LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity.

Ozlem Sarikaya Bayram,Gerhard H Braus,Kap-Hoon Han,Oliver Valerius,Min Ni,Jae-Hyuk Yu,Hee Soo Park,Stefan Irniger,Jennifer Gerke,Ozgür Bayram

doi:10.1371/journal.pgen.1001226

Abstract

VeA is the founding member of the velvet superfamily of fungal regulatory proteins. This protein is involved in light response and coordinates sexual reproduction and secondary metabolism in Aspergillus nidulans. In the dark, VeA bridges VelB and LaeA to form the VelB-VeA-LaeA (velvet) complex. The VeA-like protein VelB is another developmental regulator, and LaeA has been known as global regulator of secondary metabolism. In this study, we show that VelB forms a second light-regulated developmental complex together with VosA, another member of the velvet family, which represses asexual development. LaeA plays a key role, not only in secondary metabolism, but also in directing formation of the VelB-VosA and VelB-VeA-LaeA complexes. LaeA controls VeA modification and protein levels and possesses additional developmental functions. The laeA null mutant results in constitutive sexual differentiation, indicating that LaeA plays a pivotal role in inhibiting sexual development in response to light. Moreover, the absence of LaeA results in the formation of significantly smaller fruiting bodies. This is due to the lack of a specific globose cell type (Hülle cells), which nurse the young fruiting body during development. This suggests that LaeA controls Hülle cells. In summary, LaeA plays a dynamic role in fungal morphological and chemical development, and it controls expression, interactions, and modification of the velvet regulators.

Highlights

Multicellular organisms have developed a variety of different cell types, which become apparent during the ontogenesis of an organism to its adult form
We have discovered two related fungal specific protein complexes that provide a molecular link among spore formation, fungal development, and secondary metabolite production
The subunit allocation of both complexes depends on each other, and they share a common subunit. These complexes comprise three related and in fungi conserved proteins of the velvet family that function in concert with a known regulator of secondary metabolism, LaeA

Summary

Introduction

Multicellular organisms have developed a variety of different cell types, which become apparent during the ontogenesis of an organism to its adult form. Cell type specificity often requires specific physiology and metabolism to allow the formation of tissues and organs exhibiting various functions for the organism. Higher fungi produce a limited number of specialized cells and serve as simple and tractable models to study cell differentiation. Filamentous fungi grow by forming polar hyphae where similar cellular units are reiterated. The tip as well as branch points of the filamentous hyphae show increased cellular activity. Specialized cells include the ubiquitous asexual or sexual spores that are often dispersed into the air for propagation, and specialized cells that are required to form spores. Sexual spore formation can require complicated fruiting bodies consisting of additional specialized cells that form various tissues [2,3,4]. Fungal differentiation is coupled to the production of various secondary metabolites including mycotoxins and antibiotics [5], which are assumed to provide a chemical shield against competitors [6]

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