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. 2000 Aug;155(4):1913–1926. doi: 10.1093/genetics/155.4.1913

Copy number lability and evolutionary dynamics of the Adh gene family in diploid and tetraploid cotton (Gossypium).

R L Small 1, J F Wendel 1
PMCID: PMC1461218  PMID: 10924485

Abstract

Nuclear-encoded genes exist in families of various sizes. To further our understanding of the evolutionary dynamics of nuclear gene families we present a characterization of the structure and evolution of the alcohol dehydrogenase (Adh) gene family in diploid and tetraploid members of the cotton genus (Gossypium, Malvaceae). A PCR-based approach was employed to isolate and sequence multiple Adh gene family members, and Southern hybridization analyses were used to document variation in gene copy number. Adh gene copy number varies among Gossypium species, with diploids containing at least seven Adh loci in two primary gene lineages. Allotetraploid Gossypium species are inferred to contain at least 14 loci. Intron lengths vary markedly between loci, and one locus has lost two introns usually found in other plant Adh genes. Multiple examples of apparent gene duplication events were observed and at least one case of pseudogenization and one case of gene elimination were also found. Thus, Adh gene family structure is dynamic within this single plant genus. Evolutionary rate estimates differ between loci and in some cases between organismal lineages at the same locus. We suggest that dynamic fluctuation in copy number will prove common for nuclear genes, and we discuss the implications of this perspective for inferences of orthology and functional evolution.

