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which they might be misrouted after cytosolic synthesis (Martin and Schnarrenberger, 1997). Although this toxicity hypothesis is eminently testable, we are unaware of any empirical evidence for it. A third hypothesis for organellar gene retention is to allow their expression to be directly and quickly regulated by the redox state of the organelle (Allen, 1993; reviewed in Race et al., 1999). Evidence for redox regulation of organellar gene expression has been reported for chloroplasts (Pfannschmidt et al., 1999) but not, to our knowledge, for mitochondria.

Although selective factors may be responsible for the transfer of some genes to the nucleus and the retention of others in the mitochondrion, chance factors may also be at work. At the stage of dual expression, whether the nuclear or mt copy of a transferred gene is retained may in some cases depend solely on the roll of the evolutionary dice —on which gene first sustains a gene-inactivating mutation, or a mutation that is either deleterious or beneficial to the gene product's function. In the latter two cases, selection would be involved in the sense that it would act to either fix the gene with the beneficial mutation or eliminate the gene with the deleterious mutation.

We are left with a picture of organelle gene transfer as a complex, historically contingent process whose outcome undoubtedly depends on a combination of mechanistically driven factors and chance mutations, together with selective forces. The process seems to be driven by the high rate of physical duplication of organelle genes into the nucleus (which appears to be true for all eukaryotes, regardless of whether functional gene transfer is still occurring), and proceeds seemingly exclusively in one direction: from organelles to nucleus. Indeed, with one disputed exception, a mutS homolog in coral mt DNA (Pont-Kingdon et al., 1995, 1998), there are no examples known of the reverse process, of functional genes moving from the nucleus to the mitochondrion or chloroplast.

Why has gene transfer been so pervasively unidirectional? Flowering plant mitochondria are certainly able to accept foreign sequences: Numerous examples are known of the uptake of chloroplast DNA (Nugent and Palmer, 1988; Palmer, 1992; Unseld et al., 1997; Marienfeld et al., 1999), nuclear DNA (Knoop et al., 1996; Unseld et al., 1997; Marienfeld et al., 1999), and sequences from other organisms (Vaughn et al., 1995; Cho et al., 1998; see below), and a few chloroplast-derived genes are expressed in the mitochondrion (Joyce and Gray, 1989; Kanno et al., 1997; Miyata et al., 1998). Nonetheless, the initial driving force (the rate of physical transfer/duplication of sequences from one genome into the other) may be much stronger toward the nucleus than in the reverse direction; certainly this seems to be the case for yeast by several orders of magnitude (Thorsness and Fox, 1990; Thorsness and Weber, 1996). Compounding this, each mt gene physically transferred to the nucleus can potentially result in func-

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