The Plastid Genome in Cladophorales Green Algae Is Encoded by Hairpin Chromosomes

Cortona, Andrea Del; Leliaert, Frédérik; Bogaert, Kenny A.; Turmel, Monique; Boedeker, Christian; Janouškovec, Jan; Lopez-Bautista, Juan; Verbruggen, Heroen; Vandepoele, Klaas; Clerck, Olivier De

doi:10.1016/j.cub.2017.11.004

Cited by 52 publications

(60 citation statements)

References 86 publications

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“…Most commonly, TGA has been reassigned from stop to tryptophan codon; this reassignment has been reported in many mitochondrial lineages (50), two bacterial lineages (51,52), and two plastid lineages [a subset of apicomplexans (53,54) and Chromera velia, a photosynthetic relative of apicomplexans (55)]. Also, two unrelated green algal plastid genomes were recently reported to use TGA as stop and sense codons (56,57). TAG occasionally encodes leucine, tyrosine, or glutamic acid (58,59), but its use for tryptophan is a novel code variant that makes the Balanophora plastome unique.…”

Section: Discussionmentioning

confidence: 99%

“…Balanophora plastids must therefore import the full suite of tRNAs required for plastid protein synthesis. Import of some or most plastid tRNAs has been postulated for many nonphotosynthetic plants (9,13,17), but import of all tRNAs for plastid protein synthesis need be invoked only for one other land plant, the holoparasite Pilostyles (19), the dinoflagellate Symbiodinium (75,76), and the green alga Boodlea (56). A key difference between the plastomes of Balanophora and these other three lineages is that only Balanophora has retained trnE, but apparently solely on account of its function in heme biosynthesis.…”

Section: Discussionmentioning

confidence: 99%

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Novel genetic code and record-setting AT-richness in the highly reduced plastid genome of the holoparasitic plant Balanophora

Barkman

Hao

et al. 2018

Proc. Natl. Acad. Sci. U.S.A.

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Plastid genomes (plastomes) vary enormously in size and gene content among the many lineages of nonphotosynthetic plants, but key lineages remain unexplored. We therefore investigated plastome sequence and expression in the holoparasitic and morphologically bizarre Balanophoraceae. The two Balanophora plastomes examined are remarkable, exhibiting features rarely if ever seen before in plastomes or in any other genomes. At 15.5 kb in size and with only 19 genes, they are among the most reduced plastomes known. They have no tRNA genes for protein synthesis, a trait found in only three other plastid lineages, and thus Balanophora plastids must import all tRNAs needed for translation. Balanophora plastomes are exceptionally compact, with numerous overlapping genes, highly reduced spacers, loss of all cis-spliced introns, and shrunken protein genes. With A+T contents of 87.8% and 88.4%, the Balanophora genomes are the most AT-rich genomes known save for a single mitochondrial genome that is merely bloated with AT-rich spacer DNA. Most plastid protein genes in Balanophora consist of ≥90% AT, with several between 95% and 98% AT, resulting in the most biased codon usage in any genome described to date. A potential consequence of its radical compositional evolution is the novel genetic code used by Balanophora plastids, in which TAG has been reassigned from stop to tryptophan. Despite its many exceptional properties, the Balanophora plastome must be functional because all examined genes are transcribed, its only intron is correctly trans-spliced, and its protein genes, although highly divergent, are evolving under various degrees of selective constraint.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Novel genetic code and record-setting AT-richness in the highly reduced plastid genome of the holoparasitic plant Balanophora

Barkman

Hao

et al. 2018

Proc. Natl. Acad. Sci. U.S.A.

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“…There has also been speculation in these cases that clpP1 has been functionally transferred to the nucleus, as intracellular gene transfer is a common and continuing phenomenon in plants (Millen et al ., ; Adams et al ., ). In the highly reorganized Boodlea composita plastome (Cortona et al ., ), clpP1 appears to have been lost and possibly transferred to the nucleus; however, on searching the assembled transcriptome (A. Del Cortona, pers. comm.)…”

