Transcription-Dependent DNA Transactions in the Mitochondrial Genome of a Yeast Hypersuppressive Petite Mutant

Dyck, Eric Van; Clayton, David A.

doi:10.1128/mcb.18.5.2976

Cited by 27 publications

(20 citation statements)

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“…In other words, the PSþ genome may be more rapidly replicated, contributing to its ability to suppress poly(A)-mediated mRNA instability. A possible parallel would be yeast petite strains, where large deletions in mitochondrial DNA are accompanied by amplification of the remaining sequences (Van Dyck and Clayton, 1998). Another possibility is that the PSþ genome fails to interact with nuclear gene products regulating genome dynamics.…”

Section: Dynamic Alteration Of Cpdna In Spa Strainsmentioning

confidence: 99%

Antisense Transcript and RNA Processing Alterations Suppress Instability of Polyadenylated mRNA in Chlamydomonas Chloroplasts

et al. 2004

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In chloroplasts, the control of mRNA stability is of critical importance for proper regulation of gene expression. The Chlamydomonas reinhardtii strain D26pAtE is engineered such that the atpB mRNA terminates with an mRNA destabilizing polyadenylate tract, resulting in this strain being unable to conduct photosynthesis. A collection of photosynthetic revertants was obtained from D26pAtE, and gel blot hybridizations revealed RNA processing alterations in the majority of these suppressor of polyadenylation (spa) strains, resulting in a failure to expose the atpB mRNA 39 poly(A) tail. Two exceptions were spa19 and spa23, which maintained unusual heteroplasmic chloroplast genomes. One genome type, termed PSþ, conferred photosynthetic competence by contributing to the stability of atpB mRNA; the other, termed PSÿ, was required for viability but could not produce stable atpB transcripts. Based on strand-specific RT-PCR, S1 nuclease protection, and RNA gel blots, evidence was obtained that the PSþ genome stabilizes atpB mRNA by generating an atpB antisense transcript, which attenuates the degradation of the polyadenylated form. The accumulation of double-stranded RNA was confirmed by insensitivity of atpB mRNA from PSþ genome-containing cells to S1 nuclease digestion. To obtain additional evidence for antisense RNA function in chloroplasts, we used strain D26, in which atpB mRNA is unstable because of the lack of a 39 stem-loop structure. In this context, when a 121-nucleotide segment of atpB antisense RNA was expressed from an ectopic site, an elevated accumulation of atpB mRNA resulted. Finally, when spa19 was placed in a genetic background in which expression of the chloroplast exoribonuclease polynucleotide phosphorylase was diminished, the PSþ genome and the antisense transcript were no longer required for photosynthesis. Taken together, our results suggest that antisense RNA in chloroplasts can protect otherwise unstable transcripts from 39!59 exonuclease activity, a phenomenon that may occur naturally in the symmetrically transcribed and densely packed chloroplast genome.

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Section: Dynamic Alteration Of Cpdna In Spa Strainsmentioning

confidence: 99%

Antisense Transcript and RNA Processing Alterations Suppress Instability of Polyadenylated mRNA in Chlamydomonas Chloroplasts

et al. 2004

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“…However, a class of mtDNA deletion [rho Ϫ ] mutants, the hypersuppressive mitochondrial genomes (10), is stably maintained in cells lacking the gene encoding mitochondrial RNA polymerase (13,35). Maintenance of hypersuppressive genomes is also independent of factors such as the histone-like protein Ab2fp or the mitochondrial transcription factor Mtf1p (44 (31). Next, mtDNA was isolated from mdj1-5 cells grown at permissive and nonpermissive temperatures and separated from nuclear DNA in a cesium chloride gradient (Fig.…”

Section: Figmentioning

confidence: 99%

Dual Role of the Mitochondrial Chaperone Mdj1p in Inheritance of Mitochondrial DNA in Yeast

Duchniewicz

Germaniuk

Westermann

et al. 1999

Molecular and Cellular Biology

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Mdj1p, a homolog of the bacterial DnaJ chaperone protein, plays an essential role in the biogenesis of functional mitochondria in the yeast Saccharomyces cerevisiae. We analyzed the role of Mdj1p in the inheritance of mitochondrial DNA (mtDNA). Mitochondrial genomes were rapidly lost in a temperature-sensitive mdj1 mutant under nonpermissive conditions. The activity of mtDNA polymerase was severely reduced in the absence of functional Mdj1p at a nonpermissive temperature, demonstrating the dependence of the enzyme on Mdj1p. At a permissive temperature, the activity of mtDNA polymerase was not affected by the absence of Mdj1p. However, under these conditions, intact [rho ؉ ] genomes were rapidly converted to nonfunctional [rho ؊ ] genomes which were stably propagated in an mdj1 deletion strain. We propose that mtDNA polymerase depends on Mdj1p as a chaperone in order to acquire and/or maintain an active conformation at an elevated temperature. In addition, Mdj1p is required for the inheritance of intact mitochondrial genomes at a temperature supporting optimal growth; this second function appears to be unrelated to the function of Mdj1p in maintaining mtDNA polymerase activity.

