Carbon metabolism and transcriptome in developmental paths differentiation of a homokaryotic Coprinopsis cinerea strain

Abstract

The balance and interplay between sexual and asexual reproduction is one of the most attractive mysteries in fungi. The choice of developmental strategy reflects the ability of fungi to adapt to the changing environment. However, the evolution of developmental paths and the metabolic regulation during differentiation and morphogenesis are poorly understood.Here, we monitor the carbohydrate metabolism and gene expression regulation during the early differentiation process from the "fungal stem cell", vegetative mycelium, to the highly differentiated tissue/cells, fruiting body, oidia or sclerotia, of a homokaryotic fruiting Coprinopsis cinerea strain A43mut B43mut pab1-1 #326, uncovering the systematic changes during morphogenesis and the evolutionary process of developmental strategies. Conversion between glucose and glycogen and conversion between glucose and beta-glucan are the main carbon flows in the differentiation processes. Genes related to carbohydrate transport and metabolism are significantly differentially expressed among paths. RNA editing, a novel layer of gene expression regulation, occurs in all four developmental paths and enriched in ImportanceFungi is a group of species with high diversity and plays essential roles to the ecosystem. The life cycle of fungi is complex in structure and delicate in function. Choice of developmental strategies and internal changes within the organism are both important for the fungus to fulfill their ecological functions, reflecting the relationship between environment and the population. This study put the developmental process of vegetative growth, sexual and asexual reproduction, resistant structure formation of a classical model basidiomycetes fungus, C. cinerea, together for the first time to view the developmental paths differentiation process with physiology, transcriptomics and evolutionary prospects. Carbohydrate assays and RNA-seq showed the changes of the fungus. Our results fill the gaps on gene expression regulation during the early stage of developmental paths differentiation, and expand our understanding of the evolutionary process of life history and reproductive strategy in fungi.

Asexual reproduction and vegetative growth of Bionectria ochroleuca in response to temperature and photoperiod

“…In Coprinopsis cinerea, major differences in carbohydrate metabolism and carbohydrate redistribution were observed during fungal development, from vegetative growth to conidiation, fruiting, and sclerotia formation under different environmental conditions (Xie et al, 2020). Such balancing processes were internally regulated by regulatory genes and metabolic genes with high flexibility (Wang et al, 2019;Xie et al, 2020).…”

Chromosome-levelde novoassembly ofCoprinopsis cinerea A43mut B43mut pab1-1#326 and genetic variant identification of mutants using Nanopore MinION sequencing

“…Genome annotation of the draft genome was done using funannotate v1.7.2, following the workflow of clean-sort-mask-train-predict-update-annotate (Palmer and Stajich, 2019). A total of 18 transcriptomes was acquired from NCBI BioProject PRJNA573620 (Xie et al, 2020) and used to help training models for gene prediction and annotation. The RNA-seq data were quality filtered using fastp with default parameters, including the window size of 4, mean quality of Q 20 and minimum read length of 15 nt (Chen et al, 2018).…”

“…Eighteen transcriptomes, including developmental stages of vegetative mycelium, oidiation, sclerotia formation, hyphal knots, primordia and young fruiting bodies (Xie et al, 2020), were used to support the genome annotation. A total of 15,250 genes was predicted in the genome, with 16,862 transcripts.…”

Examining the macro-evolution and genetic background of complex multicellular structures in mushroom-forming fungi (Agaricomycetes)

“…It was also showed that carbohydrate metabolism has an essential role in the initiation of the fruiting body (Brunt and Moore, 1989). Changes in expression of genes associated with glycogen metabolism were shown through the development of C. cinerea (Krizsán et al, 2019;Xie et al, 2020). Furthermore, the accumulation of glycogen in the basal region of the secondary hyphal knot was also observed (Matthews and Niederpruem, 1973;van der Valk and Marchant, 1978).…”

“…Among coprinoid species, Coprinopsis cinerea became a model mushroom, having a plethora of genetically modified mutants strains (Kües, 2000) and it was among the first fungal genomes which were sequenced (Stajich et al, 2010). Thanks to genetic and bulk RNA-seq analyses of C. cinerea, our knowledge on the genetic background of mushroom development have been further widened (Plaza et al, 2014;Muraguchi et al, 2015;Krizsán et al, 2019;Xie et al, 2020).…”