Abstract
LaeA and VeA coordinate secondary metabolism and differentiation in response to light signals in Aspergillus spp. Their orthologs, ChLae1 and ChVel1, were identified in the maize pathogen Cochliobolus heterostrophus, known to produce a wealth of secondary metabolites, including the host selective toxin, T-toxin. Produced by race T, T-toxin promotes high virulence to maize carrying Texas male sterile cytoplasm (T-cms). T-toxin production is significantly increased in the dark in wild type (WT), whereas Chvel1 and Chlae1 mutant toxin levels are much reduced in the dark compared to WT. Correspondingly, expression of T-toxin biosynthetic genes (Tox1) is up-regulated in the dark in WT, while dark-induced expression is much reduced/minimal in Chvel1 and Chlae1 mutants. Toxin production and Tox1 gene expression are increased in ChVEL1 overexpression (OE) strains grown in the dark and in ChLAE1 strains grown in either light or dark, compared to WT. These observations establish ChLae1 and ChVel1 as the first factors known to regulate host selective toxin production. Virulence of Chlae1 and Chvel1 mutants and OE strains is altered on both T-cms and normal cytoplasm maize, indicating that both T-toxin mediated super virulence and basic pathogenic ability are affected. Deletion of ChLAE1 or ChVEL1 reduces tolerance to H2O2. Expression of CAT3, one of the three catalase genes, is reduced in the Chvel1 mutant. Chlae1 and Chvel1 mutants also show decreased aerial hyphal growth, increased asexual sporulation and female sterility. ChLAE1 OE strains are female sterile, while ChVEL1 OE strains are more fertile than WT. ChLae1 and ChVel1 repress expression of 1,8-dihydroxynaphthalene (DHN) melanin biosynthesis genes, and, accordingly, melanization is enhanced in Chlae1 and Chvel1 mutants, and reduced in OE strains. Thus, ChLae1 and ChVel1 positively regulate T-toxin biosynthesis, pathogenicity and super virulence, oxidative stress responses, sexual development, and aerial hyphal growth, and negatively control melanin biosynthesis and asexual differentiation.
Highlights
In filamentous fungi, development and secondary metabolism are intimately coordinated [1,2]
LaeA was first characterized as a global regulator of secondary metabolism in A. nidulans; like veA mutants, loss of functional LaeA leads to reduced production of ST, penicillin, and lovastatin [12]
Microarray analysis of Aspergillus fumigatus wild type (WT) and laeA mutants demonstrated that LaeA controls 13 of 22 secondary metabolite gene clusters [13]; similar analyses with A. flavus revealed that at least 20 of 55 clusters were reduced in a laeA deletion mutant [14]
Summary
Development and secondary metabolism are intimately coordinated [1,2]. The VeA orthologs have been reported to control biosynthesis of various secondary metabolites such as aflatoxin, cyclopiazonic acid, and aflatrem by Aspergillus flavus [10] gibberellin (GA), fumonisin, fusarin C, and bikaverin by Fusarium fujikuroi [8], fumonisin and fusarin by Fusarium verticillioides [7] and trichothecenes by Fusarium graminearum [11]. LaeA was first characterized as a global regulator of secondary metabolism in A. nidulans; like veA mutants, loss of functional LaeA leads to reduced production of ST, penicillin, and lovastatin [12]. LaeA was reported to play a role in asexual and sexual development of A. nidulans [15], and asexual development in Penicillium chrysogenum [5] and F. fujikuroi [8]
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