Interference of aqueous and ethanolic solutions of Adiantum latifolium Lam. (Pteridaceae) leaves on in vitro Ceratocystis cacaofunesta mycelial growth

Interferência de soluções aquosas e alcoólicas de folhas de Adiantum latifolium Lam. (Pteridaceae) no crescimento micelial de Ceratocystis cacaofunesta in vitro

Matheus Bomfim da Cruz Dhierllate Ferreira de Sousa Leticia de Almeida Oliveira Jerônimo Pereira de França Lucimar Pereira de França Aline Oliveira Conceição Alba Lucilvânia Fonseca Chaves About the authors

ABSTRACT

Ceratocystis cacaofunesta is the etiologic agent of “Ceratocystis wilt of cacao”, an irreversible disease that affects the vascular system of the plant. The management of the disease is difficult and economic and alternative solutions are needed. The medicinal plants compounds are known to have antimicrobial activity, and they could be an alternative choice in the C. cacaofunesta control. Considering this, this work aimed to verify the in vitro antifungal activity of aqueous and alcoholic solutions of Adiantum latifolium leaves on C. cacaofunesta. Plant material was collected at Atlantic Forest biome in cacao cultivation area in South of Bahia state. Aqueous and ethanolic solutions were made by boiling and maceration in 70% ethanol, respectively. After filtration, they were added to culture medium at 1, 5 and 10% dilution. A 7 mm disc colony of C. cacaofunesta was inoculated in the middle of the well containing Sabouraud dextrose agar (SDA) and the mycelial growth was observed. Controls consisted on SDA with sterile water or 70% ethanol at the same dilution of treatments, and Tebuconazole at 4 μg.mL-1. Neither aqueous nor ethanolic solutions inhibited the mycelial growth. However, aqueous solution presence induced a higher mycelial growth rate. Conversely, aqueous solution treatment induced mycelial growth. Tebuconazole showed important mycelial growth inhibition and it could be considered in C. cacaofunesta propagation control in areas where genetic selection or handling management still fail.

KEYWORDS
maidenhair fern; Cocoa; mold; Atlantic Forest

RESUMO

A espécie Ceratocystis cacaofunesta é o agente etiológico do mal-do-facão, patogenia caracterizada por danos irreversíveis no sistema vascular da planta. O controle da doença é difícil e a busca por soluções alternativas e econômicas é necessária. Sabe-se que os compostos das plantas medicinais possuem atividade microbiana e podem ser uma opção alternativa no controle de C. cacaofunesta. Baseado nisso, esse trabalho se propôs a verificar in vitro o potencial antifúngico das soluções aquosa e alcóolica de Adiantum latifolium sobre C. cacaofunesta. O material vegetal foi coletado no bioma Mata Atlântica em área de plantio de cacau, no sul da Bahia. Solução aquosa foi obtida por decocção e solução etanólica por maceração em etanol 70%. As soluções foram filtradas e adicionadas ao meio de cultura em diluições de 1, 5 e 10%. Inocularam-se fragmentos de 7 mm de colônia de C. cacaofunesta no centro do meio de cultura contendo ágar Sabouraud dextrose (ASD) e se observou o crescimento do disco micelial. Os controles consistiram em SDA com água estéril ou etanol a 70% na mesma diluição de tratamentos e o antifúngico Tebuconazol a 4 μg.mL-1. Nenhuma concentração das soluções aquosa e alcóolica inibiu o crescimento micelial. Entretanto, a presença de solução aquosa induziu maior crescimento micelial. O antifúngico Tebuconazol apresentou efeito redutor importante do crescimento micelial e pode ser uma alternativa no controle da propagação do C. cacaofunesta em locais onde a seleção genética e o manejo adequado de instrumentos no momento da poda apresentam falhas.

