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. 2001 Jul;158(3):1203–1215. doi: 10.1093/genetics/158.3.1203

Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus).

A Ludwig 1, N M Belfiore 1, C Pitra 1, V Svirsky 1, I Jenneckens 1
PMCID: PMC1461728  PMID: 11454768

Abstract

Sturgeon (order Acipenserformes) provide an ideal taxonomic context for examination of genome duplication events. Multiple levels of ploidy exist among these fish. In a novel microsatellite approach, data from 962 fish from 20 sturgeon species were used for analysis of ploidy in sturgeon. Allele numbers in a sample of individuals were assessed at six microsatellite loci. Species with approximately 120 chromosomes are classified as functional diploid species, species with approximately 250 chromosomes as functional tetraploid species, and with approximately 500 chromosomes as functional octaploids. A molecular phylogeny of the sturgeon was determined on the basis of sequences of the entire mitochondrial cytochrome b gene. By mapping the estimated levels of ploidy on this proposed phylogeny we demonstrate that (I) polyploidization events independently occurred in the acipenseriform radiation; (II) the process of functional genome reduction is nearly finished in species with approximately 120 chromosomes and more active in species with approximately 250 chromosomes and approximately 500 chromosomes; and (III) species with approximately 250 and approximately 500 chromosomes arose more recently than those with approximately 120 chromosomes. These results suggest that gene silencing, chromosomal rearrangements, and transposition events played an important role in the acipenseriform genome formation. Furthermore, this phylogeny is broadly consistent with previous hypotheses but reveals a highly supported oceanic (Atlantic-Pacific) subdivision within the Acipenser/Huso complex.

