Comparative cytology of the infection process of Colletotrichum sublineola falcate and oval conidia in susceptible and resistant sorghum cultivars
DOI:
https://doi.org/10.33448/rsd-v9i11.10211Keywords:
Oval conidia; Falcate conidia; Conidial dimorphism; Sorghum bicolor; Pathogen-host interaction.Abstract
The primary infection mode of Colletotrichum sublineola, the causal agent of anthracnose in sorghum, occurs through falcate conidia produced blasticaly from conidiophores in acervuli. A secondary type of conidium, the oval conidium, smaller in size and distinct ontogeny from the falcate ones, is also produced by this pathogen. The objective of this study was to compare, by light microscopy, the infection process between both conidia, the ovals and falcados conidia from C. sublineola, in resistant and susceptible sorghum cultivars to anthracnose. Leaves of sorghum plants with 25 days old from BR009 (susceptible) and SC283 (resistant) cultivars were detached and inoculated with both conidia obtained from 204.01 pathogenic isolate and the process of infection was observed by optical microscopy between 2 to 168 hours after inoculation (AI). Both conidia germinated 2 hours AI and, regardless of the cultivar, after 4 hours AI, rounded appressoria with smooth surface were formed directly from the falcate conidium, while slightly irregular appressoria were formed at the tip of the germinative tubes emitted by the oval conidia. At the susceptible cultivar, appressoria were formed with higher frequency by falcate conidia, while at the resistant cultivar these structures were formed with higher frequency by the oval conidia. Penetration pores and infection hyphae were observed in all the inoculated materials with both conidia. Disease symptoms were observed first on the inoculated material with falcate conidia and mainly on the susceptible cultivar. Lesions with acervuli containing falcate conidia were found at all treatments, thus completing the infection cycle.
References
Anand, T., Bhaskaran, R., Raguchander, T., Karthikeyan, G., Rajesh, M., & Senthilraja, G. (2008). Production of Cell Wall Degrading Enzymes and Toxins by Colletotrichum capsici and Alternaria alternata Causing Fruit Rot of Chillies. Journal of Plant Protection Research,
(4), 437–451. https://doi. org/10.2478/v10045-008-0053-2
Anjago, W. M., Zhou, T., Zhang, H., Shi, M., Yang, T., Zheng, H., & Wang, Z. (2018). Regulatory Network of Genes Associated with Stimuli Sensing, Signal Transduction and Physiological Transformation of Appressorium in Magnaporthe oryzae. Mycology, 9(3), 211–222. doi:10.1080/21501203.2018.1492981
Bailey, J. A., O'connell, R. J., Pring, R. J., & Nash, C (1992). Infection Strategies of Colletotrichum Species. In: Bailey, J. A. & Jeger, M. J. (Eds.) Colletotrichum: Biology, Pathology and Control. Wallingfor, Oxon, UK: C.A.B. International, p.88-120.
Basavaraju, P., Shetty, N. P., Shetty, H. S., de Neergaard, E., & Jorgensen, H. J. (2009). Infection Biology and Defense Responses in Sorghum Against Colletotrichum sublineolum. Journal of Applied Microbiology, 107(2), 404-415. https://doi.org/10.1111/j.1365-2672.2009.04234.x
Bourett, T. M., & Howard, R. J. (1990). In vitro Development of Penetration Structures in The Rice Blast Fungus Magnaporthe grisea. Canadian Journal of Botany, 68(2), 329–342. https://doi.org/10.1139/b90-044
Boyd, L. A., Ridout, C., O'Sullivan, D. M., Leach, J. E., & Leung, H. (2013). Plant-Pathogen Interactions: Disease Resistance in Modern Agriculture. Trends in genetics, 29(4), 233–240. https://doi.org/10.1016/j.tig.2012.10.011
Browning, M., Rowley, L. V., Zeng, P., Chandlee, J. M., & Jack-Son, N. (1999). Morphological, Pathogenic and Genetic Comparisons of Colletotrichum graminicola Isolates from Poaceae. Plant Disease, 83(3), 286-292. https://doi.org/10.1094/PDIS.1999.83.3.286
Casela, C. R., Ferreira, A. S., & Santos, F. G. (1998). Associação de Virulência de Colletotrichum graminicola à Resistência Genética em Sorgo. Fitopatologia Brasileira. 23(2), 143-146.