PALAVRAS-CHAVE
avenca; cacaueiro; mal-do-facão; Mata Atlântica

Ceratocystis wilt is a fungal disease characterized by wilting and death of cacao (Theobroma cacao L.) (OLIVEIRA; LUZ, 2005OLIVEIRA, M.L.; LUZ, E.D.M.N. (Eds.). Murcha-de-Ceratocystis. In: OLIVEIRA, M.L.; LUZ, E.D.M.N. Identificação e manejo das principais doenças do cacaueiro no Brasil. 1. ed. Ilhéus, Bahia: CEPLAC/ CEPEC/SEFIT, 2005. p.55-63.). Along with witches’ broom (Moniliophthora (syn. Crinipellis) perniciosa) and frosty pod rot (Moniliophthora rorert) constitutes the main important agent of production losses in North-eastern Brazilian cacao crops (OLIVEIRA; LUZ, 2005OLIVEIRA, M.L.; LUZ, E.D.M.N. (Eds.). Murcha-de-Ceratocystis. In: OLIVEIRA, M.L.; LUZ, E.D.M.N. Identificação e manejo das principais doenças do cacaueiro no Brasil. 1. ed. Ilhéus, Bahia: CEPLAC/ CEPEC/SEFIT, 2005. p.55-63.; ENGELBRECHT et al., 2007ENGELBRECHT, C.J.B.; HARRINGTON, T.C.; ALFENAS, A.C.; SUAREZ, C. Genetic variation in populations of the cacao wilt pathogen, Ceratocystis cacaofunesta. Plant Pathology, v.56, n.6, p.923-933, 2007. https://doi.org/10.1111/j.1365-3059.2007.01735.x
https://doi.org/10.1111/j.1365-3059.2007...
).

The etiologic agent in Brazilian crops is Ceratocystis cacaofunesta Engelbr. & T.C. Harr. (BASTOS; EVANS, 1978BASTOS, C.N.; EVANS, H.C. Ocorrência de Ceratocystis fimbriata Ell&Halst. na Amazônia Brasileira. Acta Amazonica, v.8, n.4, p.543-544, 1978. http://dx.doi.org/10.1590/1809-43921978084543
http://dx.doi.org/10.1590/1809-439219780...
; BAKER et al., 2003BAKER, C.J.; HARRINGTON, T.C.; KRAUSS, U.; ALFENAS, A.C. Genetic variability and host specialization in the Latin American clade of Ceratocystis fimbriata. Phytopathology, v. 93, n.10, p.1274-1284, 2003. https://doi.org/10.1094/PHYTO.2003.93.10.1274
https://doi.org/10.1094/PHYTO.2003.93.10...
; ALMEIDA et al., 2005ALMEIDA, L.C.C.; COSTA, A.Z.M.; LOPES, J.R.M.; BEZERRA, J.L. Distribuição geográfica da murcha-de-Ceratocystis do cacaueiro na Bahia, Brasil. Agrotrópica, Ilhéus, v.17, p.83-86, 2005.; ENGELBRECHT; HARRINGTON, 2005ENGELBRECHT, C.J.B.; HARRINGTON, T.C. Intersterility, morphology, and taxonomy of Ceratocystis fimbriata on sweet potato, cacao, and sycamore. Mycologia, v.97, n.1, p.57-69, 2005. https://doi.org/10.3852/mycologia.97.1.57
https://doi.org/10.3852/mycologia.97.1.5...
) a species belonging to Ceratocystis fimbriata complex (ENGELBRECHT et al., 2007ENGELBRECHT, C.J.B.; HARRINGTON, T.C.; ALFENAS, A.C.; SUAREZ, C. Genetic variation in populations of the cacao wilt pathogen, Ceratocystis cacaofunesta. Plant Pathology, v.56, n.6, p.923-933, 2007. https://doi.org/10.1111/j.1365-3059.2007.01735.x
https://doi.org/10.1111/j.1365-3059.2007...
; FERREIRA et al., 2010FERREIRA, M.; HARRINGTON, T.J.; THORPE, D.; ALFENAS, A. Genetic diversity and interfertility among highly differentiated populations of Ceratocystis fimbriata in Brazil. Plant Pathology, v.59, n.4, p.721-735, 2010. https://doi.org/10.1111/j.1365-3059.2010.02275.x
https://doi.org/10.1111/j.1365-3059.2010...
; CAB INTERNATIONAL, 2019CAB INTERNATIONAL. Ceratocystis fimbriata (Ceratocystis blight). Invasive Species Compendium. Wallingford, UK: CAB International, 2019.).

