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RNA Biology in Plant Organelles
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Special Issue "RNA Biology in Plant Organelles"

A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Plant, Algae and Fungi Cell Biology".

Deadline for manuscript submissions: closed (31 December 2020) | Viewed by 17717

Special Issue Editors

Dr. Philippe Giegé

E-Mail Website
Guest Editor
Institute of Plant Molecular Biology, IBMP-CNRS, University of Strasbourg, 67084 Strasbourg, France
Interests: plant gene expression; mitochondria and chloroplasts; RNA binding proteins; RNA maturation; translation; ribosomes
Dr. Laurence Marechal-Drouard

E-Mail Website
Guest Editor
Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, 67084 Strasbourg, France
Interests: higher plants; green algae (Chlamydomonas); transfer RNAs; tRNA-derived fragments; translation apparatus; mitochondria

Special Issue Information

Dear Colleagues,

Mitochondria and chloroplasts are essential components of the plant cell. They are derived from the successive endosymbiosis of an alpha-proteobacterial and a cyanobacterial ancestor. Compared with other eukaryotes, RNA metabolism in plant organelles is complex and combines bacterial-like traits with novel features that evolved in the host cell. These complex RNA processes are regulated by families of nuclear-encoded RNA binding proteins, often specific to eukaryotes and prominent in the green lineage. The variety of RNA precursors accumulating in chloroplasts and mitochondria highlights the importance of posttranscriptional processes to determine the size and abundance of transcripts. In he recent years, tremendous progress has occurred in identifying novel factors, often belonging to the large family of helical repeat modular proteins and in understanding how these factors are organized into functional complexes. However, major gaps remain, in particular in understanding how independent RNA processes are interconnected to achieve organellar gene expression and how these pathways are regulated during plant development or in response to environmental cues.

This Special Issue aims to summarize the current knowledge on RNA metabolism in plant organelles, from RNA transcription to translation, with a special focus on their unique features that are controlled by plant-specific trans-factors.

We look forward to your contributions.

Dr. Philippe Giegé
Dr. Laurence Marechal-Drouard
Guest Editors

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. Cells 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

  • photosynthetic organisms
  • mitochondria and chloroplasts
  • gene expression and regulation
  • transcriptomic
  • epitranscriptomic
  • RNA binding proteins

Published Papers (7 papers)

