Mitochondrial DNA of Chlamydomonas reinhardtii: the structure of the ends of the linear 15.8-kb genome suggests mechanisms for DNA replication

Vahrenholz, C.; Riemen, Gudula; Pratje, Elke; Dujon, Bernard; Michaelis, Georg

doi:10.1007/bf00351798

Cited by 136 publications

(96 citation statements)

References 35 publications

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“…Telomeric sequences from Chlamydomonas are believed to prevent end-to-end fusion and degradation of the linear mitochondrial DNA molecules (Randolph-Anderson et al, 1993) and to be essential for DNA replication (Vahrenholz et al, 1993). As mentioned in the description of the hybridization experiments, the restriction fragments characteristic of the asymmetrical dimer were always present on the blots, whereas in several cases, the fragments typical of the monomers were not detected.…”

Section: Discussionmentioning

confidence: 97%

“…Its small 15.8-kb linear mitochondrial genome has been totally sequenced, and all of the genes residing in the organelle have been identified (Vahrenholz et al, 1993; Figure 1). Moreover, several mutations altering the mitochondrial genes encoding apocytochrome b ( cob gene) or subunit 1 of cytochrome c oxidase ( cox1 gene) have been characterized (Matagne et al, 1989;Dorthu et al, 1992;Randolph-Anderson et al, 1993;Colin et al, 1995).…”

Section: Introductionmentioning

confidence: 99%

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Alteration of Dark Respiration and Reduction of Phototrophic Growth in a Mitochondrial DNA Deletion Mutant of Chlamydomonas Lacking cob, nd4, and the 3′ End of nd5

Duby

Matagne

1999

Plant Cell

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We describe here a new type of mitochondrial mutation ( dum24 ; for dark uniparental minus inheritance) of the unicellular photosynthetic alga Chlamydomonas reinhardtii . The mutant fails to grow under heterotrophic conditions and displays reduced growth under both photoautotrophic and mixotrophic conditions. In reciprocal crosses between mutant and wild-type cells, the meiotic progeny only inherit the phenotype of the mating-type minus parent, indicating that the dum24 mutation exclusively affects the mitochondrial genome. Digestion with various restriction enzymes followed by DNA gel blot hybridizations with specific probes demonstrated that dum24 cells contain four types of altered mitochondrial genomes: deleted monomers lacking cob , nd4 , and the 3 Ј end of the nd5 gene; deleted monomers deprived of cob , nd4 , nd5 , and the 5 Ј end of the cox1 coding sequence; and two types of dimers produced by end-to-end fusions between monomers similarly or differently deleted. Due to these mitochondrial DNA alterations, complex I activity, the cytochrome pathway of respiration, and presumably, the three phosphorylation sites associated with these enzyme activities are lacking in the mutant. The low respiratory rate of the dum24 cells results from the activities of rotenoneresistant NADH dehydrogenase, complex II, and alternative oxidase, with none of these enzymes being coupled to ATP production. To our knowledge, this type of mitochondrial mutation has never been described for photosynthetic organisms or more generally for obligate aerobes.

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Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Alteration of Dark Respiration and Reduction of Phototrophic Growth in a Mitochondrial DNA Deletion Mutant of Chlamydomonas Lacking cob, nd4, and the 3′ End of nd5

Duby

Matagne

1999

Plant Cell

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“…Conversely, all of the characterized green algal mitochondrial genomes from outside this clade map in genome assemblies and/or gel electrophoresis studies as unit-sized circular chromosomes save for the mtDNAs of some Lobochlamys taxa, which may be linear fragmented (Borza et al, 2009). Studies on linear green algal mtDNAs have revealed a range of interesting telomeric sequences and structures, including inverted repeats, 3´ overhangs, and closed single-stranded loops (Vahrenholz et al, 1993;Smith & Lee, 2008). Since mitochondria lack telomerase, it is presumed that the elaborate termini of linear mtDNAs help the genome overcome the end replication problem, as defined by Olovnikov (1971) and Watson (1972).…”

