Removal of Retained Introns Regulates Translation in the Rapidly Developing Gametophyte of Marsilea vestita

Boothby, Thomas E.; Zipper, Richard S.; Weele, Corine M. van der; Wolniak, Stephen M.

doi:10.1016/j.devcel.2013.01.015

Cited by 113 publications

(115 citation statements)

References 77 publications

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“…S6): When desiccated membranes are rehydrated, they become transiently leaky, making the uptake of large macromolecules possible (29), which has been exploited previously to introduce large nucleic acids and drugs into the cytoplasm of rehydrating anhydrobiotic cells (30)(31)(32). In addition, when tardigrades, rotifers, and other anhydrobionts desiccate, genomic double-stranded breakages and other damage are induced (19,33,34), and there appear to be robust mechanisms for repairing this damage (19,34).…”

mentioning

confidence: 99%

Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade

Boothby

Tenlen

Smith

et al. 2015

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

169

189

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Horizontal gene transfer (HGT), or the transfer of genes between species, has been recognized recently as more pervasive than previously suspected. Here, we report evidence for an unprecedented degree of HGT into an animal genome, based on a draft genome of a tardigrade, Hypsibius dujardini. Tardigrades are microscopic eight-legged animals that are famous for their ability to survive extreme conditions. Genome sequencing, direct confirmation of physical linkage, and phylogenetic analysis revealed that a large fraction of the H. dujardini genome is derived from diverse bacteria as well as plants, fungi, and Archaea. We estimate that approximately one-sixth of tardigrade genes entered by HGT, nearly double the fraction found in the most extreme cases of HGT into animals known to date. Foreign genes have supplemented, expanded, and even replaced some metazoan gene families within the tardigrade genome. Our results demonstrate that an unexpectedly large fraction of an animal genome can be derived from foreign sources. We speculate that animals that can survive extremes may be particularly prone to acquiring foreign genes.

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mentioning

confidence: 99%

Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade

Boothby

Tenlen

Smith

et al. 2015

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

169

189

View full text Add to dashboard Cite

show abstract

“…28,29 For example, nuclei of the fern Marsilea vestita are known to store intron-retaining transcripts during rapid post-transcriptionally controlled spermatogenesis. 30 We have also recently observed the accumulation of poly(A) RNA in the cell nucleus following stress induced by removal of the cell wall. 31 Together with our observation of the decrease in transcription and increased levels of poly(A) RNA, this finding suggests an enhanced stabilization of RNA that is already present in the cell.…”

Section: Discussionmentioning

confidence: 92%

Regulation of poly(A) RNA retention in the nucleus as a survival strategy of plants during hypoxia

2016

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Last finding indicates that post-transcriptional processes are significant in low-oxygen conditions, but their nature is poorly understood. Here, we localized poly(A) RNA and mRNA coding proteins involved and not involved with resistance to hypoxia in Lupinus luteus and Arabidopsis thaliana during submergence and after recovery of aerobic conditions. We showed a strong nuclear accumulation of poly(A) RNA and 6 of 7 studied mRNAs with a concurrent strong reduction in RNA polymerase II transcription during hypoxia. In this study, the nucleus did not accumulate mRNA of the ADH1 (alcohol dehydrogenase 1) gene, which is a core hypoxia gene. The RNA accumulation in the nucleus is among the mechanisms of post-transcriptional gene regulation that prevents translation. However re-aeration was accompanied by a strong increase in the amount of the mRNAs in the cytoplasm and a simultaneous decrease in nuclear mRNAs. This finding indicates that the nucleus is a storage site for those of mRNAs which are not involved in the response to hypoxia for use by the plants after the hypoxic stress. In this study, the highest intensity of RNA accumulation occurred in Cajal bodies (CBs); the intensity of accumulation was inversely correlated with transcription. Under hypoxia, ncb-1 mutants of Arabidopsis thaliana with a complete absence of CBs died sooner than wild type (WT), accompanied by a strong reduction in the level of poly(A) RNA in the nucleus. These results suggest that the CBs not only participate in the storage of the nuclear RNA, but they also could take part in its stabilization under low-oxygen conditions.

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“…Likewise, in the male gametophyte of the water fern, Marsilea, mRNAs are translationally repressed due to intron retention. mRNAs become translationally activated as introns are removed, a process that also requires exon junction complex components (Hart and Wolniak, 1999;van der Weele et al, 2007;Boothby et al, 2013).…”

Section: Translational Control In Developmentmentioning

confidence: 99%

Translational Regulation of Cytoplasmic mRNAs

Roy

Arnim

2013

The Arabidopsis Book

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Translation of the coding potential of a messenger RNA into a protein molecule is a fundamental process in all living cells and consumes a large fraction of metabolites and energy resources in growing cells. Moreover, translation has emerged as an important control point in the regulation of gene expression. At the level of gene regulation, translational control is utilized to support the specific life histories of plants, in particular their responses to the abiotic environment and to metabolites. This review summarizes the diversity of translational control mechanisms in the plant cytoplasm, focusing on specific cases where mechanisms of translational control have evolved to complement or eclipse other levels of gene regulation. We begin by introducing essential features of the translation apparatus. We summarize early evidence for translational control from the pre-Arabidopsis era. Next, we review evidence for translation control in response to stress, to metabolites, and in development. The following section emphasizes RNA sequence elements and biochemical processes that regulate translation. We close with a chapter on the role of signaling pathways that impinge on translation.

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Removal of Retained Introns Regulates Translation in the Rapidly Developing Gametophyte of Marsilea vestita

Cited by 113 publications

References 77 publications

Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade

Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade

Regulation of poly(A) RNA retention in the nucleus as a survival strategy of plants during hypoxia

Translational Regulation of Cytoplasmic mRNAs

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