Second Genesis of a Plastid Organelle
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COMMENTARY Second genesis of a plastid organelle Ross F. Waller1 School of Botany, University of Melbourne, Melbourne, Victoria 3010, Australia ne of the more remarkable A dosymbiont might seem unlikely, we know discoveries of 20th century bi- that it happens a lot. Both experimental O ology is that all eukaryotes are and anecdotal evidence tells us that chimeras of two or more dif- chunks of organelle DNA are frequently ferent cells (1). The tree of life does not transferred to the nucleus (7). The next just bifurcate through successive specia- step is to express the nuclear copy of the tion events; its branches also graft, one Paulinella endosymbiont gene, to start synthesizing onto another, merging lineages to produce this endosymbiont protein on cytosolic ri- novel fruit. Our mitochondria, and the B bosomes (Fig. 1C). This step might require photosynthetic plastids of plants and al- only the “dumb luck” of the gene in- gae, are proof of the success of these new tegrating within an appropriate nuclear combinations. Both organelles were ac- sequence to promote expression. Re- quired from separate bacterial lineages, petitive gene transfers might be enough to where a useful bacterium was internalized ensure that this integration is eventually and maintained within the host cell— achieved. However, now the cell faces the a process known as endosymbiosis. These further challenge of transferring the pro- organelles are no mere hitchhikers. They tein across the membrane barriers sur- have been elaborately integrated with their rounding the endosymbiont, back to its hosts, so intimately that even their genes C functional location. have been relinquished to the host cell to How proteins first achieve translocation allow these partnerships to truly operate across the endosymbiont membranes is an as one. To achieve this, the host cell open question (Fig. 1C) (8, 9). They might learned to take responsibility for express- pass through existing pore-forming com- ing the organelle genes and delivering the ? plexes, already in place to handle some protein products back into the organelle other cargo (10). Or they might be de- according to its requirements. Our un- livered by membrane vesicle, if by chance derstanding of how these seminal ach- they are routed into the host cell endo- ievements of organellogenesis occurred, membrane system (11). In either case (or however, is obscured by their antiquity, D a combination of these), only once they both organelles arising ∼1+ billion years are transported into the endosymbiont in ago (2). It is akin to studying modern jet sufficient quantity to provide adequate aircraft in the hope of reconstructing the function can the endosymbiont-encoded Wright brothers’ first daring attempts at copy of the gene finally be lost. If regula- flight. Iterative leaps of technology often tory control of this protein is necessary for mask the formative innovations. However, function, then the nucleus-encoded gene now we have a chance to revisit this pro- too must achieve this. cess, as Nowack and Grossman in PNAS Loss of the endosymbiont gene copy is (3) show that the new photosynthetic en- the final act in genetic integration of the Paulinella chromatophora Fig. 1. Steps for genetic integration of an endo- endosymbiont with its host, and to many dosymbiont of A symbiont with its host. ( ) Following bacterial in- this act is the threshold for achieving or- has also commenced this journey of ternalization, metabolic sharing and coordinated genetic integration. B ganelle status (12). However, if early traf- bacterial division enable a stable relationship. ( ) fi Plastids show remarkable diversity Copies of endosymbiont genome fragments (red) cking of proteins initially used existing across plants and the variously pigmented are known to frequently transfer to host nuclei. transport machinery designed for other algae, but it is now generally agreed that (C) Fortuitous expression of endosymbiont gene molecules, it probably would not have fi fi fi they all stem from a single endosymbiotic products (cyan) on cytosolic ribosomes provides been very ef cient or speci c. Re nement gain of a β-cyanobacterium (4, 5). This the opportunity for some protein to be trans- of a dedicated route for organelle proteins single origin of plastids implies that es- ported back to the endosymbiont and provide would likely be required. This would have function. (D)Refinement of specific transport the further advantage that proteins of tablishing a novel organelle from a bacte- fi routes (lock and keys) provides ef ciency and op- other transferred organelle genes could rium is a challenging undertaking and not portunity for further endosymbiont genes to be frequently repeated, despite the obvious established in the nucleus. Endosymbiont copies adopt this route (or routes) and obviate benefits of acquiring photosynthesis. To of genes can be lost only once function is provided the need to reinvent targeting with every D understand