BIOACEITES ESENCIALES INHIBEN A Moniliophthora roreri (Cif. Y Par.) Evans et al., CAUSANTE DE LA MONILIASIS EN EL CULTIVO DEL CACAO

Autores/as

  • Ariste Gómez-López Universidad Autónoma Chapingo
  • Luciano Martínez-Bolaños
  • Gonzalo Ortiz-Gil Universidad Autónoma Chapingo
  • Misael Martínez-Bolaños Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias
  • Carlos H. Avendaño-Arrazate Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias
  • Eleodoro Hernández-Meneses Colegio de Postgraduados

Palabras clave:

Aceites esenciales, antifúngico, podredumbre de vaina helada, Thobroma cacao, agricultura sostenible

Resumen

La moniliasis causada por el hongo, Moniliophthora roreri, es una de las enfermedades más destructiva del cacao en México y Latinoamérica. El patógeno afecta al fruto en sus diferentes etapas de desarrollo causando pérdidas drásticas en la producción. En el presente estudio se evalúo el efecto antifúngico de aceites esenciales derivado de plantas contra el crecimiento de M. roreri, en medio de cultivo PDA. El aceite esencial de Origanum vulgare, Schinus molle, Syzygium aromaticum, Thymus vulgaris, Pimenta dioica y Cinnamomum zeylanicum, inhibieron el crecimiento total de M. roreri a 500 µl L-1. T. vulgaris causó el mayor porcentaje de inhibición del hongo con valores CMI50 67.65 µL L-1 y CMI95 107.6 µL L-1. Los resultados del estudio aportan conocimiento básico sobre el  uso de fitoquímicos y desarrollo de compuestos para el manejo integral sustentable de la moniliasis.

Citas

Ali SS, Melnick RL, Crozier J, Phillips-Mora W, Strem MD, Shao J, Zhang D, Sicher R, Meinhardt L, Bailey BA. 2014. Successful pod infections by Moniliophthora roreri result in differential Theobroma cacao gene expression depending on the clone’s level of tolerance. Molecular

Plant Pathology 15: 698-710. https://doi.org/10.1111/mpp.12126

Asbahani AE, Miladi K, Badri W, Sala M, Addi EHA, Casabianca H, Mousadik AE, Hartmann D, Jilale A, Renaud FNR, Elaissari A. 2015. Essential oils: from extraction to encapsulation. International Journal of Pharmaceutics 483: 220-243. https://doi.org/10.1016/j.ijpharm.2014.12.069

Avendaño-Arrazate CH, Guillén-Díaz S, Hernández-Gómez E. 2018. “Regalo de Dios”: clon de cacao (Theobroma cacao L.) tolerante a Moniliophthora roreri Cif & Par, para la renovación de las zonas cacaoteras de México. Revista Agroproductividad 11: 173-176.

Avendaño-Arrazate CH, Hernández-Gómez E, Solís-Bonilla JL, Cueto-Moreno J, Zamarripa-Colmenero A. 2019. “CAERI 1” y “CAERI 2”, Nuevos clones de cacao (Theobroma cacao L.). Revista Agroproductividad 12: 73-77. https://doi.org/10.32854/agrop.v0i0.1392

Bailey BA, Crozier J, Sicher RC, Strem MD, Melnick RL, Carazzolle MF, Costa GG, Pereira GA, Zhang D, Maximova S. 2013. Dynamic changes in pod and fungal physiology associated with the shift from biotrophy to necrotrophy during the infection of Theobroma cacao by Moniliophthora roreri. Physiological Molecular Plant Pathology 81: 84-96. https://doi.org10.1016/j.pmpp.2012.11.005

Bailey BA, Melnick RL, Strem MD, Crozier J, Shao J, Sicher R, Phillips MW, Ali SS, Zhang D, Meinhard L. 2014. Differential gene expression by Moniliophthora roreri while overcoming cacao tolerance in the field. Molecular Plant Pathology 15: 711-729. https://doi.org/10.1111/mpp.12134

Bailey BA, Evans HC, Phillips MW, Ali SS, Meinhard LW. 2018. Moniliophthora roreri, causal agent of cacao frosty pod rot. Molecular Plant Pathology 19: 1580-1594. https://doi.org/10.1111/mpp.12648

Bateman RP, Hidalgo E, García J, Arroyo C, Hoopen GM, Adonijah V, Krauss U. 2005. Application of chemical and biological agents for the management of frosty pod rot (Moniliophthora roreri) in Costa Rican cocoa (Theobroma cacao). Annals of Applied Biology 147: 129-138. https://doi.org/10.1111/j.1744-7348.2005.00012.x