Fungicides, hygienic techniques (OLIVEIRA; LUZ, 2005OLIVEIRA, M.L.; LUZ, E.D.M.N. (Eds.). Murcha-de-Ceratocystis. In: OLIVEIRA, M.L.; LUZ, E.D.M.N. Identificação e manejo das principais doenças do cacaueiro no Brasil. 1. ed. Ilhéus, Bahia: CEPLAC/ CEPEC/SEFIT, 2005. p.55-63.) and genetic resistance selection of cacao trees (SILVA et al., 2012SILVA, S.D.V.M.; PINTO, L.R.M.; OLIVEIRA, B.F.; DAMACENO, V.O.; PIRES, J.L.; DIAS, C.T.S. Resistência de progênies de cacaueiro à murcha-de-Ceratocystis. Tropical Plant Pathology, v.37, n.3, p.191-195, 2012. http://dx.doi.org/10.1590/S1982-56762012000300005
http://dx.doi.org/10.1590/S1982-56762012...
) have been considered in Ceratocystis wilt management; however, the short period between appearance of the disease and plant death turns this disease control difficult (SILVA et al., 2012SILVA, S.D.V.M.; PINTO, L.R.M.; OLIVEIRA, B.F.; DAMACENO, V.O.; PIRES, J.L.; DIAS, C.T.S. Resistência de progênies de cacaueiro à murcha-de-Ceratocystis. Tropical Plant Pathology, v.37, n.3, p.191-195, 2012. http://dx.doi.org/10.1590/S1982-56762012000300005
http://dx.doi.org/10.1590/S1982-56762012...
) and research in this area are still needed.

