Antagonism of saprobe fungi from semiarid areas of the Northeast of Brazil against Sclerotinia sclerotiorum and biocontrol of soybean white mold

Douglas Casaroto Peitl, Ciro Hideki Sumida, Ricardo Marcelo Gonçalves, Sérgio Florentino Pascholati, Maria Isabel Balbi-Peña

Abstract


The antagonistic activity of 25 saprobe fungi from semiarid areas of Northeast Brazil was evaluated against Sclerotinia sclerotiorum (Lib.) de Bary (Helotiales: Sclerotiniaceae). Four fungi [Myrothecium sp. Tode (Hypocreales: Stachybotryaceae) isolate 2, Volutella minima Höhn. (Hypocreales: Nectriaceae), Phialomyces macrosporus P.C. Misra & P.H.B. Talbot (Pezizomycotina) and Dictyosporium tetraseriale Goh, Yanna & K.D. Hyde (Pleosporales: Dictyosporiaceae)] were selected and further tested their ability to inhibit mycelial growth, sclerotia formation and ascospore germination of S. sclerotiorum and to control white mold on soybean plants. V. minima and P. macrosporus filtrates at 50% effectively suppressed mycelial growth and Myrothecium sp. isolate 2 completely suppressed sclerotia formation and inhibited ascospore germination by over 95%, the same result as commercial fungicide fluazinam. Soybean plants pre-treated with Myrothecium sp. isolate 2, P. macrosporus, and V. minima and inoculated with S. sclerotiorum showed a reduction of 55.8%, 79.7%, and 83.2% of area under disease progress curve (AUDPC) of white mold, respectively, in relation to water. Collectively, these results underline the antagonistic activity of V. minima, P. macrosporus, and Myrothecium sp. isolate 2 against S. sclerotiorum and their potential as biocontrol agents of soybean white mold.

Keywords


Biological control; Glycine max; Saprobic fungi; Sclerotinia stem rot.

Full Text:

PDF

References


Abawi, G., & Grogan, R. (1979). Epidemiology of diseases caused by Sclerotinia species. Phytopathology, 69(8), 899-904. doi: 10.1094/Phyto-69-899

Abdullah, M. T., Ali, N. Y., & Suleman, P. (2008). Biological control of Sclerotinia sclerotiorum (Lib.) de with Trichoderma harzianum and Bacillus amyloliquefaciens. Crop Protection, 27(10), 1354-1359. doi: 10.1016/j.cropro.2008.05.007

Almeida, A. M. R., Ferreira, L. P., Yorinori, J. T., Silva, J. F. V., Henning, A. A., Godoy, C. V., & Costamilan, L. M. M. M. (2005). Doenças da soja (Glycine max). In L. Amorim, Jorge, A. M. R., & Bergamin, A. Fº (Eds.), Manual de fitopatologia (4a ed., pp. 569-588). São Paulo: Editora Agronômica Ceres, BR.

Almeida, D. A. C., Izabel, T. S. S., & Gusmão, L. F. P. (2011). Fungos conidiais do bioma Caatinga I. Novos registros para o continente americano. Rodriguésia, 62(1), 43-53. doi: 10.1590/2175-7860201162104

Ávila, Z. R., Carvalho, S. S., Braúna, L. M., Gomes, D. M. P. A., Silva, M. C. F., & Mello, S. C. M. M. (2005). Seleção de isolados de Trichoderma spp. antagônicos a Sclerotium rolfsii e Sclerotinia sclerotiorum. (Boletim Técnico. 2005). Brasilia, DF: EMBRAPA Recursos Genéticos.

Barbosa, F. R., & Gusmão, L. F. P. (2011). Conidial fungi from semi-arid Caatinga Biome of Brazil. Rare freshwater hyphomycetes and other new records. Mycosphere, 2(4), 475-485. Recuperado de http:// mycosphere.org/pdfs/MC2_4_No10.pdf

Bardin, S. D., & Huang, H. C. (2001). Research on biology and control of Sclerotinia diseases in Canada1. Canadian Journal Plant Pathology, 23(1), 88-98. doi: 10.1080/07060660109506914

Barros, D. C. M., Fonseca, I. C. B., Balbi-Peña, M. I., Pascholati, S. F. & Peitl, D. C. (2015). Biocontrol of Sclerotinia sclerotiorum and white mold of soybean using saprobic fungi from semi-arid areas of Northeastern Brazil. Summa Phytopathologica, 41(4), 251-255. doi: 10.1590/0100-5405/2086

Boland, G. J., & Hall, R. (1994). Index of plant hosts of Sclerotinia sclerotiorum. Canadian Journal Plant Pathology, 16(2), 93-108. doi: 10.1080/07060669409500766

Botrel, D. A. (2013). Fungos sapróbios como agentes de biocontrole da mancha aureolada do cafeeiro causada por Pseudomonas syringae pv. garcae. Dissertação de mestrado, Universidade Federal de Lavras, Lavras, MG, Brasil.

