Abstract

Fruiting bodies are among the most complex multicellular structures formed by fungi, and the molecular mechanisms that regulate their development are far from understood. However, studies with a number of fungal model organisms have started to shed light on this developmental process. One of these model organisms is Sordaria macrospora, a filamentous ascomycete from the order Sordariales. This fungus has been a genetic model organism since the 1950s, but its career as a model organism for molecular genetics really took off in the 1990s, when the establishment of a transformation protocol, a mutant collection, and an indexed cosmid library provided the methods and resources to start revealing the molecular mechanisms of fruiting body development. In the 2000s, “omics” methods were added to the S. macrospora tool box, and by 2020, 58 developmental genes have been identified in this fungus. This review gives a brief overview of major method developments for S. macrospora, and then focuses on recent results characterizing different processes involved in regulating development including several regulatory protein complexes, autophagy, transcriptional and chromatin regulation, and RNA editing.Key points•Sordaria macrospora is a model system for analyzing fungal fruiting body development.•More than 100 developmental mutants are available for S. macrospora.•More than 50 developmental genes have been characterized in S. macrospora.

Highlights

  • Sordaria macrospora is a filamentous ascomycete with a decades-long history as a model organism to study fruitingThis article is dedicated to Prof

  • S. macrospora is able to outcross; different strains, e.g., developmental mutants, can be crossed in the laboratory (Esser and Straub 1956). For such classical genetic analyses, another advantage of S. macrospora is the production of its ascospores as ordered tetrads, which means that each ascus contains the four meiotic products of a single meiosis, and that the order of spores in the ascus allows distinguishing between alleles that segregated in the first versus the second meiotic division (Kück et al 2009)

  • The blue light sensor and transcription factor White Collar 1 gains a histone deacetylase domain by RNA editing of its transcripts at late stages of fruiting body formation (Blank-Landeshammer et al 2019). Why proteins need these new functions during development, if A-to-I RNA editing is a prerequisite for ascospore formation, how editing is catalyzed in fungi, and how it evolved are open questions that have to be answered by future research

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Summary

Introduction

Transcriptomics analysis of young fruiting bodies of the wild type and the pro mutant identified more than 400 genes that are differentially regulated during development and are dependent on pro for correct expression, this control might be indirect (Teichert et al 2012). Genome-wide analyses of nucleosome positioning as well as cytosine methylation in the Δasf mutant compared with the wild type failed to identify changes that would explain the expression changes in weakly expressed genes (Schumacher et al 2018); additional analyses, for example of histone modifications, will be needed to address this question Another chromatin modifier recently identified to be required for fruiting body formation in S. macrospora is spt (Lütkenhaus et al 2019). Why proteins need these new functions during development, if A-to-I RNA editing is a prerequisite for ascospore formation, how editing is catalyzed in fungi, and how it evolved are open questions that have to be answered by future research

Conclusions
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