Fungicides have been used to avoid dispersion of Ceratocystis agent and substances reported to have effect on species of this genus are Benzimidazole class such as Carbendazim, Methyl Thiophanate, Benomyl (PEREIRA; SANTOS, 1986PEREIRA, J.C.R.; SANTOS, A.F. Avaliação de fungicidas e técnicas de aplicação no controle de Ceratocystisfimbriata, em seringueira. Fitopatologia Brasileira, v.11, n.4, p.811-816, 1986.) and Triazoles such as Tebuconazole (TOCHETTO et al., 2017TOCHETTO, N.; FORTUNA, D.; VALDEBENITO SANHUEZA, R.M. Chemical control of Ceratocystis fimbriata the causal agent of kiwi treewil tunder controlled conditions. CONGRESSO PAULISTA DE FITOPATOLOGIA, 40., Campinas. Proceedings... Campinas, 2017. Available from: http://www.summanet.com.br/summanet-site/congressos/2017/Resumos/Resumo40CPFito_141.pdf. Access on: Aug. 25 2019.
http://www.summanet.com.br/summanet-site...
). Nevertheless, resistance to these drugs (NISHIJIMA; SMALLEY, 1979NISHIJIMA, W.T.; SMALLEY, E.B. Ceratocystis ulmi tolerance to methyl-2-benzimidazole carbamate and other related fungicides. Phytopathology, v.69, n.1, p.69-73, 1979. http://dx.doi.org/10.1094/Phyto-69-69
http://dx.doi.org/10.1094/Phyto-69-69...
) has already been reported. Searching for new possibilities to handle with Ceratocystis, medicinal plant metabolites have been considered as excellent options due to easy access, low cost and less or no toxicity to the environment (STANGARLIN et al., 1999STANGARLIN, J.R.; SCHWAN-ESTRADA, K.R.F.; CRUZ, M.E.S.; NOZAKI, M.H. Plantas medicinais e controle alternativo de fitopatógenos. Biotecnologia, Ciência e Desenvolvimento, Brasília, v.11, p.16-21, 1999.; FIORI et al., 2000FIORI, A.C.G.; SCHWAN-ESTRADA, K.R.F.; STANGARLIN, J.R.; VIDA, J.B.; SCAPIM, C.A.; CRUZ, M.E.S.; PASCHOLATI, S.F. Antifungal activity of leaf extracts and essential oils of some medicinal plants against Didymellabryoniae. Journal of Phytopathology, v.148, n.7-8, p.483-487, 2000. https://doi.org/10.1046/j.1439-0434.2000.00524.x
https://doi.org/10.1046/j.1439-0434.2000...
; VENTUROSO et al., 2011VENTUROSO, L.R.; BACCHI, L.M.A.; GAVASSONI, W.L. Atividade antifúngica de extratos vegetais sobre o desenvolvimento de fitopatógenos. Summa Phytopathologica, v.37, n.1, p.18-23, 2011. http://dx.doi.org/10.1590/S0100-54052011000100003
http://dx.doi.org/10.1590/S0100-54052011...
). In this context, ferns have been considered useful medicinal plants (PAN et al., 2011PAN, C.; CHEN, Y.G.; MA X.Y.; JIANG, J.H.; HE, F.; ZHAN, Y. Phytochemical Constituents and Pharmacological Activities of Plants from the Genus Adiantum: A Review. Tropical Journal of Pharmaceutical Research, v.10, n.5, p.681-692, 2011. http://dx.doi.org/10.4314/tjpr.v10i5.18
http://dx.doi.org/10.4314/tjpr.v10i5.18...
; CAO et al., 2017CAO, H.; CHAI, T.T.; WANG, X.; MORAIS-BRAGA, M.F.B.; YANG, J.H.; WONG, F.C.; WANG, R.; YAO, H.; CAO, J.; CORNARA, L.; BURLANDO, B.; WANG, Y.; XIAO, J.; COUTINHO, H.D.M. Phytochemicals from fern species: potential for medicine applications. Phytochemistry Reviews, v.16, n.3, p.379-440, 2017. http://dx.doi.org/10.1007/s11101-016-9488-7
http://dx.doi.org/10.1007/s11101-016-948...
). Specially, the Adiantum genus has been traditionally used in Brazil to treat respiratory diseases (HARAGUCHI; CARVALHO, 2010HARAGUCHI, L.M.M.; CARVALHO, O.B. (Eds.). Plantas Medicinais: do curso de plantas medicinais. São Paulo: Secretaria Municipal do Verde e do Meio Ambiente, Divisão Técnica Escola Municipal de Jardinagem, 2010. 248p.) being the hypoglycemic and anti-inflammatory (IBRAHEIM et al., 2011IBRAHEIM, Z.Z.; AHMED, S.A.; GOUDA, G.Y. Phytochemical and biological studies of Adiantumcapillus-veneris. Saudi Pharmaceutical Journal, v.19, n.2, p.65-74, 2011. http://dx.doi.org/10.1016/j.jsps.2011.01.007
http://dx.doi.org/10.1016/j.jsps.2011.01...
) effects of A. latifollium proved in the literature. In addition, species of the same genus, the A. capillus-veneris, has been indicated as alternative treatment in the control of phytopathogens with promising results (FORMIGHIERI et al., 2010FORMIGHIERI, A.P.; STANGARLIN, J.R.; MEINERZ, C.C.; FRANZENER, G.; SCHWAN-ESTRADA, K.R.F. Avaliação do potencial da planta Adiantumcapillus-veneris(l.) no controle de fitopatógenos. Arquivos do Instituto Biológico, São Paulo, v.77, n.3, p.487-496, 2010.). Therefore, in this study, we verified the in vitro antifungal potential of Adiantum latifolium on C. cacaofunesta mycelial growth.

Leaves of A. latifolium were obtained from a cocoa-cabruca or cabruca agroforestry system (AGUIAR et al., 2003AGUIAR, A.P.; CHIARELLO, A.G.; MENDES, S.L.; MATOS, E.N. The Central and Serra do Mar Corridors in the Brazilian Atlantic Forest. In: GALINDO-LEAL, C.; CÂMARA, I.G. The Atlantic Forest of South America: biodiversity status, threats, and outlook. Washington: Conservation International, 2003. p.118-132.) at: -14.7889003753662 long: -39.0494003295898, botany identified and registered under voucher number HUESC12.156. After dryness (60°C for 72 hours), leaves were powdered to produce aqueous and ethanolic solutions. For aqueous solution, 26 g of vegetal powder were boiled in 100 mL of distilled water for 3 minutes. The decoction was filtered in Whatman number 2 filter followed by filtration on 0,20 μm diameter Sartorius membrane. For ethanolic solution, 26 g of powdered vegetal were imbibed in 100 mL of 70% ethanol protected from light for 72 hours. The ethanolic solution was also filtered and stored in aliquots until use.

