HDA-2-Containing Complex Is Required for Activation of Catalase-3 Expression in Neurospora crassa
Open Access
- 14 June 2022
- journal article
- research article
- Published by American Society for Microbiology in mBio
- Vol. 13 (4), e0135122
- https://doi.org/10.1128/mbio.01351-22
Abstract
Clearance of reactive oxygen species (ROS) is critical to the survival of aerobic organisms. In the model filamentous fungus Neurospora crassa, catalase-3 (cat-3) expression is activated in response to H2O2-induced ROS stress. It is essential for aerobic organisms to maintain the homeostasis of intracellular reactive oxygen species (ROS) for survival and adaptation to the environment. In line with other eukaryotes, the catalase of Neurospora crassa is an important enzyme for clearing ROS, and its expression is tightly regulated by the growth phase and various oxidative stresses. Our study reveals that, in N. crassa, histone deacetylase 2 (HDA-2) and its catalytic activity positively regulate the expression of the catalase-3 (cat-3) gene. HDA-2, SIF-2, and SNT-1 may form a subcomplex with such a regulation role. As expected, deletion of HDA-2 or SIF-2 subunit increased acetylation levels of histone H4, indicating that loss of HDA-2 complex fails to deacetylate H4 at the cat-3 locus. Furthermore, loss of HDA-2 or its catalytic activity led to dramatic decreases of TFIIB and RNA polymerase II (RNAP II) recruitment at the cat-3 locus and also resulted in high deposition of H2A.Z at the promoter and transcription start site (TSS) regions of the cat-3 gene. Collectively, this study strongly demonstrates that the HDA-2-containing complex activates the transcription of the cat-3 gene by facilitating preinitiation complex (PIC) assembly and antagonizing the inhibition of H2A.Z at the cat-3 locus through H4 acetylation. IMPORTANCE Clearance of reactive oxygen species (ROS) is critical to the survival of aerobic organisms. In the model filamentous fungus Neurospora crassa, catalase-3 (cat-3) expression is activated in response to H2O2-induced ROS stress. We found that histone deacetylase 2 (HDA-2) positively regulates cat-3 transcription in N. crassa; this is widely divergent from the classical repressive role of most histone deacetylases. Like HDA-2, the SIF-2 or SNT-1 subunit of HDA-2-containing complex plays a positive role in cat-3 transcription. Furthermore, we also found that HDA-2-containing complex provides an appropriate chromatin environment to facilitate PIC assembly and to antagonize the inhibition role of H2A.Z at the cat-3 locus through H4 acetylation. Taken together, our results establish a mechanism for how the HDA-2-containing complex regulates transcription of the cat-3 gene in N. crassa.Funding Information
- MOST | National Key Research and Development Program of China (2018YFA0900500)
- National Natural Science Foundation of China (31771383)
This publication has 57 references indexed in Scilit:
- Ubiquitin Ligase Components Cullin4 and DDB1 Are Essential for DNA Methylation in Neurospora crassaOnline Journal of Public Health Informatics, 2010
- Multilayered control of gene expression by stress-activated protein kinasesThe EMBO Journal, 2009
- Dimethylation of H3K4 by Set1 Recruits the Set3 Histone Deacetylase Complex to 5′ Transcribed RegionsCell, 2009
- Evolution of Catalases from Bacteria to HumansAntioxidants and Redox Signaling, 2008
- A suite of Gateway® cloning vectors for high‐throughput genetic analysis in Saccharomyces cerevisiaeYeast, 2007
- The band mutation in Neurospora crassa is a dominant allele of ras-1 implicating RAS signaling in circadian outputGenes & Development, 2007
- CKI and CKII mediate the FREQUENCY-dependent phosphorylation of the WHITE COLLAR complex to close the Neurospora circadian negative feedback loopGenes & Development, 2006
- A Eukaryote without Catalase-Containing Microbodies: Neurosporacrassa Exhibits a Unique Cellular Distributionof Its Four CatalasesEukaryotic Cell, 2006
- A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factorsProceedings of the National Academy of Sciences of the United States of America, 2006
- Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT MethodMethods, 2001