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Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey

Nature Genetics volume 30, pages 411–415 (2002)Cite this article

Abstract

Although the complete genome sequences of over 50 representative species have revealed the many duplicated genes in all three domains of life1,2,3,4, the roles of gene duplication in organismal adaptation and biodiversity are poorly understood. In addition, the evolutionary forces behind the functional divergence of duplicated genes are often unknown, leading to disagreement on the relative importance of positive Darwinian selection versus relaxation of functional constraints in this process5,6,7,8,9,10. The methodology of earlier studies relied largely on DNA sequence analysis but lacked functional assays of duplicated genes, frequently generating contentious results11,12. Here we use both computational and experimental approaches to address these questions in a study of the pancreatic ribonuclease gene (RNASE1) and its duplicate gene (RNASE1B) in a leaf-eating colobine monkey, douc langur. We show that RNASE1B has evolved rapidly under positive selection for enhanced ribonucleolytic activity in an altered microenvironment, a response to increased demands for the enzyme for digesting bacterial RNA. At the same time, the ability to degrade double-stranded RNA, a non-digestive activity characteristic of primate RNASE1, has been lost in RNASE1B, indicating functional specialization and relaxation of purifying selection. Our findings demonstrate the contribution of gene duplication to organismal adaptation and show the power of combining sequence analysis and functional assays in delineating the molecular basis of adaptive evolution.

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Figure 1: Protein sequences and genomic structures of RNASE1 and RNASE1B of primates.
Figure 2: Phylogenetic relationships among RNASE1 and RNASE1B of primates.
Figure 3: Tests of the molecular clock hypothesis for RNASE1 and RNASE1B of douc langur.
Figure 4: Enzyme activities of recombinant RNASE1B, RNASE1 and mutant forms of RNASE1.

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References

  1. Tomb, J.F. et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539–547 (1997).

    Article  CAS  Google Scholar 

  2. Makarova, K.S. et al. Comparative genomics of the Archaea (Euryarchaeota): evolution of conserved protein families, the stable core, and the variable shell. Genome Res. 9, 608–628 (1999).

    CAS  PubMed  Google Scholar 

  3. Rubin, G.M. et al. Comparative genomics of the eukaryotes. Science 287, 2204–2215 (2000).

    Article  CAS  Google Scholar 

  4. Gaudieri, S., Kulski, J.K., Dawkins, R.L. & Gojobori, T. Different evolutionary histories in two subgenomic regions of the major histocompatibility complex. Genome Res. 9, 541–549 (1999).

    CAS  PubMed  Google Scholar 

  5. Ohno, S. Ancient linkage groups and frozen accidents. Nature 244, 259–262 (1973).

    Article  Google Scholar 

  6. Goodman, M., Moore, G.W. & Matsuda, G. Darwinian evolution in the genealogy of haemoglobin. Nature 253, 603–608 (1975).

    Article  CAS  Google Scholar 

  7. Li, W.H. & Gojobori, T. Rapid evolution of goat and sheep globin genes following gene duplication. Mol. Biol. Evol. 1, 94–108 (1983).

    CAS  PubMed  Google Scholar 

  8. Kimura, M. The Neutral Theory of Molecular Evolution. (Cambridge University Press, Cambridge, 1983).

    Book  Google Scholar 

  9. Zhang, J., Rosenberg, H.F. & Nei, M. Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc. Natl Acad. Sci. USA 95, 3708–3713 (1998).

    Article  CAS  Google Scholar 

  10. Hughes, A.L. Adaptive Evolution of Genes and Genomes (Oxford University Press, New York, 1999).

    Google Scholar 

  11. Brookfield, J.F. & Sharp, P.M. Neutralism and selectionism face up to DNA data. Trends Genet. 10, 109–111 (1994).

    Article  CAS  Google Scholar 

  12. Charlesworth, B., Charlesworth, D., Nurminsky, D.I. & Hartl, D.L. How was the Sdic gene fixed? Nature 400, 519–520 (1999).

    Article  CAS  Google Scholar 

  13. Kay, R.N.B. & Davies, A.G. in Colobinem Monkeys: Their Ecology, Behaviour and Evolution (eds Davies, A.G. & Oates, J.F.) 229–250 (Cambridge University Press, Cambridge, 1994).

    Google Scholar 

  14. Barnard, E.A. Biological function of pancreatic ribonuclease. Nature 221, 340–344 (1969).

    Article  CAS  Google Scholar 

  15. Beintema, J.J. The primary structure of langur (Presbytis entellus) pancreatic ribonuclease: adaptive features in digestive enzymes in mammals. Mol. Biol. Evol. 7, 470–477 (1990).