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Research

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15 pages, 1963 KiB  
Article
Transcriptional Landscape and Splicing Efficiency in Arabidopsis Mitochondria
by
Laura E. Garcia
and
M. Virginia Sanchez-Puerta
Cells 2021, 10(8), 2054; https://doi.org/10.3390/cells10082054 - 11 Aug 2021
Cited by 3 | Viewed by 1932
Abstract
Plant mitochondrial transcription is initiated from multiple promoters without an apparent motif, which precludes their identification in other species based on sequence comparisons. Even though coding regions take up only a small fraction of plant mitochondrial genomes, deep RNAseq studies uncovered that these [...] Read more.
Plant mitochondrial transcription is initiated from multiple promoters without an apparent motif, which precludes their identification in other species based on sequence comparisons. Even though coding regions take up only a small fraction of plant mitochondrial genomes, deep RNAseq studies uncovered that these genomes are fully or nearly fully transcribed with significantly different RNA read depth across the genome. Transcriptomic analysis can be a powerful tool to understand the transcription process in diverse angiosperms, including the identification of potential promoters and co-transcribed genes or to study the efficiency of intron splicing. In this work, we analyzed the transcriptional landscape of the Arabidopsis mitochondrial genome (mtDNA) based on large-scale RNA sequencing data to evaluate the use of RNAseq to study those aspects of the transcription process. We found that about 98% of the Arabidopsis mtDNA is transcribed with highly different RNA read depth, which was elevated in known genes. The location of a sharp increase in RNA read depth upstream of genes matched the experimentally identified promoters. The continuously high RNA read depth across two adjacent genes agreed with the known co-transcribed units in Arabidopsis mitochondria. Most intron-containing genes showed a high splicing efficiency with no differences between cis and trans-spliced introns or between genes with distinct splicing mechanisms. Deep RNAseq analyses of diverse plant species will be valuable to recognize general and lineage-specific characteristics related to the mitochondrial transcription process. Full article
(This article belongs to the Special Issue RNA Biology in Plant Organelles)
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13 pages, 2353 KiB  
Article
The Pentatricopeptide Repeat Protein MEF100 Is Required for the Editing of Four Mitochondrial Editing Sites in Arabidopsis
by
Bernard Gutmann
,
Michael Millman
,
Lilian Vincis Pereira Sanglard
,
Ian Small
and
Catherine Colas des Francs-Small
Cells 2021, 10(2), 468; https://doi.org/10.3390/cells10020468 - 22 Feb 2021
Cited by 3 | Viewed by 2154
Abstract
In Arabidopsis thaliana there are more than 600 C-to-U RNA editing events in the mitochondria and at least 44 in the chloroplasts. Pentatricopeptide repeat (PPR) proteins provide the specificity for these reactions. They recognize RNA sequences in a partially predictable fashion via key [...] Read more.
In Arabidopsis thaliana there are more than 600 C-to-U RNA editing events in the mitochondria and at least 44 in the chloroplasts. Pentatricopeptide repeat (PPR) proteins provide the specificity for these reactions. They recognize RNA sequences in a partially predictable fashion via key amino acids at the fifth and last position in each PPR motif that bind to individual ribonucleotides. A combined approach of RNA-Seq, mutant complementation, electrophoresis of mitochondrial protein complexes and Western blotting allowed us to show that MEF100, a PPR protein identified in a genetic screen for mutants resistant to an inhibitor of γ -glutamylcysteine synthetase, is required for the editing of nad1-493, nad4-403, nad7-698 and ccmFN2-356 sites in Arabidopsis mitochondria. The absence of editing in mef100 leads to a decrease in mitochondrial Complex I activity, which probably explains the physiological phenotype. Some plants have lost the requirement for MEF100 at one or more of these sites through mutations in the mitochondrial genome. We show that loss of the requirement for MEF100 editing leads to divergence in the MEF100 binding site. Full article
(This article belongs to the Special Issue RNA Biology in Plant Organelles)
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25 pages, 6134 KiB  
Article
Arabidopsis Mitochondrial Transcription Termination Factor mTERF2 Promotes Splicing of Group IIB Introns
by
Kwanuk Lee
,
Dario Leister
and
Tatjana Kleine
Cells 2021, 10(2), 315; https://doi.org/10.3390/cells10020315 - 03 Feb 2021
Cited by 14 | Viewed by 2494
Abstract
Plastid gene expression (PGE) is essential for chloroplast biogenesis and function and, hence, for plant development. However, many aspects of PGE remain obscure due to the complexity of the process. A hallmark of nuclear-organellar coordination of gene expression is the emergence of nucleus-encoded [...] Read more.
Plastid gene expression (PGE) is essential for chloroplast biogenesis and function and, hence, for plant development. However, many aspects of PGE remain obscure due to the complexity of the process. A hallmark of nuclear-organellar coordination of gene expression is the emergence of nucleus-encoded protein families, including nucleic-acid binding proteins, during the evolution of the green plant lineage. One of these is the mitochondrial transcription termination factor (mTERF) family, the members of which regulate various steps in gene expression in chloroplasts and/or mitochondria. Here, we describe the molecular function of the chloroplast-localized mTERF2 in Arabidopsis thaliana. The complete loss of mTERF2 function results in embryo lethality, whereas directed, microRNA (amiR)-mediated knockdown of MTERF2 is associated with perturbed plant development and reduced chlorophyll content. Moreover, photosynthesis is impaired in amiR-mterf2 plants, as indicated by reduced levels of photosystem subunits, although the levels of the corresponding messenger RNAs are not affected. RNA immunoprecipitation followed by RNA sequencing (RIP-Seq) experiments, combined with whole-genome RNA-Seq, RNA gel-blot, and quantitative RT-PCR analyses, revealed that mTERF2 is required for the splicing of the group IIB introns of ycf3 (intron 1) and rps12. Full article
(This article belongs to the Special Issue RNA Biology in Plant Organelles)
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24 pages, 1547 KiB  
Article
Differentially Expressed Genes Shared by Two Distinct Cytoplasmic Male Sterility (CMS) Types of Silene vulgaris Suggest the Importance of Oxidative Stress in Pollen Abortion
by
Manuela Krüger
,
Oushadee A. J. Abeyawardana
,
Claudia Krüger
,
Miloslav Juříček
and
Helena Štorchová
Cells 2020, 9(12), 2700; https://doi.org/10.3390/cells9122700 - 16 Dec 2020
Cited by 6 | Viewed by 2289
Abstract
Cytoplasmic male sterility (CMS), encoded by the interacting mitochondrial and nuclear genes, causes pollen abortion or non-viability. CMS is widely used in agriculture and extensively studied in crops. Much less is known about CMS in wild species. We performed a comparative transcriptomic analysis [...] Read more.
Cytoplasmic male sterility (CMS), encoded by the interacting mitochondrial and nuclear genes, causes pollen abortion or non-viability. CMS is widely used in agriculture and extensively studied in crops. Much less is known about CMS in wild species. We performed a comparative transcriptomic analysis of male sterile and fertile individuals of Silene vulgaris, a model plant for the study of gynodioecy, to reveal the genes responsible for pollen abortion in this species. We used RNA-seq datasets previously employed for the analysis of mitochondrial and plastid transcriptomes of female and hermaphrodite flower buds, making it possible to compare the transcriptomes derived from three genomes in the same RNA specimen. We assembled de novo transcriptomes for two haplotypes of S. vulgaris and identified differentially expressed genes between the females and hermaphrodites, associated with stress response or pollen development. The gene for alternative oxidase was downregulated in females. The genetic pathways controlling CMS in S. vulgaris are similar to those in crops. The high number of the differentially expressed nuclear genes contrasts with the uniformity of organellar transcriptomes across genders, which suggests these pathways are evolutionarily conserved and that selective mechanisms may shield organellar transcription against changes in the cytoplasmic transcriptome. Full article
(This article belongs to the Special Issue RNA Biology in Plant Organelles)
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Review

