Effect of temperature on disease severity of charcoal rot of melons caused byMacrophomina phaseolina: implications for selection of resistance sources

[EN] Macrophomina phaseolinais the causal agent of charcoal rot disease of melons causing significant losses worldwide. Use of resistant cultivars is a desirable method for controlling this disease, but there is no information about the influence of temperature on the resistant behavior found in melon accessions. The purpose of the present study was to assess the effect of temperature on the reaction of six melon accessions selected previously for their resistant response toM. phaseolina. Accessions were inoculated withM. phaseolinaisolate CMM-1531 and grown under accurately controlled environmental conditions at different temperature regimes (25, 28, 31, and 34 degrees C) in a replicated experiment. The increase in temperature increased the severity of symptoms in most genotypes, but this effect was less pronounced in the highly susceptible control, the cultivar 'Piel de sapo', and in the most resistant accession, the wild AfricanagrestisAg-15591Ghana, that remained resistant even at 34 degrees C. The use of several screening temperatures allowed a better characterization of accessions that behaved similarly as highly resistant at 25 degrees C (Con-Pat81Ko, Dud-QMPAfg, Can-NYIsr and Ag-C38Nig), but in which resistance breaking was observed with temperature rises. Temperatures of 28 degrees C and 31 degrees C were sufficient to make Dud-QMPAfg, Ag-C38Nig and Can-NYIsr moderately resistant, whereas Con-Pat81Ko remained highly resistant. All these genotypes were susceptible at 34 degrees C, which suggest that are not suitable for hot-climate growing areas. The most promising accession was Ag-15591Ghana, whose resistance was confirmed in two greenhouse experiments under stressful temperatures (>34 degrees C). The behavior of these sources should be confirmed in naturally infested fields, but the controlled screening methods presented here are essential to characterize new resistance sources and to conduct genetic studies when a high number of plants must be managed under controlled environmental conditions.This work was supported by Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior CAPES (Brazil). This study was also partially supported by the Spanish Ministerio de Economia y Competitividad project AGL2014-53398-C2-2-R, by the Spanish Ministerio de Ciencia, Innovacion y Universidades project AGL2017-85563-C2-1-R and by the Conselleria d'Educacio, Investigacio, Cultura i Esports de la Generalitat Valenciana PROMETEO project para grupos de excelencia/2017/078 (cofunded with FEDER funds).Linhares, CMDS.; Ambrosio, MMQ.; Castro, G.; Barros Torres, S.; Esteras Gómez, C.; Nunes, GHDS.; Picó Sirvent, MB. (2020). Effect of temperature on disease severity of charcoal rot of melons caused byMacrophomina phaseolina: implications for selection of resistance sources. European Journal of Plant Pathology. 158(2):431-441. https://doi.org/10.1007/s10658-020-02083-w4314411582Akhtar, K. P., Sarwar, G., & Arshad, H. M. I. (2011). Temperature response, pathogenicity, seed infection and mutant evaluation against Macrophomina phaseolina causing charcoal rot disease of sesame. Archives of Phytopathology and Plant Protection, 44(4), 320–330.Al-Mawaali, Q. S., Al-Sadi, A. M., Al-Said, F. A., & Deadman, M. L. (2013). Etiology, development and reaction of muskmelon to vine decline under arid conditions of Oman. Phytopathologia Mediterranea, 52(3), 457–465.Ambrósio, M. M. Q., Dantas, A. C. A., Martínez-Perez, E., Medeiros, A. C., Nunes, G. H. S., & Picó, M. B. (2015). Screening a variable germplasm collection of Cucumis melo L. for seedling resistance to Macrophomina phaseolina. Euphytica, 206(2), 287–300.Andrade, D. E. G. T., Michereff, S. J., Biondi, C. M., Nascimento, C. W. A., & Sales Jr., R. (2005). Frequência de fungos associados ao colapso do meloeiro e relação com características físicas, químicas e microbiológicas dos solos. Summa Phytopathologica, 31(4), 326–331.Apablaza, H. (1993). Charcoal rot of melon and watermelon (Macrophomina phaseolina (Tassi) Goidanich) in the metropolitan region of Chile. Ciencia e Investigación Agraria, 20(3), 101–105.Bakhshi, E., Safaie, N., & Shams-Bakhsh, N. (2018). Bacillus amyloliquefaciens