Identification and Expression of Some Plant Cell Wall-Degrading Enzymes Present in Three Ontogenetics Stages of Thecaphora frezii, a Peanut (<i>Arachis hypogaea</i> L.) Pathogenic Fungus — Oak Academic Publishing
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Identification and Expression of Some Plant Cell Wall-Degrading Enzymes Present in Three Ontogenetics Stages of Thecaphora frezii, a Peanut (<i>Arachis hypogaea</i> L.) Pathogenic Fungus
Cátedra de Biotecnología, Facultad de Ciencias Químicas, Unidad Asociada al CONICET: área de Cs. Agrarias, Ingeniería, Cs. Biológicas, Universidad Católica de Córdoba, Córdoba, Argentina
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Centro de Excelencia en Productos y Procesos de Córdoba—CEPROCOR, Santa María de Punilla, Córdoba, Argentina
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Centro de Excelencia en Productos y Procesos de Córdoba—CEPROCOR, Santa María de Punilla, Córdoba, Argentina
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CONICET, Santa María de Punilla, Córdoba, Argentina
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Cátedra de Biotecnología, Facultad de Ciencias Químicas, Unidad Asociada al CONICET: área de Cs. Agrarias, Ingeniería, Cs. Biológicas, Universidad Católica de Córdoba, Córdoba, Argentina
,
Cátedra de Biotecnología, Facultad de Ciencias Químicas, Unidad Asociada al CONICET: área de Cs. Agrarias, Ingeniería, Cs. Biológicas, Universidad Católica de Córdoba, Córdoba, Argentina
1 Cátedra de Biotecnología, Facultad de Ciencias Químicas, Unidad Asociada al CONICET: área de Cs. Agrarias, Ingeniería, Cs. Biológicas, Universidad Católica de Córdoba, Córdoba, Argentina
2 Centro de Excelencia en Productos y Procesos de Córdoba—CEPROCOR, Santa María de Punilla, Córdoba, Argentina
3 Centro de Excelencia en Productos y Procesos de Córdoba—CEPROCOR, Santa María de Punilla, Córdoba, Argentina
4 CONICET, Santa María de Punilla, Córdoba, Argentina
5 Cátedra de Biotecnología, Facultad de Ciencias Químicas, Unidad Asociada al CONICET: área de Cs. Agrarias, Ingeniería, Cs. Biológicas, Universidad Católica de Córdoba, Córdoba, Argentina
6 Cátedra de Biotecnología, Facultad de Ciencias Químicas, Unidad Asociada al CONICET: área de Cs. Agrarias, Ingeniería, Cs. Biológicas, Universidad Católica de Córdoba, Córdoba, Argentina
Peanuts can be affected by the presence of pathogenic microorganisms. The fungus Thecaphora frezii ( T. frezii ), which belongs to the taxonomic class Ustilaginomycetes, is the causal agent of the disease known as “peanut smut”. The life cycle of this fungus includes three stages, namely teliospores, basidiospores and hyphae. In the hyphae stage, infection occurs in the peanut plant, which requires the involvement of some enzymes secreted by the fungus. These include the Plant Cell Wall-Degrading Enzymes (PCWDEs), which degrade various polysaccharides. This study aimed to identify the presence of transcript for enzymes belonging to the PCWDEs from three stages of T. frezii . For this, total RNA was extracted from the three ontogenetic stages of T. frezii . These samples were analyzed using an RNA-Seq approach and some transcripts were quantified using Real Time PCR. The analysis of the data provided by the RNA-Seq of the three T. frezii stages, it was possible to identify some transcripts that could encode enzymes compatible with polysaccharides degradation that are part of the plant cell wall. In T. frezii transcriptome, 40 deduced proteins would be enzymes with functions of PCWDEs were identified. They were divided into 27 glycoside hydrolases; two polysaccharide lyases; three carbohydrate esterases and eight enzymes with auxiliary activities. In addition, the fungal SNF1 gene was identified whose activity could be affected by high glucose level, and indirectly influence the levels of some PCWDEs. The analysis of the PCWDEs could help to understand part of the fungal infection process and possibly find substances that can control its development.
