Resistance estimation to Phytophthora palmivora in cacao genotypes using artificial inoculation and natural infection in the field
Estimación de la resistencia a Phytophthora palmivora en genotipos de cacao empleando inoculación artificial e infección natural en campo
DOI:
https://doi.org/10.15446/rfnam.v76n3.104812Keywords:
Average lesion diameter, Black pod disease, Cacao disease, Disease severity index, Oomycetes (en)Diámetro medio de lesión, Mazorca negra, Enfermedades del cacao, Indice de severidad de la enfermedad, Oomicetos (es)
Black pod disease (BPD) is a severe biotic disorder affecting cacao trees in tropical regions generating an estimated global production reduction of approximately 20 to 30%. Accordingly, this study aimed to investigate the correlation between two artificial inoculation methods for Phytophthora palmivora and their potential association with natural infection in cacao clones. Incidence (%) and severity in detached pods (average lesion diameter) and leaf discs (disease severity index) were evaluated. The inoculation in pods at 6 DAI (Days After Inoculation) indicated the highest lesion diameter values for clone CCN51 (9.83 cm); hence, it was categorized as the most susceptible. Conversely, clones IMC67 (5.30 cm) and PA46 (5.27 cm), with the lowest lesion diameter values, were classified as moderately susceptible. Similar outcomes were observed in the leaf disc infection test, corroborating the susceptibility categorization of all six clones at 10 DAI. The leaf disc infection method showed a significantly positive correlation with the detached pod infection method, highlighting the feasibility of employing leaf inoculation to classify clones based on their susceptibility to BPD. Significant differences in aggressiveness were established between the isolates from different Colombian cacao regions. These findings were consistently reflected in the field, where the CCN51 clone exhibited the highest susceptibility compared to TSH565 and ICS95. This research proposes using the leaf technique to assess the aggressivity of Phytophthora palmivora isolates in cacao trees in Colombia.
La pudrición negra de la mazorca (PNM) es un desorden biótico limitante que afecta los árboles de cacao en regiones tropicales, generando pérdidas que se estiman entre el 20 y el 30% de la producción mundial. Por lo tanto, el objetivo de este estudio fue evaluar la correlación entre dos métodos frente a la inoculación de Phytophthora palmivora y su asociación con la infección natural en clones de cacao. Se evaluó la incidencia (%) y severidad de la enfermedad en frutos desprendidos (diámetro medio de la lesión) y en discos de hoja (índice de severidad de la enfermedad). La inoculación en frutos a los 6 DDI (días después de la inoculación), indicó los valores más altos de diámetro de la lesión para el clon CCN51(9,83 cm) por lo que fue categorizado como el más susceptible y los clones IMC67 (5,30 cm) y PA46 (5,27 cm) (con los valores más bajos de diámetro de la lesión), como moderadamente susceptibles. Resultados similares fueron encontrados en la prueba de infección en discos de hojas, corroborando la clasificación de la susceptibilidad de los cinco clones a los 10 DDI. El método de infección en disco de hoja presentó una correlación significativamente positiva con el método de infección en fruto desprendido, indicando la empleabilidad de los dos métodos para la categorización de los clones para la enfermedad PNM. Diferencias significativas en la agresividad fueron establecidas entre los aislamientos evaluados de diferentes regiones colombianas. La asociación directa se mostró en campo, donde el clon CCN51 fue el más susceptible en comparación con los clones TSH565 e ICS95. Esta investigación propone el uso de la técnica foliar para la evaluación de la agresividad de aislados de Phytophthora palmivora en árboles de cacao en Colombia.
References
Adeniyi D (2019) Diversity of cacao pathogens and impact on yield and global production. Pp 43-62. In: Aikpokpodion PO (ed) Theobroma Cacao: Deploying science for sustainability of global cocoa economy, First edition. IntechOpen, London. DOI: https://doi.org/10.5772/intechopen.81993
Arciniegas A (2005) Caracterización de árboles superiores de cacao (Theobroma cacao L.) seleccionados por el programa de mejoramiento genético del CATIE. CATIE, Turrialba (Costa Rica).
