Abstract
Brown eye spot (BES) disease caused by the fungus Cercospora coffeicola is present in all coffee-producing regions of the world. Heritability has been estimated in studies of Cercospora leaf spot disease resistance in several crops, but there are few studies characterizing the genetic heritability of the phenotypic characteristics of the fungus. Therefore, this study aims to verify the existence of heritability of the aggressiveness components (disease severity, sporulation and cercosporin production) in C. coffeicola isolates. Additionally, we estimate the effect of the municipalities (geographic origin) to check their influence on the fungus aggressiveness components. Variation in heritability was observed for each of the three aggressiveness components evaluated. Cluster analysis showed the genetic variability of C. coffeicola isolates, however there was no grouping of C. coffeicola isolates according to their geographic origin. Based on the results obtained, a group of C. coffeicola isolates with high severity and heritability values were selected with the potential to be used in the development and screening of resistant coffee cultivars.
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Almeida, A. M. R., Piuga, F. F., Marin, S. R. R., Binneck, E., Sartori, F., Costamilan, L. M., & Lopes, M. (2005). Pathogenicity, molecular characterization, and cercosporin content of Brazilian isolates of Cercospora kikuchii. Fitopatologia Brasileira, 30, 594–602. https://doi.org/10.1590/S0100-41582005000600005
Barbosa Junior, M. P., Pozza, E. A., Neto, H. S., Silva, M. L. S., Pozza, A. A. A., Guimarães, R. J., & Souza, P. E. (2019). Brown eye spot in coffee subjected to different drip irrigation and fertilization management. Australasian Plant Pathology, 48, 245–252. https://doi.org/10.1007/s13313-019-0623-y
Borges, V., Ferreira, P. V., Soares, L., Santos, G. M., & Santos, A. M. M. (2010). Seleção de clones de batata-doce pelo procedimento REML/BLUP. Acta Scientiarum Agronomy, 32(4), 643–649.
Botelho, D. M. S., Resende, M. L. V., Andrade, V. T., Pereira, A. A., Patricio, F. R. A., Junior, R., Pedro, M., Ogoshi, C., & Rezende, J. C. (2017). Cercosporiosis resistance in coffee germplasm collection. Euphytica, 213, 117. https://doi.org/10.1007/s10681-017-1901-9
Choquer, M., Dekkers, K. L., Chen, H. Q., Cao, L., Ueng, P. P., Daub, M. E., & Chung, K. R. (2005). The CTB1 gene encoding a fungal polyketide synthase is required for cercosporin biosynthesis and fungal virulence of Cercospora nicotianae. Molecular Plant-Microbe Interactions, 18(5), 468–476. https://doi.org/10.1094/MPMI-18-0468
Cruz, C. D. (2013). GENES: A software package for analysis in experimental statistics and quantitative genetics. Acta Scientiarum Agronomy, 35(3), 271–276.
Custódio, A. A. P., Pozza, E. A., Guimarães, S. S. C., Koshikumo, E. S. M., Hoyos, J. M. A., & Souza, P. E. S. (2011). Comparação e validação de escalas diagramáticas para cercosporiose em folhas de cafeeiro. Ciência agrotecnologia, 35(6), 1067–1076.
Daub, M. E., & Chung, K. R. (2009). Photoactivated perylenequinone toxins in plant pathogenesis. In H. Deising (Ed.), The Mycota V. Plant Relationship (2nd ed., pp. 201–219). Springer-Verlag.
Daub, M. E., & Ehrenshaft, M. (2000). The photoactivated Cercospora toxin cercosporin: contributions to plant disease and fundamental biology. Annual Review of Phytopathology, 38(1), 461-490. https://doi.org/10.1146/annurev.phyto.38.1.461
Dell’Acqua, R., Mantovani, E. S., Braghini, M. T., Oliveira, C. M. G., Harakava, R., Robaina, A. S., & Patricio, F. R. (2011). Variabilidade in vitro, in vivo e molecular de isolados de Cercospora coffeicola. Tropical Plant Pathology, 36, 313–326.
Duangsong, U., Laosatiti, K., Somta, P., & Srinives, P. (2018). Genetics of resistance to Cercospora leaf spot disease caused by Cercospora canenscens and Pseudocercospora cruenta in yardlong bean (Vigna unguiculata ssp. sesquipedalis) ×× grain cowpea bean (V. unguiculata ssp. Unguiculata) populations. Journal of Genetics, 97, 1451–1456. https://doi.org/10.1007/s12041-018-1003-z
Resende, M.D.V, & Duarte, J.B. (2007). Precisão e controle de qualidade em experimentos de avaliação de cultivares. Pesquisa Agropecuaria Tropical, 37(3), 182–194.
Gilbert, J., Abramson, D., McCallum, B., & Clear, R. (2002). Comparison of Canadian fusarium graminearum isolates for aggressiveness, vegetative compatibility, and production of ergosterol and mycotoxins. Mycopathologia, 153, 209–215.
