Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron.

Abstract

Most chloroplast and mitochondrial proteins are encoded by nuclear genes that once resided in the organellar genomes. Transfer of most of these genes appears to have occurred soon after the endosymbiotic origin of organelles, and so little is known about the process. Our efforts to understand how chloroplast genes are functionally transferred to the nuclear genome have led us to discover the most recent evolutionary gene transfer yet described. The gene rpl22, encoding chloroplast ribosomal protein CL22, is present in the chloroplast genome of all plants examined except legumes, while a functional copy of rpl22 is located in the nucleus of the legume pea. The nuclear rpl22 gene has acquired two additional domains relative to its chloroplast ancestor: an exon encoding a putative N‐terminal transit peptide, followed by an intron which separates this first exon from the evolutionarily conserved, chloroplast‐derived portion of the gene. This gene structure suggests that the transferred region may have acquired its transit peptide by a form of exon shuffling. Surprisingly, phylogenetic analysis shows that rpl22 was transferred to the nucleus in a common ancestor of all flowering plants, at least 100 million years preceding its loss from the legume chloroplast lineage.

Exon shuffling and the origin of the mitochondrial targeting function in plant cytochrome c1 precursor.

“…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.…”

Conservation of Plastid Sequences in the Plant Nuclear Genome for Millions of Years Facilitates Endosymbiotic Evolution

“…There still exist some chloroplast genes that can be functionally transferred to the nucleus. For example, chloroplast genes such as accD (Magee et al, 2010), infA (Millen et al, 2001), rpl22 (Gantt et al, 1991), and rpl32 (Cusack and Wolfe, 2007;Ueda et al, 2007) were recently functionally transferred from the chloroplast to the nucleus in some angiosperms (for review, see Rousseau-Gueutin et al, 2011). The number of genes that can be functionally transferred might be larger since analyses of the gene content of all plastomes sequenced so far showed that the ndh, psaI, rps16, rpl23, rpl33, or ycf4 genes were lost in some angiosperms (Magee et al, 2010).…”

Complete plastid genome sequence of the chickpea (Cicer arietinum) and the phylogenetic distribution of rps12 and clpP intron losses among legumes (Leguminosae)

“…Clearly, most plastid genomic rearrangements among legumes are restricted to the papilionoids with the exception of the loss of the rpl22 gene (Downie and Palmer, 1992;Doyle et al, 1995), which characterizes all taxa sampled from all three subfamilies of legumes, and the loss of the rpl2 intron in numerous species of the caesalpinioid genus Bauhinia (Lai et al, 1997). Interestingly, the rpl22 gene has not been lost from any other land plants (Downie and Palmer, 1992), and a functional copy has been isolated from the nuclear genome in Pisum sativum (Gantt et al, 1991).…”