Botrel, D. A., Laborde, M. C. F., Ferreira, M. C., Medeiros, F. H. V., Resende, M. L. V., Ribeiro, P. M., Jr.,... Gusmão, L. F. P. (2018). Saprobic fungi as biocontrol agents of halo blight (Pseudomonas syringae pv. garcae) in coffee clones. Coffee Science, 13(3), 283-291. doi: 10.25186/cs.v13i3.1438

Chun, D., Kao, L. B., Lockwood, J. L., & Isleib, T. G. (1987). Laboratory and field assessment of resistance in soybean to stem rot caused by Sclerotinia sclerotiorum. Plant Disease, 71(9), 811-815. doi: 10.1094/ PD-71-0811

Danielson, G. A., Nelson, B. D., & Helms, T. C. (2004). Effect of sclerotinia stem rot on yield of soybean inoculated at different growth stages. Plant Disease, 88(3), 297-300. doi: 10.1094/PDIS.2004.88.3.297

Dhingra, O. D., Mendonça, H. L., & Macedo, D. M. (2009). Doenças e seu controle. Tecnologia de produção e usos da soja. Londrina: Mecenas.

Dudareva, N., Negre, F., Nagegowda, D. A., & Orlova, I. (2006). Plant volatiles: recent advances and future perspectives. Critical Reviews Plant Sciences, 25(5), 417-440. doi: 10.1080/07352680600899973

Elias, L. M., Domingues, M. V. P. F., Moura, K. E., Harakava, R., & Patricio, F. R. A. (2016). Selection of Trichoderma isolates for biological control of Sclerotinia minor and S. sclerotiorum in lettuce. Summa Phytopatholica, 42(3), 216-221. doi: 10.1590/0100-5405/2147

Figueirêdo, G. S., Figueirêdo, L. C., Cavalcanti, F. C. N., Santos, A. C., Costa, A. F., & Oliveira, N. T. (2010). Biological and chemical control of Sclerotinia sclerotiorum using Trichoderma spp. and Ulocladium atrum and pathogenicity to bean plants. Brazilian Archives of Biology and Technology, 53(1), 1-9. doi: 10.1590/S1516-89132010000100001

Fry, W. E. (1978). Quantification of general resistance of potato cultivars and fungicide effects for integrated control of potato late blight [caused by Phytophthora infestans]. Phytopathology, 68(11), 1650-1655. Recuperado de https://www.apsnet.org/publications/phytopathology/backissues/Documents/1978 Articles/Phyto68n11_1650.PDF

Geraldine, A. M., Lopes, F. A. C., Carvalho, D. D. C., Barbosa, E. T., Rodrigues, A. R., Brandão, R. S.,... Lobo, M., Jr. (2013). Cell wall-degrading enzymes and parasitism of sclerotia are key factors on field biocontrol of white mold by Trichoderma spp. Biological Control, 67(3), 308-316. doi: 10.1016/j. biocontrol.2013.09.013

Grau, C. R., & Hartman, G. L. (2015). Sclerotinia stem rot. In: G. L. Hartman, J. C. Rupe, E. J. Sikora, L. L. Domier, J. A. Davis, & K. L. Steffey (Eds.), Compendium of soybean diseases and pests (pp. 59-62). St. Paul: American Phytopathological Society.

Hoffman, D. D., Hartman, G. L., Mueller, D. S., Leitz, R. A., Nichkell, C. D., & Pedersen, W. L. (1998). Yield and seed quality of soybean cultivars infected with Sclerotinia sclerotiorum. Plant Disease, 82(7), 826-829. doi: 10.1094/PDIS.1998.82.7.826

Kamal, M. M., Lindbeck, K. D., Savocchia, S., & Ash, G. J. (2015). Biological control of sclerotinia stem rot of canola using antagonistic bacteria. Plant Pathology, 64(6), 1375-1384. doi: 10.1111/ppa.12369

Kottb, M., Gigolashvili, T., Großkinsky, D. K., & Piechulla, B. (2015). Trichoderma volatiles effecting Arabidopsis: from inhibition to protection against phytopathogenic fungi. Frontiers in Microbiology, (6), 995. doi: 10.3389/fmicb.2015.00995

Kull, L. S., Vuong, T. D., Powers, K. S., Eskridge, K. M., Steadman, J. R., & Hartman, G. L. (2003). Evluation of resistance screening methods for sclerotinia stem rot of soybean and dry bean. Plant Disease, 87(12), 1471-1476. doi: 10.1094/PDIS.2003.87.12.1471