    CAS  PubMed  Google Scholar 

  16. Goodman, M. et al. Toward a phylogenetic classification of primates based on DNA evidence complemented by fossil evidence. Mol. Phylogenet. Evol. 9, 585–598 (1998).

    Article  CAS  Google Scholar 

  17. Fitch, W.M. Toward defining the course of evolution: minimum change for a specific tree topology. Syst. Zool. 20, 406–416 (1971).

    Article  Google Scholar 

  18. Zhang, J. & Nei, M. Accuracies of ancestral amino acid sequences inferred by parsimony, likelihood, and distance methods. J. Mol. Evol. 44, S139–S146 (1997).

    Article  CAS  Google Scholar 

  19. Tajima, F. Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135, 599–607 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Delsen, E. in Colobine Monkeys: Their Ecology, Behaviour and Evolution (eds Davies, A.G. & Oates, J.F.) 11–44 (Cambridge University Press, Cambridge, 1994).

    Google Scholar 

  21. Li, W.H. Molecular Evolution 221–224 (Sinauer Associates, Sunderland, Massachusetts, 1997).

    Google Scholar 

  22. Zhang, J. Rates of conservative and radical nonsynonymous nucleotide substitutions in mammalian nuclear genes. J. Mol. Evol. 50, 56–68 (2000).

    Article  CAS  Google Scholar 

  23. Sorrentino, S. & Libonati, M. Structure-function relationships in human ribonucleases: main distinctive features of the major RNase types. FEBS Lett. 404, 1–5 (1997).

    Article  CAS  Google Scholar 

  24. Guyton, A.C. & Hall, J.E. Textbook of Medical Physiology 9th edn (Saunders, London, 1996).

    Google Scholar 

  25. Code, C.F. Handbook of Physiology Vol. III (American Physiological Association, Washington DC, 1968).

    Google Scholar 

  26. Futami, J. et al. Tissue-specific expression of pancreatic-type RNases and RNase inhibitor in humans. DNA Cell Biol. 16, 413–419 (1997).

    Article  CAS  Google Scholar 

  27. Hughes, A.L. The evolution of functionally novel proteins after gene duplication. Proc. R. Soc. Lond. B Biol. Sci. 256, 119–124 (1994).

    Article  CAS  Google Scholar 

  28. Lynch, M. & Force, A. The probability of duplicate gene preservation by subfunctionalization. Genetics 154, 459–473 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120 (1980).

    Article  CAS  Google Scholar 

  30. Rooney, A.P. & Zhang, J. Rapid evolution of a primate sperm protein: relaxation of functional constraint or positive Darwinian selection? Mol. Biol. Evol. 16, 706–710 (1999).

    Article  CAS  Google Scholar 

  31. Zhang, J., Kumar, S. & Nei, M. Small-sample tests of episodic adaptive evolution: a case study of primate lysozyme genes. Mol. Biol. Evol. 14, 1335–1338 (1997).

    Article  CAS  Google Scholar 

  32. Rosenberg, H.F. & Dyer, K.D. Eosinophil cationic protein and eosinophil-derived neurotoxin. Evolution of novel function in a primate ribonuclease gene family. J. Biol. Chem. 270, 21539–21544 (1995).

    Article  CAS  Google Scholar 

  33. Libonati, M. & Floridi, A. Breakdown of double-stranded RNA by bull semen ribonuclease. Eur. J. Biochem. 8, 81–87 (1969).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank K. Dyer for technical assistance and J. Beintema, A. Rooney and three anonymous referees for their comments on early versions of the manuscript. This work was supported in part by a start-up fund and a Rackham grant from the University of Michigan (to J.Z.) and grants from the Natural Science Foundation of China and Chinese Academy of Sciences (to Y.P.Z.).

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Authors and Affiliations

  1. Laboratory of Host Defenses, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA

    Jianzhi Zhang & Helene F. Rosenberg

  2. Departments of Ecology and Evolutionary Biology and Molecular, Cellular and Developmental Biology, University of Michigan, 3003 Natural Sciences Building, 830 North University Avenue, Ann Arbor, 48109, Michigan, USA

    Jianzhi Zhang

  3. Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China

    Ya-ping Zhang

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  1. Jianzhi Zhang
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Correspondence to Jianzhi Zhang.

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Zhang, J., Zhang, Yp. & Rosenberg, H. Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey. Nat Genet 30, 411–415 (2002). https://doi.org/10.1038/ng852

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