Taken to extremes: Loss of plastid rpl32 in Streptophyta and Cuscuta's unconventional solution for its replacement

The evolution of plant genomes is riddled with exchanges of genetic material within one plant (endosymbiotic gene transfer/EGT) and between unrelated plants (horizontal gene transfer/HGT). These exchanges have left their marks on plant genomes. Parasitic plants with their special evolutionary niche provide ample examples for these processes because they are under a reduced evolutionary pressure to maintain autotrophy and thus to conserve their plastid genomes. On the other hand, the close physical connections with different hosts enabled them to acquire genetic material from other plants. Based on an analysis of an extensive dataset including the parasite Cuscuta campestris and other parasitic plant species, we identified a unique evolutionary history of rpl32 genes coding for an essential plastid ribosomal subunit in Cuscuta. Our analysis suggests that the gene was most likely sequestered by HGT from a member of the Oxalidales order serving as host to an ancestor of the Cuscuta subgenus Grammica. Oxalidales had suffered an ancestral EGT of rpl32 predating the evolution of the genus Cuscuta. The HGT subsequently relieved the plastid rpl32 from its evolutionary constraint and led to its loss from the plastid genome. The HGT-based acquisition in Cuscuta is supported by a high sequence similarity of the mature L32 protein between species of the subgenus Grammica and representatives of the Oxalidales, and by a surprisingly conserved transit peptide, whose functionality in Cuscuta was experimentally verified. The findings are discussed in view of an overall pattern of EGT events for plastid ribosomal subunits in Streptophyta.