Abstract
The antagonistic capacity of Meyerozyma caribbica subjected to hydric and thermal stress and microencapsulated by spray drying against Colletotrichum gloeosporioides was evaluated. M. caribbica grown in medium modified with 1.5 M NaCl and 38 °C increased its viability to 126.36 and 108.78% at a water activity (aw) = 0.98 and 0.96, respectively, compared to the control (100%, aw = 1.0) after 48 h of incubation. Under the same conditions, yeast enhanced its antagonistic activity from 49.27 up to 75.11%. Then, the biocontrol efficacy of different treatments with fresh, stressed, or microencapsulated yeast was evaluated on the incidence and severity of anthracnose disease in avocado fruits. All treatments showed 100% incidence at 10 d of storage at 27 °C; however, all treatments reduced the severity of the disease compared with the control treatment. The best results were obtained with the microencapsulated stressed yeast, which reduced the lesion diameter by 45.43% compared with the control. This study demonstrated the capacity of M. caribbica subject to hydric and thermal stress to increase its viability, improve biocontrol efficacy, and show potential for future preharvest stage applications in avocado fruits.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abadias M, Teixidó N, Usall J, Viñas I, Magan N (2001) Improving water stress tolerance of the biocontrol yeast Candida sake grown in molasses-based media by physiological manipulation. Can J Microbiol 47:123–129. https://doi.org/10.1139/cjm-47-2-123
Aguirre-Güitrón L, Calderón-Santoyo M, Ortiz-Basurto RI, Bautista-Rosales PU, Ragazzo-Sánchez JA (2018) Optimisation of the spray drying process of formulating the post-harvest biocontrol agent Meyerozyma caribbica. Biocontrol Sci Technol 28:574–590. https://doi.org/10.1080/09583157.2018.1468997
Aguirre-Güitrón L, Calderón-Santoyo M, Bautista-Rosales PU, Ragazzo-Sánchez JA (2019) Application of powder formulation of Meyerozyma caribbica for postharvest control of Colletotrichum gloeosporioides in mango (Mangifera indica L.). Lwt 113:108271. https://doi.org/10.1016/j.lwt.2019.108271
An B, Li B, Qin G, Tian S (2012) Exogenous calcium improves viability of biocontrol yeasts under heat stress by reducing ROS accumulation and oxidative damage of cellular protein. Curr Microbiol 65:122–127. https://doi.org/10.1007/s00284-012-0133-4
Bautista-Rosales PU, Calderon-Santoyo M, Servín-Villegas R, Ochoa-Álvarez NA, Ragazzo-Sánchez JA (2013) Action mechanisms of the yeast Meyerozyma caribbica for the control of the phytopathogen Colletotrichum gloeosporioides in mangoes. Biol Control 65:293–301. https://doi.org/10.1016/j.biocontrol.2013.03.010
Bill M, Sivakumar D, Thompson AK, Korsten L (2014) Avocado Fruit Quality Management during the Postharvest Supply Chain. Food Rev Int 30:169–202. https://doi.org/10.1080/87559129.2014.907304
Bustos P, Bórquez R (2013) Influence of Osmotic Stress and Encapsulating Materials on the Stability of Autochthonous Lactobacillus plantarum after Spray Drying. Dry Technol 31:57–66. https://doi.org/10.1080/07373937.2012.717325
Campos-Martínez A, Velázquez-del Valle MG, Flores-Moctezuma HE, Suárez-Rodríguez R, Ramírez-Trujillo JA, Hernández-Lauzardo AN (2016) Antagonistic yeasts with potential to control Colletotrichum gloeosporioides (Penz.) Penz. and Sacc. and Colletotrichum acutatum J.H. Simmonds on Avocado Fruits Crop Prot 89:101–104. https://doi.org/10.1016/j.cropro.2016.07.001
Carbó A, Teixidó N, Usall J, Solsona C, Torres R (2019) Shelf life improvement of the biocontrol agent Candida sake CPA-1 by suitable package and storage conditions. Biocontrol 64:435–446. https://doi.org/10.1007/s10526-019-09944-2