Bieng MAN, Alem L, Curtet C, Tixier P. 2017. Tree spacing impacts the individual incidence of Moniliophthora roreri disease in cacao agroforests. Pest Management Science 73: 2386-2392. https://doi.org/10.1002/ps.4635

Calo JR, Crandall PG, O’Bryan CA, Ricke SC. 2015. Essential oils as antimicrobials in food systems–A review. Food Control 54: 111-119. http://doi.org/10.1016/j.foodcont.2014.12.040

Campo JA, Vanega P. 2012. Evaluación de aceites esenciales de tomillo (Thymus vulgaris) y orégano (Origanum vulgare) como microbicidas y conservantes en mazorcas tiernas de maíz (Zea mays L.). Acta Agronómica 61: 43- 44.

Carson CF, Hammer KA, Riley TV. 2006. Melaleuca alternifolia (tea tree) oil: a review of antimicrobial and other medicinal properties. Clinical Microbiology Reviews 19: 50-62. https://doi.org/10.1128/CMR.19.1.50-62.2006

Cháves LC, Matin SAM, Fuentes ZE, Viuda MM, Fernández LJ, Sendra E, Sayas E, Pérez AJA. 2012. Role of oregano (Origanum vulgare) essential oil as a surface fungus inhibitor on fermented sausages: Evaluation of its effect on microbial and physicochemical characteristics. Journal of Food Protection 75: 104-111. https://doi.org/10.4315/0362-028X.JFP-11-184

Chávez MME, González ERR, Ramos GA, Plascencia JM, Gutierrez MP. 2018a. Effect of pepper tree (Schinus molle) essential oil-loaded chitosan bio-nanocomposites on postharvest control of Colletotrichum gloesosporioides and quality in avocado (Persea americana) cv. Hass. Food Science Biotechnology 27: 1871-1875. https://doi.org/10.1007/s10068-018-0410-5

Chávez MME, Luque AA, Gutiérrez MP, Cortez RM, Burgos HA, Lizardi MJ, Plascencia JM. 2018b. Effect of chitosan-pepper tree (Schinus molle) essential oil biocomposites on the growth kinetics, viability and membrane integrity of Colletotrichum gloesporioides. Revista Mexicana de Ingeniería Química 17: 29-45.

Cubillos G. 2017. Frosty Pod Rot, disease that affect the cocoa (Theobroma cacao) crops in Colombia. Crop Protection 96: 77-82. https://doi.org/10.1016/j.cropro.2017.01.011

Daferera DJ, Ziogas BN, Polission MG. 2003. The effectiveness of plant essential oils on the growth of Botrytis cinerea, Fusarium sp. and Clavibacter michiganensis subsp. michiganensis. Crop Protection 22: 39-44. https://doi.org/10.1016/S0261-2194(02)00095-9

De Billerbeck VG, Roques CG, Bessiere JM, Fonvieille JL, Dargent R. 2001. Effects of Cymbopogon nardus (L.) W. Watson essential oil on the growth and morphogenesis of Aspergillus niger. Canadian Journal Microbiology 47: 9-17. https://doi.org/10.1139/w00-117

Evans HC. 2007. Cacao diseases-The trilogy revised. Phytopathology 97: 1640-1643. https://doi.org/10.1094/phyto.97.12.1640

Evans HC, Stalpers JA, Samson RA, Benny GL. 1978. On the taxonomy of Monilia roreri, an important pathogen of Theobroma cacao in South America. Canadian Journal of Botany 56: 2528-2532. https://doi.org/10.1139/b78-305

[FAO] Food and Agriculture Organization. [internet]. 2019. Datos sobre alimentación y agricultura. [cited 2020 Jul 21]. Disponible en: http://www.fao.org/faostat/

Ghfir B, Fonvieille JL, Dargent R. 1997. Influence of essential oil of Hyssopus officinalis on the chemical composition of the walls of Aspergillus fumigatus (Fresenius). Mycopathologia 138: 7-12. https://doi.org/10.1023/A:1006876018261

Hasheminejad N, Khodaiyan F, Safari M. 2019. Improving the antifungal activity of clove essential oil encapsulated chitosan nanoparticles. Food Chemistry 275: 113-122. http://doi.org/10.1016/j.foodchem.2018.09.085

Isman BM. 2000. Plant essential oils for pest and disease management. Crop Protection 19: 603-608. https://doi.org/10.1016/S0261-2194(00)00079-X

