Structure and evolution of Apetala3, a sex-linked gene in Silene latifolia
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
20718967
PubMed Central
PMC3095310
DOI
10.1186/1471-2229-10-180
PII: 1471-2229-10-180
Knihovny.cz E-zdroje
- MeSH
- alely MeSH
- chromozomy rostlin genetika MeSH
- DNA rostlinná genetika MeSH
- exony MeSH
- introny MeSH
- molekulární evoluce * MeSH
- promotorové oblasti (genetika) MeSH
- regulace genové exprese u rostlin MeSH
- repetitivní sekvence nukleových kyselin MeSH
- retroelementy MeSH
- rostlinné geny MeSH
- rostlinné proteiny genetika MeSH
- sekvenční analýza DNA MeSH
- Silene genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- DNA rostlinná MeSH
- retroelementy MeSH
- rostlinné proteiny MeSH
BACKGROUND: The evolution of sex chromosomes is often accompanied by gene or chromosome rearrangements. Recently, the gene AP3 was characterized in the dioecious plant species Silene latifolia. It was suggested that this gene had been transferred from an autosome to the Y chromosome. RESULTS: In the present study we provide evidence for the existence of an X linked copy of the AP3 gene. We further show that the Y copy is probably located in a chromosomal region where recombination restriction occurred during the first steps of sex chromosome evolution. A comparison of X and Y copies did not reveal any clear signs of degenerative processes in exon regions. Instead, both X and Y copies show evidence for relaxed selection compared to the autosomal orthologues in S. vulgaris and S. conica. We further found that promoter sequences differ significantly. Comparison of the genic region of AP3 between the X and Y alleles and the corresponding autosomal copies in the gynodioecious species S. vulgaris revealed a massive accumulation of retrotransposons within one intron of the Y copy of AP3. Analysis of the genomic distribution of these repetitive elements does not indicate that these elements played an important role in the size increase characteristic of the Y chromosome. However, in silico expression analysis shows biased expression of individual domains of the identified retroelements in male plants. CONCLUSIONS: We characterized the structure and evolution of AP3, a sex linked gene with copies on the X and Y chromosomes in the dioecious plant S. latifolia. These copies showed complementary expression patterns and relaxed evolution at protein level compared to autosomal orthologues, which suggests subfunctionalization. One intron of the Y-linked allele was invaded by retrotransposons that display sex-specific expression patterns that are similar to the expression pattern of the corresponding allele, which suggests that these transposable elements may have influenced evolution of expression patterns of the Y copy. These data could help researchers decipher the role of transposable elements in degenerative processes during sex chromosome evolution.
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Charlesworth D, Charlesworth B, Marais G. Steps in the evolution of heteromorphic sex chromosomes. Heredity. 2005;95:118–28. doi: 10.1038/sj.hdy.6800697. PubMed DOI
Marshall Graves JA. Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. Annu Rev Genet. 2008;42:565–86. doi: 10.1146/annurev.genet.42.110807.091714. PubMed DOI
Ming R, Moore PH. Genomics of sex chromosomes. Curr Opin Plant Biol. 2007;10:123–30. doi: 10.1016/j.pbi.2007.01.013. PubMed DOI
Negrutiu I, Vyskot B, Barbacar N, Georgiev S, Monéger F. Dioecious plants. A key to the early events of sex chromosome evolution. Plant Physiology. 2001;127:1418–1424. doi: 10.1104/pp.010711. PubMed DOI PMC
Ainsworth C. Boys and girls come out to play: The molecular biology dioecious plants. Ann Bot-London. 2000;86:211–221. doi: 10.1006/anbo.2000.1201. DOI
Blackburn KB. Sex chromosomes in plants. Nature. 1923;112:687–688. doi: 10.1038/112687c0. DOI
Winge O. On sex chromosomes, sex determination and preponderance of females in some dioecious plants. CR Trav Lab Carlsberg. 1923;15:1–26.
