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Journal of Integrative Agriculture  2020, Vol. 19 Issue (2): 541-550    DOI: 10.1016/S2095-3119(19)62675-4
Special Issue: 植物抗病遗传合辑Plant Disease-resistance Genetics 植物细菌真菌合辑Plant Bacteria/Fungus
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Bioinformatic analysis and functional characterization of the cfem proteins in maize anthracnose fungus Colletotrichum graminicola
GONG An-dong1, 2, JING Zhong-ying1, ZHANG Kai1, TAN Qing-qun1, WANG Guo-liang1, 3, LIU Wen-de1
1 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
2 College of Life Science, Xinyang Normal University, Xinyang 464000, P.R.China
3 Department of Plant Pathology, The Ohio State University, Columbus, Ohio 43210, USA
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Abstract  
Fungal secreted proteins that contain the Common in Fungal Extracellular Membrane (CFEM) domain are important for pathogenicity.  The hemibiotrophic fungus Colletotrichum graminicola causes the serious anthracnose disease of maize.  In this study, we identified 24 CgCFEM proteins in the genome of C. graminicola.  Phylogenic analysis revealed that these 24 proteins (CgCFEM1–24) can be divided into 2 clades based on the presence of the trans-membrane domain.  Sequence alignment analysis indicated that the amino acids of the CFEM domain are highly conserved and contain 8 spaced cysteines, with the exception that CgCFEM1 and CgCFEM24 lack 1 and 2 cysteines, respectively.  Ten CgCFEM proteins with a signal peptide and without the trans-membrane domain were considered as candidate effectors and, thus were selected for structural prediction and functional analyses.  The CFEM domain in the candidate effectors can form a helical-basket structure homologous to the Csa2 protein in Candida albicans, which is responsible for haem acquisition and pathogenicity.  Subcellular localization analysis revealed that these effectors accumulate in the cell membrane, nucleus, and cytosolic bodies.  Additionally, 5 effectors, CgCFEM6, 7, 8, 9 and 15, can suppress the BAX-induced programmed cell death in Nicotiana benthamiana with or without the signal peptide.  These results demonstrate that these 10 CgCFEM candidate effectors with different structures and subcellular localizations in host cells may play important roles during the pathogenic processes on maize plants.
 
Keywords:  CFEM domain        candidate effector        anthracnose disease        maize        Colletotrichum graminicola  
Received: 26 December 2018   Accepted:
Fund: This study was supported by the National Program for Support of Top-notch Young Professionals of China.
Corresponding Authors:  Correspondence LIU Wen-de, Tel/Fax: +86-10-62815921, E-mail: liuwende@caas.cn   

Cite this article: 

GONG An-dong, JING Zhong-ying, ZHANG Kai, TAN Qing-qun, WANG Guo-liang, LIU Wen-de. 2020.

Bioinformatic analysis and functional characterization of the cfem proteins in maize anthracnose fungus Colletotrichum graminicola
. Journal of Integrative Agriculture, 19(2): 541-550.

