Genomic Insights into Plastid Evolution

Abstract

<jats:title>Abstract</jats:title> <jats:p>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.</jats:p>

A non-photosynthetic green alga illuminates the reductive evolution of plastid electron transport systems

“…Plastids are widely known as light-dependent cellular powerhouse organelles supplying sugar through photosynthesis to the algal and plant cells [ 1 – 6 ]. However, research over the past decade has shown that plastids exist on a functional and evolutionary continuum that includes a variety of non-photosynthetically functioning organelles [ 7 , 8 , 11 – 21 ]. Nevertheless, the evolutionary transitions of the electron transport system and the branched pathways for the electron sink between photosynthetic and non-photosynthetic plastids have remained unclear.…”

“…It also retains the most reduced system of photosynthetic electron transport comprising only Fd and FNR [ 9 , 10 ]. However, recent investigations have greatly expanded the spectrum of known functions of remnant plastids in non-photosynthetic algal/plant lineages [ 11 – 19 ] and have been reviewed in recent papers [ 20 , 21 ]. For example, the non-photosynthetic diatom plastid in Nitzschia sp.…”

Comparative Plastid Genomics of Non-Photosynthetic Chrysophytes: Genome Reduction and Compaction

“…Nevertheless, from the data in hand we propose a modified model of chrysophyte plastid evolution, as follows ( Figure 5 ). The red alga-type plastid of photosynthetic chrysophytes stems from a secondary (or possibly) tertiary endosymbiotic event in an ancestor shared with other plastid-bearing stramenopiles (see Sibbald and Archibald, 2020 and references therein; Figure 5 , ①). Much later, after the diversification of chrysophytes, Spumella -like flagellates lost their photosynthesis-related genes on multiple occasions ( Figure 5 , ②, ③).…”

“…The loss of photosynthesis in autotrophic organisms containing primarily and secondarily derived plastids has occurred multiple times during the course of eukaryotic evolution ( Kim and Archibald, 2009 ; Hadariová et al., 2018 ; Maciszewski and Karnkowska, 2019 ; Sibbald and Archibald, 2020 ). Although the loss of most or all photosynthesis-related genes leads to a reduction in plastid genome size and complexity, most non-photosynthetic taxa retain a plastid genome.…”

Highlight: The Colorful History of Plastids

“…Despite the importance of this event, a variety of aspects of plastid evolution have long remained shrouded in mystery. In a review in Genome Biology and Evolution , Shannon Sibbald and John Archibald highlight emerging genome data in this field and provide new insight into plastid evolution ( Sibbald and Archibald 2020 ).…”