%2BD3MXlvFSrtrc%3D Occurrence Handle10.1073/pnas.171304798
M. Ricchetti F. Tekaia B. Dujon (2004) ArticleTitleContinued colonization of the human genome by mitochondrial DNA PLoS Biol. 2 1313–1324 Occurrence Handle1:CAS:528:DC%2BD2cXns1egtL4%3D Occurrence Handle10.1371/journal.pbio.0020273
K. Sakamoto N. Ohmido K. Fukui H. Kamada S. Satoh (2000) ArticleTitleSite-specific accumulation of a LINE-like retrotransposon in a sex chromosome of the dioecous plant Cannabis sativa Plant Mol. Biol. 44 723–732 Occurrence Handle11202435 Occurrence Handle1:CAS:528:DC%2BD3MXotVKrsQ%3D%3D Occurrence Handle10.1023/A:1026574405717
S. Sato H. Kotani Y. Nakamura et al. (1997) ArticleTitleStructural analysis of Arabidopsis thaliana chromosome 5. I. Sequence features of the 1.6 Mb regions covered by twenty physically assigned P1 clones DNA Res. 4 215–230 Occurrence Handle9330910 Occurrence Handle1:CAS:528:DyaK2sXlsFems7c%3D Occurrence Handle10.1093/dnares/4.3.215
S. Sato T. Kaneko Y. Nakamura E. Asamizu T. Kato S. Tabata (2001) ArticleTitleStructural analysis of a Lotus japonicus genome. I. Sequence features and mapping of fifty-six TAC clones which cover the 5.4 Mb regions of the genome DNA Res. 8 311–318 Occurrence Handle11853318 Occurrence Handle1:CAS:528:DC%2BD38XhtFGhsLk%3D Occurrence Handle10.1093/dnares/8.6.311
F. Shibata (2000) ArticleTitleDifferentiation and the polymorphic nature of the Y chromosome revealed by repetitive sequences in the dioecious plant, Rumex acetosa Chromosome Res. 8 229–236 Occurrence Handle10841050 Occurrence Handle1:CAS:528:DC%2BD3cXjvVSjsrc%3D Occurrence Handle10.1023/A:1009252913344
F. Shibata M. Hizume Y. Kuroki (1999) ArticleTitleChromosome painting of Y chromosome and isolation of a Y chromosome-specific repetitive sequences in the dioecious plant Rumex acetosa Chromosoma 108 266–270 Occurrence Handle10460415 Occurrence Handle1:CAS:528:DyaK1MXlt1Sjt74%3D Occurrence Handle10.1007/s004120050377
J. Siroky M.A. Lysak J. Dolezel E. Kejnovsky B. Vyskot (2001) ArticleTitleHeterogeneity of rDNA distribution and genome size in Silene spp Chromosome Res. 9 387–393 Occurrence Handle11448040 Occurrence Handle1:CAS:528:DC%2BD3MXltVels7s%3D Occurrence Handle10.1023/A:1016783501674
M. Steinemann S. Steinemann (1992) ArticleTitleDegenerating Y chromosome of Drosophila miranda: a trap for retrotransposons Proc. Natl. Acad. Sci. USA 89 7591–7595 Occurrence Handle1323846 Occurrence Handle1:CAS:528:DyaK38XmtVKitLg%3D Occurrence Handle10.1073/pnas.89.16.7591
M. Steinemann S. Steinemann (1998) ArticleTitleEnigma of Y chromosome degeneration: Neo-Y and neo-X chromosomes of Drosophila miranda, a model for sex chromosome evolution Genetica 103 409–420 Occurrence Handle10.1023/A:1017058119760
R.M. Stupar J.W. Lilly Ch.D. Town Z. Cheng S. Kaul C.R. Buell J.M. Jiang (2001) ArticleTitleComplex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats Proc. Natl. Acad. Sci. USA 98 5099–5103 Occurrence Handle11309509 Occurrence Handle1:CAS:528:DC%2BD3MXjt1Onsrc%3D Occurrence Handle10.1073/pnas.091110398
H. Telenius N.P. Carter C.E. Bebb M. Nordenskjold B.A.J. Ponder A. Tunnacliffe (1992) ArticleTitleDegenerate oligonucleotide-primed PCR: general amplification of target DNA by a single degenerate primer Genomics 13 718–725 Occurrence Handle1639399 Occurrence Handle1:CAS:528:DyaK38Xmt1OhsLY%3D Occurrence Handle10.1016/0888-7543(92)90147-K
J.N. Timmis M.A. Ayliffe Ch.Y. Huang W. Martin (2004) ArticleTitleEndosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes Nature Rev. Genet. 5 123–135 Occurrence Handle1:CAS:528:DC%2BD2cXptVOhtw%3D%3D Occurrence Handle10.1038/nrg1271
InstitutionalAuthorNameThe Arabidopsis Genome Initiative (2000) ArticleTitleAnalysis of the genome sequence of the flowering plant Arabidopsis thaliana Nature 408 796–815 Occurrence Handle10.1038/35048692
S.O. Triboush N.G. Danilenko O.G. Davydenko (1998) ArticleTitleA method for isolation of chloroplast DNA and mitochondrial DNA from sunflower Plant Mol. Biol. 16 183–189 Occurrence Handle1:CAS:528:DyaK1MXjs1OrtLk%3D Occurrence Handle10.1023/A:1007487806583
B. Vyskot R. Hobza (2004) ArticleTitleGender in plants: sex chromosomes are emerging from the fog Trends Genet. 20 432–438 Occurrence Handle15313552 Occurrence Handle1:CAS:528:DC%2BD2cXmsl2isLc%3D Occurrence Handle10.1016/j.tig.2004.06.006
Q. Yuan J. Hill J. Hsiao K. Moffat S. Ouyang Z. Cheng J. Jiang C.R. Buell (2002) ArticleTitleGenome sequencing of 239-kb region of rice chromosome 10 L reveals a high frequency of gene duplication and a large chloroplast DNA insertion Mol. Genet. Genom. 267 713–720 Occurrence Handle1:CAS:528:DC%2BD38Xnsl2kuro%3D Occurrence Handle10.1007/s00438-002-0706-1
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Kejnovsky, E., Kubat, Z., Hobza, R. et al. Accumulation of chloroplast DNA sequences on the Y chromosome of Silene latifolia . Genetica 128, 167–175 (2006). https://doi.org/10.1007/s10709-005-5701-0
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DOI: https://doi.org/10.1007/s10709-005-5701-0