Restricted access
A comparative analysis of the evolutionary relationship between diet and enzyme targeting in bats, marsupials and other mammals
Published:22 April 2005https://doi.org/10.1098/rspb.2004.3011
Abstract
The subcellular distribution of the enzyme alanine : glyoxylate aminotransferase (AGT) in the livers of different mammals appears to be related to their natural diets. Thus, AGT tends to be mitochondrial in carnivores, peroxisomal in herbivores, and both mitochondrial and peroxisomal in omnivores. To what extent this relationship is an incidental consequence of phylogenetic structure or an evolutionarily meaningful adaptive response to changes in dietary selection pressure is unknown. In order to distinguish between these two possibilities, we have determined the subcellular distribution of AGT in the livers of 22 new mammalian species, including members of three orders not studied before. In addition, we have analysed the statistical relationship between AGT distribution and diet in all 77 mammalian species, from 12 different orders, for which the distribution is currently known. Our analysis shows that there is a highly significant correlation between AGT distribution and diet, independent of phylogeny. This finding is compatible with the suggestion that the variable intracellular targeting of AGT is an adaptive response to episodic changes in dietary selection pressure. To our knowledge, this is the first example of such a response being manifested at the molecular and cellular levels across the breadth of Mammalia.
References
-
Bininda-Emonds O.R.P, Gittleman J.L& Purvis A . 1999 Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol. Rev. 74, 143–175. Crossref, PubMed, Web of Science, Google Scholar -
Birdsey G.M& Danpure C.J . 1998 Evolution of alanine : glyoxylate aminotransferase intracellular targeting. Structural and functional analysis of the guinea pig gene. Biochem. J. 331, 49–60. Crossref, PubMed, Web of Science, Google Scholar -
Birdsey G.M, Lewin J, Cunningham A, Bruford M.W& Danpure C.J . 2004 Differential enzyme targeting as an evolutionary adaptation to herbivory in carnivora. Mol. Biol. Evol. 21, 632–646. Crossref, PubMed, Web of Science, Google Scholar -
Danpure C.J . 1997 Variable peroxisomal and mitochondrial targeting of alanine:glyoxylate aminotransferase in mammalian evolution and disease. Bioessays. 19, 317–326. Crossref, PubMed, Web of Science, Google Scholar -
Danpure C.J Primary hyperoxaluria. The molecular and metabolic bases of inherited disease, Scriver C.R, 8th edn 2001pp. 3323–3367. Eds. New York:McGraw-Hill. Google Scholar -
Danpure C.J, Guttridge K.M, Fryer P, Jennings P.R, Allsop J& Purdue P.E . 1990 Subcellular distribution of hepatic alanine : glyoxylate aminotransferase in various mammalian species. J. Cell. Sci. 97, 669–678. Crossref, PubMed, Web of Science, Google Scholar -
Danpure C.J, Fryer P, Jennings P.R, Allsop J, Griffiths S& Cunningham A . 1994 Evolution of alanine : glyoxylate aminotransferase 1 peroxisomal and mitochondrial targeting. A survey of its subcellular distribution in the livers of various representatives of the classes Mammalia, Aves and Amphibia. Eur. J. Cell Biol. 64, 295–313. PubMed, Web of Science, Google Scholar -
Felsenstein J . 1985 Phylogenies and the comparative method. Am. Nat. 125, 1–15. Crossref, Web of Science, Google Scholar -
Holbrook J.D& Danpure C.J . 2002 Molecular basis for the dual mitochondrial and cytosolic localization of alanine : glyoxylate aminotransferase in amphibian liver cells. J. Biol. Chem. 277, 2336–2344. Crossref, PubMed, Web of Science, Google Scholar -
Holbrook J.D, Birdsey G.M, Yang Z, Bruford M.W& Danpure C.J . 2000 Molecular adaptation of alanine : glyoxylate aminotransferase targeting in primates. Mol. Biol. Evol. 17, 387–400. Crossref, PubMed, Web of Science, Google Scholar -
Huchon D, Madsen O, Sibbald M.J, Ament K, Stanhope M.J, Catzeflis F, de Jong W.W& Douzery E.J . 2002 Rodent phylogeny and a timescale for the evolution of Glires: evidence from an extensive taxon sampling using three nuclear genes. Mol. Biol. Evol. 19, 1053–1065. Crossref, PubMed, Web of Science, Google Scholar -
Ichiyama A, 2000 Oxalate synthesis in mammals: properties and subcellular distribution of serine : pyruvate/alanine : glyoxylate aminotransferase in the liver. Mol. Urol. 4, 333–340. PubMed, Google Scholar -
Jones K.E, Purvis A, MacLarnon A, Bininda-Emonds O.R& Simmons N.B . 2002 A phylogenetic supertree of bats (Mammalia: Chiroptera). Biol. Rev. 77, 223–259. Crossref, PubMed, Web of Science, Google Scholar -
Lewin J, Dhillon A.P, Sim R, Mazure G, Pounder R.E& Wakefield A.J . 1995 Persistent measles virus infection of the intestine: confirmation by immunogold electron microscopy. Gut. 36, 564–569. Crossref, PubMed, Web of Science, Google Scholar -
