The CfSnt2-Dependent Deacetylation of Histone H3 Mediates Autophagy and Pathogenicity of Colletotrichum fructicola

Zhenhong Chen; He Li; Shengpei Zhang

doi:10.3390/jof8090974

journal article Open Access Sep 18, 2022

The CfSnt2-Dependent Deacetylation of Histone H3 Mediates Autophagy and Pathogenicity of Colletotrichum fructicola

Zhenhong Chen He Li

Shengpei Zhang

Journal of Fungi Vol. 8 No. 9 pp. 974 · MDPI AG

View at Publisher Save 10.3390/jof8090974

Abstract

Camellia oleifera is one of the most valuable woody edible-oil crops, and anthracnose seriously afflicts its yield and quality. We recently showed that the CfSnt2 regulates the pathogenicity of Colletotrichum fructicola, the dominant causal agent of anthracnose on C. oleifera. However, the molecular mechanisms of CfSnt2-mediated pathogenesis remain largely unknown. Here, we found that CfSnt2 is localized to the nucleus to regulate the deacetylation of histone H3. The further transcriptomic analysis revealed that CfSnt2 mediates the expression of global genes, including most autophagy-related genes. Furthermore, we provided evidence showing that CfSnt2 negatively regulates autophagy and is involved in the responses to host-derived ROS and ER stresses. These combined functions contribute to the pivotal roles of CfSnt2 on pathogenicity. Taken together, our studies not only illustrate how CfSnt2 functions in the nucleus, but also link its roles on the autophagy and responses to host-derived stresses with pathogenicity in C. fructicola.

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References

49

[1]

Chen "Identification of Rubisco rbcL and rbcS in Camellia oleifera and their potential as molecular markers for selection of high tea oil cultivars" Front. Plant Sci. (2015) 10.3389/fpls.2015.00189

[2]

Di, T.M., Yang, S.L., Du, F.Y., Zhao, L., Li, X.H., Xia, T., and Zhang, X.F. (2018). Oleiferasaponin A(2), a novel saponin from camellia oleifera Abel. seeds, inhibits lipid accumulation of hepG2 cells through regulating fatty acid metabolism. Molecules, 23. 10.3390/molecules23123296

[3]

Profiling and quantification of phenolic compounds in Camellia seed oils: Natural tea polyphenols in vegetable oil

Xiaoqin Wang, Qiumei Zeng, María del Mar Contreras et al.

Food Research International 2017 10.1016/j.foodres.2017.09.089

[4]

Gong "Chromosome-level genome of Camellia lanceoleosa provides a valuable resource for understanding genome evolution and self-incompatibility" Plant J. (2022) 10.1111/tpj.15739

[5]

Gong "Full-length transcriptome from Camellia oleifera seed provides insight into the transcript variants involved in oil biosynthesis" J. Agric. Food Chem. (2020) 10.1021/acs.jafc.0c05381

[6]

Li, H., Zhou, G.Y., Liu, J.A., and Xu, J. (2016). Population genetic analyses of the fungal pathogen Colletotrichum fructicola on tea-oil trees in China. PLoS ONE, 11. 10.1371/journal.pone.0156841

[7]

Chen "Histone deacetylase CfSnt2 regulates the growth, development and pathogenicity of Colletotrichum fructicola" Mycosystema (2022)

[8]

Singh, R.K., Gonzalez, M., Kabbaj, M.H.M., and Gunjan, A. (2012). Novel E3 ubiquitin ligases that regulate histone protein levels in the budding yeast Saccharomyces cerevisiae. PLoS ONE, 7. 10.1371/journal.pone.0036295

[9]

Yang "Identifying cooperative transcription factors by combining ChIP-chip data and knockout data" Cell Res. (2010) 10.1038/cr.2010.146

[10]

Baker "The yeast Snt2 protein coordinates the transcriptional response to hydrogen peroxide-mediated oxidative stress" Mol. Cell. Biol. (2013) 10.1128/mcb.00025-13

[11]

Denisov "The transcription factor SNT2 is involved in fungal respiration and reactive oxidative stress in Fusarium oxysporum and Neurospora crassa" Physiol. Mol. Plant Pathol. (2011) 10.1016/j.pmpp.2011.07.007

[12]

Denisov "Inactivation of Snt2, a BAH/PHD-containing transcription factor, impairs pathogenicity and increases autophagosome abundance in Fusarium oxysporum" Mol. Plant Pathol. (2011) 10.1111/j.1364-3703.2010.00683.x

[13]

He "MoSnt2-dependent deacetylation of histone H3 mediates MoTor-dependent autophagy and plant infection by the rice blast fungus Magnaporthe oryzae" Autophagy (2018) 10.1080/15548627.2018.1458171

[14]

Liu "Autophagy regulates programmed cell death during the plant innate immune response" Cell (2005) 10.1016/j.cell.2005.03.007