Chandralekha A, Tavanandi AH, Amrutha N, Hebbar HU, Raghavarao KS, Gadre R (2016) Encapsulation of yeast (Saccharomyces cereviciae) by spray drying for extension of shelf life. Dry Technol 34:1307–1318. https://doi.org/10.1080/07373937.2015.1112808
Desmond C, Stanton C, Fitzgerald GF, Collins K, Paul R (2002) Environmental adaptation of probiotic lactobacilli towards improvement of performance during spray drying. Int Dairy J 12:183–190. https://doi.org/10.1016/S0958-6946(02)00040-7
FAOSTAT (2019) Prod stat: crops. FAO Statistical database (faostat), Food and Agriculture Organization of the United Nations (FAO). http://www.fao.org/faostat/en/#data/QC
Fu N, Chen XD (2011) Towards a maximal cell survival in convective thermal drying processes. Food Res Int 44:1127–1149. https://doi.org/10.1016/j.foodres.2011.03.053
González-Estrada RR, Ascencio-Valle F, Ragazzo-Sánchez JA, Calderón-Santoyo M (2017) Use of a marine yeast as a biocontrol agent of the novel pathogen Penicillium citrinum on Persian lime. Emir J Food Agr 29:114–122. https://doi.org/10.9755/ejfa.2016-09-1273
Gotor-Vila A, Usall J, Torres R, Ramos MC, Teixidó N (2017) Environmental stress responses of the Bacillus amyloliquefaciens CPA-8-formulated products on nectarines and peaches. Sci Hortic 225:359–365. https://doi.org/10.1016/j.scienta.2017.07.015
Grzegorczyk M, Żarowska B, Restuccia C, Cirvilleri G (2017) Postharvest biocontrol ability of killer yeasts against Monilinia fructigena and Monilinia fructicola on stone fruit. Food Microbiol 61:93–101. https://doi.org/10.1016/j.fm.2016.09.005
Hernández-Montiel LG, Ochoa JL, Troyo-Diéguez E, Larralde-Corona CP (2010) Biocontrol of postharvest blue mold (Penicillium italicum Wehmer) on Mexican lime by marine and citrus Debaryomyces hansenii isolates. Postharvest Biol Technol 56(2):181–187. https://doi.org/10.1016/j.postharvbio.2009.12.010
Iñiguez-Moreno M, González-Gutiérrez KN, Ragazzo-Sánchez JA, Nárvaez-Zapata JA, Sandoval-Contreras T, Calderón-Santoyo M (2020a) Morphological and molecular identification of the causal agents of post-harvest diseases in avocado fruit, and potential biocontrol with Meyerozyma caribbica. Arch Phytopathol Plant Prot. https://doi.org/10.1080/03235408.2020.1834806
Iñiguez-Moreno M, Ragazzo-Sánchez JA, Barros-Castillo JC, Sandoval-Contreras T, Calderón-Santoyo M (2020b) Sodium alginate coatings added with Meyerozyma caribbica: Postharvest biocontrol of Colletotrichum gloeosporioides in avocado (Persea americana Mill. Cv. Hass). Postharvest Biol Technol 163:111123. https://doi.org/10.1016/j.postharvbio.2020.111123
Ippolito A, Nigro F (2000) Impact of preharvest application of biological control agents on postharvest diseases of fresh fruits and vegetables. Crop Prot 19:715–723. https://doi.org/10.1016/S0261-2194(00)00095-8
Kim IY, Pusey PL, Zhao Y, Korban SS, Choi H, Kim KK (2012) Controlled release of Pantoea agglomerans E325 for biocontrol of fire blight disease of apple. J Control Release 161:109–115. https://doi.org/10.1016/j.jconrel.2012.03.028
Lahlali R, Jijakli MH (2009) Enhancement of the biocontrol agent Candida oleophila (strain O) survival and control efficiency under extreme conditions of water activity and relative humidity. Biol Control 51:403–408. https://doi.org/10.1016/j.biocontrol.2009.07.014
Liu J, Wisniewski M, Droby S, Tian S, Hershkovitz V, Tworkoski T (2011) Effect of heat shock treatment on stress tolerance and biocontrol efficacy of Metschnikowia fructicola. FEMS Microbiol Ecol 76:145–155. https://doi.org/10.1111/j.1574-6941.2010.01037.x
López-Cruz R, Ragazzo-Sánchez JA, Calderón-Santoyo M (2020) Microencapsulation of Meyerozyma guilliermondii by spray drying using sodium alginate and soy protein isolate as wall materials: a biocontrol formulation for anthracnose disease of mango. Biocontrol Sci Technol 0:1–17. https://doi.org/10.1080/09583157.2020.1793910
