The tobacco plastid <i>acc</i>D gene is essential and is required for leaf development

Kode, Vasumathi; Mudd, Elisabeth A.; Iamtham, Siriluck; Day, Anil

doi:10.1111/j.1365-313x.2005.02533.x

Cited by 220 publications

(200 citation statements)

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“…When tobacco plants were transformed with a construct designed to disrupt the accD gene, homoplasmic plastid transformants could not be obtained, evidently because loss of all wild-type copies of accD would be lethal. Tobacco plants selected to carry some defective accD genes exhibited severe leaf development defects (Kode et al 2005). Furthermore, accD transcription and protein accumulation is evidently important in the specialized type of chloroplasts found in tomato fruit, where photosynthetic genes are down-regulated but accD expression is up-regulated (Kahlau and Bock 2008).…”

Section: Discussionmentioning

confidence: 99%

A comparative genomics approach identifies a PPR-DYW protein that is essential for C-to-U editing of the Arabidopsis chloroplast accD transcript

Robbins¹,

Heller²,

Hanson³

2009

RNA

112

123

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Several nuclear-encoded proteins containing pentatricopeptide repeat (PPR) motifs have previously been identified to be transfactors essential for particular chloroplast RNA editing events through analysis of mutants affected in chloroplast biogenesis or function. Other PPR genes are known to encode proteins involved in other aspects of organelle RNA metabolism. A function has not been assigned to most members of the large plant PPR gene family. Arabidopsis and rice each contain over 400 PPR genes, of which about a fifth exhibit a C-terminal DYW domain. We describe here a comparative genomics approach that will facilitate identification of the role of RNA-binding proteins in organelle RNA metabolism. We have implemented this strategy to identify an Arabidopsis nuclear-encoded gene RARE1 that is required for editing of the chloroplast accD transcript. RARE1 carries 15 PPR motifs, an E/E+ and a DYW domain, whereas previously reported editing factors CRR4, CRR21, and CLB19 lack a DYW domain. The accD gene encodes the b carboxyltransferase subunit of acetyl coA carboxylase, which catalyzes the first step in fatty acid biosynthesis in chloroplasts. Despite a lack of accD C794 editing and lack of restoration of an evolutionarily conserved leucine residue in the b carboxyltransferase protein, rare1 mutants are unexpectedly robust and reproduce under growth room conditions. Previously the serine-to-leucine alteration caused by editing was deemed essential in the light of the finding that a recombinantly expressed ''unedited'' form of the pea acetyl coA carboxylase was catalytically inactive.Keywords: chloroplast; RNA editing; accD; RARE1; pentatricopeptide; trans-factor INTRODUCTION Vascular plant organelle transcripts undergo C-to-U RNA editing (for review, see Hanson et al. 1996;Bock 2000;Tillich et al. 2005;Shikanai 2006). In Arabidopsis, 34 editing events are known to occur in chloroplast transcripts (Tillich et al. 2005;Chateigner-Boutin and Small 2007), while 508 Cs are known to be modified to Us in Arabidopsis mitochondria (Bentolila et al. 2008). The amino acid encoded by edited transcripts often differs from the one predicted from unedited transcripts, usually resulting in increased evolutionary conservation of the amino acid sequence from the one predicted from genomic sequence (Gualberto et al. 1989), although start and stop codons in organelle transcripts are also sometimes created by C-to-U editing (Wintz and Hanson 1991;Kudla et al. 1992). The residues modified by RNA editing are often important for the three-dimensional structure of the protein (Yura and Go 2008). RNA editing appears to be a mechanism to correct defective organelle genes at the transcript level.The suite of particular C-to-U editing events varies from one plant species to another, even though RNA editing probably arose in an ancestor common to the land plants (Tillich et al. 2006). Between divergent species, such as between dicots and monocots, RNA editing C targets vary considerably. In species that do not contain a particular C-...

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Section: Discussionmentioning

confidence: 99%

A comparative genomics approach identifies a PPR-DYW protein that is essential for C-to-U editing of the Arabidopsis chloroplast accD transcript

Robbins¹,

Heller²,

Hanson³

2009

RNA

112

123

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“…However, the plastid genome of higher plants contains many essential genes that are not amenable to functional analysis by targeted inactivation (i.e., knockout by insertional or deletional mutagenesis). These essential plastid genes include components of the gene expression machinery (44)(45)(46), essential metabolic enzymes (47), as well as several open reading frames of unknown function (48). The synthetic theophylline riboswitch can now be used to construct (37).…”