Horbach, R., Navarro-Quesada, A.R., Knogge, W. and Deising, H.B. (2011) When and How to Kill a Plant Cell: Infection Strategies of Plant Pathogenic Fungi. Journal of Plant Physiology, 168, 51-62. https://doi.org/10.1016/j.jplph.2010.06.014
Abdulkhair, W.M. and Alghuthaymi, M.A. (2016) Plant Pathogens. In: Rigobelo, E., Ed., Plant Growth, IntechOpen, London, 49-59. https://doi.org/10.5772/65325
Kubicek, C.P., Starr, T.L. and Glass, N.L. (2014) Plant Cell Wall-Degrading Enzymes and Their Secretion in Plant-Pathogenic Fungi. Annual Review of Phytopathology, 52, 427-451. https://doi.org/10.1146/annurev-phyto-102313-045831
Vorwerk, S., Somerville, S. and Somerville, C. (2004) The Role of Plant Cell Wall Polysaccharide Composition in Disease Resistance. Trends in Plant Science, 9, 203-209. https://doi.org/10.1016/j.tplants.2004.02.005
Williamson, G., Kroon, P.A. and Faulds, C.B. (1998) Hairy Plant Polysaccharides: A Close Shave with Microbial Esterases. Microbiology, 144, 2011-2023. https://doi.org/10.1099/00221287-144-8-2011
Hückelhoven, R. (2007) Cell Wall-Associated Mechanisms of Disease Resistance and Susceptibility. Annual Review of Phytopathology, 45, 101-127. https://doi.org/10.1146/annurev.phyto.45.062806.094325
Henrissat, B., Coutinho, P.M. and Davies, G.J. (2001) A Census of Carbohydrate-Active Enzymes in the Genome of Arabidopsis Thaliana. Plant Molecular Biology, 47, 55-72. https://doi.org/10.1023/A:1010667012056
Cantarel, B.L., Coutinho, P.M., Rancurel, C., Bernard, T., Lombard, V. and Henrissat, B. (2009) The Carbohydrate-Active EnZymes Database (CAZy): An Expert Resource for Glycogenomics. Nucleic Acids Research, 37, D233-D238. https://doi.org/10.1093/nar/gkn663
Levasseur, A., Drula, E., Lombard, V., Coutinho, P.M. and Henrissat, B. (2013) Expansion of the Enzymatic Repertoire of the CAZy Database to Integrate Auxiliary Redox Enzymes. Biotechnology for Biofuels, 6, Article No. 41. https://doi.org/10.1186/1754-6834-6-41
Zhao, Z., Liu, H., Wang, C. and Xu, J.-R. (2014) Comparative Analysis of Fungal Genomes Reveals Different Plant Cell Wall Degrading Capacity in Fungi. BMC Genomics, 15, Article No. 6. https://doi.org/10.1186/1471-2164-15-6
Krapovickas, A. and Gregory, W.C. (2007) Taxonomía Del Género Arachis (Leguminosae). Bonplandia, 16, 1. https://doi.org/10.30972/bon.160158
Córdoba Bolsa de Cereales (2015) Campana 2014/2015. Producción Final de Maní, Córdoba, Argentina. Informe Especial No. 69.
Pitt, J.I., Dyer, S.K. and McCammon, S. (1991) Systemic Invasion of Developing Peanut Plants by Aspergillus flavus. Letters in Applied Microbiology, 13, 16-20. https://doi.org/10.1111/j.1472-765X.1991.tb00558.x
Fernandez, E.M., Rosolem, C.A., Maringoni, A.C. and Oliveira, D.M.T. (1997) Fungus Incidence on Peanut Grains as Affected by Drying Method and Ca Nutrition. Field Crops Research, 52, 9-15. https://doi.org/10.1016/S0378-4290(96)03461-2
Rossetto, C.A.V., Viegas, é. de C. and Lima, T. de M. (2003) Contaminacao Fúngica Do Amendoim Em Funcao Das Doses de Calcário e épocas de Amostragem. Bragantia, 62, 437-445. https://doi.org/10.1590/S0006-87052003000300010
Backman, P.A., Bell, D.K., Ben-Yephet, Y., Beute, M.K., Black, M.C., Boswell, T.E., et al. (1997) Compendium of Peanut Diseases. 2nd Edition. American Phytopathological Society, Saint Paul.