Lister A.M . 2004 The impact of the quaternary ice ages on mammalian evolution. Phil. Trans. R. Soc. B. 359, 221–242. Link, Web of Science, Google Scholar -
Lumb M.J, Purdue P.E& Danpure C.J . 1994 Molecular evolution of alanine/glyoxylate aminotransferase 1 intracellular targeting: analysis of the feline gene. Eur. J. Biochem. 221, 53–62. Crossref, PubMed, Google Scholar -
Lumb M.J, Drake A.F& Danpure C.J . 1999 Effect of N-terminal alpha helix formation on the dimerization and intracellular targeting of alanine : glyoxylate aminotransferase. J. Biol. Chem. 274, 20 587–20 596. Crossref, Web of Science, Google Scholar -
Messier W& Stewart C.B . 1997 Episodic adaptive evolution of primate lysozymes. Nature. 385, 151–154. Crossref, PubMed, Web of Science, Google Scholar -
Mori M, Oda T, Nishiyama K, Serikawa T, Yamada J& Ichiyama A . 1992 A single serine:pyruvate aminotransferase gene on rat chromosome 9q34–q36. Genomics. 13, 686–689. Crossref, PubMed, Web of Science, Google Scholar -
Noguchi T Amino acid metabolism in animal peroxisomes. Peroxisomes in biology and medicine, Fahimi H.D& Sies H . 1987pp. 234–243. Eds. Berlin:Springer. Crossref, Google Scholar -
Nowak R.M Walker's mammals of the world. 5th edn. 1991 Baltimore:John Hopkins University Press. Google Scholar -
Oatey P.B, Lumb M.J& Danpure C.J . 1996 Molecular basis of the variable mitochondrial and peroxisomal localisation of alanine : glyoxylate aminotransferase. Eur. J. Biochem. 241, 374–385. Crossref, PubMed, Google Scholar -
Oda T, Yanagisawa M& Ichiyama A . 1982 Induction of serine : pyruvate aminotransferase in rat liver organelles by glucagon and a high-protein diet. J. Biochem. (Tokyo). 91, 219–232. Crossref, PubMed, Web of Science, Google Scholar -
Oda T, Miyajima H, Suzuki Y& Ichiyama A . 1987 Nucleotide sequence of the cDNA encoding the precursor for mitochondrial serine : pyruvate aminotransferase of rat liver. Eur. J. Biochem. 168, 537–542. Crossref, PubMed, Google Scholar -
Oda T, Funai T& Ichiyama A . 1990 Generation from a single gene of two mRNAs that encode the mitochondrial and peroxisomal serine : pyruvate aminotransferase of rat liver. J. Biol. Chem. 265, 7513–7519. Crossref, PubMed, Web of Science, Google Scholar -
Osborne M.J, Christidis L& Norman J.A . 2002 Molecular phylogenies of the Diprotodontia (kangaroos, wombats, koala, possums, and allies). Mol. Phylogenet. Evol. 25, 219–228. Crossref, PubMed, Web of Science, Google Scholar -
Pagel M . 1997 Inferring evolutionary processes from phylogenies. Zool. Scr. 26, 331–348. Crossref, Web of Science, Google Scholar -
Pagel M . 1999 Inferring the historical patterns of biological evolution. Nature. 401, 877–884. Crossref, PubMed, Web of Science, Google Scholar -
Purdue P.E, Takada Y& Danpure C.J . 1990 Identification of mutations associated with peroxisome-to-mitochondrion mistargeting of alanine/glyoxylate aminotransferase in primary hyperoxaluria type 1. J. Cell. Biol. 111, 2341–2351. Crossref, PubMed, Web of Science, Google Scholar -
Purdue P.E, Lumb M.J, Fox M, Griffo G, Hamon Benais C, Povey S& Danpure C.J . 1991 Characterization and chromosomal mapping of a genomic clone encoding human alanine : glyoxylate aminotransferase. Genomics. 10, 34–42. Crossref, PubMed, Web of Science, Google Scholar -
Purdue P.E, Lumb M.J& Danpure C.J . 1992 Molecular evolution of alanine : glyoxylate aminotransferase 1 intracellular targeting. Analysis of the marmoset and rabbit genes. Eur. J. Biochem. 207, 757–766. Crossref, PubMed, Google Scholar -
Purvis A . 1995 A composite estimate of primate phylogeny. Phil. Trans. R. Soc. B. 348, 405–421. Link, Web of Science, Google Scholar -
Purvis A& Rambaut A . 1995 Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comput. Appl. Biosci. 11, 247–251. PubMed, Google Scholar -
Springer M.S, Murphy W.J, Eizirik E& O'Brien S.J . 2003 Placental mammal diversification and the cretaceous–tertiary boundary. Proc. Natl Acad. Sci. USA. 100, 1056–1061. Crossref, PubMed, Web of Science, Google Scholar -
Stewart C.B, Schilling J.W& Wilson A.C . 1987 Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature. 330, 401–404. Crossref, PubMed, Web of Science, Google Scholar -
Takada Y, Kaneko N, Esumi H, Purdue P.E& Danpure C.J . 1990 Human peroxisomal l-alanine : glyoxylate aminotransferase. Evolutionary loss of a mitochondrial targeting signal by point mutation of the initiation codon. Biochem. J. 268, 517–520. Crossref, PubMed, Web of Science, Google Scholar -
Takayama T, Fujita K, Suzuki K, Sakaguchi M, Fujie M, Nagai E, Watanabe S, Ichiyama A& Ogawa Y . 2003 Control of oxalate formation from l-hydroxyproline in liver mitochondria. J. Am. Soc. Nephrol. 14, 939–946. Crossref, PubMed, Web of Science, Google Scholar
