Gα-cAMP/PKA pathway positively regulates pigmentation, chaetoglobosin A biosynthesis and sexual development in Chaetomium globosum

PLoS One. 2018 Apr 13;13(4):e0195553. doi: 10.1371/journal.pone.0195553. eCollection 2018.

Abstract

Sensing the environmental signals, the canonical Gα-cAMP/PKA pathway modulates mycelial growth and development, and negatively regulates some secondary metabolism in filamentous fungi, e.g. aflatoxin in Aspergillus nidulans. Here we report the characterization of this signaling pathway in Chaetomium globosum, a widely spread fungus known for synthesizing abundant secondary metabolites, e.g. chaetoglobosin A (ChA). RNAi-mediated knockdown of a putative Gα-encoding gene gna-1, led to plural changes in phenotype, e.g. albino mycelium, significant restriction on perithecium development and decreased production of ChA. RNA-seq profiling and qRT-PCR verified significantly fall in expression of corresponding genes, e.g. pks-1 and CgcheA. These defects could be restored by simultaneous knock-down of the pkaR gene encoding a regulatory subunit of cAMP-dependent protein kinase A (PKA), suggesting that pkaR had a negative effect on the above mentioned traits. Confirmatively, the intracellular level of cAMP in wild-type strain was about 3.4-fold to that in gna-1 silenced mutant pG14, and addition of a cAMP analog, 8-Br-cAMP, restored the same defects, e.g., the expression of CgcheA. Furthermore, the intracellular cAMP in gna-1 and pkaR double silenced mutant was approaching the normal level. The following activity inhibition experiment proved that the expression of CgcheA was indeed regulated by PKA. Down-regulation of LaeA/VeA/SptJ expression in gna-1 mutant was also observed, implying that Gα signaling may crosstalk to other regulatory pathways. Taken together, this study proposes that the heterotrimeric Gα protein-cAMP/PKA signaling pathway positively mediates the sexual development, melanin biosynthesis, and secondary metabolism in C. globosum.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chaetomium / cytology
  • Chaetomium / genetics
  • Chaetomium / growth & development*
  • Chaetomium / metabolism*
  • Cyclic AMP / metabolism*
  • Cyclic AMP-Dependent Protein Kinases / metabolism*
  • Fungal Proteins / genetics
  • GTP-Binding Protein alpha Subunits / metabolism*
  • Genomics
  • Indole Alkaloids / metabolism*
  • Melanins / biosynthesis
  • Pigmentation*
  • RNA Interference
  • Signal Transduction
  • Transcription, Genetic

Substances

  • Fungal Proteins
  • GTP-Binding Protein alpha Subunits
  • Indole Alkaloids
  • Melanins
  • chaetoglobosins
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases

Grants and funding

This work is supported by a National Natural Science Foundation of China (NSFC grant #31470251 to XZ), a National Basic Research Program of China (“973” Program # 2007CB707801 to XZ), a grant from the Fundamental Research Funds for the Central Universities (# 2015NT10 to XH), and an Open Fund of Key Laboratory of Cell Proliferation and Regulation Biology, Ministry of Education (# 201502 to XH).