High genetic diversity in arbuscular mycorrhizal fungi influence cadmium uptake and growth of cocoa plants





Biodiversity, mycorrhizae, phytoremediation, Theobroma


Soil cadmium (Cd) represents a problem in cocoa farms in Peru. The objective of this study was to evaluate the effect of the diversity of arbuscular mycorrhizal fungi (AMF) from different provinces of the Peruvian Amazon on cadmium uptake and cacao plant growth under nursery conditions. Germinated seeds were inoculated with different AMF species, at a rate of 1500 spores, in substrates conformed by 1:2 sand and agricultural soil, with two levels of addition of Cd (0 and 5 mg·kg-1). The height of the plant and leaf area, and colonization and mycelium of AMF were evaluated; likewise, Cd levels were quantified in the soil and the stems of the cocoa seedlings. A completely randomized design with a bifactorial arrangement was used with eight treatments and eight  replications  per  treatment,  which  were  compared  by  ANOVA  and  mean  separation  by  Tukey's  test.  The  results indicate that the AMF species from the Mariscal Cáceres province consortium promoted greater plant height and leaf area, while the species from the Lamas consortium presented a greater reduction of cadmium in soil and stems. Therefore, the diversity of AMF species associated with cocoa plants could be considered a potential tool to immobilize Cd and improve growth in cocoa plants.


Download data is not yet available.


Aguilera P., C. Marín, F. Oehl, R. Godoy, F. Borie y P.E. Cornejo. 2017. Selection of aluminum tolerant cereal genotypes strongly influences the arbuscular mycorrhizal fungal communities in an acidic Andosol. Agriculture, Ecosystems and Environment 246: 86-93.

Aguirre-Forero, S.E., N.V. Piraneque-Gambasica y J.R. Vásquez-Polo. 2021. Contenido de metales pesados en suelos y tejidos de cacao en el departamento del Magdalena, Colombia: énfasis en cadmio. Entramado 16(2): 298-310.

Barraza F., E. Schreck, E. Schreck, T. Lévêque, G. Uzu, F. López, J. Ruales, J. Prunier, A. Marquet y L. Maurice. 2017. Cadmium bioaccumulation and gastric bioaccessibility in cacao: a field study in areas impacted by oil activities in Ecuador, Environ. Pollut. 229: 950-963.

Blaudez D., C. Jacob, K. Turnau, J.V. Colpaert, U. Ahonen-Jonnarth, R. Finlay et al. 2000. Differential responses of ectomycorrhizal fungi to heavy metals in vitro. Mycol Res 104: 1366-1371.

Brundrett, M.C., Y. Piche y R.L. Peterson. 1984. A new method for observing the morphology of vesicular-arbuscular mycorrhizae. Can. J. Bot. 62: 2128-2134.

Cabral L., C.R.F. Sousa, A.J. Giachini y J.O. Siqueira. 2015. Arbuscular mycorrhizal fungi in phytoremediation of contaminated areas by trace elements: mechanisms and major benefits of their applications. Word J. Microbiol. Biotechnol. 31(11): 1655-1664.

Das, S.C. y H.A. AL-Naemi. 2019. Toxicidad por cadmio: estrés oxidativo, inflamación y lesiones tisulares. Enfermedades Profesionales y Medicina Ambiental 7(4): 144-163.

Del Águila, K.M., G. Vallejos-Torres, L.A. Arévalo y A.G. Becerra. 2018. Inoculación de consorcios micorrícicos arbusculares en Coffea arabica, variedad Caturra en la región San Martín, Información Tecnológica 29(1): 137-146.

Fengge, Z., L. Moha, L. Yang, Ch. Yeye y X. Yan. 2019. Effects of arbuscular mycorrhizal fungi, biochar and cadmium on the yield and element uptake of Medicago sativa. Science of the Total Environment. 655: 1150-1158.