as a biocontrol agent improves the management of charcoal root rot in melon. Journal of Agricultural Science and Technology, 20, 597–607.Bankole, S. A., Ikotun, B., & Ekpo, E. J. A. (1999). Fungal deterioration of melon seeds stored in jute sacks and polyethylene bags in ago-Iwoye, southwestern Nigeria. Mycopathologia, 146(3), 135–146.Bashir, M. R. (2017). Impact of global climate change on charcoal rot of sesame caused by Macrophomina phaseolina. Journal of Horticulture, 4, 1.Bianchini, A., Maringoni, A. C., & Carneiro, S. M. T. P. G. (2005). Doenças do feijoeiro. In H. Kimati, L. Amorim, A. Bergamin Filho, L. E. A. Camargo, & J. A. M. Rezende (Eds.), Manual de fitopatologia: Doenças das plantas cultivadas (pp. 333–349). São Paulo, Brazil: Ceres.Blanco-López, M. A., & Jiménez-Díaz, R. M. (1983). Effect of irrigation on susceptibility of sunflower to Macrophomina phaseoli. Plant Disease, 67, 1214–1217.Bruton, B. D., & Miller, M. E. (1997). Occurrence of vine decline diseases of melons in Honduras. Plant Disease, 81(6), 696–696.Bruton, B. D., & Wann, E. V. (1996). Charcoal rot. In T. A. Zitter, D. L. Hopkins, & C. E. Thomas (Eds.), Compendium of cucurbit diseases (pp. 49–50). St. Paul, USA: APS Press.Chung, B. N., Lee, J. H., Kang, B., Koh, S. W., Joa, J. H., Choi, K. S., & Ahn, J. J. (2018). HR-mediated defense response is overcome at high temperatures in Capsicum species. The Plant Pathology Journal, 34(1), 71–77.Cohen, R., Elkabetz, M., & Edelstein, M. (2016). Variation in the responses of melon and watermelon to Macrophomina phaseolina. Crop Protection, 85, 46–51.Cohen, R., Omari, N., Porat, A., & Edelstein, M. (2012). Management of Macrophomina wilt in melons using grafting or fungicide soil application: Pathological, horticultural and economical aspects. Crop Protection, 35, 58–63.Cohen, R., Tyutyunik, J., Fallik, E., Oka, Y., Tadmor, Y., & Edelstein, M. (2016). Phytopathological evaluation of exotic watermelon germplasm as a basis for rootstock breeding. Scientia Horticulturae, 165, 203–210.Dantas, A. M. M., Ambrósio, M. M. Q., Nascimento, S. R. C., Senhor, R. F., Cézar, M. A., & Lima, J. S. S. (2013). Incorporation of plant materials in the control of root pathogens in muskmelon. Revista Agro@ambiente On-line, 7(3), 338–344.Durner, E. (2019). Effective analysis of interactive effects with non-normal data using the aligned rank transform, ARTool and SAS® university edition. Horticulturae, 5, 57.Edraki, V., & Banihashemi, Z. (2010). Phenotypic diversity among isolates of Macrophomina phaseolina and its relation to pathogenicity. Iranian Journal of Plant Pathology, 46(4), 93–100.El-Kolaly, G. A. A., & Abdel-Sattar, M. A. (2013). The etiology of sudden wilt disease syndrome on melon in Egypt. Nature and Science, 11(11), 79–87.El-Sappah, A. H., Islam, M. M., El-Awady, H. H., Yan, S., Qi, S., Liu, J., et al. (2019). Tomato natural resistance genes in controlling the root-knot nematode. Genes, 10, 925.FAO. (2019). FAOSTAT: Food and Agriculture Organization Corporate Statistical Database. Available at: http://faostat3.fao.org/home/S. Accessed July 8, 2019.García-Jiménez, J., Armengol, J., Sales, R., Jordá, C., & Bruton, B. D. (2000). Fungal pathogens associated with melon collapse in Spain. EPPO Bull, 30(2), 169–173.Garrett, K. A., Dendy, S. P., Frank, E. E., Rouse, M. N., & Travers, S. E. (2006). Climate change effects on plant disease: Genomes to ecosystems. Annual Review of Phytopathology, 44, 489–509.Groenewald, J. Z., & Crous, P. W. (2014). Genetic diversity in Macrophomina phaseolina, the causal agent of charcoal rot. Phytopathologia Mediterranea, 53, 250–268.Islam, S., Haque, S., Islam, M. M., Emdad, E. M., Halim, A., Hossen, Q. M., et al. (2012). Tools to kill: Genome of one of the most destructive plant pathogenic fungi Macrophomina phaseolina. BMC Genomics, 13, 493–509.Jacob, C. J., Krarup, C., Díaz, G. A., & Latorre, B. A. (2013). A severe outbreak of charcoal rot in cantaloupe melon caused by Macrophomina phaseolina in Chile. Plant Disease, 97, 141.Machado, A. R., Pinho, D. B., Soares, D. J., Medeiros-Gomes, A. A., & Pereira, O. L. (2018). Bayesian analyses of five gene regions reveal a new phylogenetic species of Macrophomina associated with charcoal rot on oilseed crops in Brazil. European Journal of Plant Pathology, 153(1), 