Cavallo, A., Novo, R. and Pérez, M. (2005) Eficiencia de Fungicidas En El Control de La Flora Fúngica Transportada Por Semillas de Maní (Arachis hypogaea L.) En La Argentina. Agriscientia, 22, 9-16. http://www.revistas.unc.edu.ar/index.php/agris/article/view/2674
Marinelli, A., March, G.J. and Oddino, C. (2008) Aspectos Biológicos y Epidemiológicos Del Carbón Del Maní (Arachis hypogaea L.) Causado Por Thecaphora Frezii Carranza & Lindquist. AgriScientia, 25, 1-5.
Carranza, J.M. and Lindquist, J.C. (1962) Thecaphora frezii n. Sp., Parásita de Arachis sp. Boletín de la Sociedad Argentina de Botánica, 10, 11-18.
Marinelli, A., March, G. and Rago, A. (1995) El Carbón Del Maní Thecaphora Frezii Sobre Arachis hypogaea L. Resúmenes VII Congreso Argentino de Micología y XVII Jornadas Argentinas de Micología, Rosario, Argentina, 134.
Cazzola, N., Gateau, M., March, G., Marinelli, A., García, J., Rago, A., et al. (2012) Intensidad y Pérdidas Ocasionadas Por Carbón Del Maní Según Regiones de Producción. 27° Jornada Nacional de Maní, 34-35.
Astiz Gassó, M. and Marinelli, A. (2003) Cultivo in Vitro de Thecaphora Frezii (Ustilaginales) Carbón Del Maní (Arachis hypogaea L). Boletín de La Sociedad Argentina de Botánica, 256.
Cazón, L.I., Paredes, J.A. and Rago, A.M. (2018) The Biology of Thecaphora frezii Smut and Its Effects on Argentine Peanut Production. In: Kimatu, J.N., Eds., Advances in Plant Pathology, IntechOpen, London, 31-46. https://doi.org/10.5772/intechopen.75837
Soria, N.W., Díaz, M.S., Figueroa, A.C., Alasino, V.R., Yang, P. and Beltramo, D.M. (2021) Identification of Chitin Synthase and Chitinase Genes in Three Ontogenetic Stages from Thecaphora frezii, the Causal Agent of Peanut Smut Disease. Physiological and Molecular Plant Pathology, 116, Article ID: 101727. https://doi.org/10.1016/j.pmpp.2021.101727
Ruiz-Herrera, J., Leon, C.G., Guevara-Olvera, L. and Carabez-Trejo, A. (1995) Yeast-Mycelial Dimorphism of Haploid and Diploid Strains of Ustilago maydis. Microbiology, 141, 695-703. https://doi.org/10.1099/13500872-141-3-695
Adolfo, A., López, C., Aboites, R., Eréndira, H., Ambriz, G. and Herrera, R. (2010) Identification of Proteins Secreted by the Fungus Ustilago maydis (De Candole) Corda (Basidiomicete) Grown under in Vitro Conditions. Revista Electrónica Nova Scientia, 2, 104-130.
Tudzynski, P. and Sharon, A. (2003) Fungal Pathogenicity Genes. Applied Mycology and Biotechnology, 3, 187-212. https://doi.org/10.1016/S1874-5334(03)80012-6
Mathioni, S.M., Beló, A., Rizzo, C.J., Dean, R.A. and Donofrio, N.M. (2011) Transcriptome Profiling of the Rice Blast Fungus during Invasive Plant Infection and in Vitro Stresses. BMC Genomics, 12, Article No. 49. https://doi.org/10.1186/1471-2164-12-49
Martínez-Soto, D., Robledo-Briones, A.M., Estrada-Luna, A.A. and Ruiz-Herrera, J. (2013) Transcriptomic Analysis of Ustilago maydis Infecting Arabidopsis Reveals Important Aspects of the Fungus Pathogenic Mechanisms. Plant Signaling & Behavior, 8, Article ID: e25059. https://doi.org/10.4161/psb.25059
Nadal, M., Garcia-Pedrajas, M.D. and Gold, S.E. (2010) The SNF11 Gene of Ustilago maydis Acts as a Dual Regulator of Cell Wall Degrading Enzymes. Phytopathology, 100, 1364-1372. https://doi.org/10.1094/MPMI-09-09-0217
Tzima, A.K., Paplomatas, E.J., Rauyaree, P., Ospina-Giraldo, M.D. and Kang, S. (2011) VdSNF1, the Sucrose Nonfermenting Protein Kinase Gene of Verticillium dahliae, Is Required for Virulence and Expression of Genes Involved in Cell-Wall Degradation. Molecular Plant-Microbe Interactions, 24, 129-142. https://doi.org/10.1094/MPMI-09-09-0217