Casela, C. R., Santos, F., & Ferreira, A. S. (2000). Associações de Patogenicidade e Diversidade Fenotípica de Colletotrichum graminicola, Agente Causal da Antracnose em Sorgo. Fitopatologia Brasileira, 25(3), 517-521.
Chaky, J., Anderson, K., Moss, M., & Vaillancourt, L. (2001). Surface Hydrophobicity and Surface Rigidity Induce Spore Germination in Colletotrichum graminicola. Phytopathology, 91(6), 558–564. https://doi.org/10.1094/PHYTO.2001.91.6.558
Chala, A., Alemu, T., Prom, L., & Tronsmo, A. (2010). Effect of Host Genotypes and Weather Variables on the Severity and Temporal Dynamics of Sorghum Anthracnose in Ethiopia. Plant Pathology Journal, 9(1), 39-46. https://doi.org/10.3923/ppj.2010.39.46
Cota, L. V., Souza, A. G. C., da Costa, R. V., Silva, D. D., Lanza, F. E., Aguiar, F. M., & Figueiredo, J. E. F. (2017). Quantification of yield losses caused by leaf anthracnose on sorghum in Brazil. Journal of Phytopathology, 165(7-8), 479-485. https://doi.org/10.1111/jph.12582
da Costa, R. V., Silva, D. D., & Cota, L. V. (2013). Antracnose Foliar do Sorgo. Sete Lagoas: Embrapa Milho e Sorgo, 18 p. (Embrapa Milho e Sorgo. Circular técnica, 196).
Crouch, J. A. & Beirn, L. A. (2009). Anthracnose of Cereals and Grasses. Fungal Diversity 39, 19-44.
Crouch, J. A., Clarke, B. B., White Jr., J. F., & Hillman, B.I. (2009). Systematic Analysis of the Falcate-Spored Graminicolous Colletotrichum and a Description of Six New Species from Warm-Season Grasses. Mycologia, 101(5), 717–732. https://doi.org/10.3852/08-230
Diéguez-Uribeondo, J., Förster, H., Soto-Estrada, A., & Adaskaveg, J. E. (2005). Subcuticular-Intracellular Hemibiotrophic and Intercellular Necro-Trophic Development of Colletotrichum acutatum on Almond. Phytopathology, 95(7), 751-758. https://doi.org/10.1094/PHYTO-95-0751
Dodds, P. N., & Rathjen, J. P. (2010). Plant Immunity: Towards an Integrated View of Plant-Pathogen Interactions. Nature Reviews Genetics, 11(8), 539-48.
https://doi.org/10.1038/nrg2812
Favaro, L. C., Araújo, W. L., Souza-Paccola, E. A., Azevedo, J. L., & Paccola-Meirelles, L. D. (2007). Colletotrichum sublineolum Genetic Instability Assessed by Mutants Resistant to Chlorate. Mycological Research, 111(1), 93-105. https://doi.org/10.1016/j.mycres.2006.08.008
Gupta, R., Lee, S. E., Agrawal, G. K., Rakwal, R., Park, S., Wang, Y., & Kim, S. T. (2015). Understanding the Plant-Pathogen Interactions in the Context of Proteomics-Generated Apoplastic Proteins Inventory. Frontiers in plant science, 6, 352. https://doi.org/10.3389/fpls.2015.00352
Joshi, R. (2018). A Review on Colletotrichum spp. Virulence Mechanism Against Host Plant Defensive Factors. Journal of Medicinal Plants Studies, 6(6), 64-67.
https://doi.org/10.22271/plants.2018.v6.i6b.02
Hamel, L. P., Nicole, M. C., Duplessis, S., & Ellis, B. E. (2012). Mitogen-Activated Protein Kinase Signaling in Plant-Interacting Fungi: Distinct Messages from Conserved Messengers. The Plant cell, 24(4), 1327–1351. https://doi.org/10.1105/tpc.112.096156
Howard, R. J., & Valent, B. (1996). Breaking and Entering: Host Penetration by the Fungal Rice Blast Pathogen Magnaporthe grisea. Annual Review of Microbiology, 50(1), 491-512. https://doi.org/10.1146/annurev.micro.50.1.491
Ishikawa, F. H., Souza, E. A., Shoji, J. Y., Connolly, L., Freitag, M., Read, N. D., & Roca, M. G. (2012). Heterokaryon Incompatibility is Suppressed Following Conidial Anastomosis Tube Fusion in a Fungal Plant Pathogen. PloS one, 7(2), e31175.