Florida, N., J. Paucar, S.S. Jacobo y F. Escobar-Mamani. 2019. Efecto de compost y NPK sobre los niveles de microorganismos y cadmio en suelo y almendra de cacao. Journal of High Andean Research 21(04): 264-273.

Garg, N. y H. Kaur. 2013. Impact of cadmium-zinc interactions on metal uptake, translocation and yield in pigeonpea genotypes colonized by arbuscular mycorrhizal fungi. Journal of Plant Nutrition. 36(1): 67-90.

Guerra-Sierra, B.E., A. Sandoval-Meza, L.S. Manrique-González y S.P. Barrera-Rangel. 2014. Ensayos preliminares in vitro de biosorción de cadmio por cepas fúngicas nativas de suelos contaminados. Innovaciencia Facultad Cienc. Exactas Fis. Naturales 2(1): 53-58.

Han, Y., O.K. Zveushe, F. Dong, Q. Ling, Y. Chen, S. Sajid et al. 2021. Unraveling the effects of arbuscular mycorrhizal fungi on cadmium uptake and detoxification mechanisms in perennial ryegrass (Lolium perenne). Sci. Total Environ. 798: 149222.

Hassan, S.E., M. Hijri y M. St-Arnaud. 2013. Effect of arbuscular mycorrhizal fungi on trace metal uptake by sunflower plants grown on cadmium contaminated soil. N. Biotechnol. 30: 780-787

Huang, H, S. Zhang, C. Bao-Dong, W. Naiying, S. Xiao-Quan y P. Christy. 2006. Uptake of atrazine and cadmium from soil by maize (Zea mays L.) in association with the arbuscular mycorrhizal fungus Glomus tunicatum. J. Agr. Food Chem. 54: 9377-9382.

Janeeshma, E. and J.T. Puthur. 2020. Direct y indirect influence of arbuscular mycorrhizae on enhancing metal tolerance of plants. Arch Microbiol. 202(1): 1-16.

Janoušková, M. y D. Pavlíková. 2010. Cadmium immobilization in the rhizosphere of arbuscular mycorrhizal plants by the fungal extraradical mycelium. Plant and Soil 332(1): 511-520.

Jinxiu, Z., S. Lin, Y. Kai, L. Mingrui, H. Yongmei, Z. Yanqun, Z. Fangdong y L. Tao. 2020. An arbuscular mycorrhizal fungus increased the macroaggregate proportion and reduced cadmium leaching from polluted soil, International Journal of Phytoremediation 22: 1-9.

Li, H., N., L.J. Luo. H.M. Zhang, Y.W. Zhao, Q.Y. Li, M.H. Cai, M.H. Wong and C.H. Mo. 2016. Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, ¿subcellular distribution and chemical forms in rice?. Sci Total Environ. 571: 1183-90

Londoño-Franco, L.F, P.T. Londoño-Muñoz y F.G. Muñoz-García. 2016. Los riesgos de los metales pesados en la salud humana y animal. Biotecnología en el Sector Agropecuario y Agroindustrial 14(2): 145-153.

MINAGRI (Ministerio de Agricultura y Riego). 2019. Plan Nacional de Cultivos. Campaña Agrícola 2019-2020 Reporte de precio y mercado de cacao, Lima, Perú. https://n9.cl/c2wa (consulta de octubre 5, 2021).

Miransari, M. 2017. Arbuscular mycorrhizal fungi and heavy metal tolerance in plants. In: Wu QS. (eds.). Arbuscular Mycorrhizas and Stress Tolerance of Plants. Springer, Singapore. 147-161.

Newman, E.I. 1966. A Method of estimating the total length of root in a sample. Journal of Applied Ecology 3(1): 139-145.

Oliva M., K. Rubio, M. Epquin y S. Marlo Gand Leiva. 2020. Cadmium uptake in native cacao trees in agricultural lands of Bagua, Peru. Agronomy 10(10): 1551.