Hedbacker, K. and Carlson, M. (2008) SNF1/AMPK Pathways in Yeast. Frontiers in Bioscience-Landmark, 13, 2408-2420. https://doi.org/10.2741/2854
Robinson, M.D., McCarthy, D.J. and Smyth, G.K. (2010) EdgeR: A Bioconductor Package for Differential Expression Analysis of Digital Gene Expression Data. Bioinformatics, 26, 139-140. https://doi.org/10.1093/bioinformatics/btp616
R Core Team (2018) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Yin, Y., Mao, X., Yang, J., Chen, X., Mao, F. and Xu, Y. (2012) DbCAN: A Web Resource for Automated Carbohydrate-Active Enzyme Annotation. Nucleic Acids Research, 40, W445-W451. https://doi.org/10.1093/nar/gks479
Huang, L., Zhang, H., Wu, P., Entwistle, S., Li, X., Yohe, T., et al. (2018) DbCAN-Seq: A Database of Carbohydrate-Active Enzyme (CAZyme) Sequence and Annotation. Nucleic Acids Research, 46, D516-D521. https://doi.org/10.1093/nar/gkx894
Blackman, L.M., Cullerne, D.P. and Hardham, A.R. (2014) Bioinformatic Characterisation of Genes Encoding Cell Wall Degrading Enzymes in the Phytophthora Parasitica Genome. BMC Genomics, 15, Article No. 785. https://doi.org/10.1186/1471-2164-15-785
Pagni, M., Ioannidis, V., Cerutti, L., Zahn-Zabal, M., Jongeneel, C. V., Hau, J., et al. (2007) MyHits: Improvements to an Interactive Resource for Analyzing Protein Sequences. Nucleic Acids Research, 35, W433-W437. https://doi.org/10.1093/nar/gkm352
Sigrist, C.J.A., de Castro, E., Cerutti, L., Cuche, B., Hulo, N., Bridge, A., et al. (2012) New and Continuing Developments at PROSITE. Nucleic Acids Research, 41, D344-D347.
National Center for Biotechnology Information. http://www.ncbi.nlm.nih.gov
El-Gebali, S., Mistry, J., Bateman, A., Eddy, S.R., Luciani, A., Potter, S.C., et al. (2019) The Pfam Protein Families Database in 2019. Nucleic Acids Research, 47, D427-D432. https://doi.org/10.1093/nar/gky995
Altschul, S., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., et al. (1997) Gapped BLAST and PSI-BLAST: A New Generation of Protein Database Search Programs. Nucleic Acids Research, 25, 3389-3402. https://doi.org/10.1093/nar/25.17.3389
Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P.M. and Henrissat, B. (2014) The Carbohydrate-Active Enzymes Database (CAZy) in 2013. Nucleic acids research, 42, D490-D495. https://doi.org/10.1093/nar/gkt1178
Park, B.H., Karpinets, T. V., Syed, M.H., Leuze, M.R. and Uberbacher, E.C. (2010) CAZymes Analysis Toolkit (CAT): Web Service for Searching and Analyzing Carbohydrate-Active Enzymes in a Newly Sequenced Organism Using CAZy Database. Glycobiology, 20, 1574-1584. https://doi.org/10.1093/glycob/cwq106
Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: Improving the Sensitivity of Progressive Multiple Sequence Alignment through Sequence Weighting, Position-Specific Gap Penalties and Weight Matrix Choice. Nucleic Acids Research, 22, 4673-4680. https://doi.org/10.1093/nar/22.22.4673
Sander, C. and Schneider, R. (1991) Database of Homology-Derived Protein Structures and the Structural Meaning of Sequence Alignment. Proteins: Structure, Function, and Genetics, 9, 56-68. https://doi.org/10.1002/prot.340090107
Mosquera, G., Giraldo, M.C., Khang, C.H., Coughlan, S. and Valent, B. (2009) Interaction Transcriptome Analysis Identifies Magnaporthe oryzae BAS1-4 as Biotrophy-Associated Secreted Proteins in Rice Blast Disease. The Plant Cell, 21, 1273-1290. https://doi.org/10.1105/tpc.107.055228
