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in Arabidopsis (Sanchez et al., 1996; Unseld et al., 1997; Marienfeld et al., 1999). In some cases, weak hybridization by a probe was observed to DNA from a species known to contain only a fragment of a gene in the mitochondrion (e.g., rps12 in Oenothera).

The hybridization results show that ribosomal protein gene content in angiosperm mitochondrial genomes varies considerably, as suggested previously (Nugent and Palmer, 1993; Unseld et al., 1997), although the magnitude of the variation and frequency of gene loss are unexpectedly high. The high number of ribosomal protein gene losses compared with the low number of respiratory gene losses is also striking. In some angiosperm lineages, the rate of ribosomal protein gene loss appears to be comparable to, or even higher than, the silent substitution rate (K.A., Y.-L.Q., and J.D.P., unpublished work), whereas in many other lineages, including the most ancient ones, there has been no loss at all. These latter lineages have retained all 14 ribosomal proteins that were present in the common ancestor of angiosperms, whereas several fairly recently arisen angiosperm lineages have lost 10 or more of the 14 genes (in one case, apparently all 14). The rate of ribosomal protein gene loss thus varies enormously across angiosperms lineages; some factor(s) must have triggered a rapid rate of loss in certain recent lineages.

The mt gene losses detected by our survey could be explained by functional transfer of the gene to the nucleus, by functional substitution by another protein (see, e.g., Sanchez et al., 1996), or by the protein being dispensable in certain plants. Six ribosomal protein genes (Grohmann et al., 1992; Wischmann and Schuster, 1995; Kadowaki et al., 1996; Sanchez et al., 1996; Perrotta et al., 1998; Figueroa et al., 1999a; Kubo et al., 1999) that are present in the mitochondrion of many flowering plants, along with the respiratory gene cox2 (Nugent and Palmer, 1991, 1993; Covello and Gray, 1992; Adams et al., 1999), have been reported to have been transferred to the nucleus. Thus, the most likely explanation for loss of a gene from the mitochondrion is transfer to the nucleus.

DO MULTIPLE GENE LOSSES REFLECT MULTIPLE GENE TRANSFERS?

Assuming that most of the genes lost from the mitochondrion have been transferred to the nucleus, then the many separate losses of each mt ribosomal protein gene and of sdh4 could reflect either an equivalent number of separate transfers, each more or less coincident in time with the loss, or a smaller number of earlier transfers (as few as one for each gene), with several or all losses stemming from the same ancestral transfer of a particular gene. The latter, early-transfer/multiple-dependent-loss model predicts a prolonged period of retention of dual intact and



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