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Exon shuffling and the origin of the mitochondrial targeting function in plant cytochrome cl precursor (Long et al., 1995)

An article that illustrates the widespread presence of introns in the eukaryotic genes coding for mitochondrial genes. As well, they show through the existence of conserved introns/exons that the targeting information for the mitochondria has been derived from another protein. This is in line with a gradual evolution of nuclear genes that were targeted to organelles.

ABSTRACT Since most of the examples of “exon shuffling” are between vertebrate genes, the view is often expressed that exon shuffling is limited to the evolutionarily recent lineage of vertebrates. Although exon shuffling in plants has been inferred from the analysis of intron phases of plant genes [Long, M., Rosenberg, C. & Gilbert, W. (1995) Proc. Nati. Acad. Sci. USA 92, 12495-12499] and from the comparison of two functionally unknown sunflower genes [Domon, C. & Steinmetz, A. (1994) Mol. Gen. Genet. 244, 312-317], clear cases of exon shuffling in plant genes remain to be uncovered. Here, we report an example of exon shuffling in two important nucleus-encoded plant genes: cytosolic glyceraldehyde-3-phosphate dehydrogenase (cytosolic GAPDH or GapC) and cytochrome cl precursor. The intron-exon structures of the shuffled region indicate that the shuffling event took place at the DNA sequence level. In this case, we can establish a donor-recipient relationship for the exon shuffling. Three amino terminal exons of GapC have been donated to cytochrome ci, where, in a new protein environment, they serve as a source of the mitochondrial targeting function. This finding throws light upon an old important but unsolved question in gene evolution: the origin of presequences or transit peptides that generally exist in nucleus-encoded organelle genes.

This finding also shows a clear role for exon shuffling in the origin of presequences or transit peptides in the nuclearly encoded organellar proteins, as speculated previously (13, 14). Cytochrome cl is a nuclearly encoded enzyme in eukaryotes. Although the presequences of human and plant cytochrome cl are unrelated, the intron patterns suggest a common ancestral nuclear gene for the mature protein. Of five introns in this region of the two genes, one is identical in position (position 1), a second pair lies within two amino acids (position 2), and a third pair lies within five amino acids (position 3) (Fig. 2b). The intron patterns suggest the possibilities of a common ancestral nuclear gene or a common ancestral transfer from the mitochondrion to the nucleus. The ancestral cytochrome cl gene in plants must have been targeted to the mitochondrion; thus this targeting sequence was replaced in the line leading to the potato by the GapC gene. This replacement may have been selected by some advantage in using the GapC promoter.

Although the origin of the targeting sequence is clear, the initial function is not, since it does not seem to have a targeting function in the donor:

Does the donor shuffled sequence from GapC have an organelle targeting function? Although the shuffled sequence exists in all GAPDH genes, including GapA and GapB that are chloroplast-specific, both GapA and GapB have additional N-terminal elements, commonly believed to be responsible for the transit of the proteins to the organelle. Furthermore, GapC does not require organelle targeting because it functions in the cytosol. If some GapC were to occur in the mitochondrion, the “presequence” in the donor gene would have served as an organelle targeter. However, the existence of GapC proteins in an organelle has not been reported to date although GapC genes are probably of mitochondrial origin (25, 30), and the general belief is that all GapC is cytoplasmic. Thus we suggest that the donor shuffled sequence is important but not sufficient for organelle targeting activity.


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