ARS2 Plays Diverse Roles in DNA Damage Response, Fungal Development, and Pathogenesis in the Plant Pathogenic Fungus Fusarium graminearum

Duc-Cuong Bui; Jung-Eun Kim; Jiyoung Shin; Jae Yun Lim; Gyung Ja Choi; Yin-Won Lee; Jeong-Ah Seo; Hokyoung Son

doi:10.3389/fmicb.2019.02326

ARS2 Plays Diverse Roles in DNA Damage Response, Fungal Development, and Pathogenesis in the Plant Pathogenic Fungus Fusarium graminearum

Front Microbiol. 2019 Oct 15:10:2326. doi: 10.3389/fmicb.2019.02326. eCollection 2019.

Authors

Duc-Cuong Bui^{1

2}, Jung-Eun Kim¹, Jiyoung Shin¹, Jae Yun Lim², Gyung Ja Choi³, Yin-Won Lee¹, Jeong-Ah Seo², Hokyoung Son¹

Affiliations

¹ Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul, South Korea.
² School of Systems Biomedical Science, Soongsil University, Seoul, South Korea.
³ Therapeutic & Biotechnology Division, Center for Eco-Friendly New Materials, Korea Research Institute of Chemical Technology, Daejeon, South Korea.

Abstract

Arsenite-resistance protein 2 (Ars2) is an important nuclear protein involved in various RNA metabolisms in animals and plants, but no Ars2 ortholog has been studied in filamentous fungi. Although it is an essential gene in most model eukaryotes, FgARS2 null mutants were viable in the plant pathogenic fungus Fusarium graminearum. The deletion of FgARS2 resulted in pleiotropic defects in various fungal developmental processes. Fgars2 mutants were irregular in nuclear division, and conidial germination was significantly retarded, causing the fungus to manifest its hypersensitive phenotypes under DNA damage stress. While FgARS2 deletion caused abnormal morphologies of ascospores and defective ascospore discharge, our data revealed that FgARS2 was not closely involved in small-non-coding RNA production in F. graminearum. The dominant nuclear localization of FgArs2-green fluorescent proteins (GFP) and abnormal nuclear division in FgARS2 deletion mutant implicated that FgArs2 functions in the nucleus. Intriguingly, we found that FgArs2 established a robust physical interaction with the cap binding complex (CBC) to form a tertiary complex CBC-Ars2 (CBCA), and disruption of any CBCA complex subunit drastically attenuated the virulence of F. graminearum. The results of the study indicate that Ars2 regulates fungal development, stress response, and pathogenesis via interaction with CBC in F. graminearum and provide a novel insight into understanding of the biological functions of Ars2 in filamentous fungi.

Keywords: DNA damage response; Fusarium graminearum; arsenite-resistance protein 2; fungal reproduction; fungal virulence.