Abstract
Transcriptional control of the cell cycle by forkhead (Fkh) transcription factors is likely associated with fungal adaptation to host and environment. Here we show that Fkh2, an ortholog of yeast Fkh1/2, orchestrates cell cycle and many cellular events of Beauveria bassiana, a filamentous fungal insect pathogen. Deletion of Fkh2 in B. bassiana resulted in dramatic down-regulation of the cyclin-B gene cluster and hence altered cell cycle (longer G2/M and S, but shorter G0/G1, phases) in unicellular blastospores. Consequently, ΔFkh2 produced twice as many, but smaller, blastospores than wild-type under submerged conditions, and formed denser septa and shorter/broader cells in aberrantly branched hyphae. In these hyphae, clustered genes required for septation and conidiation were remarkedly up-regulated, followed by higher yield and slower germination of aerial conidia. Moreover, ΔFkh2 displayed attenuated virulence and decreased tolerance to chemical and environmental stresses, accompanied with altered transcripts and activities of phenotype-influencing proteins or enzymes. All the changes in ΔFkh2 were restored by Fkh2 complementation. All together, Fkh2-dependent transcriptional control is vital for the adaptation of B. bassiana to diverse habitats of host insects and hence contributes to its biological control potential against arthropod pests.
Highlights
Transcriptional control of the cell cycle by forkhead (Fkh) transcription factors is likely associated with fungal adaptation to host and environment
As indicated by our data, Fkh[2] is free of any paralogue in B. bassiana and can regulate transcriptional expression of many target proteins required for cell cycle, hyphal septation, asexual development, antioxidant reaction, multidrug resistance, UV damage repair and conidial adhesion, thereby exerting profound effects on the fungal cell cycle, morphogenesis, conidiation, cell size and density, carbon/nitrogen utilization, multistress tolerance and virulence
Deletion of Fkh[2] in B. bassiana resulted in remarkable down-regulation of the CLB2-cluster genes (Clb[2], Swi[5], Ace[2], Cdc[5], Cdc[15] and Cdc25) essential for the cell cycle and mitosis[33,34,35], well in agreement with their transcriptional changes previously observed in yeast Fkh1/2 double-deletion mutants[8,11,12,47]
Summary
Transcriptional control of the cell cycle by forkhead (Fkh) transcription factors is likely associated with fungal adaptation to host and environment. There are only four FKH proteins in Saccharomyces cerevisiae, comprising Hcm[1], Fhl[1], Fkh[1] and Fkh[28] The latter two share a forkhead-associated domain (FHA), and are different from Hcm[1] and Fhl[1] and partially redundant in regulating periodic expression of cell-cycle-dependent genes in early M phase[9,10]. Blastospores turn back to hyphae, which must penetrate again through the cuticle for outhgrowth and conidiophore development so as to produce conidia on cadaver surface for survival, dispersion or new infecton cycle It is unclear how B. bassiana Fkh[2] is involved in the regulation of cell cycle and biological control potential dependent upon multistress tolerance and virulence. In B. bassiana, Fkh[2] was required for cell cycle progression, hyphal septation, and cell size and density but for many more biological processes of the fungal entomopathogen than of the model yeasts, including carbon/nitrogen utilization, asexual development, host infection, and cellular responses to fungicides, osmotic agents, high temperature and UV-B irradiation
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