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Selected References

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  1. Biol M. C., Lenoir D., Hugueny I., Louisot P. Hormonal regulation of glycosylation process in rat small intestine: responsiveness of fucosyl-transferase activity to hydrocortisone during the suckling period, unresponsiveness after weaning. Biochim Biophys Acta. 1992 Jan 13;1133(2):206–212. doi: 10.1016/0167-4889(92)90070-r. [DOI] [PubMed] [Google Scholar]
  2. Chang C., Meyerowitz E. M. Molecular cloning and DNA sequence of the Arabidopsis thaliana alcohol dehydrogenase gene. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1408–1412. doi: 10.1073/pnas.83.5.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Charlesworth D., Liu F. L., Zhang L. The evolution of the alcohol dehydrogenase gene family by loss of introns in plants of the genus Leavenworthia (Brassicaceae). Mol Biol Evol. 1998 May;15(5):552–559. doi: 10.1093/oxfordjournals.molbev.a025955. [DOI] [PubMed] [Google Scholar]
  4. Clegg M. T., Cummings M. P., Durbin M. L. The evolution of plant nuclear genes. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7791–7798. doi: 10.1073/pnas.94.15.7791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cronn R. C., Small R. L., Wendel J. F. Duplicated genes evolve independently after polyploid formation in cotton. Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14406–14411. doi: 10.1073/pnas.96.25.14406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cronn R. C., Zhao X., Paterson A. H., Wendel J. F. Polymorphism and concerted evolution in a tandemly repeated gene family: 5S ribosomal DNA in diploid and allopolyploid cottons. J Mol Evol. 1996 Jun;42(6):685–705. doi: 10.1007/BF02338802. [DOI] [PubMed] [Google Scholar]
  7. Dennis E. S., Gerlach W. L., Pryor A. J., Bennetzen J. L., Inglis A., Llewellyn D., Sachs M. M., Ferl R. J., Peacock W. J. Molecular analysis of the alcohol dehydrogenase (Adh1) gene of maize. Nucleic Acids Res. 1984 May 11;12(9):3983–4000. doi: 10.1093/nar/12.9.3983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dennis E. S., Sachs M. M., Gerlach W. L., Finnegan E. J., Peacock W. J. Molecular analysis of the alcohol dehydrogenase 2 (Adh2) gene of maize. Nucleic Acids Res. 1985 Feb 11;13(3):727–743. doi: 10.1093/nar/13.3.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ellstrand N. C., Lee J. M., Foster K. W. Alcohol dehydrogenase isozymes in grain sorghum (Sorghum bicolor): evidence for a gene duplication. Biochem Genet. 1983 Feb;21(1-2):147–154. doi: 10.1007/BF02395398. [DOI] [PubMed] [Google Scholar]
  10. Eyre-Walker A., Gaut R. L., Hilton H., Feldman D. L., Gaut B. S. Investigation of the bottleneck leading to the domestication of maize. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4441–4446. doi: 10.1073/pnas.95.8.4441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Freeling M., Bennett D. C. Maize Adh1. Annu Rev Genet. 1985;19:297–323. doi: 10.1146/annurev.ge.19.120185.001501. [DOI] [PubMed] [Google Scholar]
  12. Frugoli J. A., McPeek M. A., Thomas T. L., McClung C. R. Intron loss and gain during evolution of the catalase gene family in angiosperms. Genetics. 1998 May;149(1):355–365. doi: 10.1093/genetics/149.1.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gaut B. S., Clegg M. T. Molecular evolution of the Adh1 locus in the genus Zea. Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5095–5099. doi: 10.1073/pnas.90.11.5095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gaut B. S., Morton B. R., McCaig B. C., Clegg M. T. Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10274–10279. doi: 10.1073/pnas.93.19.10274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gaut B. S., Peek A. S., Morton B. R., Clegg M. T. Patterns of genetic diversification within the Adh gene family in the grasses (Poaceae). Mol Biol Evol. 1999 Aug;16(8):1086–1097. doi: 10.1093/oxfordjournals.molbev.a026198. [DOI] [PubMed] [Google Scholar]
  16. Gottlieb L. D. Conservation and duplication of isozymes in plants. Science. 1982 Apr 23;216(4544):373–380. doi: 10.1126/science.216.4544.373. [DOI] [PubMed] [Google Scholar]
  17. Innan H., Tajima F., Terauchi R., Miyashita N. T. Intragenic recombination in the Adh locus of the wild plant Arabidopsis thaliana. Genetics. 1996 Aug;143(4):1761–1770. doi: 10.1093/genetics/143.4.1761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lander E. S., Green P., Abrahamson J., Barlow A., Daly M. J., Lincoln S. E., Newberg L. A., Newburg L. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics. 1987 Oct;1(2):174–181. doi: 10.1016/0888-7543(87)90010-3. [DOI] [PubMed] [Google Scholar]
  19. Loguercio L. L., Wilkins T. A. Structural analysis of a hmg-coA-reductase pseudogene: insights into evolutionary processes affecting the hmgr gene family in allotetraploid cotton (Gossypium hirsutum L.). Curr Genet. 1998 Oct;34(4):241–249. doi: 10.1007/s002940050393. [DOI] [PubMed] [Google Scholar]
  20. Miyashita N. T., Innan H., Terauchi R. Intra- and interspecific variation of the alcohol dehydrogenase locus region in wild plants Arabis gemmifera and Arabidopsis thaliana. Mol Biol Evol. 1996 Feb;13(2):433–436. doi: 10.1093/oxfordjournals.molbev.a025603. [DOI] [PubMed] [Google Scholar]
  21. Morton B. R., Gaut B. S., Clegg M. T. Evolution of alcohol dehydrogenase genes in the palm and grass families. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11735–11739. doi: 10.1073/pnas.93.21.11735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
  23. Osterman J. C., Dennis E. S. Molecular analysis of the ADH1-Cm allele of maize. Plant Mol Biol. 1989 Aug;13(2):203–212. doi: 10.1007/BF00016138. [DOI] [PubMed] [Google Scholar]
  24. Perry D. J., Furnier G. R. Pinus banksiana has at least seven expressed alcohol dehydrogenase genes in two linked groups. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13020–13023. doi: 10.1073/pnas.93.23.13020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pokorny R. M., Dietz A. B., Galandiuk S., Neibergs H. L. Improved resolution of asymmetric-PCR SSCP products. Biotechniques. 1997 Apr;22(4):606–608. doi: 10.2144/97224bm06. [DOI] [PubMed] [Google Scholar]
  26. Reinisch A. J., Dong J. M., Brubaker C. L., Stelly D. M., Wendel J. F., Paterson A. H. A detailed RFLP map of cotton, Gossypium hirsutum x Gossypium barbadense: chromosome organization and evolution in a disomic polyploid genome. Genetics. 1994 Nov;138(3):829–847. doi: 10.1093/genetics/138.3.829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rozas J., Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. doi: 10.1093/bioinformatics/15.2.174. [DOI] [PubMed] [Google Scholar]
  28. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  29. Sang T., Donoghue M. J., Zhang D. Evolution of alcohol dehydrogenase genes in peonies (Paeonia): phylogenetic relationships of putative nonhybrid species. Mol Biol Evol. 1997 Oct;14(10):994–1007. doi: 10.1093/oxfordjournals.molbev.a025716. [DOI] [PubMed] [Google Scholar]
  30. Small R. L., Ryburn J. A., Wendel J. F. Low levels of nucleotide diversity at homoeologous Adh loci in allotetraploid cotton (Gossypium L.). Mol Biol Evol. 1999 Apr;16(4):491–501. doi: 10.1093/oxfordjournals.molbev.a026131. [DOI] [PubMed] [Google Scholar]
  31. Small R. L., Ryburn J. A., Wendel J. F. Low levels of nucleotide diversity at homoeologous Adh loci in allotetraploid cotton (Gossypium L.). Mol Biol Evol. 1999 Apr;16(4):491–501. doi: 10.1093/oxfordjournals.molbev.a026131. [DOI] [PubMed] [Google Scholar]
  32. Sun H. W., Plapp B. V. Progressive sequence alignment and molecular evolution of the Zn-containing alcohol dehydrogenase family. J Mol Evol. 1992 Jun;34(6):522–535. doi: 10.1007/BF00160465. [DOI] [PubMed] [Google Scholar]
  33. Vieira C. P., Vieira J., Charlesworth D. Evolution of the cycloidea gene family in Antirrhinum and Misopates. Mol Biol Evol. 1999 Nov;16(11):1474–1483. doi: 10.1093/oxfordjournals.molbev.a026059. [DOI] [PubMed] [Google Scholar]
  34. Wendel J. F. New World tetraploid cottons contain Old World cytoplasm. Proc Natl Acad Sci U S A. 1989 Jun;86(11):4132–4136. doi: 10.1073/pnas.86.11.4132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wendel J. F., Schnabel A., Seelanan T. Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):280–284. doi: 10.1073/pnas.92.1.280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wolfe K. H., Li W. H., Sharp P. M. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9054–9058. doi: 10.1073/pnas.84.24.9054. [DOI] [PMC free article] [PubMed] [Google Scholar]

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