Epigenetic and transcriptional control of sexual development in the multicellular Sordariomycete fungi

SUMMARY Many Sordariomycete fungi produce flask-shaped perithecia that encapsulate meiotic cells and facilitate dispersion of sexual spores. Perithecial development represents a striking example of complex multicellularity in fungi, requiring coordinated gene regulation through transcriptional, chromatin-based, and post-transcriptional mechanisms. This review summarizes recent work to dissect sexual development in several well-studied fungi: Neurospora crassa , Sordaria macrospora , Podospora anserina , and Fusarium graminearum . Studies with these fungi have uncovered interconnected regulatory mechanisms that coordinate fruiting body development. Transcription factor networks control differentiation of perithecial tissues and cell types. Chromatin regulators, such as histone chaperones, ATP-dependent chromatin remodelers, acetyltransferases, and Polycomb Repressive Complex 2, impact major developmental transitions. In addition, post-transcriptional mechanisms that operate during sexual development play critical regulatory roles. Recoding of the transcriptome by A-to-I mRNA editing is specific to perithecia and is essential for sexual development of N. crassa and F. graminearum . Finally, sex-specific genome defense pathways protect genome integrity and are essential for the completion of meiosis in some species. We summarize recent advances and highlight the remarkable regulatory complexity underlying fruiting body development in Sordariomycete fungi. In addition, we identify key open questions for future research.