A SINGLE ORIGIN OF PLASTIDS REVISITED: CONVERGENT EVOLUTION IN ORGANELLAR GENOME CONTENT¹

Abstract

In recent years a consensus has emerged from molecular phylogenetic investigations favoring a common endosymbiotic ancestor for all chloroplasts. It is within this conceptual framework that most comparative analyses of eukaryotic biochemistry and genetics now are interpreted. One of the first and most influential sources of data leading to this consensus is the remarkable similarity in genome content among all major plastid lineages. Here we report statistical analyses of two sequence data sets, genes encoding ribosomal proteins and transfer RNAs, from representatives of the three primary plastid lineages and a mitochondrion. The latter almost certainly originated in an independent endosymbiotic association and serves as a control for similarity due to convergent evolution. When genes related to organelle‐specific function are factored out, plastid genomes appear to be no more similar to each other than they are to the mitochondrion. Total similarities in gene content, measured as deviations from the expectation from a process of random gene loss, are correlated with the extent of reduction in the two genomes compared. They do not appear to reflect putative evolutionary relationships among plastids. These analyses indicate that similarities in plastid genome content are better explained by convergent evolution due to constraint on gene loss than by a shared evolutionary history. A review of other data cited as support for a single plastid origin suggests that the alternative hypothesis of multiple origins is at least equally consistent in most cases.

Monophyly of Archaeplastida supergroup and relationships among its lineages in the light of phylogenetic and phylogenomic studies. Are we close to a consensus?

“…Therefore, it generally is assumed that the primary endosymbiosis happened only once in the common ancestor of all Archaeplastida members [10,26,27]. Such a view requires monophyly of both primary plastids and their hosts, which is, however, still controversial because the clear similarity of plastids and their monophyly are also consistent with alternative scenarios for the evolution of the Archaeplastida supergroup [28][29][30][31][32][33] (Fig. 1).…”

“…1). This could lead to the same phylogenetic tree topology as in the case of a single plastid origin [28,32,33]. Finding a cyanobacterial lineage that clearly breaks up the monophyly of Archaeplastida plastids would refute the single plastid origin concept.…”

“…Three scenarios have been proposed (Fig. 1) that are compatible with the unquestionable monophyly of plastid genes, and explain both similar and different plastid features of Archaeplastida members (for wide discussion see [27][28][29][30][31][32][33]41,83,121,122]). One of them assumes that multiple independent primary endosymbioses occurred involving closely related cyanobacteria and separate Archaeplastida lineages.…”

Comparative Analysis of the Complete Plastid Genome Sequence of the Red Alga Gracilaria tenuistipitata var. liui Provides Insights into the Evolution of Rhodoplasts and Their Relationship to Other Plastids

“…Plastid origin occurred via primary and secondary endosymbiosis. The first involves the engulfment of a photosynthetic prokaryote (cyanobacterium) and is believed to have occurred once in evolution (but see Stiller and Hall 1997;Stiller et al 2003), giving rise to the protoalga that is the ultimate root of all plastids. This primary plastid eventually became established in the first algae that split into two lineages.…”

The Glaucophyta: the blue-green plants in a nutshell

“…Overall, the TOC-TIC complexes of the three archaeplastidian lineages comprise both protein components evolved from the plastid cyanobacterial ancestor (e.g., Toc75 and Tic20) and, importantly, proteins recruited from the host collection (Tic110 and Toc34) [8]. This shared phylogenetic mosaicism (i.e., common recruitments of non-cyanobacterial proteins) of the Archaeplastida TOC-TIC components favors the unique origin of primary plastids over the possibility of multiple independent origins (but see [88][89][90]). Shared phylogenetic mosaicism is also seen in other key plastidlocalized biochemical pathways in glaucophytes, red algae and viridiplants.…”