https://doi.org/10.1371/journal.pone.0031175
Khan, A., & Hsiang, T. (2003). The Infection Process of Colletotrichum graminicola and Relative Aggressiveness on Four Turfgrass Species. Canadian journal of microbiology, 49(7), 433–442. https://doi.org/10.1139/w03-059
Kubo, Y. & Furusawa, I. (1986). Localization of Melanin in Appressoria of Colletotrichum lagenarium. Canadian Journal of Microbiology, 32(3), 280-282. https://doi.org/10.1139/m86-054
Liao, C. Y., Chen, M. Y., Chen, Y. K., Kuo, K. C., Chung, K. R., & Lee, M. H. (2012). Formation of Highly Branched Hyphae by Colletotrichum acutatum within the Fruit Cuticles of Capsicum spp. Plant Pathology, 6(2), 262-270. https://doi.org/10.1111/j.1365-3059.2011.02523.x
Lins, S. R. O., Alves, E., & Abreu, M. S. (2007). Estudos Histopatológicos de Colletotrichum spp. em Plântulas de Cafeeiro. Fitopatologia Brasileira, 32(6), 488-495. https://doi.org/10.1590/S0100-41582007000600006.
Maia, F. G. M., Armesto, C., Zacan, W. L. A., Maia, J., & ABREU, M. S. (2011). Efeito da Temperatura no Crescimento Micelial, Produção e Germinação de Conídios de Colletotrichum spp. Isolados de Mangueira com Sintomas de Antracnose. Bioscience Journal, 27(2), 205-210. http://www.seer.ufu.br/index.php/biosciencejournal/article/view/7581
Mendgen, K., & Hahn, M. (2002). Plant Infection and the Establishment of Fungal Biotrophy. Trends in plant Science, 7(8), 352–356. https://doi.org/10.1016/s1360-1385(02)02297-5
Mota, S. F., Barcelos, Q. L., Dias, M. A., & Souza, E. A. (2016). Variability of Colletotrichum spp in common bean. Genetics and Molecular Research, 15(2), 10.4238/gmr.15027176. https://doi.org/10.4238/gmr.15027176
Nishihara, N. (1975). Two Types of Conidia of Colletotrichum graminicola (Ces.) G. W. Wils. Formed on Artificial Media and their Pathogenicity. Annual Phytopathology Society Japan, 41(2), 171-175. https://doi.org/10.3186/jjphytopath.41.171
Nordzieke, D. E., Sanken, A., Antelo, L., Raschke, A., Deising, H. B., & Pöggeler, S. (2019). Specialized Infection Strategies of Falcate and Oval Conidia of Colletotrichum graminicola. Fungal Genetics and Biology, 133, 103276. https://doi.org/10.1016/j.fgb.2019.103276.
Nunes, M. P., Souza-Paccola, E. A., Nobrega, G. M. A., & Paccola-Meirelles, L.D. (2010). Use of Oval Conidia as a Tool to Assess the Genetic Transfer among Colletotrichum sublineolum Mutants.. Brazilian Archives of Biology and Technology, 53(1), 171-178.