Section: Discussionmentioning

confidence: 99%

Extreme variation in rates of evolution in the plastid Clp protease complex

et al. 2019

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Eukaryotic cells represent an intricate collaboration between multiple genomes, even down to the level of multi-subunit complexes in mitochondria and plastids. One such complex in plants is the caseinolytic protease (Clp), which plays an essential role in plastid protein turnover. The proteolytic core of Clp comprises subunits from one plastid-encoded gene (clpP1) and multiple nuclear genes. The clpP1 gene is highly conserved across most green plants, but it is by far the fastest evolving plastid-encoded gene in some angiosperms. To better understand these extreme and mysterious patterns of divergence, we investigated the history of clpP1 molecular evolution across green plants by extracting sequences from 988 published plastid genomes. We find that clpP1 has undergone remarkably frequent bouts of accelerated sequence evolution and architectural changes (e.g. a loss of introns and RNA-editing sites) within seed plants. Although clpP1 is often assumed to be a pseudogene in such cases, multiple lines of evidence suggest that this is rarely true. We applied comparative native gel electrophoresis of chloroplast protein complexes followed by protein mass spectrometry in two species within the angiosperm genus Silene, which has highly elevated and heterogeneous rates of clpP1 evolution. We confirmed that clpP1 is expressed as a stable protein and forms oligomeric complexes with the nuclear-encoded Clp subunits, even in one of the most divergent Silene species. Additionally, there is a tight correlation between amino acid substitution rates in clpP1 and the nuclear-encoded Clp subunits across a broad sampling of angiosperms, suggesting continuing selection on interactions within this complex.

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“…There has also been speculation in these cases that clpP1 has been functionally transferred to the nucleus, as intracellular gene transfer is a common and ongoing phenomenon in plants (Millen et al ., 2001; Adams, Qiu, et al ., 2002). In the highly reorganized Boodlea composita plastome (Cortona et al ., 2017), clpP1 appears to have been lost and possibly transferred to the nucleus, though we find that distinguishing clpP1 from its nuclear paralogs is difficult in this case due to deep sequence divergence. Thus, we are not aware of any clear examples of plastid clpP1 transfer to the nucleus in green plants.…”

Section: Discussionmentioning

confidence: 99%

Extreme variation in rates of evolution in the plastid Clp protease complex

Williams

Friso

Wijk

et al. 2018

Preprint

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1Eukaryotic cells represent an intricate collaboration between multiple genomes, even down to the 2 level of multisubunit complexes in mitochondria and plastids. One such complex in plants is the 3 caseinolytic protease (Clp), which plays an essential role in plastid protein turnover. The 4 proteolytic core of Clp comprises subunits from one plastid-encoded gene (clpP1) and multiple 5 nuclear genes. The clpP1 gene is highly conserved across most green plants, but it is by far the 6 fastest evolving plastid-encoded gene in some angiosperms. To better understand these extreme 7 and mysterious patterns of divergence, we investigated the history of clpP1 molecular evolution 8 across green plants by extracting sequences from 988 published plastid genomes. We find that 9 clpP1 has undergone remarkably frequent bouts of accelerated sequence evolution and 10 architectural changes (e.g., loss of introns and RNA-editing sites) within seed plants. Although 11 clpP1 is often assumed to be a pseudogene in such cases, multiple lines of evidence suggest that 12 this is rarely the case. We applied comparative native gel electrophoresis of chloroplast protein 13 complexes followed by protein mass spectrometry in two species within the angiosperm genus 14 Silene, which has highly elevated and heterogeneous rates of clpP1 evolution. We confirmed that 15 clpP1 is expressed as a stable protein and forms oligomeric complexes with the nuclear-encoded 16 Clp subunits, even in one of the most divergent Silene species. Additionally, there is a tight 17 correlation between amino-acid substitution rates in clpP1 and the nuclear-encoded Clp subunits 18 across a broad sampling of angiosperms, suggesting ongoing selection on interactions within this 19 complex. 21Rates of sequence evolution vary dramatically across genes and genomes. Understanding 22 the forces that determine such variation is one of the defining goals in the field of molecular 23 evolution. In seed plants, the plastid genome (plastome) generally evolves two-to six-fold more 24 slowly than the nuclear genome (Wolfe et al., 1987; Drouin et al., 2008; Smith and Keeling, 25 2015). However, among angiosperms, there is considerable heterogeneity in the rate of plastome 26 evolution. Many lineages have maintained a slowly-evolving plastome, while others have 27 experienced drastic rate increases (Jansen et al., 2007). For instance, among close relatives 28 within the tribe Sileneae there have been at least three recent and independent increases in 29 plastome evolutionary rate (Erixon and Oxelman, 2008; Sloan, Triant, Forrester, et al., 2014). 30 Similar accelerations have been documented in the Campanulaceae (Haberle et al., 2008; a structural level, plastome gene order has largely been conserved, with most angiosperms 34 retaining the structural organization that was present in the most recent common ancestor of this 35 group (Raubeson and Jansen, 2005). However, the sporadic increases in rates of plastome 36 sequence evolution have often been accompanied by structural ...

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The Plastid Genome in Cladophorales Green Algae Is Encoded by Hairpin Chromosomes

Cited by 52 publications

References 86 publications

Novel genetic code and record-setting AT-richness in the highly reduced plastid genome of the holoparasitic plant Balanophora

Novel genetic code and record-setting AT-richness in the highly reduced plastid genome of the holoparasitic plant Balanophora

Extreme variation in rates of evolution in the plastid Clp protease complex

Extreme variation in rates of evolution in the plastid Clp protease complex

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