Vyskot B, Hobza R. Gender in plants: sex chromosomes are emerging from the fog. Trends Genet. 2004;20:432–438. doi: 10.1016/j.tig.2004.06.006. PubMed DOI
Matsunaga S, Hizume M, Kawano S, Kuroiwa T. Cytological analysis in Melandrium album: genome size, chromosome size and fluorescence in situ hybridization. Cytologia. 1994;59:135–149.
Vagera J, Paulíková D, Doležel J. The development of male and female regenerants by in vitro androgenesis in dioecious plant Melandrium album. Ann Bot. 1994;73:455–459. doi: 10.1006/anbo.1994.1056. DOI
Veuskens J, Ye D, Oliveira M, Ciupercescu DD, Installe P, Verhoven HA, Negrutiu I. Sex determination in the dioecious Melandrium album - androgenetic embryogenesis requires the presence of the X-chromosome. Genome. 1992;35:8–16.
Westergaard M. Aberrant Y chromosomes and sex expression in Melandrium album. Hereditas. 1946;32:419–443. doi: 10.1111/j.1601-5223.1946.tb02784.x. PubMed DOI
Westergaard M. The mechanism of sex determination in dioecious flowering plants. Adv Genet. 1958;9:217–281. full_text. PubMed
Farbos I, Veuskens J, Vyskot B, Oliveira M, Hinnisdaels S, Aghmir A, Mouras A, Negrutiu I. Dimorphism in white campion: Deletion on the Y chromosome results in afloral asexual phenotype. Genetics. 1999;151:1187–1196. PubMed PMC
Lebel-Hardenack S, Hauser E, Law TF, Schmid J, Grant SR. Mapping of sex determination loci on the white campion (Silene latifolia) Y chromosome using amplified fragment length polymorphism. Genetics. 2002;160:717–25. PubMed PMC
Bergero R, Charlesworth D, Filatov DA, Moore RC. Defining regions and rearrangements of the Silene latifolia Y chromosome. Genetics. 2008;178:2045–53. doi: 10.1534/genetics.107.084566. PubMed DOI PMC
Babushok DV, Ostertag EM, Kazazian HH Jr. Current topics in genome evolution: molecular mechanisms of new gene formation. Cell Mol Life Sci. 2007;64:542–54. doi: 10.1007/s00018-006-6453-4. PubMed DOI PMC
Kaessmann H, Vinckenbosch N, Long M. RNA-based gene duplication: mechanistic and evolutionary insights. Nat Rev Genet. 2009;10:19–31. doi: 10.1038/nrg2487. PubMed DOI PMC
Lahn BT, Pearson NM, Jegalian K. The human Y chromosome, in the light of evolution. Nat Rev Genet. 2001;2:207–216. doi: 10.1038/35056058. PubMed DOI
Emerson JJ, Kaessmann H, Betrán E, Long M. Extensive gene traffic on the mammalian X chromosome. Science. 2004;303:537–40. doi: 10.1126/science.1090042. PubMed DOI
Kejnovsky E, Hobza R, Kubat Z, Cermak T, Vyskot B. The role of repetitive DNA in structure and evolution of sex chromosomes in plants. Heredity. 2009;102:533–541. doi: 10.1038/hdy.2009.17. PubMed DOI
Bachtrog D. Expression profile of a degenerating neo-Y chromosome in Drosophila. Curr Biology. 2006;16:1694–1699. doi: 10.1016/j.cub.2006.07.053. PubMed DOI
Matsunaga S, Isono E, Kejnovsky E, Vyskot B, Kawano S, Charlesworth D. Duplicative transfer of MADS box gene to a plant Y chromosome. Mol Biol Evol. 2003;20:1062–1069. doi: 10.1093/molbev/msg114. PubMed DOI
Zluvova J, Janousek B, Negrutiu I, Vyskot B. Comparison of the X and Y chromosome organization in Silene latifolia. Genetics. 2005;170:1431–4. doi: 10.1534/genetics.105.040444. PubMed DOI PMC
Nicolas M, Marais G, Hykelova V, Janousek B, Laporte V, Vyskot B, Mouchiroud D, Negrutiu I, Charlesworth D, Monéger F. A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PloS Biol. 2005;3:47–56. doi: 10.1371/journal.pbio.0030004. PubMed DOI PMC