https://doi.org/10.1590/S1516-89132010000100021
O’Connell, R. J., Thon, M. R., Hacquard, S., Amyotte, S. G., Kleemann, J., Torres, M. F., et al. (2012). Life Style Transitions in Plant Pathogenic Colletotrichum Fungi Deciphered by Genome and Transcriptome Analyses. Nature Genetics, 44, 1060-1065. https://doi.org/10.1038/ng.2372
Pain, N. A., Green, J. R., Jones, G. L., & O´Connell, R. J. (1996). Composition and Organization of Extracellular Matrices around Germ-Tubes and Appressoria of Colletotrichum lindemuthianum. Protoplasma, 190, 119-130. https://doi.org/10.1007/BF01281311
Panaccione, D. G., Vaillancourt, L. J., & Hanau, R. M. (1989). Conidial Dimorphism in Colletotrichum graminicola. Mycologia. 81(6), 876-883. https://doi.org/10.2307/3760106
Pande, S., Mughogho, L. K., Bandyopadhyay, R., & Karunaknr, R. I. (1991). Variation in Pathogenicity and Cultural Characteristics on Sorghum Isolates of Collelotrichum graminicola in India. Plant Disease, 75(8), 778-783. https://doi.org/10.1094/PD-75-0778.
Pereira, I. S., Abreu M. S. de; Alves E., & Ferreira, J. B (2009). Estudos Histopatológicos da Interação Colletotrichum gloeosporioides – Cafeeiro. Bragantia, 68(1), 117-123. https://doi.org/10.1590/S0006-87052009000100013
Prom, L. K., Perumal, R., Erpelding, J., Isakeit, T., Montes-Garcia, N., & Magill, C. W. A. (2009). Pictorial Technique for Mass Screening of Sorghum Germplasm for Anthracnose (Colletotrichum sublineolum) Resistance. The Open Agriculture Journal, 3(1), 20-25. https://doi.org/10.2174/1874331500903010020
Rhoden, S., Lucas, A., Evangelista, C., de Lima, F., Deprá, I., Nascimento, R., & Pamphile, J. (2019). Aspectos Físicos, Químicos e Genéticos na Interação Patógeno Planta Hospedeira. SaBios-Revista de Saúde e Biologia, 14(1), 34-41. http://revista2.grupointegrado.br/revista/index.php/sabios2/article/view/1338
Ribeiro, P. C. O., Machado Jr, R., Silva, R. A., & Santos, C. V. (2020). Híbridos Triplos: Antracnose do Sorgo sob Controle. Campo & Negócio, https://revistacampoenegocios.com.br/hibridos-triplos-antracnose-do-sorgo-sob-controle/
Roca, M. G., Davide, L. C., Davide, L. M. C., Mendes-Costa, M. C., Schwan, R. F., & Wheals, A.E. (2004). Conidial Anastomosis Fusion Between Colletotrichum Species. Mycological Research, 108(11), 1320-1326. https://doi.org/10.1017/S0953756204000838
Santos, L. V., Queiroz, M. V., Santana, M. F, Soares, M. A., Barros, E. G., Araújo, E. F., & Langin, T. (2012). Development of New Molecular Markers for the Colletotrichum Genus Using Retrocl1 Sequences. World Journal of Microbiology and Biotechnology, 28(3), 1087–1095. https://doi.org/10.1007/s11274-011-0909-x
Santos, G. R., Rodrigues, A. C., Bonifácio, A., Chagas Jr., A. F, & Tschoeke, P. H., (2014). Severidade de Antracnose em Folhas de Sorgo Submetido a Doses Crescentes de Silício. Revista Ciência Agronômica, 45(2), 403-408.
https://doi.org/10.1590/S1806-66902014000200023
Silva, D. D., Casela, C. R., Castro, H. A. de, Santos, F. G., & Ferreira, A.S. (2008). Diversidade Populacional de Colletotrichum sublineolum em Seis Localidades No Brasil. Summa Phytopathologica, 34(2), 149-155. https://doi.org/10.1590/S0100-54052008000200007.
Silva, D. D., Cota, L. V., da Costa, R. V., & Parreira, D. F. (2014). Principais Doenças do Sorgo. Informe Agropecuário, 35(278), 102-111.
da Silva, L. L., Alvarado-Moreno, H. L., Correia, H. L. N., Santana, M. F., & Queiroz, M. V. (2020). Colletotrichum: Species Complexes, Lifestyle, and Peculiarities of some Sources of Genetic Variability. Applied Microbiology and Biotechnology, 104(5), 1891–1904. https://doi.org/10.1007/s00253-020-10363-y.
