Dinoflagellate chloroplasts as a model for extreme genome reduction and fragmentation in organelles – The COCOA principle for gene retention

Abstract

The genomes of peridinin-containing dinoflagellate chloroplasts have a very unusual organisation. These genomes are highly fragmented and greatly reduced, with most of the usual complement of chloroplast genes relocated to the nucleus. Dinoflagellate chloroplasts highlight evolutionary changes that are found to varying extents in a number of other organelle genomes. These include the chloroplast genome of the green alga Boodlea and other Cladophorales, and the mitochondrial genomes of blood-sucking and chewing lice, the parasitic plant Rhopalocnemis phalloides, the red alga Rhodosorus marinus and other members of the Stylonematophyceae, diplonemid flagellates, and some Cnidaria. Consideration of the coding content of the remnant chloroplast genomes indicates that organelles may preferentially retain genes for proteins important in initiating assembly of complexes, and the same is largely true for mitochondria. We propose a new principle, of CO-location for COntrol of Assembly (COCOA), indicating the importance of retaining these genes in the organelle. This adds to, but does not invalidate, the existing hypotheses of the multisubunit completion principle, CO-location for Redox Regulation (CORR) and Control by Epistasy of Synthesis (CES).