Pawlowska, T.E. y I. Charvat. 2004. Heavy-metal stress and development patterns of arbuscular mycorrhizal fungi. Appl. Environ. Microbiol. 70(11): 6643-6649.

Phillips, J.M. y D.S. Hayman. 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection, Transactions of the British Mycological Society 55(1): 158-161.

Redon, P.O., T. Beguiristain y C. Leyval. 2008. Influence of Glomus intraradices on Cd partitioning in a pot experiment with Medicago truncatula in four contaminated soils. Soil Biol. Biochem. 40: 2710-2712.

R Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (consulta de septiembre 30, 2021).

Scaccabarozzi, D., L. Castillo, A. Aromatisi, L. Milne, A. Búllon y M. Muñoz-Rojas. 2020. Soil, site, and management factors affecting cadmium concentrations in cacao-growing soils. Agronomy 10(6): 806.

Sun, H., Y. Xie, Y. Zheng, Y. Lin y F. Yang. 2018. La mejora por hongos micorrízicos arbusculares de la capacidad de remediación del Cd y los factores relacionados con la calidad de la bioenergía de cinco cultivares de pasto varilla en suelos contaminados con Cd. PeerJ, 6, e4425.

Tantalean, E. y M. A. Huauya. 2017. Distribución del contenido de cadmio en los diferentes órganos del cacao CCN-51 en suelo aluvial y residual en las localidades de Jacintillo y Ramal de Aspuzana. Revista de Investigación de Agroproducción Sustentable 1(2): 69-78.

U.S. EPA. 1996. Method 3050B: Acid Digestion of Sediments, Sludges, and Soils, Revision 2. Washington, DC. https://n9.cl/76t47 (consulta de octubre 5, 2021).

Vallejos-Torres, G., T. Sánchez, M.A. García, M. Trigoso y L.A. Arévalo. 2019. Efecto de hongos formadores de micorrizas arbusculares en clones de café (Coffea arabica) variedad Caturra. Acta Agronómica 68(4): 278-284.

Wang, F., S. Zhang, P. Cheng, S. Zhang y Y. Sun. 2020. Effects of soil amendments on heavy metal immobilization and accumulation by maize grown in a multiple-metal-contaminated soil and their potential for safe crop production. Toxics 8(4): 102 (6 p.).

Wang, F.Y., Z.Y. Shi, X.F. Xu, X.G. Wang y Y.J. Li. 2013. Contribution of AM inoculation and cattle manure to lead and cadmium phytoremediation by tobacco plants. Environ Sci. Process Impacts 15(4): 794-801.

Wipf, D., F. Krajinski, D. van Tuinen, G. Recorbet y P.E. Courty. 2019. Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal Networks. New Phytologist 223(3): 1127-1142.

Yongqiang, Y., W. Li, J. Chang, W. Gen, M. Fang, W. Yujiao y Y. Dongguang. 2021. Effects of arbuscular mycorrhizal fungi on the

growth and toxic element uptake of Phragmites australis (Cav.) Trin. ex Steud under zinc/cadmium stress. Ecotoxicology and Environmental Safety 213: 112023.

Zhang, X., B. Chen y R. Ohtomo. 2015. Mycorrhizal effects on growth, P uptake and Cd tolerance of the host plant vary among

different AM fungal species. Soil Science and Plant Nutrition 61(2): 359-368.

Zug, K.L., H.A. Huamaní, F. Meyberg, F. Meyberg y J.S. Cierjacks. 2019. Cadmium accumulation in peruvian cacao (Theobroma cacao L.) and opportunities for mitigation. Water Air Soil Pollution 230(3): 72-80.



How to Cite

Vallejos-Torres, G., Ruíz-Valles, R., Chappa-Santa María, C. E., Gaona-Jiménez, N., & Marín, C. (2021). High genetic diversity in arbuscular mycorrhizal fungi influence cadmium uptake and growth of cocoa plants. Bioagro, 34(1), 75-84. https://doi.org/10.51372/bioagro341.7