Integration of plastids with their hosts: Lessons learned from dinoflagellates

Abstract

After their endosymbiotic acquisition, plastids become intimately connected with the biology of their host. For example, genes essential for plastid function may be relocated from the genomes of plastids to the host nucleus, and pathways may evolve within the host to support the plastid. In this review, we consider the different degrees of integration observed in dinoflagellates and their associated plastids, which have been acquired through multiple different endosymbiotic events. Most dinoflagellate species possess plastids that contain the pigment peridinin and show extreme reduction and integration with the host biology. In some species, these plastids have been replaced through serial endosymbiosis with plastids derived from a different phylogenetic derivation, of which some have become intimately connected with the biology of the host whereas others have not. We discuss in particular the evolution of the fucoxanthin-containing dinoflagellates, which have adapted pathways retained from the ancestral peridinin plastid symbiosis for transcript processing in their current, serially acquired plastids. Finally, we consider why such a diversity of different degrees of integration between host and plastid is observed in different dinoflagellates and how dinoflagellates may thus inform our broader understanding of plastid evolution and function.

Keywords: chloroplast genomes; dinotoms; minicircle; poly(U) tail; transcript editing.

Fig. 1.

Evolution of dinoflagellates and their plastids. (Upper) An evolutionary tree of dinoflagellates and their closest relatives, adapted from ref. . The evolutionary relationships in this tree are taken from refs. , , and 91); for simplicity, only a representative sample of dinoflagellate species is shown. The endosymbiotic acquisition and secondary loss of each individual plastid lineage, the loss of nonphotosynthesis genes from the peridinin plastid lineage, and the origins of minicircles, poly(U) tail addition, and transcript editing in peridinin and fucoxanthin plastids are labeled on the diagram. It is not clear from current data whether the loss of nonphotosynthesis genes and the evolution of minicircle gene organization occurred in the peridinin lineage before or after the divergence of basal dinoflagellates such as Perkinsus, Oxyrrhis, and Hematodinium (which have since lost the capacity for photosynthesis entirely); accordingly, the earliest and latest evolutionary points at which these events can have occurred are shown on the tree, labeled with question marks. (Lower) Tabulates key features of the different plastid lineages discussed in this manuscript.

Fig. 2.

Application of ancestral plastid pathways to serially acquired dinoflagellate plastids. This diagram shows how pathways associated with the peridinin plastid may have come to function in serially acquired dinoflagellate plastid lineages. For clarity, only the first membrane around each plastid is shown. Early dinoflagellates possessed a peridinin plastid, which was maintained by pathways [such as poly(U) tail addition and editing] encoded within the nucleus (A). In some lineages, this plastid was replaced by others (such as the fucoxanthin plastid) through serial endosymbiosis (B). Although the ancestral peridinin plastid was lost in these lineages, some of the nucleus-encoded genes associated with its function were retained (C) and, after the serial endosymbiosis event, were applied to the replacement plastid, changing its biology (D).