89–100.Manici, L. M., Caputo, F., & Cerato, C. (1995). Temperature responses of isolates of Macrophomina phaseolina from different climatic regions of sunflower production in Italy. Plant Disease, 79(8), 834–838.Marinho, R. E. M., Sales Jr., R., Maracajá, P. B., Silva, G. F., Costa, F. M., & Silva, E. C. (2002). Identificação da microflora associada a raízes de meloeiro nos estados do Rio Grande do Norte e Ceará. Revista Caatinga, 15(1), 25–28.Medeiros, A. C., Melo, D. R. M., Ambrósio, M. M. Q., Nunes, G. H. S., & Costa, J. M. (2015). Métodos de inoculação de Rhizoctonia solani e Macrophomina phaseolina em meloeiro (Cucumis melo). Summa Phytopathologica, 41(4), 281–286.Miyasaka, S. (2008). Manejo da biomassa e do solo visando à sustentabilidade da agricultura brasileira. São Paulo: Navegar.Nascimento, P. G. M. L., Ambrósio, M. M. Q., Freitas, F. C. L., Cruz, B. L. S., Dantas, A. M. M., Junior, R. S., et al. (2018). Incidence of root rot of muskmelon in different soil management practices. European Journal of Plant Pathology, 152(2), 433–446.Negreiros, A. M. P., Sales, R., Leon, M., Melo, N. J. D., Michereff, S. J., Ambrósio, M. M. D., et al. (2019). Identification and pathogenicity of Macrophomina species collected from weeds in melon fields in northeastern Brazil. Journal of Phytopathology, 167(6), 326–337.Nunes, G. H. S., Aragão, F. A. S., Nunes, E. W. L. P., Costa, J. M., & Ricarte, A. O. (2016). Melhoramento de Melão. In C. Nick & A. Borém (Eds.), Melhoramento de Hortaliças (pp. 331–363). Viçosa, Brazil: Universidade Federal de Viçosa.Pitrat, M. (2017). Melon genetic resources: Phenotypic diversity and horticultural taxonomy. In R. Grumet, N. Katzir, & J. Garcia-Mas (Eds.), Genetics and genomics of Cucurbitaceae (pp. 25–59). Cham, Switzerland: Springer Nature.Pivonia, S., Cohen, R., Kigel, J., & Katan, J. (2002). Effect of soil temperature on disease development in melon plants infected by Monosporascus cannonballus. Plant Pathology, 51(4), 472–479.Reuveni, R., Krikun, J., Nachmias, A., & Shlevin, E. (1982). The role of Macrophomina phaseolina in a collapse of melon plants in Israel. Phytoparasitica, 10(1), 51–56.Salari, M., Panjehkeh, N., Nasirpoor, Z., & Abkhoo, J. (2012). Reaction of melon (Cucumis melo L.) cultivars to soil-borne plant pathogenic fungi in Iran. African Journal of Biotechnology, 11(87), 15324–15329.Sales-Júnior, R., Oliveira, O. F., Medeiros, E. V., Guimarães, I. M., & Correia, K. C. (2012). Ervas daninhas como hospedeiras alternativas de patógenos causadores do colapso do meloeiro. Revista Ciência Agronômica, 43(1), 195–198.Sales-Júnior, R., Senhor, R. F., Michereff, S. J., & Negreiros, A. M. P. (2019). Reaction of melon genotypes to the root’s rot caused by Monosporascus. Revista Caatinga, 32(1), 288–294.Sarr, M. P., Ndiaye, M., Groenewald, J. Z., & Crous, P. W. (2014). Genetic diversity in Macrophomina phaseolina, the causal agent of charcoal rot. Phytopathologia Mediterranea, 53, 250–268.Scott, A. J., & Knott, M. A. (1974). Cluster analysis method for grouping means in the analysis of variance. Biometrics, 30(3), 507–512.Siegel, S., & Castellani Jr., N. J. (1988). Nonparametric statistics for the behavioral sciences. New York: McGraw-Hill.Tok, F. M., Dervis, S., & Arslan, M. (2018). Host selective virulence, temperature response and genetic diversity in Macrophomina phaseolina isolates from sesame and peanut in southern Turkey. Fresenius Environmental Bulletin, 27(11), 7374–7380.USDA. (2019). United States Department of Agriculture (USDA): Fungal databases, U. S. National Fungus Collections. https://nt.ars-grin.gov/fungaldatabases/. Accessed July 10, 2019.Walker, G. E. (1994). First report of Macrophomina phaseolina associated with vine decline in muskmelon in South Australia. Plant Disease, 78(6), 640.Wobbrock, J. O., Findlater, L., Gergle, D., & Higgins, J. J. (2011). The aligned rank transform for nonparametric factorial analyses using only ANOVA procedures. In Proceedings of the SIGCHI conference on human factors in computing systems (pp. 143–146). New York, USA: ACM.Wosula, E. N. (2017). Effect of temperature on wheat streak mosaic disease development in winter wheat. Plant Disease, 101(2), 324–330.Zhao, L., Cai, J., He, W., & Zhang, Y. (2019). Macrophomina vaccinii sp. nov. causing blueberry stem blight in China. MycoKeys, 55, 1–14