Souza-Paccola, E. A., Favaro, L. C. L., Bomfeti, C. A., Mesquita, S. F. P., & Paccola-Meirelles, L. D. (2003a). Cultural Characterization and Conidial Dimorphism in Colletotrichum sublineolum. Journal Phytopathology, 151(7-8) 383-388. https://doi.org/10.1046/j.1439-0434.2003.00735.x
Souza-Paccola, E. A., Fávaro, L. C. L., Casela, C. R., & Paccola-Meirelles, L. D. (2003b). Genetic Recombination in Colletotrichum sublineolum. Journal Phytopathology, 151(6), 329-334. https://doi.org/10.1046/j.1439-0434.2003.00727.x
Souza-Paccola, E. A., Bomfeti, C. A., Tanaka, F. A. O., Junior, N. S. M., Colauto, N. B., Figueiredo, J. E. F., & Paccola-Meirelles, L. D. (2015). Novel Insights into the Early Stages of Infection by Oval Conidia of Colletotrichum sublineolum. Scientia Agricola, 72(4), 351–355. http://dx.doi.org/10.1590/0103-9016-2014-0409
Stutts, L. R., & Vermerris, W. (2020). Elucidating Anthracnose Resistance Mechanisms in Sorghum-A Review. Phytopathology, PHYTO04200132RVW. Advance online publication. https://doi.org/10.1094/PHYTO-04-20-0132-RVW
Sutton, B. C. (1968). The Appressoria of Colletotrichum graminicola and C. falcatum. Canadian Journal Botany, 46(7), 873-876. http://dx.doi.org/ https://doi.org/10.1139/b68-115
Thakur, R. P. & Mathur, K. (2000). Anthracnose. In: Frederiksen, R.A. & Odvody, G. (Eds.) Compendium of Sorghum Diseases. APS Press. St. Paul.
Vaillancourt, L. J. & Hanau, R. M. (1992). Genetic and Morphological Comparisons of Glomerella (Colletotrichum) Isolates from Maize and from Sorghum. Experimental Mycology, 16(3), 219-229. http://dx.doi.org/10.1016/0147-5975(92)90030-U
Vargas, W. A., Martín, J. ́ M. S., Rech, G. E., Rivera L. P., Benito, E.P., Díaz-Mínguez, J. M., Thon, M. R., & Sukno, S. A. (2012). Plant Defense Mechanisms are Activated During Biotrophic and Necrotrophic Development of Colletotricum graminicola in maize. Plant physiology, 158 (3):1342-1358. https://doi.org/10.1104/pp.111.190397
Xavier, K. V., Pfeiffer, T., Parreira, D. F., Chopra, S., & Vaillancourt, L. (2017). Aggressiveness of Colletotrichum sublineola Strains from Sorghum bicolor and S. halepense to Sweet Sorghum Variety Sugar Drip, and Their Impact on Yield. Plant disease, 101(9), 1578–1587. https://doi.org/10.1094/PDIS-09-16-1238-RE
Wharton, P. S., & Julian, A. M. (1996). A Cytological Study of Compatible and Incompatible Interactions Between Sorghum Bicolor and Colletotrichum sublineolum. New Phytologist, 134(1), 25-34. https://doi.org/10.1111/j.1469-8137.1996.tb01143.x
Wharton, P. S., Julian, A. M. & O´Connell R. J. (2001). Ultrastructure of the Infection of Sorghum bicolor by Colletotrichum sublineolum. Phytopathology, 91(2), 149-158. https://doi.org/10.1094/PHYTO.2001.91.2.149
Wharton, P. S., & Schilder, A. C. (2008). Novel Infection Strategies of Colletotrichum acutatum on Ripe Blueberry Fruit. Plant Pathology, 57(1), 122-134.
https://doi.org/10.1111/j.1365-3059.2007.01698.x
Wyatt, T. T., Wosten, H. A., & Dijksterhuis, J. (2013). Fungal Spores for Dispersion in Space and Time. Advances in Applied Microbiology, 85, 43-91. https://doi.org/10.1016/B978-0-12-407672-3.00002-2
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2020 Edneia Aparecida de Souza-Paccola; Isadora Fernanda Sperandio; Walter Fernandes Meirelles; Giani Andrea Linde; Nelson Barros Colauto; Luzia Doretto Paccola-Meirelles
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.