Song, Y.D., Hsu, C.C., Lew, S.Q. and Lin, C.H. (2020) Candida Tropicalis RON1 Is Required for Hyphal Formation, Biofilm Development, and Virulence but Is Dispensable for N-Acetylglucosamine Catabolism. Medical Mycology, 59, 379-391. https://doi.org/10.1093/mmy/myaa063
Geiser, E., Reindl, M., Blank, L.M., Feldbrügge, M. and Wierckx, N. (2016) Activating Intrinsic Carbohydrate-Active Enzymes of the Smut Fungus Ustilago maydis for the Degradation of Plant Cell Wall Components. Applied and Environmental Microbiology, 82, 5174-5185. https://doi.org/10.1128/AEM.00713-16
Soberanes-Gutiérrez, C. V., Pérez-Rueda, E., Ruíz-Herrera, J. and Galán-Vásquez, E. (2021) Identifying Genes Devoted to the Cell Death Process in the Gene Regulatory Network of Ustilago maydis. Frontiers in Microbiology, 12, Article ID: 680290. https://doi.org/10.3389/fmicb.2021.680290
Darino, M., Chia, K., Marques, J., Aleksza, D., Soto-Jiménez, L.M., Saado, I., et al. (2021) Ustilago Maydis Effector Jsi1 Interacts with Topless Corepressor, Hijacking Plant Jasmonate/Ethylene Signaling. New Phytologist, 229, 3393-3407. https://doi.org/10.1111/nph.17116
Livak, K.J. and Schmittgen, T.D. (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2 -ΔΔCT Method. Methods, 25, 402-408. https://doi.org/10.1006/meth.2001.1262
Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M. and Robledo, C.W. (2016) InfoStat Versión 2016. Grupo Infostat, FCA, Universidad Nacional de Córdoba, Argentina. https://www.infostat.com.ar
Sützl, L., Laurent, C.V.F.P., Abrera, A.T., Schütz, G., Ludwig, R. and Haltrich, D. (2018) Multiplicity of Enzymatic Functions in the CAZy AA3 Family. Applied Microbiology and Biotechnology, 102, 2477-2492. https://doi.org/10.1007/s00253-018-8784-0
Aspeborg, H., Coutinho, P.M., Wang, Y., Brumer, H. and Henrissat, B. (2012) Evolution, Substrate Specificity and Subfamily Classification of Glycoside Hydrolase Family 5 (GH5). BMC Evolutionary Biology, 12, Article No. 186. https://doi.org/10.1186/1471-2148-12-186
Fernández-Leiro, R., Pereira-Rodríguez, á., Cerdán, M.E., Becerra, M. and Sanz-Aparicio, J. (2010) Structural Analysis of Saccharomyces Cerevisiae α-Galactosidase and Its Complexes with Natural Substrates Reveals New Insights into Substrate Specificity of GH27 Glycosidases. Journal of Biological Chemistry, 285, 28020-28033. https://doi.org/10.1074/jbc.M110.144584
Marinelli, A.D., March, G.J. and Oddino, C.M. (2017) Enfermedades Fúngicas Del Maní. In: Giayetto, E.M., Ed., El Cultivo Del Maní En Córdoba, 2nd Edition, Río Cuarto, Córdoba, 285-317.
Rajeswari, P. (2015) In Vitro Inhibition of Cellulolytic Enzymes of Fusarium Oxysporum by Trichoderma Spp and Pseudomonas Fluorescens on Arachis hypogaea L. International Journal of Applied Sciences and Biotechnology, 3, 106-110. https://doi.org/10.3126/ijasbt.v3i1.12138
Rytioja, J., Hildén, K., Yuzon, J., Hatakka, A., de Vries, R.P. and Makela, M.R. (2014) Plant-Polysaccharide-Degrading Enzymes from Basidiomycetes. Microbiology and Molecular Biology Reviews, 78, 614-649. https://doi.org/10.1128/MMBR.00035-14
Ludin, K., Jiang, R. and Carlson, M. (1998) Glucose-Regulated Interaction of a Regulatory Subunit of Protein Phosphatase 1 with the Snf1 Protein Kinase in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America, 95, 6245-6250. https://doi.org/10.1073/pnas.95.11.6245
Ahuatzi, D., Riera, A., Peláez, R., Herrero, P. and Moreno, F. (2007) Hxk2 Regulates the Phosphorylation State of Mig1 and Therefore Its Nucleocytoplasmic Distribution. Journal of Biological Chemistry, 282, 4485-4493. https://doi.org/10.1074/jbc.M606854200