The Histone Deacetylases MoRpd3 and MoHst4 Regulate Growth, Conidiation, and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae

Chaoxiang Lin; Xue Cao; Ziwei Qu; Shulin Zhang; Naweed I Naqvi; Yi Zhen Deng

doi:10.1128/mSphere.00118-21

The Histone Deacetylases MoRpd3 and MoHst4 Regulate Growth, Conidiation, and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae

mSphere. 2021 Jun 30;6(3):e0011821. doi: 10.1128/mSphere.00118-21. Online ahead of print.

Authors

Chaoxiang Lin¹, Xue Cao², Ziwei Qu³, Shulin Zhang⁴, Naweed I Naqvi^{3

5}, Yi Zhen Deng¹

Affiliations

¹ State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural Universitygrid.20561.30, Guangzhou, China.
² Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, South China Agricultural Universitygrid.20561.30, Guangzhou, China.
³ grid.226688.0Temasek Life Sciences Laboratory, National University of Singapore, Singapore.
⁴ Department of Plant Pathology, College of Plant Protection, grid.411389.6Anhui Agricultural University, Hefei, China.
⁵ Department of Biological Sciences, National University of Singapore, Singapore.

Abstract

As the causal agent of the blast disease, Magnaporthe oryzae is one of the most destructive fungal pathogens of rice. Histone acetylation/deacetylation is important for remodeling of chromatin superstructure and thus altering gene expression. In this study, two genes encoding histone deacetylases, namely, MoRPD3 and MoHST4, were identified and functionally characterized in M. oryzae. MoHst4 was required for proper mycelial growth and pathogenicity, whereas overproduction of MoRpd3 led to loss of pathogenicity, likely due to a block in conidial cell death and restricted invasive growth within the host plants. Green fluorescent protein (GFP)-MoRpd3 localized to the nucleus and cytoplasm in vegetative hyphae and developing conidia. By comparative transcriptomics analysis, we identified potential target genes epigenetically regulated by histone deacetylases (HDACs) containing MoRpd3 or MoHst4, which may contribute to conidia formation and/or conidial cell death, which is a prerequisite for successful appressorium-mediated host invasion. Taken together, our results suggest that histone deacetylases MoRpd3 and MoHst4 differentially regulate mycelial growth, asexual development, and pathogenesis in M. oryzae. IMPORTANCE HDACs (histone deacetylases) regulate various aspects of growth, development, and pathogenesis in plant-pathogenic fungi. Most members of HDAC classes I to III have been functionally characterized, except for orthologous Rpd3 and Hst4, in the rice blast fungus Magnaporthe oryzae. In this study, we assessed the function of MoRpd3 and MoHst4 by reverse genetics and found that they differentially regulate M. oryzae vegetative growth, asexual development, and infection. Particularly, MoRpd3 negatively regulates M. oryzae pathogenicity, likely through suppression of conidial cell death, which we recently reported as being critical for appressorium maturation and functioning. Overall, this study broadens our understanding of fungal pathobiology and its critical regulation by histone modification(s) during cell death and in planta differentiation.

Keywords: HDAC; Hst4; Magnaporthe oryzae; Rpd3; Sin3; histone deacetylation complex; pathogenesis.