Leão-Ferreira, S. M., Pascholati, S. F., Gusmão. L. F., & Castañeda Ruiz, R. F. (2013). Conidial fungi from the semi-arid Caatinga biome of Brazil. Three new species and new records. Nova Hedwigia, 96(3-4), 479-494. doi: 10.1127/0029-5035/2013/0084

Li, Q., Ning, P., Zheng, L., Huang, J., Li, G., & Hsiang, T. (2012). Effects of volatile substances of Streptomyces globisporus JK-1 on control of Botrytis cinerea on tomato fruit. Biological Control, 61(2), 113-120. doi: 10.1016/J.BIOCONTROL.2011.10.014

McCredie, T. A., & Sivasithamparam, K. (1985). Fungi mycoparasitic on sclerotia of Sclerotinia sclerotiorum in some. Western Australian soils. Transactions of the British Mycological Society, 84(4), 736-739. doi: 10.1016/S0007-1536(85)80133-9

Morath, S. U., Hung, R., & Bennett, J. W. (2012). Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biology Reviews, 26(2-3), 73-83. doi: 10.1016/J. FBR.2012.07.001

Morton, J. G., & Hall, R. (1989). Factors determining the efficacy of chemical control of white mold in white bean. Canadian Journal Plant Pathology, 11(3), 297-302. doi: 10.1080/07060668909501116

Nicot, P. C., Avril, F., Duffaud, M., Leyronas, C., Troulet, C., Villeneuve, F., & Bardin, M. (2019). Differential susceptibility to the mycoparasite Paraphaeosphaeria minitans among Sclerotinia sclerotiorum isolates. Tropical Plant Pathology, 44(1), 82-93. doi: 10.1007/s40858-018-0256-7

Oliveira, J. A. (1991). Efeito do tratamento fungicida em sementes e no controle de tombamento de plântulas de pepino (Cucumis sativus L.) e pimentão (Capsicum annum L.). Tese de doutorado, Universidade Federal de Lavras. Lavras, MG, Brasil.

Peitl, D. C., Araujo, F. A., Gonçalves, R. M., Santiago, D. C., Sumida, C. H., & Balbi-Peña, M. I. (2017). Biological control of bacterial spot of tomato by saprobe fungi from semi-arid areas of northeastern Brazil. Semina: Ciências Agrárias, 38(3), 1251-1263. doi: 10.5433/1679-0359.2017v38n3p1251

Pichersky, E., Noel, J. P., & Dudareva, N. (2006). Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science, 311(5762), 808-811. doi: 10.1126/science.1118510

Pierozzi, C. G. (2013). Fungos sapróbios do semiárido nordestino: aspectos fisiológicos, ação no controle da ferrugem e indução de enraizamento em mudas de eucalipto. Dissertação de mestrado, Universidade Estadual Paulista, Faculdade de Ciências Agronômicas, Botucatu, SP, Brasil.

Rabeendran, N., Jones, E. E., Moot, D. J., & Stewart, A. (2006). Biocontrol of Sclerotinia lettuce drop by Coniothyrium minitans and Trichoderma hamatum. Biological Control, 39(3), 352-362. doi: 10.1016/J. BIOCONTROL.2006.06.004

Resende, R. S., Milagres, C. A., Rezende, D., Aucique-Perez, C. E., & Rodrigues, F. A. (2015). Bioprospecting of saprobe fungi from the semi-arid north-east of Brazil for the control of anthracnose on sorghum. Journal of Phytopathology, 163(10), 787-794. doi: 10.1111/jph.12376

Ribeiro, A. I., Costa, E. S., Thomasi, S. S., Brandão, D. F. R., Vieira, P. C., Fernandes, J. B.,... Silva, M. F. G. F. (2018). Biological and chemical control of Sclerotinia sclerotiorum using Stachybotrys levispora and its secondary metabolite griseofulvin. Journal Agriculture and Food Chemistry, 66(29), 7627-7632. doi: 10.1021/acs.jafc.7b04197

Rodríguez, G. A. A., Abreu, M. S., Pinto, F. A. M. F., Monteiro, A. C. A., Núñez, Á. M. P., Resende, M. L. V.,... Medeiros, F. H. V. (2016). Phialomyces macrosporus decreases anthracnose severity on coffee seedlings by competition for nutrients and induced resistance. Biological Control, 103, 19-128. doi: 10. 1016/J.BIOCONTROL.2016.08.009

Santa Izabel, T. D. S., & Gusmão, L. F. P. (2018). Richness and diversity of conidial fungi associated with plant debris in three enclaves of Atlantic Forest in the Caatinga biome of Brazil. Plant Ecology and Evolution, 151(1), 35-47. doi: 10.5091/plecevo.2018.1332

Sarma, B. K., Ameer Basha, S., Singh, D. P., & Singh, U. P. (2007). Use of non-conventional chemicals as an alternative approach to protect chickpea (Cicer arietinum) from Sclerotinia stem rot. Crop Protection, 26(7), 1042-1048. doi: 10.1016/j.cropro.2006.09.015

Shaner, G., & Finney, R. E. (1977). The effect of nitrogen fertilization on the expression of slow-mildewing resistance in Knox wheat. Phytopathology, 67(8), 1051-1056. doi: 10.1094/Phyto-67-1051.