Kejnovsky E, Kubat Z, Macas J, Hobza R, Mracek J, Vyskot B. A novel family of gypsy-like retrotransposons harboring an amplified tandem repeat. Molecular Genetics and Genomics. 2006;276:254–263. doi: 10.1007/s00438-006-0140-x. PubMed DOI
Matsunaga S, Kawano S, Takano H, Uchida H, Sakai A, Kuroiwa T. Isolation and developmental expression of male reproductive organ-specific genes in a dioecious campion, Melandrium album (Silene latifolia) Plant J. 1996;10:679–89. doi: 10.1046/j.1365-313X.1996.10040679.x. PubMed DOI
Bergero R, Forrest A, Kamau E, Charlesworth D. Evolutionary strata on the X chromosomes of the dioecious plant Silene latifolia: evidence from new sex-linked genes. Genetics. 2007;175:1945–54. doi: 10.1534/genetics.106.070110. PubMed DOI PMC
Kejnovský E, Vrána J, Matsunaga S, Soucek P, Siroký J, Dolezel J, Vyskot B. Localization of male-specifically expressed MROS genes of Silene latifolia by PCR on flow-sorted sex chromosomes and autosomes. Genetics. 2001;158:1269–77. PubMed PMC
Hobza R, Hrusakova P, Safar J, Bartos J, Janousek B, Zluvova J, Michu E, Dolezel J, Vyskot B. MK17, a specific marker closely linked to the gynoecium suppression region on the Y chromosome in Silene latifolia. Theoretical and Applied Genetics. 2006;113:280–287. doi: 10.1007/s00122-006-0293-3. PubMed DOI
Hobza R, Vyskot B. Laser microdissection- based analysis of plant sex chromosomes. Methods Cell Biol. 2007;82:433–53. full_text. PubMed
Wilson MA, Makova KD. Evolution and survival on eutherian sex chromosomes. PloS Genet. 2009;5:e1000568. doi: 10.1371/journal.pgen.1000568. PubMed DOI PMC
Moore RC, Kozyreva O, Lebel-Hardenack S, Siroky J, Hobza R, Vyskot B, Grant SR. Genetic and functional analysis of DD44, a sex-linked gene from the dioecious plant Silene latifolia, provides clues to early events in sex chromosome evolution. Genetics. 2003;163:321–334. PubMed PMC
Marais G, Nicolas M, Bergero R, Chambrier P, Kejnovsky E, Monéger F, Hobza R, Widmer A, Charlesworth D. Evidence for degeneration of the Y chromosome in the dioecious plant Silene latifolia. Current Biology. 2008;18:545–549. doi: 10.1016/j.cub.2008.03.023. PubMed DOI
Kubat Z, Hobza R, Vyskot B, Kejnovsky E. Microsatellite accumulation on the Y chromosome in Silene latifolia. Genome. 2008;51:350–356. doi: 10.1139/G08-024. PubMed DOI
Hobza R, Lengerova M, Svoboda J, Kubekova H, Kejnovsky E, Vyskot B. An accumulation of tandem DNA repeats on the Y chromosome in Silene latifolia during early stages of sex chromosome evolution. Chromosoma. 2006;115:376–382. doi: 10.1007/s00412-006-0065-5. PubMed DOI
Kejnovsky E, Kubat Z, Hobza R, Lengerova M, Sato I, Tabata S, Fukui K, Matsunaga S, Vyskot B. Accumulation of chloroplast DNA sequences on the Y chromosome of Silene latifolia. Genetica. 2006;128:167–175. doi: 10.1007/s10709-005-5701-0. PubMed DOI
Cermak T, Kubat Z, Hobza R, Koblizkova A, Widmer A, Macas J, Vyskot B, Kejnovsky E. Survey of repetitive sequences in Silene latifolia with respect to their distribution on sex chromosomes. Chromosome Research. 2008;16:961–976. doi: 10.1007/s10577-008-1254-2. PubMed DOI
Filatov DA, Howell EC, Groutides C, Armstrong SJ. Recent spread of a retrotransposon in the Silene latifolia genome, apart from the Y chromosome. Genetics. 2009;181:811–7. doi: 10.1534/genetics.108.099267. PubMed DOI PMC
