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Sexual stage-specific A-to-I mRNA editing is mediated by tRNA-editing enzymes in fungi

Zhuyun Bian1, Zeyi Wang1, Diwen Wang1

  • 1Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907.

Proceedings of the National Academy of Sciences of the United States of America
|March 11, 2024
PubMed

Insights

Fungal A-to-I RNA editing occurs during sexual reproduction, catalyzed by adenosine-deaminase-acting-on-tRNA (ADAT) FgTAD2. This enzyme uses a stage-specific isoform and cofactors, distinct from metazoan ADARs, to modify messenger RNA (mRNA).

Area of Science:

  • Molecular Biology
  • RNA Biology
  • Fungal Genetics

Background:

  • Adenosine-to-Inosine (A-to-I) RNA editing, primarily attributed to ADARs, was thought to be exclusive to metazoans.
  • Previous research indicated genome-wide mRNA editing in filamentous ascomycetes, specifically during sexual reproduction.
  • Adenosine/cytosine deaminase genes, including TAD2 and TAD3 orthologs, were implicated in A-to-I editing.

Purpose of the Study:

  • To genetically and biochemically characterize the role of *FgTAD2*, an adenosine-deaminase-acting-on-tRNA (ADAT) gene, in mRNA editing in *Fusarium graminearum*.
  • To investigate the stage-specific nature and catalytic activity of FgTAD2 in fungal RNA editing.

Main Methods:

  • Utilized genetic approaches, including repeat-induced point (RIP) mutation and site-directed mutagenesis, to analyze *FgTAD2* function.
  • Employed biochemical assays, including in vitro editing assays and mass spectrometry, to characterize FgTAD2 protein activity and interactions.
  • Investigated the expression of a sexual-stage-specific isoform of *FgTAD2* and its heterodimerization with *FgTAD3*.

Main Results:

  • *FgTAD2* exhibits a sexual-stage-specific isoform and forms heterodimers with the inactive *FgTAD3*.
  • Seventeen *FgTAD2* mutations identified via RIP affected mRNA editing during sexual reproduction but not tRNA editing or vegetative growth.
  • Specific mutations (H352Y, Q375*) confirmed the functional importance in sexual reproduction and mRNA editing; purified FgTAD2-His from perithecia showed mRNA editing activity, unlike that from vegetative hyphae. The H352Y mutation impaired mRNA editing activity but not ADAT activity.

Conclusions:

  • FgTAD2, an ADAT, catalyzes A-to-I mRNA editing in *Fusarium graminearum* through a stage-specific isoform and cofactors during sexual reproduction.
  • This mechanism differs from metazoan ADAR-mediated editing, highlighting a distinct pathway for RNA editing in fungi.
  • The study identifies key residues and potential cofactors involved in fungal mRNA editing, opening avenues for further research into RNA modification in eukaryotes.
Keywords:
A-to-I editingFusarium graminearumGibberella zeaeascosporogenesissexual reproduction

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