Rapid evolution of the plastid translational apparatus in a nonphotosynthetic plant: Loss or accelerated sequence evolution of tRNA and ribosomal protein genes

Abstract

The vestigial plastid genome of Epifagus virginiana (beechdrops), a nonphotosynthetic parasitic flowering plant, is functional but lacks six ribosomal protein and 13 tRNA genes found in the chloroplast DNAs of photosynthetic flowering plants. Import of nuclear gene products is hypothesized to compensate for many of these losses. Codon usage and amino acid usage patterns in Epifagus plastic genes have not been affected by the tRNA gene losses, though a small shift in the base composition of the whole genome (toward A+T-richness) is apparent. The ribosomal protein and tRNA genes that remain have had a high rate of molecular evolution, perhaps due to relaxation of constraints on the translational apparatus. Despite the compactness and extensive gene loss, one translational gene (infA, encoding initiation factor 1) that is a pseudogene in tobacco has been maintained intact in Epifagus.

Many Parallel Losses of infA from Chloroplast DNA during Angiosperm Evolution with Multiple Independent Transfers to the Nucleus

“…Three more infA pseudogenes were found, in Pentas (Rubiaceae), Campanula (Campanulaceae), and Conopholis (Orobanchaceae) ( Figure 1). The loss of infA in the nonphotosynthetic plant Conopholis is in contrast to the presence of an intact gene in its close relative Epifagus (Wolfe et al, 1992b). On the basis of an interpretation of the distribution of infA losses and retentions in terms of the species' phylogeny, we conclude that there were at least four independent losses within the asterid clade (Figure 1).…”

“…These five genes are accD , ycf1 , and ycf2 (pseudogenes in rice and maize; Hiratsuka et al, 1989;Maier et al, 1995), rpl23 (pseudogene in spinach; Thomas et al, 1988), and infA (pseudogene in tobacco, Arabidopsis, and Oenothera elata ; Shinozaki et al, 1986;Wolfe et al, 1992b;Sato et al, 1999;Hupfer et al, 2000). Other chloroplast gene losses in angiosperms that have been confirmed by sequencing include rpl22 , rps16 , and ycf4 (open reading frame 184), all of which have been lost in some or all legumes (Gantt et al, 1991;Nagano et al, 1991;Doyle et al, 1995;K.H.…”

The Chloroplast trnT–trnF Region in the Seed Plant Lineage Gnetales

“…Recent large-scale analyses have shown that the cistron comprised of the three tRNA genes is a uniquely shared characteristic of land plants (Quandt et al, 2004); in green algae, the trnF gene is located farther away from the other two genes. The trnT and trnL genes are lost, and the trnLtrnF region is disrupted, in a few nonphotosynthetic flowering plants, such as Epifagus virginiana (Orobanchaceae [Wolfe et al 1992]) (Fig. 1C).…”

“…Note the pseudogenized ndhK and ndhC and the lack of ndhJ compared to mosses, ferns, and angiosperms. C Map of Epifagus virginiana, a nonphotosynthetic angiosperm, modified from Wolfe et al (1992). Note the loss of trnT, trnL, and ndh genes and the pseudogenization of trnS, atpB, and rbcL.…”

Mutational Pressure Drives Evolution of Synonymous Codon Usage in Genetically Distinct Oenothera plastomes

“…Since most proteins in the chloroplast are essential for photosynthesis, protein coding regions of chloroplast are highly conserved in higher plants, although a few exceptions exist (22,23). In plastidic genome, mutational pressure favours high representation of A/T and it appears to be the major factor shaping SCUB (24 -26).…”