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Plants
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Co-Adaptation between the Nuclear and Organelle Genomes in Plants
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Co-Adaptation between the Nuclear and Organelle Genomes in Plants

A special issue of Plants (ISSN 2223-7747).

Deadline for manuscript submissions: closed (1 April 2020) | Viewed by 17941

Special Issue Editor

Dr. Françoise Budar

E-Mail Website
Guest Editor
Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, 78000 Versailles, France
Interests: cytoplasmic genetics; cytoplasmic male sterility; plant reproduction; cytonuclear co-adaptation; mitochondrial gene expression

Special Issue Information

Dear Colleagues,

Co-adaptation between plant nuclear and organelle genomes is theoretically expected to occur whenever a nuclear-encoded factor—most often a protein—interacts with an organelle gene or gene product, and when genetic variation in either partner has consequences in the phenotypic output of the molecular interaction. Mitochondria and chloroplasts have pivotal roles in energy metabolism in plant cells but are also important players in the response of plants to their environment. It is increasingly evident that cytonuclear interactions are relevant for adaptive and agronomically important phenotypes—beyond the well-known cytoplasmic male sterilities—including germination, fitness in challenging environments, response to biotic and abiotic stresses, and metabolic composition of harvested products.

A deeper and more comprehensive knowledge of the co-adaptation between nuclear and organelle genomes will undoubtedly enhance our understanding of the coordinated evolution of plant genomes. It will also provide important insights into plant adaptation to their environment, in particular by connecting the organelle retrograde signaling pathways to genetic variation, and suggest new paths for the consideration of cytoplasmic variants in crop breeding strategies.

As a contribution to this objective, this Special Issue of Plants will highlight genetic and molecular interactions between nuclear and organelle genes and their effects on the plant phenotype and adaptation to the environment. It will also explore the extent of genetic variation in cytoplasmic genomes and their nuclear partners, and the evolution mechanisms at work.

Dr. Françoise Budar
Guest Editor

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Plants is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • organelle genetic diversity in plants
  • nuclear-encoded organelle factors
  • co-adaptation
  • genome co-evolution
  • molecular co-evolution
  • diversifying selection
  • cytoplasmic male sterility and restoration
  • nuclear-encoded factors for maintenance and expression of organelle genomes
  • cytoplasmic genetic resources in crops
  • cytoplasmic breeding
  • role of organelles in plant adaptation to their environment
  • nuclear–organelle conflicts

Published Papers (5 papers)

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Research

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31 pages, 4701 KiB  
Article
The Consequences of a Disruption in Cyto-Nuclear Coadaptation on the Molecular Response to a Nitrate Starvation in Arabidopsis
by Fabien Chardon, Gwendal Cueff, Etienne Delannoy, Fabien Aubé, Aurélia Lornac, Magali Bedu, Françoise Gilard, Stéphanie Pateyron, Hélène Rogniaux, Audrey Gargaros, Hakim Mireau, Loïc Rajjou, Marie-Laure Martin-Magniette and Françoise Budar
Plants 2020, 9(5), 573; https://doi.org/10.3390/plants9050573 - 1 May 2020
Viewed by 3048
Abstract
Mitochondria and chloroplasts are important actors in the plant nutritional efficiency. So, it could be expected that a disruption of the coadaptation between nuclear and organellar genomes impact plant response to nutrient stresses. We addressed this issue using two Arabidopsis accessions, namely Ct-1 [...] Read more.
Mitochondria and chloroplasts are important actors in the plant nutritional efficiency. So, it could be expected that a disruption of the coadaptation between nuclear and organellar genomes impact plant response to nutrient stresses. We addressed this issue using two Arabidopsis accessions, namely Ct-1 and Jea, and their reciprocal cytolines possessing the nuclear genome from one parent and the organellar genomes of the other one. We measured gene expression, and quantified proteins and metabolites under N starvation and non-limiting conditions. We observed a typical response to N starvation at the phenotype and molecular levels. The phenotypical response to N starvation was similar in the cytolines compared to the parents. However, we observed an effect of the disruption of genomic coadaptation at the molecular levels, distinct from the previously described responses to organellar stresses. Strikingly, genes differentially expressed in cytolines compared to parents were mainly repressed in the cytolines. These genes encoded more mitochondrial and nuclear proteins than randomly expected, while N starvation responsive ones were enriched in genes for chloroplast and nuclear proteins. In cytolines, the non-coadapted cytonuclear genomic combination tends to modulate the response to N starvation observed in the parental lines on various biological processes. Full article
(This article belongs to the Special Issue Co-Adaptation between the Nuclear and Organelle Genomes in Plants)
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Review

