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En Bloc Duplications, Mutation Rates, and Densities of Amino Acid Changes Clarify the Evolution of Vertebrate α-1,3/4-Fucosyltransferases

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Abstract

Numerous vertebrates have four α-1,3/4-fucosyltransferase genes (FUT9, FUT7, FUT4, and FUT Lewis) belonging to the same family. Until now, studies on the evolution of this family have mainly focused on Lewis genes but how the other α-1,3/4-fucosyltransferases have emerged from a common ancestor is not well known. In order to define the respective roles of duplications and mutations, we have compared amino acid sequences representative of bony fish (Takifugu rubripes), amphibians (Xenopus laevis), birds (Gallus gallus), and mammals (Bos taurus). The FUT tree has two fundamental branches, each split into two subfamilies. We found evidence for two duplication events, dated around 710–760 Myr and 590–640 Myr, respectively, compatible with the hypothesis of two rounds of whole genome duplications in chordate genomes, before the emergence of bony vertebrates. Based on the Homo sapiens (human) physical map, we identified blocks of paralogues belonging to regions of FUT9 (6q16), FUT4 (11q21), FUT7 (9q34), and FUT Lewis (19p13) and to a region on HSA1p that is devoid of any FUT. In zebrafish (Danio rerio), an orthologue region of HSA1 harbors an FUT9 specific to bony fish, showing that duplications are not restricted to a single FUT gene but involve blocks of paralogues. In addition, sets of genes within each block clarify the order of duplication events and, as a result, the order of α-1,3/4-fucosyltransferase gene emergence. We have also determined the mutation rates and the density of amino acid changes along protein sequences in each α-1,3/4-fucosyltransferase subfamily during the main vertebrate transitions. After the emergence of tetrapods, the mutation rate of FUT9 decreased dramatically, suggesting the early acquisition of a crucial fucosyltransferase activity in the first stages of development. The FUT7 mutation rate, which in tetrapod ancestors is about half that in amniote ancestors, may be related to the role of this gene in immune systems. In contrast to other subfamilies, we found a constant mutation rate in FUT Lewis and a rather homogeneous amino acid density change, independently of the vertebrate transition, suggesting that hitherto Lewis epitopes have dispensable functions.

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Ackowledgments

This work was supported by grants from the Conseil Regional du Limousin. Thanks are due to Dr. Naoko Takezaki for his help in running the Lintree program. We thank Pr. Véronique Blanquet for helpful comments.

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  1. INRA, UMR 1061, Université de Limoges, 123 avenue Albert Thomas, Limoges, F-87060, GDR CNRS 2590, France

    Daniel Petit, Abderrahman Maftah, Raymond Julien & Jean-Michel Petit

  2. Faculté des Sciences et Techniques, 123 avenue Albert Thomas, 87060, Limoges cedex, France

    Daniel Petit, Abderrahman Maftah, Raymond Julien & Jean-Michel Petit

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  1. Daniel Petit
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  2. Abderrahman Maftah
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Correspondence to Jean-Michel Petit.

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Petit, D., Maftah, A., Julien, R. et al. En Bloc Duplications, Mutation Rates, and Densities of Amino Acid Changes Clarify the Evolution of Vertebrate α-1,3/4-Fucosyltransferases. J Mol Evol 63, 353–364 (2006). https://doi.org/10.1007/s00239-005-0189-x

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