[15]

Tor, a Phosphatidylinositol Kinase Homologue, Controls Autophagy in Yeast

Takeshi Noda, Yoshinori Ohsumi

Journal of Biological Chemistry 1998 10.1074/jbc.273.7.3963

[16]

Dementhon "Characterization of IDI-4, a bZIP transcription factor inducing autophagy and cell death in the fungus Podospora anserina" Mol. Microbiol. (2004) 10.1111/j.1365-2958.2004.04235.x

[17]

Historical landmarks of autophagy research

Yoshinori Ohsumi

Cell Research 2014 10.1038/cr.2013.169

[18]

Talbot "The emerging role of autophagy in plant pathogen attack and host defence" Curr. Opin. Plant Biol. (2009) 10.1016/j.pbi.2009.05.008

[19]

Li "Methods to Study Autophagocytosis in Magnaporthe oryzae" Methods Mol. Biol. (2021) 10.1007/978-1-0716-1613-0_14

[20]

Zhu "Current opinions on autophagy in pathogenicity of fungi" Virulence (2019) 10.1080/21505594.2018.1551011

[21]

Kershaw "Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease" Proc. Natl. Acad. Sci. USA (2009) 10.1073/pnas.0901477106

[22]

Zhu "VASt-domain protein regulates autophagy, membrane tension, and sterol homeostasis in rice blast fungus" Autophagy (2021) 10.1080/15548627.2020.1848129

[23]

Zheng, H., Miao, P., Lin, X., Li, L., Wu, C., Chen, X., Abubakar, Y.S., Norvienyeku, J., Li, G., and Zhou, J. (2018). Small GTPase Rab7-mediated FgAtg9 trafficking is essential for autophagy-dependent development and pathogenicity in Fusarium graminearum. PLoS Genet., 14. 10.1371/journal.pgen.1007546

[24]

Guo "Functional analysis of the autophagy-related protein CfAtg8 in Colletotrichum fructicola" Mycosystema (2021)

[25]

Yin "Histone acetyltransferase MoHat1 acetylates autophagy-related proteins MoAtg3 and MoAtg9 to orchestrate functional appressorium formation and pathogenicity in Magnaporthe oryzae" Autophagy (2019) 10.1080/15548627.2019.1580104

[26]

Zhang "Phototrophy and starvation-based induction of autophagy upon removal of Gcn5-catalyzed acetylation of Atg7 in Magnaporthe oryzae" Autophagy (2017) 10.1080/15548627.2017.1327103

[27]

Wang "Post-translational regulation of autophagy is involved in intra-microbiome suppression of fungal pathogens" Microbiome (2021) 10.1186/s40168-021-01077-y

[28]

The Histone Acetyltransferase CfGcn5 Regulates Growth, Development, and Pathogenicity in the Anthracnose Fungus Colletotrichum fructicola on the Tea-Oil Tree

Shengpei Zhang, Siqi Chen, He Li

Frontiers in Microbiology 2021 10.3389/fmicb.2021.680415

[29]

Ding "The tig1 histone deacetylase complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae" Plant Cell (2010) 10.1105/tpc.110.074302

[30]

Wang "Regulation of Autophagy by mTOR Signaling Pathway" Adv. Exp. Med. Biol. (2019) 10.1007/978-981-15-0602-4_3

[31]

Marroquin-Guzman, M., and Wilson, R.A. (2015). GATA-Dependent Glutaminolysis Drives Appressorium Formation in Magnaporthe oryzae by Suppressing TOR Inhibition of cAMP/PKA Signaling. PLoS Pathog., 11. 10.1371/journal.ppat.1004851

[32]

Nakatogawa "Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion" Cell (2007) 10.1016/j.cell.2007.05.021

[33]

Qian "Phosphatase-associated protein MoTip41 interacts with the phosphatase MoPpe1 to mediate crosstalk between TOR and cell wall integrity signalling during infection by the rice blast fungus Magnaporthe oryzae" Environ. Microbiol. (2021) 10.1111/1462-2920.15136

[34]

TOR Signaling and Nutrient Sensing

Thomas Dobrenel, Camila Caldana, Johannes Hanson et al.

Annual Review of Plant Biology 2016 10.1146/annurev-arplant-043014-114648

[35]

The Ustilago maydis Effector Pep1 Suppresses Plant Immunity by Inhibition of Host Peroxidase Activity

Christoph Hemetsberger, Christian Herrberger, Bernd Zechmann et al.

