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nucleus occurs at a surprisingly high frequency in angiosperm evolution, especially, it would appear, in some groups of flowering plants (see preceding section).

MITOCHONDRIAL GENE TRANSFER IN ACTION: RECENT TRANSFER OF COX2 TO THE NUCLEUS IN LEGUMES

The most extensively studied example of recent mt gene transfer in flowering plants (or any group of eukaryotes) is the cytochrome oxidase subunit 2 gene (cox2) in legumes (Nugent and Palmer, 1991, 1993; Covello and Gray, 1992; Adams et al., 1999). Cox2, present in the mitochondrion of virtually all plants, was transferred to the nucleus during recent legume evolution (Adams et al., 1999). Examination of nuclear and mt cox2 presence and expression in over 25 legume genera has revealed a wide range of intermediate stages in the process of mt gene transfer, providing a portrayal of the gene transfer process in action (Fig. 2; Adams et al., 1999). Cox2 was transferred to the nucleus via an edited RNA intermediate (Nugent and Palmer, 1991; Covello and Gray, 1992). Once nuclear cox2 was activated, a state of dual intact and expressed genes—of transcompartmental functional redundancy—was established; this transition stage persists most fully (i.e., with both compartments' cox2 genes highly expressed in terms of steady-stated, properly processed RNAs; COX2 protein levels have not been assayed) only in Dumasia among the many studied legumes. Four other, phylogenetically disparate legumes also retain intact and expressed copies of cox2 in both compartments, but with only one of the two genes expressed at a high enough level, in the one tissue type examined thus far, to presumably support respiration (Fig. 2). Silencing of either nuclear or mt cox2 has occurred multiple times and in a variety of ways, including disruptive insertions or deletions, cessation of transcription or RNA editing, and partial to complete gene loss (Adams et al., 1999). Based on phylogenetic evidence, we infer that mt cox2 and nuclear cox2 have been silenced approximately three to five times each during the evolution of the studied legumes (Fig. 2). Although cox2 in legumes is the only known example of gene inactivation after recent transfer and activation in the nucleus, a comparative phylogenetic approach might reveal that the nuclear copy of other recently transferred organelle genes has become inactivated in one or more species related to the single plant studied so far.

ROLES OF SELECTION AND CHANCE IN MITOCHONDRIAL GENE TRANSFERS DURING ANGIOSPERM EVOLUTION

All but the last step (gene loss) in the complicated and evolutionarily unidirectional process by which mt genes move to the nucleus and disap-



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