Summary
The maintenance of a proper distribution of charged amino acid residues might be expected to be an important factor in protein evolution. We therefore compared the inferred changes in charge during the evolution of 43 protein families with the changes expected on the basis of random base substitutions. It was found that certain proteins, like the eye lens crystallins and most histones, display an extreme avoidance of changes in charge. Other proteins, like phospholipase A2 and ferredoxin, apparently have sustained more charged replacements than expected, suggesting a positive selection for changes in charge. Depending on function and structure of a protein, charged residues apparently can be important targets for selective forces in protein evolution. It appears that actual biased codon usage tends to decrease the proportion of charged amino acid replacements. The influence of nonrandomness of mutations is more equivocal. Genes that use the mitochondrial instead of the universal code lower the probability that charge changes will occur in the encoded proteins.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Barlow DJ, Thornton JM (1983) Ion-pairs in proteins. J Mol Biol 168:867–885
Bernardi G, Mouchiroud D, gautier C, Bernardi G (1988) Compositional patterns in vertebrate genomes: conservation and change in evolution. J Mol Evol 28:7–18
Blundell TL, Sibanda MJ, Sternberg MJE, Thornton JM (1987) Knowledge-based prediction of protein structures and the design of novel molecules. Nature 326:347–352
Clarke B (1970) Selective constraints on amino-acid substitutions during evolution of proteins. Nature 228:159–160
Dayhoff MO, Park CM, McLaughlin PJ (1972) Building a phylogenetic tree: cytochromec. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5. National Biomedical Research Foundation, Washington DC, pp 7–16
Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in proteins. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, Suppl 3. National Biomedical Research Foundation, Washington DC
Delaye M, Tardieu A (1983) Short-range order of crystallinproteins accounts for eye lens transparency. Nature 302:415–417
Dickerson RE (1971) The structure of cytochromec and the rates of molecular evolution. J Mol Evol 1:26–45
Doolittle RF (1979) Protein evolution. In: Neurath H, Hill RL (eds) The proteins, ed 2, vol 4. Academic Press, New York, pp 1–118
Grantham R (1974) Amino acid difference formula to help explain protein evolution. Science 185:862–864
Grantham R, Perrin P, Mouchiroud D (1986) In: Dawkins R, Ridley M (eds) Oxford surveys in evolutionary biology, vol 3, Oxford University Press, Oxford
Honig BB, Hubbell WL, Flewelling RF (1986) Electrostatic interactions in membranes and proteins. Annu Rev Biophys Biophys Chem 15:163–193
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
Kornberg RD (1977) Structure of chromatin. Annu Rev Biochem 46:931–954
Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132
Li W-H, Wu C-I, Luo C-C (1984) Nonrandomness of point mutation as reflected in nucleotide substitutions in pseudogenes and its evolutionary implications. J Mol Evol 21:58–71
Lipman DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227:1435–1441
Maruyama T, Gojobori T, Aota SI, Ikemura T (1986) Codon usage tabulated from the GenBank genetic sequence data. Nucleic Acids Res 14:r151-r153
Matthews JB (1985) Electrostatic effects in proteins. Annu Rev Biophys Biophys Chem 14:387–417
Miller S, Janin J, Lesk AM, Chothia C (1987) Interior and surface of monometric proteins. J Mol Biol 196:641–656
Nei M (1975) Molecular population genetics and evolution. North-Holland Publishing Company, Amsterdam, p 25
Ohno S (1970) Evolution by gene duplication. Springer-Verlag, New York
Peetz EW, Thomson G, Hedrick PW (1986) Charge changes in protein evolution. Mol Biol Evol 3:84–94
Perrin P, Bernardi G (1987) Directional fixation of mutations in vertebrate evolution. J Mol Evol 26:301–310
Perutz MF (1978) Electrostatic effects in proteins. Science 201:1187–1191
Peterson CA, Piatigorsky J (1986) Preferential conservation of the globular domains of the βA3/A1-crystallin polypeptide of the chicken eye lens. Differentiation 19:134–153
Preparata G, Saccone C (1987) A simple quantitative model of the molecular clock. J Mol Evol 26:7–15
Rose GD, Geselowitz AR, Lesser GJ, Lee RH, Zehfus MH (1985) Hydrophobicity of amino acid residues in globular proteins. Science 229:834–838
Sharp PM, Cowe E, Higgins DG, Shields DC, Wolfe KH, Wright F (1988) Codon usage patterns inEscherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster andHomo sapiens; a review of the considerable within-species diversity. Nucleic Acids Res 16:8207–8211
Slingsby C (1985) Structural variation in lens crystallins. Trends Biochem Sci 10:281–284
Slingsby C, Driessen HPC, Mahadevan D, Bax B, Blundell TL (1988) Evolutionary and functional relationships between the basic and acidic β-crystallins. Exp Eye Res 46:375–403
Stapel SO, Zweers A, Dodemont HJ, Kan JH, de Jong WW (1985) ε-crystallin, a novel avian and reptilian eye lens protein. Eur J Biochem 147:129–136
Sternberg MJE, Hayes FRF, Russell AJ, Thomas PG, Fersht AR (1987) Prediction of electrostatic effects of engineering of protein charges. Nature 330:86–88
Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85:2653–2657
Summers LJ, Slingsby C, Blundell TL, den Dunnen JT, Moormann RJM, Schoenmakers JGG (1986) Structural variation in mammalian γ-crystallins based on computer graphics analyses of human, rat and calf sequences. I. Core packing and surface properties. Exp Eye Res 43:77–92
Tardieu A, Laporte D, Licinio P, Krop B, Delaye M (1986) Calf lens α-crystallin quaternary structure. A three-layer tetrahedral model. J Mol Biol 192:711–724
Tomazic SJ, Klibanov AM (1988) Why is oneBacillus α-amylase more resistant against irreversible thermoinactivation than another? J Biol Chem 263:3092–3096
Vogel H, Zuckerkandl E (1971) The evolution of polarity relations in globins. In: Neyman J (ed) Proceedings of the Sixth Berkeley Symposium on Mathematical Statistics and Probability, vol 5, Darwinian, neo-Darwinian, and non-Darwinian evolution. University of California Press, Berkeley, pp 155–176
Wada A, Nakamura H (1981) Nature of the charge distribution in proteins. Nature 293:757–758
Waite M (1988) The phospholipases. In: Hanahan DJ (ed) Handbook of lipid research, vol. 5. Plenum, New York
Warshel A, Russell ST (1984) Calculations of electrostatic interactions in biological systems and in solutions. Q Rev Biophys 17:283–422
Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639
Zuckerkandl E (1975) The appearance of new structures and functions in proteins during evolution. J Mol Evol 7:1–57
Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–116
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Leunissen, J.A.M., van den Hooven, H.W. & de Jong, W.W. Extreme differences in charge changes during protein evolution. J Mol Evol 31, 33–39 (1990). https://doi.org/10.1007/BF02101790
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02101790