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“…In support of this mechanism, each mtDNA replication origin shares sequence similarity with the heavy-strand replication origin of mammalian mtDNA, including the presence of a transcription promoter and three GC-rich clusters (2, 13). RNA synthesized by Rpo41 from mtDNA replication-origin promoters has been detected, and an endoribonuclease that cleaves the synthesized RNA at sites that correspond to regions of transition from RNA to DNA synthesis has been detected (3,49,53). The intact replication-origin promoter is required for hypersuppressiveness (36).…”

mentioning

confidence: 99%

“…The intact replication-origin promoter is required for hypersuppressiveness (36). However, this transcription-dependent process is not the sole mechanism for the initiation of mtDNA replication, since both the replication origin and RPO41 are dispensable for the maintenance of [rho Ϫ ] mtDNA (18,53). In addition, it has been reported that the selective inheritance of hypersuppressive [rho Ϫ ] mtDNA relative to nonhypersuppres-sive [rho Ϫ ] mtDNA (lacking a replication origin) is independent of RPO41 (34).…”

mentioning

confidence: 99%

DNA Recombination-Initiation Plays a Role in the Extremely Biased Inheritance of Yeast [rho⁻] Mitochondrial DNA That Contains the Replication Origin ori5

Ling

Hori

Shibata

2007

Molecular and Cellular Biology

111

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Hypersuppressiveness, as observed inEukaryotic cells gain most of the energy required for cellular functions by oxidative respiration in mitochondria. These organelles contain hundreds to thousands of copies of a mitochondrial DNA (mtDNA) genome that encodes components essential for respiration and protein synthesis. Generally, mitochondrial alleles segregate during vegetative cell growth (vegetative segregation), and all copies of mtDNA within a cell or an individual generally have the same sequence (homoplasmy). In patients with mitochondrial myopathies, the progressive accumulation of mtDNA with large deletions leads to a heteroplasmic state in specific tissues (20; for review, see references 43 and 54). This phenomenon may be caused by the selective replication and/or segregation of mtDNA bearing the deletion; however, genetic analysis of mtDNA processes in mammals has been hampered by the strict maternal inheritance of mitochondria. The yeast Saccharomyces cerevisiae is a suitable model system because of its biparental mtDNA inheritance (14).The extremely biased inheritance of mtDNA with a large deletion is known in S. cerevisiae as "hypersuppressiveness. Two mechanisms for the initiation of mtDNA replication in yeast have been proposed: mitochondrial transcriptional RNA polymerase (Rpo41)-primed initiation and recombination-mediated initiation. Rpo41-primed DNA replication is similar to that observed in mammalian mitochondria. In support of this mechanism, each mtDNA replication origin shares sequence similarity with the heavy-strand replication origin of mammalian mtDNA, including the presence of a transcription promoter and three GC-rich clusters (2, 13). RNA synthesized by Rpo41 from mtDNA replication-origin promoters has been detected, and an endoribonuclease that cleaves the synthesized RNA at sites that correspond to regions of transition from RNA to DNA synthesis has been detected (3,49,53). The intact replication-origin promoter is required for hypersuppressiveness (36). However, this transcription-dependent process is not the sole mechanism for the initiation of mtDNA replication, since both the replication origin and RPO41 are dispensable for the maintenance of [rho Ϫ ] mtDNA (18,53). In addition, it has been reported that the selective inheritance of hypersuppressive [rho Ϫ ] mtDNA relative to nonhypersuppres-* Corresponding author. Mailing address:

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Transcription-Dependent DNA Transactions in the Mitochondrial Genome of a Yeast Hypersuppressive Petite Mutant

Cited by 27 publications

References 50 publications

Antisense Transcript and RNA Processing Alterations Suppress Instability of Polyadenylated mRNA in Chlamydomonas Chloroplasts

Antisense Transcript and RNA Processing Alterations Suppress Instability of Polyadenylated mRNA in Chlamydomonas Chloroplasts

Dual Role of the Mitochondrial Chaperone Mdj1p in Inheritance of Mitochondrial DNA in Yeast

DNA Recombination-Initiation Plays a Role in the Extremely Biased Inheritance of Yeast [rho⁻] Mitochondrial DNA That Contains the Replication Origin ori5

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Transcription-Dependent DNA Transactions in the Mitochondrial Genome of a Yeast Hypersuppressive Petite Mutant

Cited by 27 publications

References 50 publications

Antisense Transcript and RNA Processing Alterations Suppress Instability of Polyadenylated mRNA in Chlamydomonas Chloroplasts

Antisense Transcript and RNA Processing Alterations Suppress Instability of Polyadenylated mRNA in Chlamydomonas Chloroplasts

Dual Role of the Mitochondrial Chaperone Mdj1p in Inheritance of Mitochondrial DNA in Yeast

DNA Recombination-Initiation Plays a Role in the Extremely Biased Inheritance of Yeast [rho−] Mitochondrial DNA That Contains the Replication Origin ori5

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DNA Recombination-Initiation Plays a Role in the Extremely Biased Inheritance of Yeast [rho⁻] Mitochondrial DNA That Contains the Replication Origin ori5