The plant mitochondrial genome: Dynamics and maintenance

doi:10.1016/j.biochi.2013.09.016

Biochimie

Volume 100, May 2014, Pages 107-120

https://doi.org/10.1016/j.biochi.2013.09.016 Get rights and content

Highlights

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Models on the structure of the mitochondrial DNA of plants are presented.
•
The relevance of plasmids in mitochondria is discussed.
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Homologous recombination is responsible for the rapid evolution of the mtDNA.
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Alternative mechanisms of recombination exist in plant mitochondria.
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An update on plant mitochondrial base excision repair is presented.

Abstract

Plant mitochondria have a complex and peculiar genetic system. They have the largest genomes, as compared to organelles from other eukaryotic organisms. These can expand tremendously in some species, reaching the megabase range. Nevertheless, whichever the size, the gene content remains modest and restricted to a few polypeptides required for the biogenesis of the oxidative phosphorylation chain complexes, ribosomal proteins, transfer RNAs and ribosomal RNAs. The presence of autonomous plasmids of essentially unknown function further enhances the level of complexity. The physical organization of the plant mitochondrial DNA includes a set of sub-genomic forms resulting from homologous recombination between repeats, with a mixture of linear, circular and branched structures. This material is compacted into membrane-bound nucleoids, which are the inheritance units but also the centers of genome maintenance and expression. Recombination appears to be an essential characteristic of plant mitochondrial genetic processes, both in shaping and maintaining the genome. Under nuclear surveillance, recombination is also the basis for the generation of new mitotypes and is involved in the evolution of the mitochondrial DNA. In line with, or as a consequence of its complex physical organization, replication of the plant mitochondrial DNA is likely to occur through multiple mechanisms, potentially involving recombination processes. We give here a synthetic view of these aspects.

Introduction

Mitochondria are key players in plant development, fitness and reproduction. Their contribution to energy production, metabolism and cell homeostasis relies on the performance of their own genetic system that makes them semi-autonomous. As in other organisms, the mitochondrial genome in plants encodes a series of essential polypeptides that build up the complexes of the oxidative phosphorylation chain, together with nuclear-encoded subunits. But plant mitochondrial DNAs (mtDNAs) have remarkable features that distinguish them from their animal and fungal counterparts. In particular, higher plants harbor large mtDNAs that are highly variable in size and structural organization. On top of that, in many plant species, mitochondria contain various forms of plasmids that replicate independently from the main chromosome. In most plant species, the mtDNA gene sequences evolve very slowly, as compared to animal mtDNA sequences, and point mutations are rare. It is believed that this is because plant mitochondria contain an active DNA recombination system that allows copy correction of mutations. Indeed, numerous studies have shown that plant mitochondrial genomes undergo extensive and high frequency homologous recombination (HR). Such processes make plant mtDNA prone to rearrangements. When not lethal, mtDNA mutations/rearrangements can generate severe phenotypes or cause cytoplasmic male sterility (CMS). Hence the requirement for efficient DNA repair and maintenance pathways in a context where oxidative pressure, replication defaults or environmental hazard generate base modifications and strand breaks. Finally, mitochondrial genome dynamics generates heteroplasmy, with alternative mtDNA configurations coexisting with the main mtDNA. Segregation of alternative mitotypes significantly contributes to the rapid evolution of the plant mtDNA structure. The present review addresses these issues, with special emphasis on the specificities of the plant mitochondrial genetic system.

Section snippets

Genome size and content

The structure of higher plant mitochondrial genomes has a number of unique features. Whereas most animals possess circular mtDNAs of 15–17 kb in size, the mitochondrial genomes of plants are much larger and differ greatly in size, even between very close species or within species [1], [2]. They commonly range between 200 and 750 kb in angiosperms [1], but with a tremendous further extension in some lineages. As an example, proliferation of dispersed repeats, expansion of existing introns and

Mitochondrial DNA replication

Replication of plant mitochondrial genomes is far from being understood. Several factors involved in organellar genome replication have been identified by sequence homology and from proteomic data. Among those, plant organellar DNA polymerases were identified by their similarities to the known mitochondrial DNA polymerase of animals and yeast. In A. thaliana, there are two organellar DNA polymerases, Pol1A and Pol1B, which are dual-targeted to both mitochondria and plastids [33], [34], [35] and

Mitochondrial plasmids

In addition to a large and dynamic main genome, mitochondria of many higher plant species contain a variety of smaller DNA molecules whose size can range from 0.7 to over 20 kb [51], [52], [53], [54]. These can be regarded as extrachromosomal replicons or plasmids that can be autonomously replicated in mitochondria because they are usually present at a high stoichiometry relative to the main genome [54]. Multimeric forms of these mitochondrial plasmids have been observed that likely result from

Recombination factors

At the core of the organellar homologous recombination (HR) activities, there are eubacterial-type RecA proteins inherited from the corresponding prokaryotic endosymbiont ancestors. RecA catalyzes DNA strand-exchange during homologous recombination. Initially, RecA polymerizes on single-stranded DNA to form a long presynaptic DNA-protein filament. In the presence of homologous double-stranded DNA, RecA catalyzes strand exchange, forming a D-loop that is a common intermediate in homologous

Recombination-dependent repair

Repair of DSBs is essential for genome stability because they can lead to collapsed replication forks, gene loss and genome instability. The sequence of plant mtDNAs revealed numerous examples of gene chimeras or fusions of unrelated sequences likely emerging from repair by illegitimate recombination, involving none or just a few nucleotides. Several of these gene chimeras have been associated with CMS phenotypes.

