New plastids, old proteins: repeated endosymbiotic acquisitions in kareniacean dinoflagellates.

Dinoflagellates are a diverse group of ecologically significant micro-eukaryotes that can serve as a model system for plastid symbiogenesis due to their susceptibility to plastid loss and replacement via serial endosymbiosis. Kareniaceae harbor fucoxanthin-pigmented plastids instead of the ancestral peridinin-pigmented ones and support them with a diverse range of nucleus-encoded plastid-targeted proteins originating from the haptophyte endosymbiont, dinoflagellate host, and/or lateral gene transfers (LGT). Here, we present predicted plastid proteomes from seven distantly related kareniaceans in three genera (Karenia, Karlodinium, and Takayama) and analyze their evolutionary patterns using automated tree building and sorting. We project a relatively limited ( ~ 10%) haptophyte signal pointing towards a shared origin in the family Chrysochromulinaceae. Our data establish significant variations in the functional distributions of these signals, emphasizing the importance of micro-evolutionary processes in shaping the chimeric proteomes. Analysis of plastid genome sequences recontextualizes these results by a striking finding the extant kareniacean plastids are in fact not all of the same origin, as two of the studied species (Karlodinium armiger, Takayama helix) possess plastids from different haptophyte orders than the rest.

The cellular machineries responsible for the division of endosymbiotic organelles.

Chloroplasts (plastids) and mitochondria evolved from endosymbiotic bacteria. These organelles perform vital functions in photosynthetic eukaryotes, such as harvesting and converting energy for use in biological processes. Consistent with their evolutionary origins, plastids and mitochondria proliferate by the binary fission of pre-existing organelles. Here, I review the structures and functions of the supramolecular machineries driving plastid and mitochondrial division, which were discovered and first studied in the primitive red alga Cyanidioschyzon merolae. In the past decade, intact division machineries have been isolated from plastids and mitochondria and examined to investigate their underlying structure and molecular mechanisms. A series of studies has elucidated how these division machineries assemble and transform during the fission of these organelles, and which of the component proteins generate the motive force for their contraction. Plastid- and mitochondrial-division machineries have important similarities in their structures and mechanisms despite sharing no component proteins, implying that these division machineries evolved in parallel. The establishment of these division machineries might have enabled the host eukaryotic ancestor to permanently retain these endosymbiotic organelles by regulating their binary fission and the equal distribution of resources to daughter cells. These findings provide key insights into the establishment of endosymbiotic organelles and have opened new avenues of research into their evolution and mechanisms of proliferation.

Insights into the Mechanisms of Chloroplast Division.

The endosymbiosis of a free-living cyanobacterium into an ancestral eukaryote led to the evolution of the chloroplast (plastid) more than one billion years ago. Given their independent origins, plastid proliferation is restricted to the binary fission of pre-existing plastids within a cell. In the last 25 years, the structure of the supramolecular machinery regulating plastid division has been discovered, and some of its component proteins identified. More recently, isolated plastid-division machineries have been examined to elucidate their structural and mechanistic details. Furthermore, complex studies have revealed how the plastid-division machinery morphologically transforms during plastid division, and which of its component proteins play a critical role in generating the contractile force. Identifying the three-dimensional structures and putative functional domains of the component proteins has given us hints about the mechanisms driving the machinery. Surprisingly, the mechanisms driving plastid division resemble those of mitochondrial division, indicating that these division machineries likely developed from the same evolutionary origin, providing a key insight into how endosymbiotic organelles were established. These findings have opened new avenues of research into organelle proliferation mechanisms and the evolution of organelles.

How do plastids and mitochondria divide?

Plastids and mitochondria are thought to have originated from free-living cyanobacterial and alpha-proteobacterial ancestors, respectively, via endosymbiosis. Their evolutionary origins dictate that these organelles do not multiply de novo but through the division of pre-existing plastids and mitochondria. Over the past three decades, studies have shown that plastid and mitochondrial division are performed by contractile ring-shaped structures, broadly termed the plastid and mitochondrial-division machineries. Interestingly, the division machineries are hybrid forms of the bacterial cell division system and eukaryotic membrane fission system. The structure and function of the plastid and mitochondrial-division machineries are similar to each other, implying that the division machineries evolved in parallel since their establishment in primitive eukaryotes. Compared with our knowledge of their structures, our understanding of the mechanical details of how these division machineries function is still quite limited. Here, we review and compare the structural frameworks of the plastid and mitochondrial-division machineries in both lower and higher eukaryotes. Then, we highlight fundamental issues that need to be resolved to reveal the underlying mechanisms of plastid and mitochondrial division. Finally, we highlight related studies that point to an exciting future for the field.

Protein maturation and proteolysis in plant plastids, mitochondria, and peroxisomes.

Plastids, mitochondria, and peroxisomes are key organelles with dynamic proteomes in photosynthetic eukaryotes. Their biogenesis and activity must be coordinated and require intraorganellar protein maturation, degradation, and recycling. The three organelles together are predicted to contain ∼200 presequence peptidases, proteases, aminopeptidases, and specific protease chaperones/adaptors, but the substrates and substrate selection mechanisms are poorly understood. Similarly, lifetime determinants of organellar proteins, such as N-end degrons and tagging systems, have not been identified, but the substrate recognition mechanisms likely share similarities between organelles. Novel degradomics tools for systematic analysis of protein lifetime and proteolysis could define such protease-substrate relationships, degrons, and protein lifetime. Intraorganellar proteolysis is complemented by autophagy of whole organelles or selected organellar content, as well as by cytosolic protein ubiquitination and degradation by the proteasome. This review summarizes (putative) plant organellar protease functions and substrate-protease relationships. Examples illustrate key proteolytic events.