Six Independent Losses of the Chloroplast DNA rpl2 Intron in Dicotyledons: Molecular and Phylogenetic Implications

Abstract

Previous studies have shown that in several angiosperms and the liverwort Marchantia the chloroplast gene rpl2, encoding ribosomal protein L2, is interrupted by an intron, but that in spinach (Spinacia oleracea, Caryophyllales) this intron has been lost. We have determined the distribution of the rpl2 intron for 390 species representing 116 angiosperm families. Filter hybridizations reveal that the intron is absent from the chloroplast genomes of all examined families of the Caryophyllales, suggesting that the intron was lost in the common ancestor of the order. Sequencing of the rpl2 gene in five genera of the Caryophyllaies and in Rumex (Polygonales) not only confirms the filter hybridization results, but also shows that for all taxa lacking the intron, the rpl2 gene has undergone a precise deletion of the intron. In all cases, it is the original rpl2 gene that has sustained loss ofits intron. This implies that in chloroplast DNA, integration ofexogenous genes (e.g., a reverse transcript of a spliced mRNA) occurs mainly by homologous, replacement recombination, rather than by illegitimate recombination elsewhere in the genome. Filter hybridizations also reveal that the rpl2 intron was lost independently in the common ancestors of at least five other lineages ofdicotyledons: Saxifragaceae (s.s.), Convolvulaceae (including Cuscuta), Menyanthaceae, two genera of Geraniaceae, and one genus of Droseraceae. The molecular and phylogenetic implications of these independent intron losses are discussed.

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

“…Comparison of the sizes of both the clpP and rps12 PCR products from a diversity of legumes, represented in Figs. 3 and 4, reveals fragments very similar in length, a result consistent with a process by which plastid introns are excised precisely and entirely, as observed earlier by Doyle et al (1995) and in other taxa by Downie et al (1991). Indeed, sequence analysis of ten taxa selected from our survey that included those with or without the clpP and rps12 introns confirms that intron excision has occurred at precisely the same points in the gene sequence in each taxon lacking the intron (MFW, unpublished data).…”

The phylogeny of Monsonia L. (Geraniaceae)

“…Thus, the ITS-and trnL-F-data unambiguously show that the former genus Sarcocaulon is nested as a paraphyletic assembledge in the genus Monsonia. Both rbcL-analyses and the fact that the rp12 intron is lost in Monsonia and Sarcocaulon have previously already indicated a close affinity between these two taxa within the Geraniaceae (Price et al 1990, Downie and Palmer 1992, Price and Palmer 1993. Almost identical flavonoid patterns, which have been classified as basal, were described for the Monsonia and the former Sarcocaulon species (Marschewski 1995).…”

“…These study showed that Monsonia and Sarcocaulon are either sister genera or congeneric and sister to the other three (or four) genera in the Geraniaceae. The close relationship between Monsonia and the former genus Sarcocaulon is also supported by the shared loss of the cpDNA rp12 intron (Price et al 1990, Downie andPalmer 1992).…”

Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns

“…Likewise, of the eight introns that have been lost, five (atpF, clpP introns 1 and 2, rpl2, rpoC1, and rps16) have been lost multiple times. Expanded taxon sampling for intron losses has identified even more extensive convergent losses for rpl2 (47), rpl16 (37), rpoC1 (48), and rps12 (49). More intensive molecular investigations will likely reveal many more cases of gene and intron losses from the plastid genome and, in some cases, evidence for the transfer of these genes to the nuclear genome.…”