Control of Development, Secondary Metabolism and Light-Dependent Carotenoid Biosynthesis by the Velvet Complex of <i>Neurospora crassa</i>

Abstract

<i>Neurospora crassa</i> is an established reference organism to investigate carotene biosynthesis and light regulation. However, there is little evidence of its capacity to produce secondary metabolites. Here, we report the role of the fungal-specific regulatory velvet complexes in development and secondary metabolism (SM) in <i>N. crassa</i> Three velvet proteins VE-1, VE-2, VOS-1, and a putative methyltransferase LAE-1 show light-independent nucleocytoplasmic localization. Two distinct velvet complexes, a heterotrimeric VE-1/VE-2/LAE-1 and a heterodimeric VE-2/VOS-1 are found <i>in vivo</i> The heterotrimer-complex, which positively regulates sexual development and represses asexual sporulation, suppresses siderophore coprogen production under iron starvation conditions. The VE-1/VE-2 heterodimer controls carotene production. VE-1 regulates the expression of >15% of the whole genome, comprising mainly regulatory and developmental features. We also studied intergenera functions of the velvet complex through complementation of <i>Aspergillus nidulans veA</i>, <i>velB</i>, <i>laeA</i>, <i>vosA</i> mutants with their <i>N. crassa</i> orthologs <i>ve-1</i>, <i>ve-2</i>, <i>lae-1</i>, and <i>vos-1</i>, respectively. Expression of VE-1 and VE-2 in <i>A. nidulans</i> successfully substitutes the developmental and SM functions of VeA and VelB by forming two functional chimeric velvet complexes <i>in vivo</i>, VelB/VE-1/LaeA and VE-2/VeA/LaeA, respectively. Reciprocally, expression of <i>veA</i> restores the phenotypes of the <i>N. crassa ve-1</i> mutant. All <i>N. crassa</i> velvet proteins heterologously expressed in <i>A. nidulans</i> are localized to the nuclear fraction independent of light. These data highlight the conservation of the complex formation in <i>N. crassa</i> and <i>A. nidulans</i> However, they also underline the intergenera similarities and differences of velvet roles according to different life styles, niches and ontogenetic processes.