PLOS Pathogens 10.1371/journal.ppat.1002684

[36]

Liu "A self-balancing circuit centered on MoOsm1 kinase governs adaptive responses to host-derived ROS in Magnaporthe oryzae" Elife (2020) 10.7554/elife.61605

[37]

Tang "Endoplasmic reticulum-associated degradation mediated by MoHrd1 and MoDer1 is pivotal for appressorium development and pathogenicity of Magnaporthe oryzae" Environ. Microbiol. (2020) 10.1111/1462-2920.15069

[38]

Yin "Shedding light on autophagy coordinating with cell wall integrity signaling to govern pathogenicity of Magnaporthe oryzae" Autophagy (2020) 10.1080/15548627.2019.1644075

[39]

Dean "The Top 10 fungal pathogens in molecular plant pathology" Mol. Plant Pathol. (2012) 10.1111/j.1364-3703.2012.00822.x

[40]

Regulation of chromatin by histone modifications

Andrew J Bannister, Tony Kouzarides

Cell Research 2011 10.1038/cr.2011.22

[41]

Lee "Histone acetyltransferase complexes: One size doesn’t fit all" Nat. Rev. Mol. Cell Biol. (2007) 10.1038/nrm2145

[42]

Jeon "Histone acetylation in fungal pathogens of plants" Plant Pathol. J. (2014) 10.5423/ppj.rw.01.2014.0003

[43]

Lee "A Histone deacetylase, Magnaporthe oryzae RPD3, regulates reproduction and pathogenic development in the rice blast fungus" mBio (2021) 10.1128/mbio.02600-21

[44]

Kurdistani "Histone acetylation and deacetylation in yeast" Nat. Rev. Mol. Cell Biol (2003) 10.1038/nrm1075

[45]

Xu "The Fng3 ING protein regulates H3 acetylation and H4 deacetylation by interacting with two distinct histone-modifying complexes" New Phytol. (2022) 10.1111/nph.18294

[46]

Bruno "Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea" Eukaryot. Cell (2004) 10.1128/ec.3.6.1525-1532.2004

[47]

HISAT: a fast spliced aligner with low memory requirements

Daehwan Kim, Ben Langmead, Steven L. Salzberg

Nature Methods 2015 10.1038/nmeth.3317

[48]

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

Michael I Love, Wolfgang Huber, Simon Anders

Genome Biology 2014 10.1186/s13059-014-0550-8

[49]

Zhang, S., Guo, Y., Li, S., Zhou, G., Liu, J., Xu, J., and Li, H. (2019). Functional analysis of CfSnf1 in the development and pathogenicity of anthracnose fungus Colletotrichum fructicola on tea-oil tree. BMC Genet., 20. 10.1186/s12863-019-0796-y

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Metrics

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Citations

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References

Details

Published: Sep 18, 2022
Vol/Issue: 8(9)
Pages: 974
License: View

Authors

Z

Zhenhong Chen

College of Forestry, Central South University of Forestry and Technology, Changsha 410004, China; Key Laboratory of National Forestry and Grassland Administration on Control of Artificial Forest Diseases and Pests in South China, Central South University of Forestry and Technology, Changsha 410004, China; Hunan Provincial Key Laboratory for Control of Forest Diseases and Pests, Central South University of Forestry and Technology, Changsha 410004, China; Key Laboratory for Non-wood Forest Cultivation and Conservation of Ministry of Education, Central South University of Forestry and Technology, Changsha 410004, China

H

He Li

College of Forestry, Central South University of Forestry and Technology, Changsha 410004, China; Key Laboratory of National Forestry and Grassland Administration on Control of Artificial Forest Diseases and Pests in South China, Central South University of Forestry and Technology, Changsha 410004, China; Hunan Provincial Key Laboratory for Control of Forest Diseases and Pests, Central South University of Forestry and Technology, Changsha 410004, China; Key Laboratory for Non-wood Forest Cultivation and Conservation of Ministry of Education, Central South University of Forestry and Technology, Changsha 410004, China

S

Shengpei Zhang

College of Forestry, Central South University of Forestry and Technology, Changsha 410004, China; Key Laboratory of National Forestry and Grassland Administration on Control of Artificial Forest Diseases and Pests in South China, Central South University of Forestry and Technology, Changsha 410004, China; Hunan Provincial Key Laboratory for Control of Forest Diseases and Pests, Central South University of Forestry and Technology, Changsha 410004, China; Key Laboratory for Non-wood Forest Cultivation and Conservation of Ministry of Education, Central South University of Forestry and Technology, Changsha 410004, China

Funding

National Natural Science Foundation of China Award: 32001317

Natural Science Foundation of Hunan Province Award: 32001317

Research Foundation of Education Bureau of Hunan Province Award: 32001317

Cite This Article

Zhenhong Chen, He Li, Shengpei Zhang (2022). The CfSnt2-Dependent Deacetylation of Histone H3 Mediates Autophagy and Pathogenicity of Colletotrichum fructicola. Journal of Fungi, 8(9), 974. https://doi.org/10.3390/jof8090974

The CfSnt2-Dependent Deacetylation of Histone H3 Mediates Autophagy and Pathogenicity of Colletotrichum fructicola

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