DNA cytosine methyltransferases differentially regulate genome-wide hypermutation and interhomolog recombination in Trichoderma reesei meiosis

Nucleic Acids Res. 2024 Sep 9;52(16):9551-9573. doi: 10.1093/nar/gkae611.

Abstract

Trichoderma reesei is an economically important enzyme producer with several unique meiotic features. spo11, the initiator of meiotic double-strand breaks (DSBs) in most sexual eukaryotes, is dispensable for T. reesei meiosis. T. reesei lacks the meiosis-specific recombinase Dmc1. Rad51 and Sae2, the activator of the Mre11 endonuclease complex, promote DSB repair and chromosome synapsis in wild-type and spo11Δ meiosis. DNA methyltransferases (DNMTs) perform multiple tasks in meiosis. Three DNMT genes (rid1, dim2 and dimX) differentially regulate genome-wide cytosine methylation and C:G-to-T:A hypermutations in different chromosomal regions. We have identified two types of DSBs: type I DSBs require spo11 or rid1 for initiation, whereas type II DSBs do not rely on spo11 and rid1 for initiation. rid1 (but not dim2) is essential for Rad51-mediated DSB repair and normal meiosis. rid1 and rad51 exhibit a locus heterogeneity (LH) relationship, in which LH-associated proteins often regulate interconnectivity in protein interaction networks. This LH relationship can be suppressed by deleting dim2 in a haploid rid1Δ (but not rad51Δ) parental strain, indicating that dim2 and rid1 share a redundant function that acts earlier than rad51 during early meiosis. In conclusion, our studies provide the first evidence of the involvement of DNMTs during meiotic initiation and recombination.

MeSH terms

  • DNA (Cytosine-5-)-Methyltransferases / genetics
  • DNA (Cytosine-5-)-Methyltransferases / metabolism
  • DNA Breaks, Double-Stranded*
  • DNA Methylation
  • Endodeoxyribonucleases / genetics
  • Endodeoxyribonucleases / metabolism
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism
  • Genome, Fungal
  • Homologous Recombination
  • Hypocreales* / genetics
  • Meiosis* / genetics

Substances

  • DNA (Cytosine-5-)-Methyltransferases
  • Fungal Proteins
  • meiotic recombination protein SPO11
  • Endodeoxyribonucleases

Supplementary concepts

  • Trichoderma reesei