C. cacaofunesta was cultivated in Sabouraud dextrose agar (SDA) (130 g/L) at 25 to 30°C and protected from light until total growth to obtain inoculum. The in vitro antifungal test was performed in 6 or 24 well plates which gives a growth area of 9.60 (for tests) and 1.93 (for controls) cm2 respectively. The A. latifolium aqueous and ethanolic solutions were incorporated in the SDA at 1, 5 and 10% proportion. Controls consisted on SDA, SDA with 70% ethanol at the same proportion of ethanolic solution (PEtOH) and ADS with 4 μg.mL-1 of Tebuconazole (Folicur 200 ec, Bayer). Each well received 7 mm discs obtained from the border of fungus colony displaced in the middle of the well. Plates stayed at 25 to 30°C and protected from light until total mycelial growth (wall of the well limit) of control (100% mycelial growth).

The antifungal test did not show inhibition of C. cacaofunesta mycelial growth by A. latifolium leaves aqueous or ethanolic solutions. Conversely, the mycelial growth of C. cacaofunesta tended to be stimulated by the aqueous solution when compared to control (Fig. 1 and Table 1). The same effect was observed by AMARAL et al. (2005)AMARAL, M.F.Z.J.; BARA, M.T.F. Avaliação da atividade antifúngica de extratos de plantas sobre o crescimento de fitopatógenos. Revista Eletrônica de Farmácia, Goiás, Suplemento, v.2, n.2, p.5-8, 2005. for Albizzia lebbeck Benth extract on Fusarium solani and Sclerotium rolfsii and VENTUROSO et al. (2011)VENTUROSO, L.R.; BACCHI, L.M.A.; GAVASSONI, W.L. Atividade antifúngica de extratos vegetais sobre o desenvolvimento de fitopatógenos. Summa Phytopathologica, v.37, n.1, p.18-23, 2011. http://dx.doi.org/10.1590/S0100-54052011000100003
http://dx.doi.org/10.1590/S0100-54052011...
testing Azadirachta indica A. Juss extract on F. solani.

Figure 1.
C. cacaofunesta mycelial growth in Sabouraud dextrose agar (SDA) supplemented with aqueous or ethanolic solutions of A. latifolium leaves. (A) Mycelial growth in Petri dishes: A — SDA + 10% ethanolic solution; B — SDA + 5% ethanolic solution; C — SDA + 1% ethanolic solution; D — SDA + 10% aqueous solution without inoculum; E — SDA + 10% aqueous solution without inoculum; F — SDA without supplementation; G — SDA + Tebuconazole at 4 μg.mL-1. (B) Mycelial growth percentage: pEtOH – pure ethanolic solution; EtOH – A. latifolium ethanolic solution; H2O – A. latifolium aqueous solution.
Table 1.
Ceratocystis cacaofunesta mycelial growth evaluation in Sabouraud dextrose agar supplemented with A. latifolium leaves aqueous and ethanolic solutions.

It is worth noting that the fungicide Tebuconazole (Folicur 200 EC) used in this study showed high inhibition on C. cacaofunesta. This fungicide is recommended for the control of Fusarium subglutinans in pineapple crops, Colletotrichum gossypii var. cephalosporioides of cotton and Alternaria porri in garlic plantation, but not for C. cacaofunesta control. Therefore, following the in vitro tests this fungicide may be an alternative to control C. cacaofunesta propagation in areas where cacao genetic selection or handling management still fail.

ACKNOWLEDGEMENTS

We are grateful to Ms. Dilze Maria Argolo Magalhães, from the Executive Committee for Cacao Plantation - CEPLAC / CEPEC collection, for kindly providing the Ceratocystis cacaofunesta strain “CC20” for in vitro testing.

