Genomic Insights into Plastid Evolution

Abstract

The origin of plastids (chloroplasts) by endosymbiosis stands as one of the most important events in the history of eukaryotic life. The genetic, biochemical, and cell biological integration of a cyanobacterial endosymbiont into a heterotrophic host eukaryote approximately a billion years ago paved the way for the evolution of diverse algal groups in a wide range of aquatic and, eventually, terrestrial environments. Plastids have on multiple occasions also moved horizontally from eukaryote to eukaryote by secondary and tertiary endosymbiotic events. The overall picture of extant photosynthetic diversity can best be described as "patchy": Plastid-bearing lineages are spread far and wide across the eukaryotic tree of life, nested within heterotrophic groups. The algae do not constitute a monophyletic entity, and understanding how, and how often, plastids have moved from branch to branch on the eukaryotic tree remains one of the most fundamental unsolved problems in the field of cell evolution. In this review, we provide an overview of recent advances in our understanding of the origin and spread of plastids from the perspective of comparative genomics. Recent years have seen significant improvements in genomic sampling from photosynthetic and nonphotosynthetic lineages, both of which have added important pieces to the puzzle of plastid evolution. Comparative genomics has also allowed us to better understand how endosymbionts become organelles.

Keywords: chloroplasts; evolution; genomics; organelles, algae, protists; phylogenomics; plastids.

Fig. 1

Schematic of the eukaryotic tree of life with an emphasis on plastid-bearing lineages and their closest relatives. The tree topology is based on recent analyses and discussion in Strassert et al. (2019), Gawryluk et al. (2019), and Burki et al. (2020). The type of plastid (primary or complex) is indicated next to each lineage. Where known, specific complex events of kleptoplasty and plastid replacements (serial secondary or tertiary) are shown. Known instances of loss of photosynthesis are indicated with a line through the plastid circle; loss of photosynthesis with loss of the plastid genome is indicated by a line through the plastid circle and an asterisk. Complete loss of a plastid is indicated by two lines through their plastid circle. Dashed lines in the tree represent regions of uncertainty with respect to the phylogenetic placement of the corresponding lineages.