The Evolutionary Origins of Plant Organelles

Alone among plant organelles, mitochondria and plastids contain genetic information, in the form of organellar genomes. These genomes specify a limited set of protein and RNA components that are essential for the normal biogenesis and functioning of these two organelles. Importantly, organellar genomes are now known to be remnant eubacterial genomes, reflecting an origin of mitochondria and plastids as eubacterial symbionts in eukaryotic cells. Through analysis of organellar gene content, gene sequence and gene organization, we have been able to trace the origin of mitochondrial and plastid genomes to particular groups of extant eubacteria, with which these organelles share a specific evolutionary ancestor. Over the past several decades, our burgeoning knowledge of organellar genomes, culminating in the complete sequences of a diverse collection of mitochondrial and plastid DNAs, has brought solid evidence to bear on over a century of speculation and debate about the nature and origin of mitochondria and plastids, a subject that is of fundamental importance to our understanding of the evolutionary emergence of the eukaryotic cell as a whole. Our current view of organelle evolution is that mitochondria (almost certainly) and plastids (very likely) each originated only once, the former from within the ?-Proteobacteria and the latter from within the Cyanobacteria. In the case of plastids, a single primary endosymbiosis event, involving a eukaryotic host cell and a cyanobacterium, was followed by a number of secondary endosymbioses, each between a (presumably) non-photosynthetic, heterotrophic eukaryotic host and a plastid-containing eukaryotic symbiont. Three lineages (green algae + land plants, red algae, glaucocystophytes) appear to contain primary plastids, whereas all other groups of algae contain secondary plastids. Early on, data derived from analysis of plant organellar DNAs was particularly persuasive in affirming a eubacterial origin of mitochondrial DNA (mtDNA) specifically from within the ?-Proteobacteria. At the same time, our emerging appreciation of the extraordinary structural variability of mtDNA, especially within the lineage of green algae and land plants, prompted questions about whether these markedly different mitochondrial genomes had separate evolutionary origins. With the availability of additional mtDNA sequences, this issue now seems settled in favour of a single (monophyletic) origin of mitochondria, with mitochondrial genomes in particular lineages (e.g., chlorophycean green algae) having highly derived genomes, unrepresentative of the ancestral state.