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Selected References

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  1. Alrubaian J., Danielson P., Fitzpatrick M., Schreck C., Dores R. M. Cloning of a second proopiomelanocortin cDNA from the pituitary of the sturgeon, Acipenser transmontanus. Peptides. 1999;20(4):431–436. doi: 10.1016/s0196-9781(99)00021-2. [DOI] [PubMed] [Google Scholar]
  2. Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
  3. Bailey G. S., Poulter R. T., Stockwell P. A. Gene duplication in tetraploid fish: model for gene silencing at unlinked duplicated loci. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5575–5579. doi: 10.1073/pnas.75.11.5575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Birstein V. J., DeSalle R. Molecular phylogeny of Acipenserinae. Mol Phylogenet Evol. 1998 Feb;9(1):141–155. doi: 10.1006/mpev.1997.0443. [DOI] [PubMed] [Google Scholar]
  5. Birstein V. J., Poletaev A. I., Goncharov B. F. DNA content in Eurasian sturgeon species determined by flow cytometry. Cytometry. 1993;14(4):377–383. doi: 10.1002/cyto.990140406. [DOI] [PubMed] [Google Scholar]
  6. Brown J. R., Beckenbach A. T., Smith M. J. Mitochondrial DNA length variation and heteroplasmy in populations of white sturgeon (Acipenser transmontanus). Genetics. 1992 Sep;132(1):221–228. doi: 10.1093/genetics/132.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown J. R., Beckenbach K., Beckenbach A. T., Smith M. J. Length variation, heteroplasmy and sequence divergence in the mitochondrial DNA of four species of sturgeon (Acipenser). Genetics. 1996 Feb;142(2):525–535. doi: 10.1093/genetics/142.2.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Buroker N. E., Brown J. R., Gilbert T. A., O'Hara P. J., Beckenbach A. T., Thomas W. K., Smith M. J. Length heteroplasmy of sturgeon mitochondrial DNA: an illegitimate elongation model. Genetics. 1990 Jan;124(1):157–163. doi: 10.1093/genetics/124.1.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Committee on Genetics American Academy of Pediatrics: Health care supervision for children with Williams syndrome. Pediatrics. 2001 May;107(5):1192–1204. [PubMed] [Google Scholar]
  10. Danielson P. B., Alrubaian J., Muller M., Redding J. M., Dores R. M. Duplication of the POMC gene in the paddlefish (Polyodon spathula): analysis of gamma-MSH, ACTH, and beta-endorphin regions of ray-finned fish POMC. Gen Comp Endocrinol. 1999 Nov;116(2):164–177. doi: 10.1006/gcen.1999.7353. [DOI] [PubMed] [Google Scholar]
  11. Dingerkus G., Howell W. M. Karyotypic analysis and evidence of tetraploidy in the North American paddlefish, Polyodon spathula. Science. 1976 Nov 19;194(4267):842–844. doi: 10.1126/science.982045. [DOI] [PubMed] [Google Scholar]
  12. Fontana F. Chromosomal nucleolar organizer regions in four sturgeon species as markers of karyotype evolution in Acipenseriformes (Pisces). Genome. 1994 Oct;37(5):888–892. doi: 10.1139/g94-126. [DOI] [PubMed] [Google Scholar]
  13. Fontana F., Lanfredi M., Chicca M., Aiello V., Rossi R. Localization of the repetitive telomeric sequence (TTAGGG)n in four sturgeon species. Chromosome Res. 1998 Jun;6(4):303–306. doi: 10.1023/a:1009222908213. [DOI] [PubMed] [Google Scholar]
  14. Krieger J., Fuerst P. A., Cavender T. M. Phylogenetic relationships of the North American sturgeons (order Acipenseriformes) based on mitochondrial DNA sequences. Mol Phylogenet Evol. 2000 Jul;16(1):64–72. doi: 10.1006/mpev.1999.0743. [DOI] [PubMed] [Google Scholar]
  15. Leipoldt M. Towards an understanding of the molecular mechanisms regulating gene expression during diploidization in phylogenetically polyploid lower vertebrates. Hum Genet. 1983;65(1):11–18. doi: 10.1007/BF00285022. [DOI] [PubMed] [Google Scholar]
  16. Lento G. M., Hickson R. E., Chambers G. K., Penny D. Use of spectral analysis to test hypotheses on the origin of pinnipeds. Mol Biol Evol. 1995 Jan;12(1):28–52. doi: 10.1093/oxfordjournals.molbev.a040189. [DOI] [PubMed] [Google Scholar]
  17. Ludwig A., May B., Debus L., Jenneckens I. Heteroplasmy in the mtDNA control region of sturgeon (Acipenser, Huso and Scaphirhynchus). Genetics. 2000 Dec;156(4):1933–1947. doi: 10.1093/genetics/156.4.1933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nadeau J. H., Sankoff D. Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution. Genetics. 1997 Nov;147(3):1259–1266. doi: 10.1093/genetics/147.3.1259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ohno S., Muramoto J., Stenius C., Christian L., Kittrell W. A., Atkin N. B. Microchromosomes in holocephalian, chondrostean and holostean fishes. Chromosoma. 1969;26(1):35–40. doi: 10.1007/BF00319498. [DOI] [PubMed] [Google Scholar]
  20. Pagel M. D., Harvey P. H. Recent developments in the analysis of comparative data. Q Rev Biol. 1988 Dec;63(4):413–440. doi: 10.1086/416027. [DOI] [PubMed] [Google Scholar]
  21. Postlethwait J. H., Woods I. G., Ngo-Hazelett P., Yan Y. L., Kelly P. D., Chu F., Huang H., Hill-Force A., Talbot W. S. Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res. 2000 Dec;10(12):1890–1902. doi: 10.1101/gr.164800. [DOI] [PubMed] [Google Scholar]
  22. Postlethwait J. H., Yan Y. L., Gates M. A., Horne S., Amores A., Brownlie A., Donovan A., Egan E. S., Force A., Gong Z. Vertebrate genome evolution and the zebrafish gene map. Nat Genet. 1998 Apr;18(4):345–349. doi: 10.1038/ng0498-345. [DOI] [PubMed] [Google Scholar]
  23. Pyatskowit J. D., Krueger C. C., Kincaid H. L., May B. Inheritance of microsatellite loci in the polyploid lake sturgeon (Acipenser fulvescens). Genome. 2001 Apr;44(2):185–191. doi: 10.1139/g00-118. [DOI] [PubMed] [Google Scholar]
  24. Rico C., Rico I., Hewitt G. 470 million years of conservation of microsatellite loci among fish species. Proc Biol Sci. 1996 May 22;263(1370):549–557. doi: 10.1098/rspb.1996.0083. [DOI] [PubMed] [Google Scholar]
  25. Stoneking M., May B., Wright J. E. Loss of duplicate gene expression in salmonids: evidence for a null allele polymorphism at the duplicate aspartate aminotransferase loci in brook trout (Salvelinus fontinalis). Biochem Genet. 1981 Dec;19(11-12):1063–1077. doi: 10.1007/BF00484565. [DOI] [PubMed] [Google Scholar]
  26. Tagliavini J., Williot P., Congiu L., Chicca M., Lanfredi M., Rossi R., Fontana F. Molecular cytogenetic analysis of the karyotype of the European Atlantic sturgeon, Acipenser sturio. Heredity (Edinb) 1999 Nov;83(Pt 5):520–525. doi: 10.1038/sj.hdy.6886150. [DOI] [PubMed] [Google Scholar]

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