Involvement of PaSNF1 in Fungal Development, Sterigmatocystin Biosynthesis, and Lignocellulosic Degradation in the Filamentous Fungus Podospora anserina.

Yuanjing Li,Yanling Qiu,Pengfei Yan,Lin Mou,Shang Liang,Ning Xie,Gang Liu,Xiaojie Lu,Shuangfei Li

doi:10.3389/fmicb.2020.01038

Yuanjing Li, Yanling Qiu + Show 7 more

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https://doi.org/10.3389/fmicb.2020.01038

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Abstract

The sucrose non-fermenting 1/AMP-activated protein kinase (SNF1/AMPK) is a central regulator of carbon metabolism and energy production in the eukaryotes. In this study, the functions of the Podospora anserina SNF1 (PaSNF1) ortholog were investigated. The ΔPaSNF1 mutant displays a delayed development of mycelium and fruiting bodies and fails to form ascospores. The expression of the PaSNF1 gene in the strain providing female organs in a cross is sufficient to ensure fertility, indicating a maternal effect. Results of environmental stress showed that ΔPaSNF1 was hypersensitive to stress, such as osmotic pressure and heat shock, and resistant to fluconazole. Interestingly, the knockout of PaSNF1 significantly promoted sterigmatocystin (ST) synthesis but suppressed cellulase [filter paperase (FPA), endoglucanase (EG), and β-glucosidase (BG)] activity. Further, transcriptome analysis indicated that PaSNF1 made positive regulatory effects on the expression of genes encoding cellulolytic enzymes. These results suggested that PaSNF1 may function in balancing the operation of primary and secondary metabolism. This study suggested that SNF1 was a key regulator concerting vegetative growth, sexual development, and stress tolerance. Our study provided the first genetic evidence that SNF1 was involved in the ST biosynthesis and that it may also be a major actor of lignocellulose degradation in P. anserina.

Highlights

Lignocellulose is one of the most abundant renewable resources on earth, mainly composed of cellulose, hemicellulose, and lignin (Jonsson et al, 2013)
A homologous protein was found in P. anserina, presenting the highest identity with N. crassa, H. jecorina, and yeast, which was 75.64, 83.63, and 41%, respectively, and designated as SNF1 (Protein ID: CAP72646.1; Pa_2_770)
The predicted amino acid sequence of P. anserina SNF1 (PaSNF1) shared an identity of 75.64% with NcSNF1 of N. crassa (CAD70761), 64.67% with HjSNF1 of H. jecorina (AF291845) (Cziferszky et al, 2003), 67.73% with FoSNF1 of Fusarium oxysporum (AAN32715) (Ospina-Giraldo et al, 2003), 66.06% with BbSNF1 of Beauveria bassiana (EJP66968) (Wang et al, 2014), 63.41% with PmSNF1 of Pestalotiopsis microspora (AUW40141) (Wang et al, 2018), 57.53% with MgSNF1 of Magnaporthe grisea (ABF48563) (Yi et al, 2008), 57.94% with SsSNF1 of Sclerotinia sclerotiorum (CAB40826) (Vacher et al, 2003), 44.35% with PdSNF1 of Penicillium digitatum (AFS18464) (Zhang et al, 2013), and 43.43% with CcSNF1 of Cochliobolus carbonum (AAD43341) (Tonukari et al, 2000)

Summary

Introduction

Lignocellulose is one of the most abundant renewable resources on earth, mainly composed of cellulose, hemicellulose, and lignin (Jonsson et al, 2013) It can be converted into different carbohydrates, including glucose, xylose, and aromatic monomer compounds, which could be applied for the production of ethanol, carbohydrates, and aromatic products (Ragauskas et al, 2014; Kawaguchi et al, 2016; Wu et al, 2018). It has promising applications in food, paper, Involvement of PaSNF1 in Fungal Development and textile industries as well as the production of biofuels and other chemicals (Paulova et al, 2015; Kubicek and Kubicek, 2016; Yenkie et al, 2016). Filamentous fungi were considered as promising candidates for producing lignocellulolytic enzymes (Couturier et al, 2016)

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