Integrative Activity of Mating Loci, Environmentally Responsive Genes, and Secondary Metabolism Pathways during Sexual Development of Chaetomium globosum

Abstract

Fungal diversity has amazed evolutionary biologists for decades. One societally important aspect of this diversity manifests in traits that enable pathogenicity. The opportunistic pathogen Chaetomium globosum is well adapted to a high-humidity environment and produces numerous secondary metabolites that defend it from predation. Many of these chemicals can threaten human health. Understanding the phases of the C. globosum life cycle in which these products are made enables better control and even utilization of this fungus. Among its intriguing traits is that it both is self-fertile and lacks any means of propagule-based asexual reproduction. By profiling genome-wide gene expression across the process of sexual reproduction in C. globosum and comparing it to genome-wide gene expression in the model filamentous fungus N. crassa and other closely related fungi, we revealed associations among mating-type genes, sexual developmental genes, sexual incompatibility regulators, environmentally responsive genes, and secondary metabolic pathways.

Transcriptional Divergence Underpinning Sexual Development in the Fungal Class Sordariomycetes

“…Stage 1 (S1) is hallmarked by development of ascogenous hyphae from the perithecium initials, stage 2 (S2) is distinguished by formation of perithecial walls surrounding the central ascogenous hyphae, stage 3 (S3) is characterized by the release of paraphysis tissues in squash mounts of perithecia and elongation of the perithecial beak in some fungi, including N. crassa and M. oryzae , stage 4 (S4) begins with development of asci in place of senescent paraphyses, and stage 5 (S5) is recognized by mature ascospores enclosed in asci. We obtained transcriptome data for C. globosum , F. graminearum , F. neocosmosporiellum , and N. crassa from our previous studies, in which all the fungal strains were grown on carrot agar medium used as a common garden environment, and their genome-wide gene expression levels were profiled at the five sexual developmental stages, including a vegetative stage right after sexual induction (S0) ( 10 , 43 – 45 ). In this study, we also profiled the developmental transcriptome for M. oryzae , which belongs to a separate and divergent clade (Magnaporthaceae) from the other four species ( Fig.…”

“…Although the three core biosynthetic genes were conserved and syntenic between F. graminearum and F. neocosmosporiellum (68 to 81% identity at protein sequence levels), the PGLX ortholog in F. neocosmosporiellum was located distal to the three core biosynthetic genes, interspersed with 17 genes, as in a related species, F. solani ( 51 , 53 ). Although the PGLX orthologs were found in the genomes of C. globosum , M. oryzae , and N. crassa , the three core biosynthetic genes were absent in these three species, which are known to produce a black perithecial pigment of melanin origin ( 45 , 54 ).…”

Secondary Metabolism Gene Clusters Exhibit Increasingly Dynamic and Differential Expression during Asexual Growth, Conidiation, and Sexual Development in Neurospora crassa

“…Environmental factors, especially environmental stress from exposure to intensive light and/or extreme temperature, play critical roles in regulating SMC activities ( 29 , 30 ). N. crassa grows with normal morphology and biology between 15°C and 37°C.…”

“…Total RNA was extracted from homogenized tissue with TRI Reagent (Molecular Research Center) as in Clark et al ( 111 ), and sample preparation and sequencing followed our previous work ( 29 , 66 , 68 ). Briefly, mRNA was purified using Dynabeads oligo(dT) magnetic separation (Invitrogen).…”

“…Environmental factors are known to regulate production of SMs in diverse fungal species, especially via transcriptional regulation by transcription factors or epigenetic mechanisms ( 7 , 10 , 29 – 32 ). For example, environmental changes can induce fungal SM toxins, pigments, and other chemicals in association with fungal stress responses to drought, reactive oxygen species, temperature, and UV light intensity ( 9 , 33 – 35 ).…”