Plastid Genome Stability and Repair

Zampini, Éric; Truche, Sébastien; Lepage, Étienne; Tremblay‐Belzile, Samuel; Brisson, Normand

doi:10.1002/9781118647110.ch7

Cited by 10 publications

(13 citation statements)

References 261 publications

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“…MMEJ inhibition by AtOSBs and Whirlies is in agreement with previous models explaining the fate of genomic DNA upon DSBs in plant organelles (10,30,62,64). Plant organelles harbor a bacterial RecA orthologue that mediates homologous recombination and a Rad52-like single-stranded annealing protein, dubbed organellar DNA-binding protein 1 (ODB1).…”

Section: Discussionsupporting

confidence: 92%

Plant organellar DNA polymerases repair double-stranded breaks by microhomology-mediated end-joining

García‐Medel

Baruch‐Torres

Peralta-Castro

et al. 2019

Nucleic Acids Research

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Double-stranded breaks (DSBs) in plant organelles are repaired via genomic rearrangements characterized by microhomologous repeats. These microhomologous signatures predict the existence of an unidentified enzymatic machinery capable of repairing of DSBs via microhomology-mediated end-joining (MMEJ) in plant organelles. Here, we show that organellar DNA polymerases from Arabidopsis thaliana (AtPolIA and AtPolIB) perform MMEJ using microhomologous sequences as short as six nucleotides. AtPolIs execute MMEJ by virtue of two specialized amino acid insertions located in their thumb subdomains. Single-stranded binding proteins (SSBs) unique to plants, AtWhirly2 and organellar single-stranded binding proteins (AtOSBs), hinder MMEJ, whereas canonical mitochondrial SSBs (AtmtSSB1 and AtmtSSB2) do not interfere with MMEJ. Our data predict that organellar DNA rearrangements by MMEJ are a consequence of a competition for the 3′-OH of a DSBs. If AtWhirlies or AtOSBs gain access to the single-stranded DNA (ssDNA) region of a DSB, the reaction will shift towards high-fidelity routes like homologous recombination. Conversely MMEJ would be favored if AtPolIs or AtmtSSBs interact with the DSB. AtPolIs are not phylogenetically related to metazoan mitochondrial DNA polymerases, and the ability of AtPolIs to execute MMEJ may explain the abundance of DNA rearrangements in plant organelles in comparison to animal mitochondria.

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Section: Discussionsupporting

confidence: 92%

Plant organellar DNA polymerases repair double-stranded breaks by microhomology-mediated end-joining

García‐Medel

Baruch‐Torres

Peralta-Castro

et al. 2019

Nucleic Acids Research

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“…There is one homolog in H. monotropa for which predictions of TargetP and DualPred are contradictory, with TargetP suggesting no transit peptide and DualPred suggesting plastid targeting. As RECA participates in plastid recombination and repair (reviewed in [ 52 ]) the loss of RECA may explain both the increase in the substitution rate of the plastid genomes and the increase in their AT-content [ 11 , 18 ], as gene conversion in plastids is GC-biased [ 53 – 55 ].…”

Section: Resultsmentioning

confidence: 99%

RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plants

2018

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BackgroundWhile photosynthesis is the most notable trait of plants, several lineages of plants (so-called full heterotrophs) have adapted to obtain organic compounds from other sources. The switch to heterotrophy leads to profound changes at the morphological, physiological and genomic levels.ResultsHere, we characterize the transcriptomes of three species representing two lineages of mycoheterotrophic plants: orchids (Epipogium aphyllum and Epipogium roseum) and Ericaceae (Hypopitys monotropa). Comparative analysis is used to highlight the parallelism between distantly related fully heterotrophic plants.In both lineages, we observed genome-wide elimination of nuclear genes that encode proteins related to photosynthesis, while systems associated with protein import to plastids as well as plastid transcription and translation remain active. Genes encoding components of plastid ribosomes that have been lost from the plastid genomes have not been transferred to the nuclear genomes; instead, some of the encoded proteins have been substituted by homologs. The nuclear genes of both Epipogium species accumulated nucleotide substitutions twice as rapidly as their photosynthetic relatives; in contrast, no increase in the substitution rate was observed in H. monotropa.ConclusionsFull heterotrophy leads to profound changes in nuclear gene content. The observed increase in the rate of nucleotide substitutions is lineage specific, rather than a universal phenomenon among non-photosynthetic plants.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4968-3) contains supplementary material, which is available to authorized users.

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“…Repeat-mediated changes in plastome architecture that neglect interactions between plastome copies, present as circular and linear multimers and complex linear-branched forms, limit illuminating hypotheses. Recombination between homologous and/or homeologous sequences within and between unit genome copies can yield various arrangements including inversions, duplications and deletions of sequence in one or both of the interacting units (Day and Madesis 2007; Maréchal and Brisson 2010; Zampini et al. 2017).…”

Section: Discussionmentioning

confidence: 99%

“…HR is an integral part of DNA maintenance in plastomes and is employed by both replication and repair pathways (Day and Madesis 2007; Maréchal and Brisson 2010; Zampini et al. 2017).…”

Section: Discussionmentioning

confidence: 99%

Lost and Found: Return of the Inverted Repeat in the Legume Clade Defined by Its Absence

Choi

Jansen

Ruhlman

2019

Genome Biology and Evolution

119

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The plant genome comprises a coevolving, integrated genetic system housed in three subcellular compartments: the nucleus, mitochondrion, and the plastid. The typical land plant plastid genome (plastome) comprises the sum of repeating units of 130–160 kb in length. The plastome inverted repeat (IR) divides each plastome monomer into large and small single copy regions, an architecture highly conserved across land plants. There have been varying degrees of expansion or contraction of the IR, and in a few distinct lineages, including the IR-lacking clade of papilionoid legumes, one copy of the IR has been lost. Completion of plastome sequencing and assembly for 19 Medicago species and Trigonella foenum-graceum and comparative analysis with other IR-lacking clade taxa revealed modest divergence with regard to structural organization overall. However, one clade contained unique variation suggesting an ancestor had experienced repeat-mediated changes in plastome structure. In Medicago minima , a novel IR of ∼9 kb was confirmed and the role of repeat-mediated, recombination-dependent replication in IR reemergence is discussed.

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Plastid Genome Stability and Repair

Cited by 10 publications

References 261 publications

Plant organellar DNA polymerases repair double-stranded breaks by microhomology-mediated end-joining

Plant organellar DNA polymerases repair double-stranded breaks by microhomology-mediated end-joining

RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plants

Lost and Found: Return of the Inverted Repeat in the Legume Clade Defined by Its Absence

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