Section: Discussionmentioning

confidence: 99%

Inducible gene expression from the plastid genome by a synthetic riboswitch

Verhounig

Karcher

Bock

2010

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

120

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Riboswitches are natural RNA sensors that regulate gene expression in response to ligand binding. Riboswitches have been identified in prokaryotes and eukaryotes but are unknown in organelles (mitochondria and plastids). Here we have tested the possibility to engineer riboswitches for plastids (chloroplasts), a genetic system that largely relies on translational control of gene expression. To this end, we have used bacterial riboswitches and modified them in silico to meet the requirements of translational regulation in plastids. These engineered switches were then tested for functionality in vivo by stable transformation of the tobacco chloroplast genome. We report the identification of a synthetic riboswitch that functions as an efficient translational regulator of gene expression in plastids in response to its exogenously applied ligand theophylline. This riboswitch provides a novel tool for plastid genome engineering that facilitates the tightly regulated inducible expression of chloroplast genes and transgenes and thus has wide applications in functional genomics and biotechnology.chloroplast | plastid transformation | translational regulation R iboswitches are natural RNA sensors that mediate control of gene expression via their capacity to bind small molecules (metabolites). They fold into RNA secondary structures whose conformation switches between an "on" state and an "off" state in response to ligand binding (reviewed, e.g., in refs. 1-4). Riboswitches can be divided into two distinct structural domains: an aptamer and an expression platform. The aptamer domain binds the metabolite and this triggers conformational changes in the expression platform, which either permit or prevent gene expression. Depending on the nature of the response to metabolite binding, "on" switches and "off" switches are distinguished. In bacteria, riboswitches reside mainly in the 5 0 untranslated regions (UTRs) of mRNAs and an emerging theme is that anabolic genes are mainly controlled by "off" switches (5-7), whereas catabolic genes are controlled by "on" switches (8), thus providing an efficient mechanism of feedback control of metabolic pathways. In bacteria, most riboswitches act at the transcriptional level [e.g., by resolution of rho-independent transcription termination hairpins (8, 9)], but a few translational switches have also been identified (5, 7). Translational riboswitches usually function via sequestration of the ribosome-binding site (Shine-Dalgarno (SD) sequence), thereby blocking translation initiation in a metabolitedependent manner. The increasing understanding of the functional principles of bacterial riboswitches and the possibility to produce novel aptamers by in vitro evolution of RNA molecules has facilitated attempts to design synthetic switches (10-12), which potentially can provide versatile tools for genetic engineering and synthetic biology applications.While, over the past years, numerous riboswitches have been discovered in prokaryotes (13) and also a few in eukaryotes including plants (14,15), ...

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“…In most plant species, heterotrophic growth also requires plastid protein biosynthesis (Ahlert et al, 2003;Rogalski et al, 2006;Alkatib et al, 2012a), presumably because a few plastid-encoded proteins affect metabolic functions that are essential for cell survival even in the presence of an exogenous carbon source (Kode et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Synthetic Lethality in the Tobacco Plastid Ribosome and Its Rescue at Elevated Growth Temperatures

et al. 2014

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ORCID ID: 0000-0001-7502-6940 (R.B.)Consistent with their origin from cyanobacteria, plastids (chloroplasts) perform protein biosynthesis on bacterial-type 70S ribosomes. The plastid genomes of seed plants contain a conserved set of ribosomal protein genes. Three of these have proven to be nonessential for translation and, thus, for cellular viability: rps15, rpl33, and rpl36. To help define the minimum ribosome, here, we examined whether more than one of these nonessential plastid ribosomal proteins can be removed from the 70S ribosome. To that end, we constructed all possible double knockouts for the S15, L33, and L36 ribosomal proteins by stable transformation of the tobacco (Nicotiana tabacum) plastid genome. We find that, although S15 and L33 function in different ribosomal particles (30S and 50S, respectively), their combined deletion from the plastid genome results in synthetic lethality under autotrophic conditions. Interestingly, the lethality can be overcome by growth under elevated temperatures due to an improved efficiency of plastid ribosome biogenesis. Our results reveal functional interactions between protein and RNA components of the 70S ribosome and uncover the interdependence of the biogenesis of the two ribosomal subunits. In addition, our findings suggest that defining a minimal set of plastid genes may prove more complex than generally believed.

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The tobacco plastid accD gene is essential and is required for leaf development

Cited by 220 publications

References 53 publications

A comparative genomics approach identifies a PPR-DYW protein that is essential for C-to-U editing of the Arabidopsis chloroplast accD transcript

A comparative genomics approach identifies a PPR-DYW protein that is essential for C-to-U editing of the Arabidopsis chloroplast accD transcript

Inducible gene expression from the plastid genome by a synthetic riboswitch

Synthetic Lethality in the Tobacco Plastid Ribosome and Its Rescue at Elevated Growth Temperatures

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