Pasyukova E, Nuzhdin S, Li W, Flavell AJ. Germ line transposition of the copia retrotransposon in Drosophila melanogaster is restricted to males by tissue-specific control of copia RNA levels. Mol Gen Genet. 1997;255:115–24. doi: 10.1007/s004380050479. PubMed DOI
Matzke MA, Birchler JA. RNAi-mediated pathways in nucleus. Nat Rev Genet. 2005;6:24–35. doi: 10.1038/nrg1500. PubMed DOI
Bouzidi MF, Franchel J, Tao Q, Stormo K, Mraz A, Nicolas P, Mouzeyar S. A sunflower BAC library suitable for PCR screening and physical mapping of targeted genomic regions. Theor Appl Genet. 2006;113:81–9. doi: 10.1007/s00122-006-0274-6. PubMed DOI
Široký J, Lysák MA, Doležel J, Kejnovský E, Vyskot B. Heterogeneity of rDNA distribution of genome size in Silene spp. Chromosome Research. 2001;9:387–393. doi: 10.1023/A:1016783501674. PubMed DOI
Sambrook J, Russell DW. Molecular cloning: a laboratory manual. 3. Cold Spring Harbor, New York; Cold Spring Harbor Laboratory Press; 2001.
Lengerova M, Kejnovsky E, Hobza R, Macas J, Grant SR, Vyskot B. Multicolor FISH mapping of the dioecious model plant, Silene latifolia. Theor Appl Genet. 2004;108:1193–1199. doi: 10.1007/s00122-003-1568-6. PubMed DOI
Katoh, Asimenos, Toh. Multiple Alignment of DNA Sequences with MAFFT. Bioinformatics for DNA Sequence Analysis edited by D. Posada (outlines DNA alignment methods and several tips including group-to-group alignment and rough clustering of a large number of sequences). Methods in Molecular Biology. 2009;537:39–64. PubMed
Stephen F, David J. Basic local alignment search tool. J Mol Biol. 1990;215:403–410. PubMed
Burge C, Karlin S. Prediction of complete gene structures in human genomic DNA. J Mol Biol. 1997;268:78–94. doi: 10.1006/jmbi.1997.0951. PubMed DOI
Salamov AA, Solovyev VV. Ab initio gene finding in Drosophila genomic DNA. Genome Res. 2000;10:516–522. doi: 10.1101/gr.10.4.516. PubMed DOI PMC
Tatusov T, Tatusov R. ORF Finder (Open Reading Frame Finder) National Center for Biotechnology Information. National Institute of Health. 2007. http://www.ncbi.nlm.nih.gov/projects/gorf/
Marchler-Bauer A, Bryant SH. "CD-Search: protein domain annotations on the fly". Nucleic Acids Res. 2004;32:327–331. doi: 10.1093/nar/gkh454. PubMed DOI PMC
Rozen S, Skaletsky HJ. In: Bioinformatics Methods and Protocols Methods in Molecular Biology. Krawetz S, Misener S, editor. Humana Press, Totowa, NJ; 2000. Primer3 on the WWW for general users and for biologist programmers; pp. 365–386. PubMed
Stothard P. The Sequence Manipulation Suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques. 2000;28:1102–1104. PubMed
Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586–91. doi: 10.1093/molbev/msm088. PubMed DOI
Gouy M, Guindon S, Gascuel O. SeaView version 4. A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27:221–4. doi: 10.1093/molbev/msp259. PubMed DOI
Desfeux C, Maurice S, Henry JP, Lejeune B, Gouyon PH. Evolution of reproductive systems in the genus Silene. Proc Biol Sci. 1996;263:409–14. doi: 10.1098/rspb.1996.0062. Ainsworth C: Boys and girls come out to play: The molecular biology dioecious plants. Ann Bot-London 2000, 86: 211-221. PubMed DOI
Sexy ways: approaches to studying plant sex chromosomes
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Identifying new sex-linked genes through BAC sequencing in the dioecious plant Silene latifolia