The GATA-Type Transcription Factor Csm1 Regulates Conidiation and Secondary Metabolism in Fusarium fujikuroi

Abstract

GATA-type transcription factors (TFs) such as the nitrogen regulators AreA and AreB, or the light-responsive TFs WC-1 and WC-2, play global roles in fungal growth and development. The conserved GATA TF NsdD is known as an activator of sexual development and key repressor of conidiation in Aspergillus nidulans, and as light-regulated repressor of macroconidia formation in Botrytis cinerea. In the present study, we functionally characterized the NsdD ortholog in Fusarium fujikuroi, named Csm1. Deletion of this gene resulted in elevated microconidia formation in the wild-type (WT) and restoration of conidiation in the non-sporulating velvet mutant Δvel1 demonstrating that Csm1 also plays a role as repressor of conidiation in F. fujikuroi. Furthermore, biosynthesis of the PKS-derived red pigments, bikaverin and fusarubins, is de-regulated under otherwise repressing conditions. Cross-species complementation of the Δcsm1 mutant with the B. cinerea ortholog LTF1 led to full restoration of WT-like growth, conidiation and pigment formation. In contrast, the F. fujikuroi CSM1 rescued only the defects in growth, the tolerance to H2O2 and virulence, but did not restore the light-dependent differentiation when expressed in the B. cinerea Δltf1 mutant. Microarray analysis comparing the expression profiles of the F. fujikuroi WT and the Δcsm1 mutant under different nitrogen conditions revealed a strong impact of this GATA TF on 19 of the 47 gene clusters in the genome of F. fujikuroi. One of the up-regulated silent gene clusters is the one containing the sesquiterpene cyclase-encoding key gene STC1. Heterologous expression of STC1 in Escherichia coli enabled us to identify the product as the volatile bioactive compound (–)-germacrene D.

Transcription Factor NsdD Regulates the Expression of Genes Involved in Plant Biomass-Degrading Enzymes, Conidiation, and Pigment Biosynthesis in Penicillium oxalicum

“…NsdD and its orthologues are identified as TFs with the conserved DNA-binding domain ZnF_GATA in many filamentous fungi (22)(23)(24)(25)(26)(27)(28)(29). Hitherto in the reported literature and this work, NsdD and its orthologues primarily played six roles, including (i) repressing asexual development in Aspergillus spp.…”

“…and its orthologs, such as Pro44 in Sordaria macrospora, Ltf1 in Botrytis cinerea, Csm1 in Fusarium fujikuroi, SUB-1 in Neurospora crassa, and SsNsd1 in Sclerotinia sclerotiorum, regulate development and/or biosynthesis of secondary metabolites (22)(23)(24)(25)(26)(27)(28). Additional functions involving stress tolerance, light response, and virulence have been observed in the plant pathogens B. cinerea, F. fujikuroi, and/or N. crassa (23,26,27). NsdD is positioned between FLB (fluffy low BrlA expression) and BrlA and functions as a repressor by downregulating brlA in Aspergillus (25,29).…”

Set1 and Kdm5 are antagonists for H3K4 methylation and regulators of the major conidiation‐specific transcription factor gene ABA1 in Fusarium fujikuroi

“…Earlier investigations have revealed several global regulators with an influence on asexual development in F. fujikuroi. Thus, the fungus-specific velvet protein Vel1 and the GATA-type TF Csm1 were shown to be an activator and repressor of conidiation respectively (Wiemann et al, 2010;Niehaus et al, 2017b) (Fig. 9A).…”

“…7C, the novel mutants are shown in comparison to Δcsm1 (regulator of conidiation and secondary metabolism). The TF-encoding gene CSM1 encodes a major repressor of conidiation in F. fujikuroi, and the respective deletion strain is characterized by a strongly elevated conidia formation relative to the WT (Niehaus et al, 2017b). Indeed, conidiogenesis was abolished in Δaba1, Δflb3 and Δflb4 mutants, while WT-like amounts of conidia were produced in Δflb2, Δflb5 and Δwet1 (Fig.…”

“…9A). CSM1 deletion in a Δvel1 background (no conidia) restored conidiogenesis (Niehaus et al, 2017b). To analyze if lack of the repressor gene CSM1 also restores conidiogenesis in Δaba1, Δflb3 and Δflb4, CSM1 was deleted in the respective mutant strains in the present work.…”