In chloroplasts there is extensive evidence for the participation of

Mitochondrial genome segregation and evolution

An important consequence of mtDNA heteroplasmy is that, from a heteroplasmic parent, individuals can segregate in which certain substoichiometric mitotypes were amplified and became the predominant mtDNA. This process is called substoichiometric shifting (SSS) [131], [132]. SSS can result in the activation or silencing of mitochondrial sequences, including the expression of gene chimeras, thus altering mitochondrial gene expression with potentially deleterious consequences to the plant. But SSS

Conclusion

In many aspects, the genetics of plant mitochondria is more complex than that of most other organisms. The capacity to integrate and/or expand intergenic non-coding sequences in the organellar genome is remarkable, especially versus the strictly compact mammalian mtDNA. One might speculate that gain of sequences is related to the competence of plant mitochondria for DNA import [141]. Notably, both the acquisition of plasmids and the import competence are shared with fungal mitochondria [142].

Acknowledgments

Our projects are funded by the French Centre National de la Recherche Scientifique (CNRS, UPR2357), the Université de Strasbourg (UdS), the Agence Nationale de la Recherche (ANR-06-MRAR-037-02, ANR-09-BLAN-0240-01) and the Ministère de la Recherche et de l'Enseignement Supérieur (Investissements d'Avenir/Laboratoire d'Excellence MitoCross).

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ReviewThe plant mitochondrial genome: Dynamics and maintenance

Highlights

Abstract

Introduction

Section snippets

Genome size and content

Mitochondrial DNA replication

Mitochondrial plasmids

Recombination factors

Recombination-dependent repair

Mitochondrial genome segregation and evolution

Conclusion

Acknowledgments

Mitochondrion

Trends Cell Biol.

Mol. Cells

Int. Rev. Cytol.

Biochim. Biophys. Acta

J. Mol. Biol.

Mol. Cell

J. Theor. Biol.

Mitochondrion

Intern. Rev. Cytol.

J. Mol. Biol.

Plasmid

Gene

Cell

Trends Plant Sci.

J. Biol. Chem.

Comparisons among two fertile and three male-sterile mitochondrial genomes of maize

Genetics

Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber

Plant Cell

Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates

PLoS Biol.

Fewer genes than organelles: extremely low and variable gene copy numbers in mitochondria of somatic plant cells

Plant J.

The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides

Nat. Genet.

Sequence and organization of the human mitochondrial genome

Nature

Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats

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

Physical mapping of the mitochondrial genome of Arabidopsis thaliana by cosmid and YAC clones

Plant J.

The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants

Mol. Genet. Genom.

Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome

Nucleic Acids Res.

Reaching for the ring: the study of mitochondrial genome structure

Curr. Genet.

Size and structure of replicating mitochondrial DNA in cultured tobacco cells

Plant Cell

High content, size and distribution of single-stranded DNA in the mitochondria of Chenopodium album (L.)

Plant Mol. Biol.

Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis

BMC Biol.

RecA-dependent DNA repair results in increased heteroplasmy of the Arabidopsis mitochondrial genome

Plant Physiol.

Crystal structures of DNA–Whirly complexes and their role in Arabidopsis organelle genome repair

Plant Cell

Small, repetitive DNAs contribute significantly to the expanded mitochondrial genome of cucumber

Genetics

Mitochondrial DNA transcription regulation and nucleoid organization

J. Inherit. Metab. Dis.

The mitochondrial nucleoid: integrating mitochondrial DNA into cellular homeostasis

Cold Spring Harb. Perspect. Biol.

Structural and functional characterizations of mung bean mitochondrial nucleoids

Nucleic Acids Res.

Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions

Plant Physiol.

Organization of mitochondrial-nucleoids in BY-2 cultured tobacco cells

Cytologia

Evidence that core histone H3 is targeted to the mitochondria in Brassica oleracea

Cell Biol. Int.

SirT3 is a nuclear NAD+-dependent histone deacetylase that translocates to the mitochondria upon cellular stress

Genes Dev.

Histone H3 is absent from organelle nucleoids in BY-2 cultured tobacco cells

Cell Biol. Int.

Actin in mung bean mitochondria and implications for its function

Review
The plant mitochondrial genome: Dynamics and maintenance

SirT3 is a nuclear NAD⁺-dependent histone deacetylase that translocates to the mitochondria upon cellular stress