Jahani M, Pira M, Aminifard MH. 2020. Antifungal effects of essential oils against Aspergillus niger in vitro and in vivo on pomegranate (Punica granatum) fruits. Scientia Horticulturae 264: 109188. http://doi.org/10.1016/j.scientia.2020.109188

Kamsu NP, Tchinda SE, Tchamenj NS, Jazet DPM, Madjouko MA, Youassi OY, Sameza ML, Tchoumbougnang F, Menut C. 2019. Antifungal activities of essential oils of cinnamon (Cinnamomum zeylanicum) and lemongrass (Cymbopogon citratus) on crown rot pathogens of banana. Indian Phytopathology 72: 131-137. http://doi.org/10.1007/s42360-018-0104-1

Kieck JS, Zug KLM, Yupanqui HAH, Gómez R, Cierjacks A. 2016. Plant diversity effects on crop yield, pathogen incidence, and secondary metabolism on cacao farms in Peruvian Amazonia. Agriculture, Ecosystems & Environment 222: 223-234. http://doi.org/10.1016/j.agee.2016.02.006

Knobloch K, Pauli A, Iberl B, Weis N, Weigand H. 1989. Antibacterial activity and antifungal properties of essential oil components. Journal Essential Oil Research 1: 119-128. https://doi.org/10.1080/10412905.1989. 9697767

Leandro-Muñoz ME, Tixier P, Germon A, Rakotobe V, Phillips MW, Maximova S, Avelino J. 2017. Effects of microclimatic variables on the symptoms and signs onset of Moniliophthora roreri, causal agent of Moniliophthora pod rot in cacao. PLoS ONE 12: e0184638. https://doi.org/10.1371/journal.pone.0184638

López MAK, Plascencia JM, Lizardi MJ, Rosas BEC, Luque AAG, Cortez RMO. 2015. Antifungal and antimycotoxigenic activity of essential oils from Eucalyptus globules, Thymus capitatus and Schinus molle. Food Science and Technology 35: 664-671. https://doi.org/10.1590/1678-457X.6732

Lozada BS, Herrera LV, Perea JA, Stashenko E, Escobar P. 2012. Efecto in vitro de aceites esenciales de tres especies de Lippia sobre Moniliophthora roreri (Cif. y Par.) Evans et al., agente causante de la moniliasis del cacao (Theobroma cacao L.). Acta Agronómica 61: 102-110.

Maridueña-Zavala MG, Freire PA, Espinoza LRF, Villavicencio VM, Jimenez FM, Cevallos CJM. 2019. Genetic characterization of Moniliophthora perniciosa from Ecuador and in vitro sensitivity to compost tea. European Journal of Plant Pathology 154: 943-959. https://doi.org/10.1007/s10658-019-01714-1

Melnick RL, Strem MD, Crozier J, Sicher RC, Bailey BA. 2013. Molecular and metabolic changes of cherelle wilt of cacao and its effect on Moniliophthora roreri. Physiological and Molecular Plant Pathology 84: 153-162. https://doi.org/10.1016/i.pmpp.2013.09.004

Nazzarro F, Fratianni F, Coppola R, De Feo V. 2017. Essential oils and antifungal activity. Pharmaceuticals 10: 1-20. https://doi.org/10.3390/ph10040086

Oliva MM, Carezzano ME, Giuliano M, Daghero J, Zygadlo J, Bogino P, Giordano W, Demo M. 2015. Antimicrobial activity of essential oils of Thymus vulgaris and Origanum vulgare on phytopathogenic strains isolated from soybean. Plant Biology 17: 758-765. https://doi.org/10.1111/plb.12282

Pandey AK, Sonker N, Singh P. 2016. Efficacy of some essential oils against Aspergillus flavus with special references to Lippia alba oil an inhibitor of fungal proliferation and aflatoxin B1production in green gram seeds during storage. Journal Food Science 81: M928-M934.

https://doi.org/10.1111/1750-3841.13254

Perumal AB, Sellamuthu PS, Nambiar RB, Sadiku ER. 2017. Effects of essential oil vapor treatment on the postharvest disease control and different defense response in two mango (Mangifera indica L.) cultivars. Food Bioprocess Technology 10: 1131-1141. https://doi.org/10.1007/s11947-017-1891-6

Phillips MW, Wilkinson MJ. 2007. Frosty pod of cacao: a disease with a limited geographic range but unlimited potential for damage. Phytopathology 97: 1644-1647. https://doi.org/10.1094/PHYTO-97-12-1644

