A complete annotation of the chromosomes of the cellulase producer Trichoderma reesei provides insights in gene clusters, their expression and reveals genes required for fitness

BACKGROUND: Investigations on a few eukaryotic model organisms showed that many genes are non-randomly distributed on chromosomes. In addition, chromosome ends frequently possess genes that are important for the fitness of the organisms. Trichoderma reesei is an industrial producer of enzymes for food, feed and biorefinery production. Its seven chromosomes have recently been assembled, thus making an investigation of its chromosome architecture possible. RESULTS: We manually annotated and mapped 9194 ORFs on their respective chromosomes and investigated the clustering of the major gene categories and of genes encoding carbohydrate-active enzymes (CAZymes), and the relationship between clustering and expression. Genes responsible for RNA processing and modification, amino acid metabolism, transcription, translation and ribosomal structure and biogenesis indeed showed loose clustering, but this had no impact on their expression. A third of the genes encoding CAZymes also occurred in loose clusters that also contained a high number of genes encoding small secreted cysteine-rich proteins. Five CAZyme clusters were located less than 50 kb apart from the chromosome ends. These genes exhibited the lowest basal (but not induced) expression level, which correlated with an enrichment of H3K9 methylation in the terminal 50 kb areas indicating gene silencing. No differences were found in the expression of CAZyme genes present in other parts of the chromosomes. The putative subtelomeric areas were also enriched in genes encoding secreted proteases, amino acid permeases, enzyme clusters for polyketide synthases (PKS)–non-ribosomal peptide synthase (NRPS) fusion proteins (PKS–NRPS) and proteins involved in iron scavenging. They were strongly upregulated during conidiation and interaction with other fungi. CONCLUSIONS: Our findings suggest that gene clustering on the T. reesei chromosomes occurs but generally has no impact on their expression. CAZyme genes, located in subtelomers, however, exhibited a much lower basal expression level. The gene inventory of the subtelomers suggests a major role of competition for nitrogen and iron supported by antibiosis for the fitness of T. reesei. The availability of fully annotated chromosomes will facilitate the use of genetic crossings in identifying still unknown genes responsible for specific traits of T. reesei. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13068-016-0488-z) contains supplementary material, which is available to authorized users.