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Terra Latinoamericana

On-line version ISSN 2395-8030Print version ISSN 0187-5779

Terra Latinoam vol.38 n.3 Chapingo Jul./Sep. 2020  Epub Jan 12, 2021 

Special number

Arbuscular mycorrhiza as a biofertilizer in production of coffee

Elizabeth Hernández-Acosta1

Dora Trejo-Aguilar2

Andrés Rivera-Fernández2 

Ronald Ferrera-Cerrato3

1Departamento de Suelos, Universidad Autónoma Chapingo. Carretera México-Texcoco km 38.5, Chapingo. 56230 Texcoco, Estado de México, México.

2Facultad de Ciencias Agrícolas, Universidad Veracruzana. Zona Universitaria. 91090 Xalapa, Veracruz, México.

3Colegio de Postgraduados, Campus Montecillo. Carretera México-Texcoco km 36.5, Montecillo. 56230 Texcoco, Estado de México, México.


In coffee plantations in southeastern Mexico, the chemical, physical and biological degradation of soils affects the production of plants. This situation economically harms the coffee growers, so it is common to place the neglect of their plantations where the cultivation tasks such as pruning and fertilization are costly. To solve the problem of fertilization, the application of arbuscular mycorrhizal inocula is recommended, its effectiveness is clear in vegetables and fruit trees. The response of two inocula (Rhizophagus aggregatus) and the consortium formed by the fungi Glomus claroides, Rhizophagus diaphanus and Paraglomus albidum (CMgrp) was evaluated in the coffee varieties garnica, catimor, caturra and catuaí, with the purpose of locating the best symbiosis plant-fungus. The variables height of the plant, dry matter, content of phosphorus in leaves, percentage of mycorrhizal colonization, percentage of mycorrhizal efficiency, percentage of phosphorus absorbed by mycorrhization and the efficiency index of mycorrhizae in the health of the plant were evaluated. (Em) The results showed that the CMgrp consortium generated the highest values and increases with respect to non-inoculated plants in the plant height and dry matter variables (177 and 1701% for garnica variety) and phosphorus content (650% in the catimor variety). The response of the plants to mycorrhization showed the best results in the garnica varieties (34.32% colonization percentage) and caturra (1670% mycorrhizal efficiency and 1651% phosphorus absorbed by mycorrhization effect). The Em index revealed that the coffee plants inoculated with the CMgrp presented better health. It is recommended to use the CMgrp consortium as a biofertilizer in coffee plants, to ensure the success of the transplant, a situation that will represent an economic and time saving for the coffee grower.

Index words: garnica; catimor; caturra and catuaí varieties; biological fertilizers


En fincas cafetaleras del sureste de México, la degradación química, física y biológica de los suelos afecta la producción de plantas. Esta situación perjudica económicamente a los cafeticultores, por lo que es común encontrar un descuido en sus plantaciones donde labores de cultivo como la poda y fertilización son costosas. Para resolver el problema del costo de fertilizantes, se recomienda la aplicación de inóculos micorrízicos arbusculares, su efectividad queda clara en hortalizas y frutales. Se evaluó la respuesta de dos inóculos del Colegio de Postgraduados, de una especie, (Rhizophagus aggregatus) y un consorcio (Glomus claroides, Rhizophagus diaphanus y Paraglomus albidum) (CMgrp) en plántulas de las variedades de café garnica, catimor, caturra y catuaí, con la finalidad de ubicar la mejor simbiosis planta-hongo. Se evaluaron las variables altura de la planta, materia seca, contenido de fósforo en hojas, porcentaje de colonización micorrízica, porcentaje de la eficiencia micorrízica, porcentaje de fósforo absorbido por la micorrización y el índice de eficiencia de la micorrización en la sanidad de la planta (E m ). Los resultados mostraron que el consorcio CMgrp generó los valores e incrementos más altos con respecto a las plantas no inoculadas en las variables altura de la planta y materia seca (1774 y 1701% para la variedad garnica respectivamente) y contenido de fósforo (650% en la variedad catimor). La respuesta de las plantas a la micorrización mostró los mejores resultados en las variedades garnica (34.32% porcentaje de colonización) y caturra (1670% de eficiencia micorrízica y 1651% fósforo absorbido por efecto de la micorrización). El índice Em reveló que las plantas de café inoculadas con el CMgrp presentaron mejor sanidad. Se recomienda utilizar al consorcio CMgrp como biofertilizante en plantas de café, para asegurar el éxito del trasplante, situación que representará un ahorro económico y de tiempo para el cafeticultor.

Palabras clave: variedades garnica; catimor; caturra y catuaí; fertilizantes biológicos


At the end of the 80s, the use of arbuscular mycorrhizal fungi (AMF) in agriculture increased as an alternative to the use of synthetic fertilizers (Berruti et al., 2016). Until now, they have been produced or commercialized in Mexico under different brands although no information on production and sale has been available (Weber, 2014). The Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP), Buckman Laboratories, Plant Healt Care, Universidad Veracruzana, Colegio de Postgraduados, Biofábrica Siglo XXI, just to mention some, produce the biofertilizer in different presentations. Many of these products contain mainly the species Rhizophagus irregularis; such is the case of BuRIZE (Buckman Lab, Estado de Mexico, MX), EndoRyza (Plant Health Care, CDMX, MX) and MicorrhizaFer (Biofábrica SXXI, CDMX, MX) according to the labels of their products.

Phosphorus is the main element that AMF translocate to the plant (Jakobsen and Hammer, 2015); however, they also mobilize water, expand the radicle exploration area through the hyphae, gaining access to nutrient and soil spaces inaccessible to roots. Despite the benefits, the plant has influence in fungus growth (Sawers et al., 2017) without forgetting that AMF also interact with other soil microorganisms (Battini et al., 2017).

