Genome-wide A-to-I RNA editing in fungi independent of ADAR enzymes
- Huiquan Liu1,
- Qinhu Wang1,
- Yi He2,
- Lingfeng Chen1,
- Chaofeng Hao1,
- Cong Jiang1,
- Yang Li3,
- Yafeng Dai1,
- Zhensheng Kang1 and
- Jin-Rong Xu1,3
- 1State Key Laboratory of Crop Stress Biology for Arid Areas, Purdue-NWAFU Joint Research Center, College of Plant Protection, Northwest A&F University, Yangling, Shaanxi 712100, China;
- 2College of Life Sciences, Northwest A&F University, Yangling, Shaanxi 712100, China;
- 3Department of Botany and Plant Pathology, Purdue University, West Lafayette, Indiana 47907, USA
- Corresponding author: jinrong{at}purdue.edu
Abstract
Yeasts and filamentous fungi do not have adenosine deaminase acting on RNA (ADAR) orthologs and are believed to lack A-to-I RNA editing, which is the most prevalent editing of mRNA in animals. However, during this study with the PUK1 (FGRRES_01058) pseudokinase gene important for sexual reproduction in Fusarium graminearum, we found that two tandem stop codons, UA1831GUA1834G, in its kinase domain were changed to UG1831GUG1834G by RNA editing in perithecia. To confirm A-to-I editing of PUK1 transcripts, strand-specific RNA-seq data were generated with RNA isolated from conidia, hyphae, and perithecia. PUK1 was almost specifically expressed in perithecia, and 90% of transcripts were edited to UG1831GUG1834G. Genome-wide analysis identified 26,056 perithecium-specific A-to-I editing sites. Unlike those in animals, 70.5% of A-to-I editing sites in F. graminearum occur in coding regions, and more than two-thirds of them result in amino acid changes, including editing of 69 PUK1-like pseudogenes with stop codons in ORFs. PUK1 orthologs and other pseudogenes also displayed stage-specific expression and editing in Neurospora crassa and F. verticillioides. Furthermore, F. graminearum differs from animals in the sequence preference and structure selectivity of A-to-I editing sites. Whereas A's embedded in RNA stems are targeted by ADARs, RNA editing in F. graminearum preferentially targets A's in hairpin loops, which is similar to the anticodon loop of tRNA targeted by adenosine deaminases acting on tRNA (ADATs). Overall, our results showed that A-to-I RNA editing occurs specifically during sexual reproduction and mainly in the coding regions in filamentous ascomycetes, involving adenosine deamination mechanisms distinct from metazoan ADARs.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.199877.115.
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Freely available online through the Genome Research Open Access option.
- Received September 18, 2015.
- Accepted January 22, 2016.
This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