possible bottlenecks in this by the nucleus-encoded copy (C and D). transfer (Fig. 1 ). In modern plastids and process it is useful to consider the se- mitochondria, the majority of organelle proteins bear a characteristic peptide ex- quence of events required to establish ships have achieved these initial tasks, a genetically integrated organelle (Fig. 1). tension that acts as a targeting signal implying that these partnerships are not so Any endosymbiotic relationship is ini- fi tially cemented by establishment of some dif cult (6). For genetic integration, the fi mutually beneficial metabolic sharing and rst step is the transfer of copies of genes Author contributions: R.F.W. wrote the paper. coordinated division of the endosymbiont from the endosymbiont to the host nucleus The author declares no conflict of interest. to ensure its persistence in the host cell. A (Fig. 1B). Whereas such meddling in the See companion article 10.1073/pnas.1118800109. great variety of endosymbiotic relation- genomic integrity of the nucleus and en- 1E-mail: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1202904109 PNAS Early Edition | 1of2 Downloaded by guest on October 4, 2021 recognized by specific receptors on the provide proof that three nucleus-encoded only certain genes to participate in these outer organelle membranes (13, 14). New genes (for photosynthetic proteins PsaE, early steps of organelle establishment gene transfers need only acquire coding PsaK1, and PsaK2) are indeed translated (e.g., protein size, structure, function, and sequence that resembles such an extension in the host cell cytoplasm and that these regulatory requirement) and, if so, what fl to join the ow of proteins back to the proteins are delivered to their site of can this tell us of the development of > organelle, and now 90% of plastid and function on the chromatophore thylakoid trafficking routes? To date, all of the mitochondrial genes have made this membranes. This information directly im- predicted chromatophore transferred transition. plies successful expression of the trans- genes are for small proteins, implying the So what can P. chromatophora tell us ferred genes in the nucleus and existence transport system is yet to reach maturity, about the challenges of organellogenesis? and no consistent targeting signals are Paulinella is a relatively obscure genus of thecate amoebae that mostly feed on cya- Nowack and Grossman apparent (3, 16, 19). Whereas the study of ancient organ- nobacteria. P. chromatophora, however, now throw light on the has established a photosynthetic endo- elles like plastids and mitochondria allows symbiont from one of its earlier meals, and final pieces of the us to ponder processes relevant to the this endosymbiont now allows it to be ex- endpoints of organellogenesis [such clusively autotrophic. Whereas plastids of organellogenesis puzzle as the Co-localization for Redox Regu- plants and algae are ∼1 billion years old lation (CORR) hypothesis for why (2), the P. chromatophora “chromato- in P. chromatophora. genes remain in organelles at all] (20), phore” is a mere ∼60 Myr old (15). So this P. chromatophora offers us lessons in the is a plastid in its infancy. The symbiont’s challenges of the start of this process. genome is still a giant compared with most of a transport system capable of importing There is no guarantee that the pathway plastid genomes (1 vs. 0.1–0.2 Mbp), proteins back into the organelle. These along which P. chromatophora is estab- fi but it is, nevertheless, reduced by approxi- ndings now allow several pertinent lishing its organelle is the same as that mately one-third compared with that of questions of organellogenesis to be asked. followed by plastids in the past. Never- α What route or routes are used for this -cyanobacteria from which it is derived theless, this system does provide a potent (15). Much of this reduction is due to nascent protein transport system? Is model of organellogenesis, particularly loss of redundant genes now that it lives existing and/or novel sorting machinery given that living relatives of both the host inside another cell, but it is also, in part, due used (Nowack and Grossman implicate vesicular traffic for at least one protein) cell and the symbiont still occur (i.e., het- to gene transfers to the nucleus. At least 30 Paulinella α of the cyanobacterial genes have been and to what extent does this represent erotrophic spp. and -cyano- shown to occur exclusively in the host’s a dedicated chromatophore targeting sys- bacteria, respectively). Thus, both the nucleus, implying that the shift in genetic tem? Have functional targeting signals ingredients and the products of this evo- control has already commenced (16–18). been developed and appended to the lutionary experiment in repeat are avail- Nowack and Grossman (3) now throw transferred coding sequences to expedite able, allowing a detailed investigation of light on the final pieces of the organello- further transfer of genetic control? Have the adaptations made during the estab- genesis puzzle in P.