The White Collar Complex Is Involved in Sexual Development of Fusarium graminearum

Abstract

Sexual spores (ascospores) of Fusarium graminearum, a homothallic ascomycetous fungus, are believed to be the primary inocula for epidemics of the diseases caused by this species in cereal crops. Based on the light requirement for the formation of fruiting bodies (perithecia) of F. graminearum under laboratory conditions, we explored whether photoreceptors play an important role in sexual development. Here, we evaluated the roles of three genes encoding putative photoreceptors [a phytochrome gene (FgFph) and two white collar genes (FgWc-1 and FgWc-2)] during sexual development in F. graminearum. For functional analyses, we generated transgenic strains lacking one or two genes from the self-fertile Z3643 strain. Unlike the wild-type (WT) and add-back strains, the single deletion strains (ΔFgWc-1 and ΔFgWc-2) produced fertile perithecia under constant light on complete medium (CM, an unfavorable medium for sexual development) as well as on carrot agar (a perithecial induction condition). The expression of mating-type (MAT) genes increased significantly in the gene deletion strains compared to the WT under both conditions. Deletion of FgFph had no significant effect on sexual development or MAT gene expression. In contrast, all of the deletion strains examined did not show significant changes in other traits such as hyphal growth, mycotoxin production, and virulence. A split luciferase assay confirmed the in vivo protein-protein interactions among three photoreceptors along with FgLaeA, a global regulator of secondary metabolism and fungal development. Introduction of an intact copy of the A. nidulans LreA and LreB genes, which are homologs of FgWc-1 and FgWc-2, into the ΔFgWc-1 and ΔFgWc-2 strains, respectively, failed to repress perithecia formation on CM in the gene deletion strains. Taken together, these results demonstrate that FgWc-1 and FgWc-2, two central components of the blue-light sensing system, negatively regulate sexual development in F. graminearum, which differs from the regulation pattern in A. nidulans.

Complex multicellularity in fungi: evolutionary convergence, single origin, or both?

“…Light sensing relays several important processes of fruiting body development, including its initiation, stimulating growth in the right direction and sensing seasonal light/dark periodicity that triggers fruiting (Pöggeler et al ., ; Kamada et al ., ). Many of these responses are mediated by the blue light receptor white collar complex (WCC) which, including its regulatory role in fruiting body development, is conserved widely (Idnurm & Heitman, ; Rodriguez‐Romero et al ., ; Verma & Idnurm, ), although the specific interaction may differ even among closely related species (Purschwitz et al ., ; Kim et al ., ). The WCC regulates sexual reproduction through mating genes (Idnurm & Heitman, ) in all fungal species examined so far (Idnurm & Heitman, ), except for budding and fission yeasts in which the WCC has been lost (Nguyen et al ., ).…”

SUB1 has photoreceptor dependent and independent functions in sexual development and secondary metabolism in Trichoderma reesei

“…BLR1 and BLR2 only play minor roles in the transcriptional regulation of the pheromone response pathway and sexual development (Seibel et al ., ), although important functions were shown for their homologues in the homothallic Fusarium graminearum (Kim et al ., ). In contrast, deletion of env1 leads to strong upregulation of both pheromone precursor and pheromone receptor genes, and causes female sterility (Seibel et al ., ).…”

The Photoreceptor Components FaWC1 and FaWC2 of Fusarium asiaticum Cooperatively Regulate Light Responses but Play Independent Roles in Virulence Expression

“…As found in the F. graminearum strain Z-3639, WCC should be required for the normal maturity of perithecia during sexual development [40]. However, another group later reported that WCC could negatively regulate sexual development in another strain of F. graminearum; the Z-3643 [30]. In the present study, the perithecial maturation and ascospore formation of F. asiaticum are dependent on the presence of the WCC.…”

“…Sexual reproduction is usually vital for the dissemination of fungal pathogens in their lifecycles, and the near-UV light is known to induce the perithecia maturation and ascospore formation in FGSC [39]. However, two independent studies reported inconsistent effects of the WCC photoreceptor on the sexual development of F. graminearum, which was probably due to the difference of the wild-type background strains used in each study [30,40]. The present work with F. asiaticum showed that the WT strain was able to form mature perithecia, in which the sexual ascospores could be found apparently.…”