Deep sequencing of the tobacco mitochondrial transcriptome reveals expressed ORFs and numerous editing sites outside coding regions

Grimes, Benjamin T; Sisay, Awa K; Carroll, Hyrum; Cahoon, A. Bruce

doi:10.1186/1471-2164-15-31

Cited by 58 publications

(57 citation statements)

References 49 publications

(62 reference statements)

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“…A total of 422 editing sites were identified in mitochondrial protein coding regions, which occupied 61% of the total editing sites. Similar editing sites were also found in tobacco and Arabidopsis , in which 557 editing sites (88% of the total) and 441 sites (97% of the total) were found in protein‐coding regions, respectively (Handa, ; Grimes et al ., ). The mRNA modifications in coding regions could prematurely terminate protein synthesis, reduce the peptide yield, and alter amino acid sequence.…”

Section: Discussionmentioning

confidence: 97%

Two pivotal RNA editing sites in the mitochondrial atp1mRNA are required for ATP synthase to produce sufficient ATP for cotton fiber cell elongation

Xiao

Líu

et al. 2018

New Phytologist

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RNA editing is a post-transcriptional maturation process affecting organelle transcripts in land plants. However, the molecular functions and physiological roles of RNA editing are still poorly understood. Using high-throughput sequencing, we identified 692 RNA editing sites in the Gossypium hirsutum mitochondrial genome. A total of 422 editing sites were found in the coding regions and all the edits are cytidine (C) to uridine (U) conversions. Comparative analysis showed that two editing sites in Ghatp1, C1292 and C1415, had a prominent difference in editing efficiency between fiber and ovule. Biochemical and genetic analyses revealed that the two vital editing sites were important for the interaction between the α and β subunits of ATP synthase, which resulted in ATP accumulation and promoted cell growth in yeast. Ectopic expression of C1292, C1415, or doubly edited Ghatp1 in Arabidopsis caused a significant increase in the number of trichomes in leaves and root length. Our results indicate that editing at C1292 and C1415 sites in Ghatp1 is crucial for ATP synthase to produce sufficient ATP for cotton fiber cell elongation. This work extends our understanding of RNA editing in atp1 and ATP synthesis, and provides insights into the function of mitochondrial edited Atp1 protein in higher plants.

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Section: Discussionmentioning

confidence: 97%

Two pivotal RNA editing sites in the mitochondrial atp1mRNA are required for ATP synthase to produce sufficient ATP for cotton fiber cell elongation

Xiao

Líu

et al. 2018

New Phytologist

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“… Estimated from the study by Grimes et al . () on tobacco mitochondrial transcriptome, 1 Truseq library (US$3350/48reactions = US$70), 1 lane Hiseq 100 nt (US$2240 by Biotechnology Resource Center, Cornell University) Total: US$2310, 635 mitochondrial editing sites in their study. Only 3% of their reads were mitochondrial. …”

Section: Resultsmentioning

confidence: 99%

High‐throughput quantification of chloroplast RNA editing extent using multiplex RT‐PCR mass spectrometry

2015

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SUMMARYRNA editing in plants, animals, and humans modifies genomically encoded cytidine or adenosine nucleotides to uridine or inosine, respectively, in mRNAs. We customized the MassARRAY System (Sequenom Inc., San Diego, CA, USA, www.sequenom.com) to assay multiplex PCR-amplified single-stranded cDNAs and easily analyse and display the captured data. By using appropriate oligonucleotide probes, the method can be tailored to any organism and gene where RNA editing occurs. Editing extent of up to 40 different nucleotides in each of either 94 or 382 different samples (3760 or 15 280 editing targets, respectively) can be examined by assaying a single plate and by performing one repetition. We have established this mass spectrometric method as a dependable, cost-effective and time-saving technique to examine the RNA editing efficiency at 37 Arabidopsis thaliana chloroplast editing sites at a high level of multiplexing. The high-throughput editing assay, named Multiplex RT-PCR Mass Spectrometry (MRMS), is ideal for large-scale experiments such as identifying population variation, examining tissue-specific changes in editing extent, or screening a mutant or transgenic collection. Moreover, the required amount of starting material is so low that RNA from fewer than 50 cells can be examined without amplification. We demonstrate the use of the method to identify natural variation in editing extent of chloroplast C targets in a collection of Arabidopsis accessions.

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“…It is not clear what type of function such a protein would have in mitochondria. Many other transcribed open reading frames with no obvious functions in mitochondria, and typically not conserved among species nor derived from the nuclear genome, have been identified in the mitochondrial genomes of rice and tobacco [33,34]. Thus plant mitochondria may contain numerous transcribed ORFs that do not code for functional proteins, with the number and type varying by species.…”

Section: Orf164 Is Expressed In Several Organ Types and In Five Othermentioning

confidence: 97%

Expression of a transferred nuclear gene in a mitochondrial genome

Qiu

Filipenko

Darracq

et al. 2014

Current Plant Biology

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a b s t r a c tTransfer of mitochondrial genes to the nucleus, and subsequent gain of regulatory elements for expression, is an ongoing evolutionary process in plants. Many examples have been characterized, which in some cases have revealed sources of mitochondrial targeting sequences and cis-regulatory elements. In contrast, there have been no reports of a nuclear gene that has undergone intracellular transfer to the mitochondrial genome and become expressed. Here we show that the orf164 gene in the mitochondrial genome of several Brassicaceae species, including Arabidopsis, is derived from the nuclear ARF17 gene that codes for an auxin responsive protein and is present across flowering plants. Orf164 corresponds to a portion of ARF17, and the nucleotide and amino acid sequences are 79% and 81% identical, respectively. Orf164 is transcribed in several organ types of Arabidopsis thaliana, as detected by RT-PCR. In addition, orf164 is transcribed in five other Brassicaceae within the tribes Camelineae, Erysimeae and Cardamineae, but the gene is not present in Brassica or Raphanus. This study shows that nuclear genes can be transferred to the mitochondrial genome and become expressed, providing a new perspective on the movement of genes between the genomes of subcellular compartments.

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Deep sequencing of the tobacco mitochondrial transcriptome reveals expressed ORFs and numerous editing sites outside coding regions

Cited by 58 publications

References 49 publications

Two pivotal RNA editing sites in the mitochondrial atp1mRNA are required for ATP synthase to produce sufficient ATP for cotton fiber cell elongation

Two pivotal RNA editing sites in the mitochondrial atp1mRNA are required for ATP synthase to produce sufficient ATP for cotton fiber cell elongation

High‐throughput quantification of chloroplast RNA editing extent using multiplex RT‐PCR mass spectrometry

Expression of a transferred nuclear gene in a mitochondrial genome

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