Barreto MA, Rosa JRBF, Holanda ISA et al (2018) QTL mapping and identification of corresponding genomic regions for black pod disease resistance to three Phytophthora species in Theobroma cacao L. Euphytica 214:1-16. https://doi.org/10.1007/S10681-018-2273-5
Brasier CM and Griffin MJ (1979) Taxonomy of Phytophthora palmivora on cocoa. Trans- actions of the British Mycological Society 72:111–143. DOI: https://doi.org/10.1016/S0007-1536(79)80015-7
de Souza V, Martins L, Pires J et al (2021) Selection of cocoa clones for resistance to Phytophthora palmivora by artificial inoculation and natural infection in the field. Tropical Plant Pathology 46:455-464. https://doi.org/10.1007/S40858-021-00427-3
Delgadillo-Durán P, Soto-Suárez M, Rodriguez-Polanco L et al (2020) A new method for the inoculation of Phytophthora palmivora (Butler) into cacao seedlings under greenhouse conditions. Plant Methods 16: 114. https://doi.org/10.1186/s13007-020-00656-8
Efombagn MIB, Bieysse D, Nyassé S, Eskes AB (2011) Selection for resistance to Phytophthora pod rot of cocoa (Theobroma cacao L.) in Cameroon: Repeatability and reliability of screening tests and field observations. Crop Protection 30:105-110. https://doi.org/10.1016/j.cropro.2010.10.012
Franco AJD, Merca FE, Rodriguez MS et al (2019) DNA-based electrochemical nanobiosensor for the detection of Phytophthora palmivora (Butler) Butler, causing black pod rot in cacao (Theobroma cacao L.) pods. Physiological and Molecular Plant Pathology 107:14–20. https://doi.org/10.1016/J.PMPP.2019.04.004
Fister AS, Leandro-Muñoz ME, Zhang D et al (2020) Widely distributed variation in tolerance to Phytophthora palmivora in four genetic groups of cacao. Tree Genetics & Genomes 16 (1): 9. https://doi.org/10.1007/s11295-019-1396-8
Gomez K and Gomez A (1984) Statistical procedures for agricultural research. 2nd edition. John Wiley & Sons, Washington D.C.
Guest D (2007) Black pod: Diverse pathogens with a global impact on cocoa yield. Plant Health Progress 97:12. https://doi.org/10.1094/PHYTO-97-12-1650
Imathiu SM, Edwards SG, Ray RV, Back M (2014) Review article: Artificial inoculum and inoculation techniques commonly used in the investigation of Fusarium head blight in cereals. Acta Phytopathologica et Entomologica Hungarica 49(2):129-139. https://doi.org/10.1556/APhyt.49.2014.2.1
Iwaro A, Bekele F, Butler D (2003) Evaluation and utilisation of cacao (Theobroma cacao L.) germplasm at the International Cocoa Genebank, Trinidad. Euphytica 130: 207-221. https://doi.org/10.1023/A:1022855131534
Ko WH (2003) Long-term storage and survival structure of three species of Phytophthora in water. Journal of General Plant Pathology. 69:186-188. https://link.springer.com/article/10.1007/s10327-003-0033-3
Legavre T, Ducamp M, Sabau X et al (2015) Identification of Theobroma cacao genes differentially expressed during Phytophthora megakarya infection. Physiological and Molecular Plant Pathology 92:1-13. https://doi.org/10.1016/J.PMPP.2015.08.005
Lessa IZV, Newman Luz EDM, Magalhães DMA et al (2020) Morfologia e agressividade de isolados de Phytophthora palmivora de cacaueiro no estado da Bahia. Summa Phytopathol 46: 228–235. https://doi.org/10.1590/0100-5405/222473
Marelli JP, Guest DI, Bailey BA et al (2019) Chocolate under threat from old and new cacao diseases. Phytopathology 109: 1331–1343. https://doi.org/10.1094/PHYTO-12-18-0477-RVW
Martins ED, Luz N, Magalhães MA et al (2018) Influência do sistema de cultivo na biogeografia das espécies de Phytophthora patogênicas ao cacaueiro na Bahia, Brasil. Agrotrópica 30:205–214. DOI: https://doi.org/10.21757/0103-3816.2018v30n3p205-214
McKinney H (1923) Influence of soil temperature and moisture on infection of wheat seedlings by Helminthosporium sativum - NALDC.J Agric Res 26:195-217.