Jenns, A. E., Daub, M. E., & Upchurch, R. G. (1989). Regulation of cercosporin accumulation in culture by medium and temperature manipulation. Phytopathology, 79, 213–219.
Lehman, J. S., & Oudemans, P. V. (2000). Variation and heritability of phenology in the fungus Monilinia vaccinii-corymbosi on blueberry. Phytopathology, 90(4), 390–395.
Li, D., Sossah, F. L., Yang, Y., Liu, Z., Dai, Y., Song, B., Fu, Y., & Li, Y. (2019). Genetic and pathogenic variability of Mycogone perniciosa isolates causing wet bubble disease on Agaricus bisporus in China. Pathogens, 8, 179.
Lima, L. M., Pozza, E. A., & Santos, F. S. (2012). Relationship between incidence of brown eye spot of coffee cherries and the chemical composition of coffee beans. Journal of Phytopathology, 160(4), 209–211. https://doi.org/10.1111/j.1439-0434.2012.01879.x
Mahmoudi, S. B., Abbaszadeh, M. S., Abbasi, S., & Farrokhinejad, R. (2018). Genetic diversity and pathogenic variability among Cercospora beticola Sacc. Isolates causing leaf spot of sugar beet in Iran. Journal Crop Protection, 7(2), 207–217.
Martins, R. B., Maffia, L. A., & Mizubuti, S. G. (2008). Genetic variability of Cercospora coffeicola from organic and conventional coffee plantings, characterized by vegetative compatibility. Phytopathology, 98(11), 1205–1211. https://doi.org/10.1094/PHYTO-98-11-1205
Mojena, R. (1977). Hierarchical grouping methods and stopping rules: An evaluation. The Computer Journal, 20, 359–363.
Nyquist, W. E., & Baker, R. J. (1991). Estimation of heritability and prediction of selection response in plant populations. Critical Reviews in Plant Sciences, 10(3), 235–322.
Omoigui, L. O., Arrey, M. O., Danmaigona, C. C., Ekeruo, G., & Timko, M. P. (2019). Inheritance of resistance to Cercospora leaf spot disease of cowpea [Vigna unguiculata (L.) Walp]. Euphytica, 215(5), 1–12.
Pariaud, B., Ravignéb, V., Halkettc, F., Goyeaua, H., Carlierb, J., & Lannoua, C. (2009). Aggressiveness and its role in the adaptation of plant pathogens. Plant Pathology, 58, 409–424. https://doi.org/10.1111/j.1365-3059.2009.02039.x
Patrício, F., Almeida, I., Barros, B., Santos, A., & Frare, P. (2008). Effectiveness of acibenzolar-S-methyl, fungicides and antibiotics for the control of brown eye spot, bacterial blight, brown leaf spot and coffee rust in coffee. Annals of Applied Biology, 152, 29–39. https://doi.org/10.1111/j.1744-7348.2007.00187.x
Patricio, F. R. A., Braghini, M. T., & Fazuoli, L. C. (2010). Resistance of plants of Coffea arabica, Coffea canephora and interespecific hybrids to brown eye spot. Bragantia, 69, 883–890. https://doi.org/10.1590/S0006-87052010000400014
Potgieter, L. (2021, March). Population Genomics of Cercospora beticola (Dissertation). Retrieved March 10, 2022, from https://macau.uni-kiel.de/receive/macau_mods_00001272. Accessed 12 Apr 2022.
Pozza, E. A., Carvalho, L. C., & Chalfoun, S. M. (2010). Sintomas de injúrias causadas por doenças em cafeeiro. In R. J. Guimarães, A. N. G. Mendes, & D. P. Baliza (Eds.), Semiologia do cafeeiro: Sintomas de desordens nutricionais, fitossanitárias e fisiológicas (pp. 68–106). Lavras.
Ramos, J. B., Resende, M. L. V. D., Botelho, D. M. D. S., Pereira, R. C. M., Reichel, T., Balieiro, A. A. F., Botega, G. P., & Abrahão, J. C. D. R. (2022). Screening coffee genotypes for brown eye spot resistance in Brazil. PloS one, 17(1), e0258822. https://doi.org/10.1371/journal.pone.0258822
R Development Core Team. (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.Rproject.org. Accessed 12 Apr 2022.
Resende, L. S., Botrel, É. P., Pozza, E. A., Roteli, K. C., Andrade, O. C. S., & Pereira, R. C. M. (2022). Effect of soil moisture, organic matter and fertilizer application on brown eye spot disease in coffee plantations. European Journal of Plant Pathology, 163, 351–367. https://doi.org/10.1007/s10658-022-02481-2
Resende, M. D. V. (2016). Software Selegen-REML/BLUP: A useful tool for plant breeding. Crop Breeding and Applied Biotechnology, 16, 330–339.