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18 pages, 314 KiB  
Review
Cytonuclear Genetic Incompatibilities in Plant Speciation
by Zoé Postel and Pascal Touzet
Plants 2020, 9(4), 487; https://doi.org/10.3390/plants9040487 - 10 Apr 2020
Cited by 32 | Viewed by 3609
Abstract
Due to the endosymbiotic origin of organelles, a pattern of coevolution and coadaptation between organellar and nuclear genomes is required for proper cell function. In this review, we focus on the impact of cytonuclear interaction on the reproductive isolation of plant species. We [...] Read more.
Due to the endosymbiotic origin of organelles, a pattern of coevolution and coadaptation between organellar and nuclear genomes is required for proper cell function. In this review, we focus on the impact of cytonuclear interaction on the reproductive isolation of plant species. We give examples of cases where species exhibit barriers to reproduction which involve plastid-nuclear or mito-nuclear genetic incompatibilities, and describe the evolutionary processes at play. We also discuss potential mechanisms of hybrid fitness recovery such as paternal leakage. Finally, we point out the possible interplay between plant mating systems and cytonuclear coevolution, and its consequence on plant speciation. Full article
(This article belongs to the Special Issue Co-Adaptation between the Nuclear and Organelle Genomes in Plants)
12 pages, 267 KiB  
Review
What Does the Molecular Genetics of Different Types of Restorer-of-Fertility Genes Imply?
by Tomohiko Kubo, Takumi Arakawa, Yujiro Honma and Kazuyoshi Kitazaki
Plants 2020, 9(3), 361; https://doi.org/10.3390/plants9030361 - 13 Mar 2020
Cited by 12 | Viewed by 4102
Abstract
Cytoplasmic male sterility (CMS) is a widely used trait for hybrid seed production. Although male sterility is caused by S cytoplasm (male-sterility inducing mitochondria), the action of S cytoplasm is suppressed by restorer-of-fertility (Rf), a nuclear gene. Hence, the genetics of [...] Read more.
Cytoplasmic male sterility (CMS) is a widely used trait for hybrid seed production. Although male sterility is caused by S cytoplasm (male-sterility inducing mitochondria), the action of S cytoplasm is suppressed by restorer-of-fertility (Rf), a nuclear gene. Hence, the genetics of Rf has attained particular interest among plant breeders. The genetic model posits Rf diversity in which an Rf specifically suppresses the cognate S cytoplasm. Molecular analysis of Rf loci in plants has identified various genes; however, pentatricopeptide repeat (PPR) protein (a specific type of RNA-binding protein) is so prominent as the Rf-gene product that Rfs have been categorized into two classes, PPR and non-PPR. In contrast, several shared features between PPR- and some non-PPR Rfs are apparent, suggesting the possibility of another grouping. Our present focus is to group Rfs by molecular genetic classes other than the presence of PPRs. We propose three categories that define partially overlapping groups of Rfs: association with post-transcriptional regulation of mitochondrial gene expression, resistance gene-like copy number variation at the locus, and lack of a direct link to S-orf (a mitochondrial ORF associated with CMS). These groups appear to reflect their own evolutionary background and their mechanism of conferring S cytoplasm specificity. Full article
(This article belongs to the Special Issue Co-Adaptation between the Nuclear and Organelle Genomes in Plants)
17 pages, 260 KiB  
Review
Genetic and Molecular Genetic Basis of Nuclear-Plastid Incompatibilities
by Vera S. Bogdanova
Plants 2020, 9(1), 23; https://doi.org/10.3390/plants9010023 - 23 Dec 2019
Cited by 9 | Viewed by 3355
Abstract
Genetic analysis of nuclear-cytoplasm incompatibilities is not straightforward and requires an elaborated experimental design. A number of species have been genetically studied, but notable advances in genetic mapping of nuclear loci involved in nuclear-plastid incompatibility have been achieved only in wheat and pea. [...] Read more.
Genetic analysis of nuclear-cytoplasm incompatibilities is not straightforward and requires an elaborated experimental design. A number of species have been genetically studied, but notable advances in genetic mapping of nuclear loci involved in nuclear-plastid incompatibility have been achieved only in wheat and pea. This review focuses on the study of the genetic background underlying nuclear-plastid incompatibilities, including cases where the molecular genetic basis of such incompatibility has been unveiled, such as in tobacco, Oenothera, pea, and wheat. Full article
(This article belongs to the Special Issue Co-Adaptation between the Nuclear and Organelle Genomes in Plants)

Other

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18 pages, 963 KiB  
Opinion
Why so Complex? The Intricacy of Genome Structure and Gene Expression, Associated with Angiosperm Mitochondria, May Relate to the Regulation of Embryo Quiescence or Dormancy—Intrinsic Blocks to Early Plant Life
by Corinne Best, Ron Mizrahi and Oren Ostersetzer-Biran
Plants 2020, 9(5), 598; https://doi.org/10.3390/plants9050598 - 8 May 2020
Cited by 19 | Viewed by 3276
Abstract
Mitochondria play key roles in cellular-energy metabolism and are vital for plant-life, such as for successful germination and early-seedling establishment. Most mitochondria contain their own genetic system (mtDNA, mitogenome), with an intrinsic protein-synthesis machinery. Although the challenges of maintaining prokaryotic-type structures and functions [...] Read more.
Mitochondria play key roles in cellular-energy metabolism and are vital for plant-life, such as for successful germination and early-seedling establishment. Most mitochondria contain their own genetic system (mtDNA, mitogenome), with an intrinsic protein-synthesis machinery. Although the challenges of maintaining prokaryotic-type structures and functions are common to Eukarya, land plants possess some of the most complex organelle composition of all known organisms. Angiosperms mtDNAs are characteristically the largest and least gene-dense among the eukaryotes. They often contain highly-variable intergenic regions of endogenous or foreign origins and undergo frequent recombination events, which result in different mtDNA configurations, even between closely-related species. The expression of the mitogenome in angiosperms involves extensive mtRNA processing steps, including numerous editing and splicing events. Why do land-plant’s mitochondria have to be so complex? The answer to this remains a matter of speculation. We propose that this complexity may have arisen throughout the terrestrialization of plants, as a means to control embryonic mitochondrial functions —a critical adaptive trait to optimize seed germination. The unique characteristics of plant mtDNA may play pivotal roles in the nuclear-regulation of organellar biogenesis and metabolism, possibly to control embryos quiescence or dormancy, essential determinants for the establishment of viable plantlets that can survive post-germination. Full article
(This article belongs to the Special Issue Co-Adaptation between the Nuclear and Organelle Genomes in Plants)
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