Merga J (2022) Epidemiology and management strategies of cocoa black pod (Phytophthora spp.). Plant Pathology & Quarantine. 12:34-39. https://doi.org/10.5943/ppq/12/1/2
Miller-Butler MA, Smith BJ, Babiker EM et al (2018) Comparison of whole plant and detached leaf screening techniques for identifying anthracnose resistance in strawberry plants. Plant Dis 102:2112-2119. https://doi.org/10.1094/pdis-08-17-1138-re
Misman N, Samsulrizal NH, Latif Noh A et al (2022) Host range and control strategies of Phytophthora palmivora in Southeast Asia Perennial Crops. Pertanika J Trop Agric Sci 45:991–1019. https://doi.org/10.47836/pjtas.45.4.09
Motamayor JC, Lachenaud P, da Silva e Mota JW et al (2008) Geographic and genetic population differentiation of the Amazonian chocolate tree (Theobroma cacao L). PLoS One 3:e3311. https://doi.org/10.1371/journal.pone.0003311
Mucherino Muñoz JJ, de Melo CAF, Santana Silva RJ et al (2021) Structural and functional genomics of the resistance of cacao to Phytophthora palmivora. Pathogens 10:961. https://doi.org/10.3390/pathogens10080961
Nyadanu D, Assuah M, Adomako B et al (2010) Efficacy of screening methods used in breeding for black pod disease resistance varieties in cocoa. African Crop Sci J 17:175-186. https://doi.org/10.4314/acsj.v17i4.54298
Nyadanu D, Akromah R, Adomako B et al (2012) Inheritance and general combining ability studies of detached pod, leaf disc and natural field resistance to Phytophthora palmivora and Phytophthora megakarya in cacao (Theobroma cacao L.). Euphytica 188:253-264. https://doi.org/10.1007/s10681-012-0717-x
Nyassé S, Cilas C, Herail C, Blaha G (1995) Leaf inoculation as an early screening test for cocoa (Theobroma cacao L.) resistance to Phytophthora black pod disease. Crop Protection 14: 657–663. https://doi.org/10.1016/0261-2194(95)00054-2
Nyassé S (1997) Etude de la diversité de Phytophthora megakarya et caractérisation de la résistance du cacaoyer (Theobroma cacao L.) à cet agent pathogène. Toulouse : INPT, 160 p. Thèse de doctorate: Sciences Agronomiques: Institut National Polytechnique de Toulouse
Palacios Bejarano CA, Afanador Kafuri L, Pardo García JM et al (2021) Identificación de aislados de Phytophthora spp. obtenidos de cultivos de cacao en Antioquia, Colombia. Acta Agronomica 70:17–26. https://doi.org/10.15446/ACAG.V70N1.70619
Paulin D, Ducamp M, Lachenaud P (2008) New sources of resistance to Phytophthora megakarya identified in wild cocoa tree populations of French Guiana. Crop Protection 27:1143-1147. https://doi.org/10.1016/j.cropro.2008.01.004
Ploetz R (2016) The impact of diseases on cacao production: A global overview. In: Cacao diseases: A history of old enemies and new encounters. Springer International Publishing pp.33-59. DOI: https://doi.org/10.1007/978-3-319-24789-2_2
Pokou ND, N’Goran JAK, Kébé I et al (2008) Levels of resistance to Phytophthora pod rot in cocoa accessions selected on-farm in Côte d’Ivoire. Crop Prot. 27:302-309. DOI: https://doi.org/10.1016/j.cropro.2007.07.012
Pokou DN, Fister AS, Winters N et al (2019) Resistant and susceptible cacao genotypes exhibit defense gene polymorphism and unique early responses to Phytophthora megakarya inoculation. Plant Mol Biol 99: 499–516. https://doi.org/10.1007/s11103-019-00832-y
Polanco LR, Carrero Gutiérrez ML, Parra EB et al (2022) Reaction of detached fruíts from selected cocoa clones to artificial inoculation with Phytophthora palmivora. Acta Agronomica 71:186194. http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0120-28122022000200186
Puig AS, Ali S, Strem M et al (2018) The differential influence of temperature on Phytophthora megakarya and Phytophthora palmivora pod lesion expansion, mycelia growth, gene expression, and metabolite profiles. Physiol Mol Plant Pathol 102:95–112. https://doi.org/10.1016/j.pmpp.2017.12.002
Puig AS, Keith LM, Matsumoto TK et al (2021) Virulence tests of Neofusicoccum parvum, Lasiodiplodia theobromae, and Phytophthora palmivora on Theobroma cacao. Eur J Plant Pathol 159:851–862. https://doi.org/10.1007/s10658-021-02210-1
Ramírez J (2016) Pérdidas económicas asociadas a la pudrición de la mazorca del cacao causada por Phytophthora spp., y Moniliophthora roreri (Cif y Par) Evans et al., en la hacienda Theobroma, Colombia. In: Rev. Protección Veg. ISSN: 224-4697.