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23 pages, 1885 KiB  
Review
The Chloroplast Trans-Splicing RNA–Protein Supercomplex from the Green Alga Chlamydomonas reinhardtii
by
Ulrich Kück
and
Olga Schmitt
Cells 2021, 10(2), 290; https://doi.org/10.3390/cells10020290 - 01 Feb 2021
Cited by 7 | Viewed by 2585
Abstract
In eukaryotes, RNA trans-splicing is a significant RNA modification process for the end-to-end ligation of exons from separately transcribed primary transcripts to generate mature mRNA. So far, three different categories of RNA trans-splicing have been found in organisms within a diverse [...] Read more.
In eukaryotes, RNA trans-splicing is a significant RNA modification process for the end-to-end ligation of exons from separately transcribed primary transcripts to generate mature mRNA. So far, three different categories of RNA trans-splicing have been found in organisms within a diverse range. Here, we review trans-splicing of discontinuous group II introns, which occurs in chloroplasts and mitochondria of lower eukaryotes and plants. We discuss the origin of intronic sequences and the evolutionary relationship between chloroplast ribonucleoprotein complexes and the nuclear spliceosome. Finally, we focus on the ribonucleoprotein supercomplex involved in trans-splicing of chloroplast group II introns from the green alga Chlamydomonas reinhardtii. This complex has been well characterized genetically and biochemically, resulting in a detailed picture of the chloroplast ribonucleoprotein supercomplex. This information contributes substantially to our understanding of the function of RNA-processing machineries and might provide a blueprint for other splicing complexes involved in trans- as well as cis-splicing of organellar intron RNAs. Full article
(This article belongs to the Special Issue RNA Biology in Plant Organelles)
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16 pages, 685 KiB  
Review
Research Progress in the Molecular Functions of Plant mTERF Proteins
by
Pedro Robles
and
Víctor Quesada
Cells 2021, 10(2), 205; https://doi.org/10.3390/cells10020205 - 21 Jan 2021
Cited by 12 | Viewed by 2538
Abstract
Present-day chloroplast and mitochondrial genomes contain only a few dozen genes involved in ATP synthesis, photosynthesis, and gene expression. The proteins encoded by these genes are only a small fraction of the many hundreds of proteins that act in chloroplasts and mitochondria. Hence, [...] Read more.
Present-day chloroplast and mitochondrial genomes contain only a few dozen genes involved in ATP synthesis, photosynthesis, and gene expression. The proteins encoded by these genes are only a small fraction of the many hundreds of proteins that act in chloroplasts and mitochondria. Hence, the vast majority, including components of organellar gene expression (OGE) machineries, are encoded by nuclear genes, translated into the cytosol and imported to these organelles. Consequently, the expression of nuclear and organellar genomes has to be very precisely coordinated. Furthermore, OGE regulation is crucial to chloroplast and mitochondria biogenesis, and hence, to plant growth and development. Notwithstanding, the molecular mechanisms governing OGE are still poorly understood. Recent results have revealed the increasing importance of nuclear-encoded modular proteins capable of binding nucleic acids and regulating OGE. Mitochondrial transcription termination factor (mTERF) proteins are a good example of this category of OGE regulators. Plant mTERFs are located in chloroplasts and/or mitochondria, and have been characterized mainly from the isolation and analyses of Arabidopsis and maize mutants. These studies have revealed their fundamental roles in different plant development aspects and responses to abiotic stress. Fourteen mTERFs have been hitherto characterized in land plants, albeit to a different extent. These numbers are limited if we consider that 31 and 35 mTERFs have been, respectively, identified in maize and Arabidopsis. Notwithstanding, remarkable progress has been made in recent years to elucidate the molecular mechanisms by which mTERFs regulate OGE. Consequently, it has been experimentally demonstrated that plant mTERFs are required for the transcription termination of chloroplast genes (mTERF6 and mTERF8), transcriptional pausing and the stabilization of chloroplast transcripts (MDA1/mTERF5), intron splicing in chloroplasts (BSM/RUG2/mTERF4 and Zm-mTERF4) and mitochondria (mTERF15 and ZmSMK3) and very recently, also in the assembly of chloroplast ribosomes and translation (mTERF9). This review aims to provide a detailed update of current knowledge about the molecular functions of plant mTERF proteins. It principally focuses on new research that has made an outstanding contribution to unravel the molecular mechanisms by which plant mTERFs regulate the expression of chloroplast and mitochondrial genomes. Full article
(This article belongs to the Special Issue RNA Biology in Plant Organelles)
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Other