Sumida, C. H., Canteri, M. G., Peitl, D. C., Tibolla, F., Orsini, I. P., Araújo, F. A.,… Calvos, N. S. (2015). Chemical and biological control of Sclerotinia stem rot in the soybean crop. Ciência Rural, 45(5), 760-766. doi: 10.1590/0103-8478cr20140198

Sumida, C. H., Daniel, J. F. S., Araujo, A. P. C. S., Peitl, D. C., Abreu, L. M., Dekker, R. F. H., & Canteri, M. G. (2018). Trichoderma asperelloides antagonism to nine Sclerotinia sclerotiorum strains and biological control of white mold disease in soybean plants. Biocontrol Science and Technology, 28(2), 142-156. doi: 10.1080/09583157.2018.1430743

Sun, P., & Yang, X. B. (2000). Light, temperature, and moisture effects on apothecium production of Sclerotinia sclerotiorum. Plant Disease, 84(12), 1287-1293. doi: 10.1094/PDIS.2000.84.12.1287

Tolêdo-Souza, E. D., & Costa, J. L. S. (2007). Métodos de inoculação de plântulas de feijoeiro para avaliação de germoplasma quanto a resistência a Sclerotinia sclerotiorum (Lib.) De Bary. Pesquisa Agropecuária Tropical, 33(32), 57-63. Recuperado de https://www.revistas.ufg.br/pat/article/view/ 2348/2330

United States Department of Agriculture (2020). World agricultural supply and demand estimates. Retrieved from https://www.usda.gov/oce/commodity/wasde/

Vinodkumar, S., Nakkeeran, S., Renukadevi, P., & Malathi, V. G. (2017). Biocontrol potentials of antimicrobial peptide producing bacillus species: multifaceted antagonists for the management of stem rot of carnation caused by Sclerotinia sclerotiorum. Frontiers in Microbiology, 8, 446. doi: 10.3389/ fmicb.2017.00446

Whipps, J. M., Sreenivasaprasad, S., Muthumeenakshi, S., Rogers, C. W., & Challen, M. P. (2008). Use of Coniothyrium minitans as a biocontrol agent and some molecular aspects of sclerotial mycoparasitism. European Journal of Plant Pathology, 121(3), 323-330. doi: 10.1007/s10658-007-9238-1

Yang, F., Abdelnabby, H., & Xiao, Y. (2015). A mutant of the nematophagous fungus Paecilomyces lilacinus (Thom) is a novel biocontrol agent for Sclerotinia sclerotiorum. Microbial Pathogenesis, 89, 169-176. doi: 10.1016/j.micpath.2015.10.012

Zancan, A. W. L., Machado, J. C., Sousa, B. F. M., & Matos, C. S. M. (2012). Mycelial growth, production and germination of sclerotia of Sclerotinia sclerotiorum in the presence of fungicides and Trichoderma harzianum. Bioscience Journal, 28(5), 782-789. Recuperado de http://www.seer.ufu.br/index.php/ biosciencejournal/article/view/13909.

Zeng, W., Wang, D., Kirk, W., & Hao, J. (2012). Use of Coniothyrium minitans and other microorganisms for reducing Sclerotinia sclerotiorum. Biological Control. 60(2), 225-232. doi: 10.1016/J. BIOCONTROL.2011.10.009

Zhang, F., Ge, H., Zhang, F., Guo, N., Wang, Y., Chen, L.,… Li, C. (2016). Biocontrol potential of Trichoderma harzianum isolate T-aloe against Sclerotinia sclerotiorum in soybean. Plant Physiology and Biochemistry, 100, 64-74. doi:10.1016/j.plaphy.2015.12.017

Zheng, Y., Xue, Q.-Y., Xu, L.-L., Xu, Q., Lu, S., Gu, C., & Guo, J.-H. (2011) A screening strategy of fungal biocontrol agents towards Verticillium wilt of cotton. Biological Control, 56(3), 209-216. doi: 10.1016/ J.BIOCONTROL.2010.11.010




DOI: http://dx.doi.org/10.5433/1679-0359.2020v41n6p2597

Semina: Ciênc. Agrár.
Londrina - PR
E-ISSN 1679-0359
DOI: 10.5433/1679-0359
E-mail: semina.agrarias@uel.br
Este obra está licenciado com uma Licença Creative Commons Atribuição-NãoComercial 4.0 Internacional