The APSES protein Sok2 is a positive regulator of sporulation in Ashbya gossypii

Summary Ashbya gossypii is a homothallic, flavinogenic, filamentous ascomycete that starts overproduction of riboflavin and fragments its mycelium quantitatively into spore producing sporangia at the end of a growth phase. Mating is not required for sporulation and the standard homothallic laborator...

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Bibliographic Details
Published in:Molecular microbiology 2017-12, Vol.106 (6), p.949-960
Main Authors: Wasserstrom, Lisa, Dünkler, Alexander, Walther, Andrea, Wendland, Jürgen
Format: Article
Language:English
Subjects:
Cyclic AMP-Dependent Protein Kinases - metabolism
Ectopic expression
Eremothecium - genetics
Eremothecium - physiology
Fragments
Fungal Proteins - genetics
Fungal Proteins - metabolism
Gene Deletion
Gene expression
Gene Expression Profiling
Gene Expression Regulation, Fungal
Kinases
Mating
Meiosis
Promoter Regions, Genetic
Protein kinase A
Protein Precursors - genetics
Protein Precursors - metabolism
Regulators
Repressor Proteins - genetics
Repressor Proteins - metabolism
Riboflavin
Riboflavin - metabolism
Saccharomyces cerevisiae
Saccharomyces cerevisiae Proteins - genetics
Saccharomyces cerevisiae Proteins - metabolism
Sporangia
Spores, Fungal - genetics
Spores, Fungal - physiology
Sporulation
Transcription factors
Transcription Factors - metabolism
Vitamin B
Yeast
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Summary:Summary Ashbya gossypii is a homothallic, flavinogenic, filamentous ascomycete that starts overproduction of riboflavin and fragments its mycelium quantitatively into spore producing sporangia at the end of a growth phase. Mating is not required for sporulation and the standard homothallic laboratory strain is a MATa strain. Here we show that ectopic expression of Saccharomyces cerevisiae MATα2 in A. gossypii completely suppresses sporulation, inhibits riboflavin overproduction and downregulates among others AgSOK2. AgSok2 belongs to a fungal‐specific group of (APSES) transcription factors. Deletion of AgSOK2 strongly reduces riboflavin production and blocks sporulation. The initiator of meiosis, AgIME1, is a transcription factor essential for sporulation. We characterized the AgIME1 promoter region required for complementation of the Agime1 mutant. Reporter assays with AgIME1 promoter fragments fused to lacZ showed that AgSok2 does not control AgIME1 transcription. However, global transcriptome analysis identified two other essential regulators of sporulation, AgIME2 and AgNDT80, as potential targets of AgSok2. Our data suggest that sporulation and riboflavin production in A. gossypii are under mating type locus and nutritional control. Sok2, a target of the cAMP/protein kinase A pathway, serves as a central positive regulator to promote sporulation. This contrasts Saccharomyces cerevisiae where Sok2 is a repressor of IME1 transcription. Our study has identified a conserved fungal developmental protein of the APSES family as a positive regulator of sporulation in Ashyba gossypii. This regulator, AgSok2, provides an essential link between nutritional signaling via the cAMP‐protein kinase A pathway and the core sporulation machinery including Ime1, Ime2 and Ndt80. Deletion of SOK2 abolishes sporulation; but interestingly, overexpression of the Saccharomyces cerevisiae MATalpha2 repressor also blocks sporulation. Our transcriptomic analyses provide evidence that alpha2 negatively regulates SOK2.
ISSN:0950-382X
1365-2958
DOI:10.1111/mmi.13859