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13 pages, 1209 KiB  
Opinion
GUN1 and Plastid RNA Metabolism: Learning from Genetics
by
Luca Tadini
,
Nicolaj Jeran
and
Paolo Pesaresi
Cells 2020, 9(10), 2307; https://doi.org/10.3390/cells9102307 - 16 Oct 2020
Cited by 7 | Viewed by 2944
Abstract
GUN1 (genomes uncoupled 1), a chloroplast-localized pentatricopeptide repeat (PPR) protein with a C-terminal small mutS-related (SMR) domain, plays a central role in the retrograde communication of chloroplasts with the nucleus. This flow of information is required for the coordinated expression of plastid and [...] Read more.
GUN1 (genomes uncoupled 1), a chloroplast-localized pentatricopeptide repeat (PPR) protein with a C-terminal small mutS-related (SMR) domain, plays a central role in the retrograde communication of chloroplasts with the nucleus. This flow of information is required for the coordinated expression of plastid and nuclear genes, and it is essential for the correct development and functioning of chloroplasts. Multiple genetic and biochemical findings indicate that GUN1 is important for protein homeostasis in the chloroplast; however, a clear and unified view of GUN1′s role in the chloroplast is still missing. Recently, GUN1 has been reported to modulate the activity of the nucleus-encoded plastid RNA polymerase (NEP) and modulate editing of plastid RNAs upon activation of retrograde communication, revealing a major role of GUN1 in plastid RNA metabolism. In this opinion article, we discuss the recently identified links between plastid RNA metabolism and retrograde signaling by providing a new and extended concept of GUN1 activity, which integrates the multitude of functional genetic interactions reported over the last decade with its primary role in plastid transcription and transcript editing. Full article
(This article belongs to the Special Issue RNA Biology in Plant Organelles)
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