Section: A Organelle Genome Evolutionmentioning

confidence: 99%

Phylogeny and Molecular Evolution of the Green Algae

Leliaert

Smith

Moreau

et al. 2012

Critical Reviews in Plant Sciences

759

655

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“…Linear-mapping mitochondrial genomes with defined telomeres are found within various green algae, protists, animals, and fungi (22,43). The telomeres of linear mtDNAs can have ornate conformations (22), such as hairpin loops (44), single-stranded overhangs (45), and/or covalently attached proteins (46), which likely preserve the chromosome ends independent of telomerase (22). The alveolate Chromera velia boasts the only known linear-mapping plastid genome, which has a telomeric arrangement mirroring those of many linear mitochondrial chromosomes (47).…”

Section: A Multiplicity Of Mitochondrial and Plastid Genome Architectmentioning

confidence: 99%

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

Smith

Keeling

2015

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

356

344

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Mitochondrial and plastid genomes show a wide array of architectures, varying immensely in size, structure, and content. Some organelle DNAs have even developed elaborate eccentricities, such as scrambled coding regions, nonstandard genetic codes, and convoluted modes of posttranscriptional modification and editing. Here, we compare and contrast the breadth of genomic complexity between mitochondrial and plastid chromosomes. Both organelle genomes have independently evolved many of the same features and taken on similar genomic embellishments, often within the same species or lineage. This trend is most likely because the nuclear-encoded proteins mediating these processes eventually leak from one organelle into the other, leading to a high likelihood of processes appearing in both compartments in parallel. However, the complexity and intensity of genomic embellishments are consistently more pronounced for mitochondria than for plastids, even when they are found in both compartments. We explore the evolutionary forces responsible for these patterns and argue that organelle DNA repair processes, mutation rates, and population genetic landscapes are all important factors leading to the observed convergence and divergence in organelle genome architecture.E ndosymbiosis can dramatically impact cellular and genomic architectures. Mitochondria and plastids exemplify this point. Each of these two types of energy-producing eukaryotic organelle independently arose from the endosymbiosis, retention, and integration of a free-living bacterium into a host cell more than 1.4 billion years ago. Mitochondria came first, evolving from an alphaproteobacterial endosymbiont in an ancestor of all known living eukaryotes, and still exist, in one form or another (1), in all its descendants (2). Plastids came later, via the "primary" endosymbiosis of a cyanobacterium by the eukaryotic ancestor of the Archaeplastida, and then spread laterally to disparate groups through eukaryote-eukaryote endosymbioses (3). Consequently, a significant proportion of the identified eukaryotic diversity has a plastid.With few exceptions (1, 4), mitochondria and plastids contain genomes-chromosomal relics of the bacterial endosymbionts from which they evolved (2, 5). Mitochondrial and plastid DNAs (mtDNAs and ptDNAs) have many traits in common, which is not surprising given their similar evolutionary histories. Both are highly reduced relative to the genomes of extant, free-living alphaproteobacteria and cyanobacteria (2, 5), and both have transferred most of their genes to the host nuclear genome and are therefore reliant on nuclear-encoded, organelle-targeted proteins for the preservation of crucial biochemical pathways and many repair-, replication-, and expression-related functions (6). Both also show a wide and perplexing assortment of genomic architectures (7,8), which has spurred various evolutionary explanations, ranging from ancient inheritance from the RNA world to selection for greater "evolvability" (9, 10).At first glance, genomic complexity w...

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Mitochondrial DNA of Chlamydomonas reinhardtii: the structure of the ends of the linear 15.8-kb genome suggests mechanisms for DNA replication

Cited by 136 publications

References 35 publications

Alteration of Dark Respiration and Reduction of Phototrophic Growth in a Mitochondrial DNA Deletion Mutant of Chlamydomonas Lacking cob, nd4, and the 3′ End of nd5

Alteration of Dark Respiration and Reduction of Phototrophic Growth in a Mitochondrial DNA Deletion Mutant of Chlamydomonas Lacking cob, nd4, and the 3′ End of nd5

Phylogeny and Molecular Evolution of the Green Algae

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

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