Ramírez Martínez J, Cárdenas Toquica M, Guevara-Suarez M et al (2021) Oomycete species associated with Theobroma cacao crops in Colombia. Plant Pathol 70:1695-1707. https://doi.org/10.1111/ppa.13410
Rêgo APB, Mora-Ocampo IY, Corrêa RX (2023) Interactions of different species of Phytophthora with cacao induce genetic, biochemical, and morphological plant alterations. Microorganisms. 11(5):1172. https://doi.org/10.3390/microorganisms11051172
Rodríguez-Polanco E, Carrero M, Parra E, Segura J (2020a) Reaction of detached fruits from selected cocoa clones to artificial inoculation with Phytophthora palmivora (Peronosporales: Peronosporaceae). Acta Agronomica 70:186-194. DOI: https://doi.org/10.15446/acag.v71n2.88841
Rodríguez-Polanco E, Morales JG, Muñoz-Agudelo M et al (2020b) Morphological, molecular and pathogenic characterization of Phytophthora palmivora isolates causing black pod rot of cacao in Colombia. Spanish J Agric Res 18:e1003-e1003. DOI: https://doi.org/10.5424/sjar/2020182-15147
Rodríguez-Polanco E, Parra EB, Bermeo PA et al (2020c) Manejo de la pudrición parda de la mazorca (Phytophthora palmivora) en cacao por aplicación conjunta de prácticas culturales y químicas. Rev Fac Ciencias Básicas 16:79-94. https://doi.org/10.18359/RFCB.4887
Rodríguez E and Vera A (2015) Identificación y manejo de la pudrición parda de la mazorca (Phytophthora sp.) en cacao, Primera ed. Corporación Colombiana de Investigación Agropecuaria, Bogotá D.C. DOI: https://doi.org/10.21930/978-958-740-197-4
Saul-Maora J, Namaliu Y, Cilas C, Blaha G (2007) Durability of field resistance to black pod disease of cacao in Papua New Guinea. 87:1423-1425. https://doi.org/10.1094/PDIS.2003.87.12.1423
Schneider C, Rasband W, Eliceiri K (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9, 671–675. https://doi.org/10.1038/nmeth.2089
Surujdeo-Maharaj S, Sreenivasan T, Motilal L, PU (2016) Black pod and other Phytophthora induced diseases of cacao: history, biology, and control. In: Bailey B, Meinhardt L (eds) Springer International Publishing. Beltsville, MD, 213-266. DOI: https://doi.org/10.1007/978-3-319-24789-2_7
Tahi G, Kébé BI, N’Goran JAK et al (2006) Expected selection efficiency for resistance to cacao pod rot (Phytophthora palmivora) comparing leaf disc inoculations with field observations. Euphytica 1491 149:35-44. https://doi.org/10.1007/S10681-005-9052-9
Tijani AA, Otuonye AH, Otusanya MO et al (2020) Testing for the resistance of newly generated hybrid cacao germplasm in the gene pool of Cocoa Research Institute of Nigeria (CRIN) against Phytophthora megakarya pathogen causing black pod disease of cocoa. bioRxiv 2020.12.07.414466. https://doi.org/10.1101/2020.12.07.414466
Villamizar-Gallardo R, Osma JF, Ortíz-Rodriguez OO (2019) Regional evaluation of fungal pathogen incidence in colombian cocoa crops. Agric 2019.9:44. https://doi.org/10.3390/AGRICULTURE9030044
Yanac Montesino R, Rosales-Huamani JA, Castillo-Sequera JL (2021) Detection of Phytophthora palmivora in cocoa fruit with deep learning. Iberian Conference on Information Systems and Technologies, CISTI. https://doi.org/10.23919/CISTI52073.2021.9476279
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