Albarouki E, Deising H B. 2013. Infection structure-specific reductive iron assimilation is required for cell wall integrity and full virulence of the maize pathogen Colletotrichum graminicola. Molecular Plant-Microbe Interactions, 26, 695–708.
Amselem J, Cuomo C A, van Kan J A, Viaud M, Benito E P, Couloux A, Coutinho P M, de Vries R P, Dyer P S, Fillinger S, Fournier E, Gout L, Hahn M, Kohn L, Lapalu N, Plummer K M, Pradier J M, Quevillon E, Sharon A, et al. 2011. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genetics, 7, e1002230.
Bai S W, Liu J, Chang C, Zhang L, Maekawa T, Wang Q Y, Xiao W K, Liu Y L, Chai J J, Takken F L, Schulze-Lefert P, Shen Q H. 2012. Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS Pathogens, 8, e1002752.
Dean R, Van Kan J A, Pretorius Z A, Hammond-Kosack K E, Di Pietro A, Spanu P D, Rudd J J, Dickman M, Kahmann R, Ellis J, Foster G D. 2012. The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology, 13, 414–430.
DeZwaan T M, Carroll A M, Valent B, Sweigard J A. 1999. Magnaporthe grisea pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. The Plant Cell, 11, 2013–2030.
Doehlemann G, van der Linde K, Assmann D, Schwammbach D, Hof A, Mohanty A, Jackson D, Kahmann R. 2009. Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathogens, 5, e1000290.
Doehlemann G, Wahl R, Horst R J, Voll L M, Usadel B, Poree F, Stitt M, Pons-Kuhnemann J, Sonnewald U, Kahmann R, Kamper J. 2008. Reprogramming a maize plant: Transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. The Plant Journal, 56, 181–195.
Gan P, Ikeda K, Irieda H, Narusaka M, O’Connell R J, Narusaka Y, Takano Y, Kubo Y, Shirasu K. 2013. Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytologist, 197, 1236–1249.
Giraldo M C, Valent B. 2013. Filamentous plant pathogen effectors in action. Nature Reviews Microbiology, 11, 800–814.
Han Y P, Li X Y, Cheng L, Liu Y C, Wang H, Ke D X, Yuan H Y, Zhang L S, Wang L. 2016. Genome-wide analysis of soybean JmjC domain-containing proteins suggests evolutionary conservation following whole-genome duplication. Frontiers in Plant Science, 7, 1800.
Kleemann J, Rincon-Rivera L J, Takahara H, Neumann U, Ver Loren van Themaat E, van der Does H C, Hacquard S, Stuber K, Will I, Schmalenbach W, Schmelzer E, O’Connell R J. 2012. Sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum. PLoS Pathogens, 8, e1002643.
Kou Y J, Tan Y H, Ramanujam R, Naqvi N I. 2017. Structure-function analyses of the Pth11 receptor reveal an important role for CFEM motif and redox regulation in rice blast. New Phytologist, 214, 330–342.
Kulkarni R D, Dean R A. 2004. Identification of proteins that interact with two regulators of appressorium development, adenylate cyclase and cAMP-dependent protein kinase A, in the rice blast fungus Magnaporthe grisea. Molecular Genetics and Genomics, 270, 497–508.
Kulkarni R D, Kelkar H S, Dean R A. 2003. An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. Trends in Biochemical Sciences, 28, 118–121.
Lacomme C, Santa Cruz S. 1999. Bax-induced cell death in tobacco is similar to the hypersensitive response. Proceedings of the National Academy of Sciences of the United States of America, 96, 7956–7961.
Lamarre C, Deslauriers N, Bourbonnais Y. 2000. Expression cloning of the Candida albicans CSA1 gene encoding a mycelial surface antigen by sorting of Saccharomyces cerevisiae transformants with monoclonal antibody-coated magnetic beads. Molecular Microbiology, 35, 444–453.
Liu W D, Liu J L, Triplett L, Leach J E, Wang G L. 2014. Novel insights into rice innate immunity against bacterial and fungal pathogens. Annual Review of Phytopathology, 52, 213–241.
Ludwig N, Lohrer M, Hempel M, Mathea S, Schliebner I, Menzel M, Kiesow A, Schaffrath U, Deising H B, Horbach R. 2014. Melanin is not required for turgor generation but enhances cell-wall rigidity in appressoria of the corn pathogen Colletotrichum graminicola. Molecular Plant-Microbe Interactions, 27, 315–327.