Phillips MW, Castillo J, Krauss U, Rodríguez E, Wilkinson MJ. 2005. Evaluation of cacao (Theobroma cacao) clones against seven Colombian isolates of Moniliophthora roreri from four pathogen genetic groups. Plant Pathology 54: 483-490. https://doi.org/10.1111/j.1365-3059.2005.01210.x

Phillips MW, Coutiño A, Ortiz CF, López AP, Hernández J, Aime MC. 2006. First report of Moniliophthora roreri causing frosty pod rot (moniliasis disease) of cocoa in México. Plant Pathology 55: 584. https://doi.org/10.1111/j.1365-3059.2006.01418.x

Phillips MW, Aime J, Wilkinson MJ. 2007. Biodiversity and biogeography of the cacao (Theobroma cacao) pathogen Moniliophthora roreri in tropical America. Plant Pathology 56: 911-922. https://doi.org/10.1111/j.1365-3059.2007.01646.x

Pineda R, Vizcaíno S, Garcia CM, Gil JH, Durango DL. 2012. Chemical composition and antifungical activity of Piper auritum Kunth and Piper holtonii against phytopathogenic

fungi. Chilean Journal of Agricultural Research 72: 507-515. https://doi.org/10.4067/S0718-58392000400008

Pino JA, Marbot R, Agüero J, Fuentes V. 2001. Essential oil from buds and leaves of clove (Syzygium aromaticum (L.) Merr. et Perry) grown in Cuba. Journal of Essential Oil Research 13: 278-279. http://doi.org/10.1080/10412905.2001.9699693

Shukla R, Kumar A, Singh P, Dubey NK. 2009. Efficacy of Lippia alba (Mill) N.E. Brown essential oil and its monoterpene aldehyde constituents against fungi isolated from some edible legume seeds and aflatoxin B1 production. International Journal of Food Microbiology 135: 165-170. https://doi.org/10.1016/j.ijfoodmicro.2009.08.002

[SIAP] Servicio de Información Agroalimentaria y Pesquera. [internet]. 2020. Anuario Estadístico de la Producción Agrícola. [cited 2020 Jun 29]. Disponible en: https://www-gob.mx/siap.

Sivakumar D, Bautista-Baños S. 2014. A review on the use of essential oils for postharvest decay control and maintenance of fruit quality during storage. Crop Protection 64: 27-37. htps://doi.org/10.1016/j.cropro.2014.05.012

Tariq S, Wani S, Rasool W, Shafi K, Bhat MA, Prabhakar A, Shalla AH, Rather MA. 2019. A comprehensive review of the bacterial, antifugal and antiviral potential of essential oils and heir chemical constituents against drug-resistant microbial pathogens. Microbial Pathogenesis 134: 103580. https://doi.org/10.1016/j.micpath.2019.103580

Tomazoni EZ, Pansera MR, Pauletti GF, Moura S, Ribeiro RTS, Schwambach J. 2015. In vitro antifungal activity of four chemotypes of Lippia alba (Verbenaceae) essential oils against Alternaria solani (Preosporeaceae) isolates. Anais da Academia Brasileira de Ciencias 88: 999-1010. https://doi.org/10.1590/0001-3765201620150019

Torres M, Ortiz CF, Téliz OD, Mora AA, Nava DC. 2011. Temporal progress and integrated management of frosty pod rot (Moniliophthora roreri) of cocoa in Tabasco, México. Journal of Plant Pathology 93: 31-36.

Turchetti G, Garzoli S, Masci VL, Sabia C, Iseppi R, Giacomello P, Tiezzi A, Ovidi E. 2020. Antimicrobial testing of Schinus molle (L.) leaf extracts and fractions followed by GC-MS investigation of biological active fractions. Molecules 25: 1-15. https://doi.org/10.3390/molecules25081977

Vilaplana R, Pazmiño L, Valencia CS. 2018. Control of anthracnose, caused by Colletotrichum musae, on postharvest organic banana by thyme oil. Postharvest Biology and Technology 138: 56-63. https://doi.org/10.1016/j.postharvbio.2017.12.008

Wijesekara ROB, Ratnatunga CM, Durbeck K. 1997. The Distillation of Essential Oils. Manufacturing and Plant Construction Handbook. Protrade. Eschborn, Germany.

Zabka M, Pavela R, Slezakova L. 2009. Antifungal effect of Pimenta dioica essential oil against dangerous pathogenic and toxinogenic fungi. Industrial Crops and Products 30: 250-253. https://doi.org/10.1016/j.indcrop.2009.04.002

Publicado

2020-10-05

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Artículos Científicos