Ruppel, E. G. (1972). Variation among isolates of Cercospora beticola from sugarbeet. Phytopathology, 6, 134–136. https://doi.org/10.1094/Phyto-62-134
Santos, L. A., Souza, P. E., Pozza, E. A., Caldeira, D. M., & Botelho, D. M. S. (2014). Nova técnica para isolar Cercospora coffeicola Berkeley &Cooke, agente etiológico da cercosporiose do cafeeiro. Coffee Science, 9(1), 142–144.
Souza, A. G. C., Herrero, S., & Daub, M. E. (2019). The toxin Cercosporin is a virulence factor for infection of coffee by Cercospora coffeicola. BioRxiv. https://doi.org/10.1101/818328
Souza, A. G. C., Maffia, L. A., & Mizubuti, E. S. G. (2012). Cultural and aggressiveness variability of Cercospora coffeicola. Journal of Phytopathology, 160, 540–546. https://doi.org/10.1111/j.1439-0434.2012.01947.x
Souza, A. G. C., Maffia, L. A., Silva, F. F., Mizubuti, E. S. G., & Teixeira, H. (2015). A time series analysis of brown eye spot progress in conventional and organic coffee production systems. Plant Pathology, 64, 157–166.
Souza, A. G. C., Rodrigues, F. A., Maffia, L. A., & Mizubuti, E. S. G. (2011). Infection process of Cercospora coffeicola on coffee leaf. Journal of Phytopathology, 159, 6–11.
Subramanian, S., & Sridhar, T. (1966). Studies on the brown-eye-spot disease (Cercospora coffeicola B. & Cke.) of coffee (Coffea arabica L.): I. - emanation of ethylene from infected leaves. Rivista Di Patologia Vegetale, 2(3), 127–132 Retrieved September 21, 2020, from http://www.jstor.org/stable/42555991. Accessed 12 Apr 2022.
Surico, G. (2013). The concepts of plant pathogenicity, virulence/avirulence and effector proteins by a teacher of plant pathology. Phytpathologia Mediterranea, 52(3), 399–417.
Upchurch, R. G., Walker, D. C., Rollins, J. A., Ehrenshaft, M., & Daub, M. E. (1991). Mutants of Cercospora kikuchii altered in cercosporin synthesis and pathogenicity. Applied and Environmental Microbiology, 57, 2940–2945.
Vale, P. A. S., Resende, M. L. V., dos Santos Botelho, D. M., Pozza, E. A., Ogoshi, C., Monteiro, A. C. A., Costa, B. H. G., & Vasconcelos, V. A. M. (2019). Temperature, incubation time and virulence of Cercospora coffeicola in the production of cercosporin. Journal of Phytopathology, 167(7–8), 371–379. https://doi.org/10.1111/jph.12802
Valencia, A. G. (1970). Estudio fisiológico de la defoliación causado por Cercospora coffeicola em el cafeto. Cenicafé, 21(3), 105–114.
Yamazaki, S., & Ogawa, T. (1972). The chemistry and stereochemistry of Cercosporin. Agricultural and Biological Chemistry, 36(10), 1707–1718. https://doi.org/10.1080/00021369.1972.10860458
Ye, G., & Smith, K. F. (2010). Marker-assisted gene pyramiding for cultivar Development. Plant Breeding Reviews, 219–256. https://doi.org/10.1002/9780470535486.ch5
Zambolim, L. (2016). Doenças do Cafeeiro. In H. Kimati et al. (Eds.), Manual de Fitopatologia: Doenças das Plantas Cultivadas (Vol. v. 2, 5th ed., pp. 193–218). Agronômica Ceres.
Zongo, A., Konate, A. K., Kadidia, K., Sawadogo, M., Sankara, P., Ntare, B. R., & Desmae, H. (2019). Diallel analysis of early leaf spot (Cercospora arachidicola Hori) disease resistance in groundnut. Journal of Agronomy, 9(15), 2–12. https://doi.org/10.3390/agronomy90100
Acknowledgments
This research was co-funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil), Consórcio Brasileiro de Pesquisa e Desenvolvimento do Café, the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG, Brazil), Instituto Nacional de Ciência de Tecnologia do Café (INCT-Café, Brazil) and Fundação para a Ciência e a Tecnologia - UNIT LEAF (UID/AGR/04129/2020, Portugal). The authors are grateful to Cyntia S Santos for her assistance in drawing up the figure.
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dos Santos Botelho, D.M., de Resende, M.L.V., Andrade, V.T. et al. Heritability of aggressiveness components in Cercospora coffeicola isolates. Eur J Plant Pathol 164, 495–505 (2022). https://doi.org/10.1007/s10658-022-02573-z
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DOI: https://doi.org/10.1007/s10658-022-02573-z