Mims C W, Vaillancourt L J. 2002. Ultrastructural characterization of infection and colonization of maize leaves by Colletotrichum graminicola, and by a C.?graminicola pathogenicity mutant. Phytopathology, 92, 803–812.
Miranda V J, Porto W F, Fernandes G D R, Pogue R, Nolasco D O, Araujo A C G, Cota L V, Freitas C G, Dias S C, Franco O L. 2017. Comparative transcriptomic analysis indicates genes associated with local and systemic resistance to Colletotrichum graminicola in maize. Scientific Reports, 7, 2483.
Nasser L, Weissman Z, Pinsky M, Amartely H, Dvir H, Kornitzer D. 2016. Structural basis of haem-iron acquisition by fungal pathogens. Nature Microbiology, 1, 16156.
Okamoto-Shibayama K, Kikuchi Y, Kokubu E, Sato Y, Ishihara K. 2014. Csa2, a member of the Rbt5 protein family, is involved in the utilization of iron from human hemoglobin during Candida albicans hyphal growth. FEMS Yeast Research, 14, 674–677.
Rolke Y, Liu S, Quidde T, Williamson B, Schouten A, Weltring K M, Siewers V, Tenberge K B, Tudzynski B, Tudzynski P. 2004. Functional analysis of H2O2-generating systems in Botrytis cinerea: The major Cu-Zn-superoxide dismutase (BCSOD1) contributes to virulence on French bean, whereas a glucose oxidase (BCGOD1) is dispensable. Molecular Plant Pathology, 5, 17–27.
Sabnam N, Roy Barman S. 2017. WISH, a novel CFEM GPCR is indispensable for surface sensing, asexual and pathogenic differentiation in rice blast fungus. Fungal Genetics and Biology, 105, 37–51.
Schliebner I, Becher R, Hempel M, Deising H B, Horbach R. 2014. New gene models and alternative splicing in the maize pathogen Colletotrichum graminicola revealed by RNA-Seq analysis. BMC Genomics, 15, 842.
Srivastava V K, Suneetha K J, Kaur R. 2014. A systematic analysis reveals an essential role for high-affinity iron uptake system, haemolysin and CFEM domain-containing protein in iron homoeostasis and virulence in Candida glabrata. Biochemical Journal, 463, 103–114.
Stephenson S A, Hatfield J, Rusu A G, Maclean D J, Manners J M.?2000. CgDN3: An essential pathogenicity gene of Colletotrichum gloeosporioides necessary to avert a hypersensitive-like response in the host Stylosanthes guianensis. Molecular Plant-Microbe Interactions, 13, 929–941.
Torres M F, Cuadros D F, Vaillancourt L J. 2014. Evidence for a diffusible factor that induces susceptibility in the Colletotrichum-maize disease interaction. Molecular Plant Pathology, 15, 80–93.
Torres M F, Ghaffari N, Buiate E A, Moore N, Schwartz S, Johnson C D, Vaillancourt L J. 2016. A Colletotrichum graminicola mutant deficient in the establishment of biotrophy reveals early transcriptional events in the maize anthracnose disease interaction. BMC Genomics, 17, 202.
Torto T A, Li S, Styer A, Huitema E, Testa A, Gow N A, van West P, Kamoun S. 2003. EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora. Genome Research, 13, 1675–1685.
Vaknin Y, Shadkchan Y, Levdansky E, Morozov M, Romano J, Osherov N. 2014. The three Aspergillus fumigatus CFEM-domain GPI-anchored proteins (CfmA-C) affect cell-wall stability but do not play a role in fungal virulence. Fungal Genetics and Biology, 63, 55–64.
Wang C L, Shim W B, Shaw B D. 2016. The Colletotrichum graminicola striatin orthologue Str1 is necessary for anastomosis and is a virulence factor. Molecular Plant Pathology, 17, 931–942.
Ye F H, Albarouki E, Lingam B, Deising H B. von Wiren N. 2014. An adequate Fe nutritional status of maize suppresses infection and biotrophic growth of Colletotrichum graminicola. Physiologia Plantarum, 151, 280–292.
Yoshino K, Irieda H, Sugimoto F, Yoshioka H, Okuno T, Takano Y. 2012. Cell death of Nicotiana benthamiana is induced by secreted protein NIS1 of Colletotrichum orbiculare and is suppressed by a homologue of CgDN3. Molecular Plant-Microbe Interactions, 25, 625–636.
Zhang Z N, Wu Q Y, Zhang G Z, Zhu Y Y, Murphy R W, Liu Z, Zou C G. 2015. Systematic analyses reveal uniqueness and origin of the CFEM domain in fungi. Scientific Reports, 5, 13032.
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