REFERENCES

  • AGUIAR, A.P.; CHIARELLO, A.G.; MENDES, S.L.; MATOS, E.N. The Central and Serra do Mar Corridors in the Brazilian Atlantic Forest. In: GALINDO-LEAL, C.; CÂMARA, I.G. The Atlantic Forest of South America: biodiversity status, threats, and outlook. Washington: Conservation International, 2003. p.118-132.
  • ALMEIDA, L.C.C.; COSTA, A.Z.M.; LOPES, J.R.M.; BEZERRA, J.L. Distribuição geográfica da murcha-de-Ceratocystis do cacaueiro na Bahia, Brasil. Agrotrópica, Ilhéus, v.17, p.83-86, 2005.
  • AMARAL, M.F.Z.J.; BARA, M.T.F. Avaliação da atividade antifúngica de extratos de plantas sobre o crescimento de fitopatógenos. Revista Eletrônica de Farmácia, Goiás, Suplemento, v.2, n.2, p.5-8, 2005.
  • BAKER, C.J.; HARRINGTON, T.C.; KRAUSS, U.; ALFENAS, A.C. Genetic variability and host specialization in the Latin American clade of Ceratocystis fimbriata Phytopathology, v. 93, n.10, p.1274-1284, 2003. https://doi.org/10.1094/PHYTO.2003.93.10.1274
    » https://doi.org/10.1094/PHYTO.2003.93.10.1274
  • BASTOS, C.N.; EVANS, H.C. Ocorrência de Ceratocystis fimbriata Ell&Halst. na Amazônia Brasileira. Acta Amazonica, v.8, n.4, p.543-544, 1978. http://dx.doi.org/10.1590/1809-43921978084543
    » http://dx.doi.org/10.1590/1809-43921978084543
  • CAB INTERNATIONAL. Ceratocystis fimbriata (Ceratocystis blight) Invasive Species Compendium. Wallingford, UK: CAB International, 2019.
  • CAO, H.; CHAI, T.T.; WANG, X.; MORAIS-BRAGA, M.F.B.; YANG, J.H.; WONG, F.C.; WANG, R.; YAO, H.; CAO, J.; CORNARA, L.; BURLANDO, B.; WANG, Y.; XIAO, J.; COUTINHO, H.D.M. Phytochemicals from fern species: potential for medicine applications. Phytochemistry Reviews, v.16, n.3, p.379-440, 2017. http://dx.doi.org/10.1007/s11101-016-9488-7
    » http://dx.doi.org/10.1007/s11101-016-9488-7
  • ENGELBRECHT, C.J.B.; HARRINGTON, T.C. Intersterility, morphology, and taxonomy of Ceratocystis fimbriata on sweet potato, cacao, and sycamore. Mycologia, v.97, n.1, p.57-69, 2005. https://doi.org/10.3852/mycologia.97.1.57
    » https://doi.org/10.3852/mycologia.97.1.57
  • ENGELBRECHT, C.J.B.; HARRINGTON, T.C.; ALFENAS, A.C.; SUAREZ, C. Genetic variation in populations of the cacao wilt pathogen, Ceratocystis cacaofunesta Plant Pathology, v.56, n.6, p.923-933, 2007. https://doi.org/10.1111/j.1365-3059.2007.01735.x
    » https://doi.org/10.1111/j.1365-3059.2007.01735.x
  • FERREIRA, M.; HARRINGTON, T.J.; THORPE, D.; ALFENAS, A. Genetic diversity and interfertility among highly differentiated populations of Ceratocystis fimbriata in Brazil. Plant Pathology, v.59, n.4, p.721-735, 2010. https://doi.org/10.1111/j.1365-3059.2010.02275.x
    » https://doi.org/10.1111/j.1365-3059.2010.02275.x
  • FIORI, A.C.G.; SCHWAN-ESTRADA, K.R.F.; STANGARLIN, J.R.; VIDA, J.B.; SCAPIM, C.A.; CRUZ, M.E.S.; PASCHOLATI, S.F. Antifungal activity of leaf extracts and essential oils of some medicinal plants against Didymellabryoniae. Journal of Phytopathology, v.148, n.7-8, p.483-487, 2000. https://doi.org/10.1046/j.1439-0434.2000.00524.x
    » https://doi.org/10.1046/j.1439-0434.2000.00524.x
  • FORMIGHIERI, A.P.; STANGARLIN, J.R.; MEINERZ, C.C.; FRANZENER, G.; SCHWAN-ESTRADA, K.R.F. Avaliação do potencial da planta Adiantumcapillus-veneris(l.) no controle de fitopatógenos. Arquivos do Instituto Biológico, São Paulo, v.77, n.3, p.487-496, 2010.
