Alternate use of divergent forms of an ancient exon in the fructose-1,6-bisphosphate aldolase gene of Drosophila melanogaster.

Abstract

The fructose-1,6-bisphosphate aldolase gene of Drosophila melanogaster contains three divergent copies of an evolutionarily conserved 3' exon. Two mRNAs encoding aldolase contain three exons and differ only in the poly(A) site. The first exon is small and noncoding. The second encodes the first 332 amino acids, which form the catalytic domain, and is homologous to exons 2 through 8 of vertebrates. The third exon encodes the last 29 amino acids, thought to control substrate specificity, and is homologous to vertebrate exon 9. A third mRNA substitutes a different 3' exon (4a) for exon 3 and encodes a protein very similar to aldolase. A fourth mRNA begins at a different promoter and shares the second exon with the aldolase messages. However, two exons, 3a and 4a, together substitute for exon 3. Like exon 4a, exon 3a is homologous to terminal aldolase exons. The exon 3a-4a junction is such that exon 4a would be translated in a frame different from that which would produce a protein with similarity to aldolase. The putative proteins encoded by the third and fourth mRNAs are likely to be aldolases with altered substrate specificities, illustrating alternate use of duplicated and diverged exons as an evolutionary mechanism for adaptation of enzymatic activities.Fructose-1,6-bisphosphate (FBP) aldolase (EC 4.1.2.13) is a glycolytic enzyme that catalyzes reversible aldol cleavage of FBP to glyceraldehyde-3-phosphate and dihydroxyacetone phosphate. Aldolases from vertebrates, plants, microorganisms, and Drosophila spp. have been characterized (17). The enzymes from higher eukaryotes, including Drosophila spp., are type I aldolases, which function as tetramers and form a Schiffs base between the substrate and an active-site lysine residue. In vertebrates, three isozymes, A, B, and C, are expressed in different tissues. The Drosophila enzyme displays 60 to 70% sequence identity with the mammalian enzymes and is most related to the type A muscle forms (27). Drosophila enzyme subunits (39 kDa) can form functional heterotetramers with certain mammalian enzymes (4), indicating a high degree of functional conservation.Several mammalian aldolase genes (5,19,21,38,42,43) and a chicken aldolase gene (6) have been characterized, revealing close structural relationships between the genes encoding the different isozymes within a species and between the genes encoding equivalent isozymes in different species. The intron-exon organization is identical in all characterized vertebrate genes.In this report, we describe the organization of the aldolase gene of Drosophila melanogaster, which shares structural features with the vertebrate genes. The Drosophila gene appears unique in that it produces transcripts with alternate 3' ends, including one with two exons substituted for the terminal exon of the aldolase-encoding mRNAs. All terminal exons are related evolutionarily to the terminal exons of vertebrate aldolase-encoding mRNAs. The unique mRNAs, if translated, could produce aldolase-related proteins that * Corresponding author.contain th...

An Estimate of Divergence Time of Parazoa and Eumetazoa and That of Cephalochordata and Vertebrata by Aldolase and Triose Phosphate Isomerase Clocks

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Drosophila Nipped-B Protein Supports Sister Chromatid Cohesion and Opposes the Stromalin/Scc3 Cohesion Factor To Facilitate Long-Range Activation of the cut Gene

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