Medina-Córdova N, López-Aguilar R, Ascencio F, Castellanos T, Campa-Córdova AI, Angulo C (2016) Biocontrol activity of the marine yeast Debaryomyces hansenii against phytopathogenic fungi and its ability to inhibit mycotoxins production in maize grain (Zea mays L.). Biol Control 97:70–79. https://doi.org/10.1016/j.biocontrol.2016.03.006
Morales H, Sanchis V, Usall J, Ramos AJ, Marín S (2008) Effect of biocontrol agents Candida sake and Pantoea agglomerans on Penicillium expansum growth and patulin accumulation in apples. Int J Food Microbiol 122:61–67. https://doi.org/10.1016/j.ijfoodmicro.2007.11.056
Rajam R, Karthik P, Parthasarathi S, Joseph GS, Anandharamakrishnan C (2012) Effect of whey protein - alginate wall systems on survival of microencapsulated Lactobacillus plantarum in simulated gastrointestinal conditions. J Funct Food 4:891–898. https://doi.org/10.1016/j.jff.2012.06.006
Reddy KB, Madhu AN, Prapulla SG (2009) Comparative survival and evaluation of functional probiotic properties of spray-dried lactic acid bacteria. Int J Dairy Technol 62:240–248. https://doi.org/10.1111/j.1471-0307.2009.00480.x
Sui Y, Wisniewski M, Droby S, Liu J (2015) Responses of yeast biocontrol agents to environmental stress. Appl Environ Microbiol 81:2968–2975. https://doi.org/10.1128/AEM.04203-14
Teixidó N, Cañamás TP, Abadias M, Usall J, Solsona C, Casals C, Viñas I (2006) Improving low water activity and desiccation tolerance of the biocontrol agent Pantoea agglomerans CPA-2 by osmotic treatments. J Appl Microbiol 101:927–937. https://doi.org/10.1111/j.1365-2672.2006.02948.x
Yakoby N, Kobiler I, Dinoor A, Prusky D (2000) pH regulation of pectate lyase secretion modulates the attack of Colletotrichum gloeosporioides on avocado fruits. Appl Environ Microbiol 66(3):1026–1030. https://doi.org/10.1128/AEM.66.3.1026-1030.2000
Wang Y, Wang P, Xia J, Yu T, Lou B, Wang J, Zheng XD (2010) Effect of water activity on stress tolerance and biocontrol activity in antagonistic yeast Rhodosporidium paludigenum. Int J Food Microbiol 143:103–108. https://doi.org/10.1016/j.ijfoodmicro.2010.07.035
Acknowledgements
The authors thank Consejo Nacional de Ciencia y Tecnología (CONACYT), Mexico, for the scholarship number 701241, awarded to Katia. N. González Gutiérrez, Tecnologico Nacional de Mexico, for the support through the project number 11168.21-P, and the company Leb Trading Products (Guacamodely) S. de R.L. de C.V. for providing the avocado fruit for this work
Funding
This research is part of the activities of the CYTED Network 319RT0576 “Desarrollo sostenible en agroalimentación y aprovechamiento de residuos industriales.” This work was financed by Tecnologico Nacional de Mexico for the support through the project number 11168.21-P.
Author information
Authors and Affiliations
Contributions
All authors had contributed to the study conception and design. Katia N. González Gutiérrez performed the experiments, data/evidence collection, application of statistical analysis, and article redaction. Juan Arturo Ragazzo Sánchez took part in the application of statistical, mathematical, and computational techniques to analyze or synthesize study data. Montserrat Calderón Santoyo carried out the formulation of overarching research goals and aims, oversight, and leadership responsibility for the research activity planning and execution, provision of study materials, reagents, and materials. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
González-Gutiérrez, K.N., Ragazzo-Sánchez, J.A. & Calderón-Santoyo, M. Application of stressed and microencapsulated Meyerozyma caribbica for the control of Colletotrichum gloeosporioides in avocado (Persea americana Mill. cv. Hass). J Plant Dis Prot 128, 1243–1251 (2021). https://doi.org/10.1007/s41348-021-00487-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41348-021-00487-2