  • HARAGUCHI, L.M.M.; CARVALHO, O.B. (Eds.). Plantas Medicinais: do curso de plantas medicinais. São Paulo: Secretaria Municipal do Verde e do Meio Ambiente, Divisão Técnica Escola Municipal de Jardinagem, 2010. 248p.
  • IBRAHEIM, Z.Z.; AHMED, S.A.; GOUDA, G.Y. Phytochemical and biological studies of Adiantumcapillus-veneris. Saudi Pharmaceutical Journal, v.19, n.2, p.65-74, 2011. http://dx.doi.org/10.1016/j.jsps.2011.01.007
    » http://dx.doi.org/10.1016/j.jsps.2011.01.007
  • NISHIJIMA, W.T.; SMALLEY, E.B. Ceratocystis ulmi tolerance to methyl-2-benzimidazole carbamate and other related fungicides. Phytopathology, v.69, n.1, p.69-73, 1979. http://dx.doi.org/10.1094/Phyto-69-69
    » http://dx.doi.org/10.1094/Phyto-69-69
  • OLIVEIRA, M.L.; LUZ, E.D.M.N. (Eds.). Murcha-de-Ceratocystis. In: OLIVEIRA, M.L.; LUZ, E.D.M.N. Identificação e manejo das principais doenças do cacaueiro no Brasil. 1. ed. Ilhéus, Bahia: CEPLAC/ CEPEC/SEFIT, 2005. p.55-63.
  • PAN, C.; CHEN, Y.G.; MA X.Y.; JIANG, J.H.; HE, F.; ZHAN, Y. Phytochemical Constituents and Pharmacological Activities of Plants from the Genus Adiantum: A Review. Tropical Journal of Pharmaceutical Research, v.10, n.5, p.681-692, 2011. http://dx.doi.org/10.4314/tjpr.v10i5.18
    » http://dx.doi.org/10.4314/tjpr.v10i5.18
  • PEREIRA, J.C.R.; SANTOS, A.F. Avaliação de fungicidas e técnicas de aplicação no controle de Ceratocystisfimbriata, em seringueira. Fitopatologia Brasileira, v.11, n.4, p.811-816, 1986.
  • SILVA, S.D.V.M.; PINTO, L.R.M.; OLIVEIRA, B.F.; DAMACENO, V.O.; PIRES, J.L.; DIAS, C.T.S. Resistência de progênies de cacaueiro à murcha-de-Ceratocystis. Tropical Plant Pathology, v.37, n.3, p.191-195, 2012. http://dx.doi.org/10.1590/S1982-56762012000300005
    » http://dx.doi.org/10.1590/S1982-56762012000300005
  • STANGARLIN, J.R.; SCHWAN-ESTRADA, K.R.F.; CRUZ, M.E.S.; NOZAKI, M.H. Plantas medicinais e controle alternativo de fitopatógenos. Biotecnologia, Ciência e Desenvolvimento, Brasília, v.11, p.16-21, 1999.
  • TOCHETTO, N.; FORTUNA, D.; VALDEBENITO SANHUEZA, R.M. Chemical control of Ceratocystis fimbriata the causal agent of kiwi treewil tunder controlled conditions. CONGRESSO PAULISTA DE FITOPATOLOGIA, 40., Campinas. Proceedings... Campinas, 2017. Available from: http://www.summanet.com.br/summanet-site/congressos/2017/Resumos/Resumo40CPFito_141.pdf Access on: Aug. 25 2019.
    » http://www.summanet.com.br/summanet-site/congressos/2017/Resumos/Resumo40CPFito_141.pdf
  • VENTUROSO, L.R.; BACCHI, L.M.A.; GAVASSONI, W.L. Atividade antifúngica de extratos vegetais sobre o desenvolvimento de fitopatógenos. Summa Phytopathologica, v.37, n.1, p.18-23, 2011. http://dx.doi.org/10.1590/S0100-54052011000100003
    » http://dx.doi.org/10.1590/S0100-54052011000100003

Publication Dates

  • Publication in this collection
    2 Dec 2019
  • Date of issue
    2019

History

  • Received
    23 Feb 2019
  • Accepted
    06 Sept 2019
Instituto Biológico Av. Conselheiro Rodrigues Alves, 1252 - Vila Mariana - São Paulo - SP, 04014-002 - São Paulo - SP - Brazil
E-mail: arquivos@biologico.sp.gov.br