The AMF associate, with close to 200 000 hosts, may have a low specificity (van der Heijden et al., 2015); however, some studies have shown that a preference or compatibility for determined species exists (Torrecillas et al., 2012; Sawers et al., 2017). On the other hand, preference may not be related to efficiency, in a way that some fungi may be more efficient than others in the same host (Zhang et al., 2015).

Mexico has a replanting program of coffee plantations - a guide for high quality coffee production - which comes from the Plan Integral de Atención al Café (PIAC) within the Plan Nacional de Desarrollo 2017-2030 (SAGARPA, 2016). The plan is set out to produce healthy and resistant plants from the nursery stage. Because coffee is a mycotrophic plant (Hernández-Acosta et al., 2018), the search for native AMF with the possibility of using them as biofertilizer is a viable option (Vincenzo et al., 2018). In Oaxaca, the production of organic coffee has increased with the practice of mycorrhizal inoculation (Noriega-Altamirano et al., 2014).

Within this context, the objective of this study was to evaluate the effect of two AMF inoculants on growth and development of four coffee varieties in the nursery stage to select the most efficient variety-fungus combination to obtain vigorous and resistant plants at transplant and promote the use of mycorrhizae as biofertilizers among coffee producers.

Materials and Methods

An experiment at nursery level was performed in Xalapa, Veracruz, México at 1399 m a.s.l. with an average annual precipitation of 1626 mm and an annual average temperature of 18 °C. Seeds of the species Coffea arabica L., varieties Garnica, Catimor, Caturra, and Catuaí were used with germination percentages of 95, 98, 97, and 90%, respectively. Two mycorrhizal inoculants were used (1) Rhizophagus aggregatus (Schenck & GS Sm) and (2) Glomus claroides, Rhizophagus diaphanus (Cano & Dalpé) and Paraglomus albidum (Walker & Rhodes) consortium (CMgrp). The colonization percentages of the propagated inoculants in onion plants were 57% for R. aggregatus and 67% for the CMgrp consortium. Both inoculants were provided by Colegio de Postgraduados, Campus Montecillo, in Texcoco, Estado de México.

The material used as substrate was a mixture of soil and organic matter (vegetal waste) in a ratio of 40:60, which was sieved and sterilized at a temperature of 120 (C for 2.5 h. The substrate had 13.82% organic matter, pH 6.5 and 33 mg kg-1 of phosphorus (Bray Method), which are the adequate characteristics for establishing coffee and AMF (Contreras et al., 2017; Bolaños et al., 2000).

For plant growth, recipients of 1 kg were used with a depth of 4 cm; at the center, 10 g of inoculant were incorporated in each experimental unit; then the coffee seed was placed, covering it with soil and on the surface a very thin layer of sterile volcanic rock to conserve humidity. The experiment lasted eleven months, during which irrigation was performed according to the plant needs until the substrate reached field capacity to avoid the presence of fungal wilting.

A complete randomized experimental design was established with 12 treatments, four varieties, two AMF inoculants, four control groups (without inoculation) and five replicates per treatment. Each experimental unit was one plant. At the end of the experiment - 335 days after sowing (DAS) - the following variables were assessed (1) plant height; (2) dry biomass; (3) leaf phosphorus content; (4) mycorrhizal colonization percentage; (5) mycorrhizal efficiency percentage, with the equation proposed by Colozzi-Filho and Siqueira (1986):

Efficiency=inoculated plant heightcontrol plant height × 100-100

(6) Absorbed phosphorus percentage by mycorrhizae, according to the equation proposed by Sieverding (1991):

PI (%)=Inoculated plant biomass × 100Control plant biomass -100

and (7) Health, leaf harm caused by Phoma costarricensis and chlorosis (yellowing due to nutrient deficiency) (Rivera, 1991), measuring five plants by means of a subjective scale. The averages to constitute and index named (mycorrhization efficiency index) were calculated by utilizing an adaptation of Likert scale (Bertram, 2007). Such index takes values from 0-5; the smaller this value is, the greater benefit it indicates and should be interpreted as a quantitative summary associated to frequency distribution starting from our scale (Table 1).

Table 1: Subjective scale to evaluate coffee seedling health and vigor (adapted from a scale proposed by Rivera, 1990). 




Healthy plants


Intense green color plants


Plant with 5% damage


Not-intense green color plants


Plants with 20% leaf damage


Green plants


Plants with 40% damage


Lemon-green plants


Plants with 60% damage


Semi-yellow plants


Plantas more than 80% damage


Yellow plants

Normalizing the indicator was useful; its value was divided by 5, in such a way that subsequently Em takes values from 0-1, interpreting that for values closer to 0 where mycorrhization efficiency is higher, and values closer to 1 are lower. The index was calculated by the following equation: Where ƒ0, ƒ1,…, ƒ k are the observed frequencies in each one of the categories associated to the values 0, 1, 2, of the defined scale in this study. Then,

Em = 1    nk     j=1k jfj

where: n= j=0kfj corresponds to the total observations (plants). In this case, and k = 5 and n = 15.

This index was designed specifically for the analysis of the data obtained in this research study. No background exists of an index such as the one used in this study.

After the normality tests, an analysis of variance (ANOVA) and Tukey’s (P ≤ 0.05) comparison of means (honestly significant difference, HSD) tests were performed with software SAS version 9.0 (SAS, 2000).

Results and discussion

Plant height

When plant height of the four coffee varieties was assessed and compared with respect to the control plants, the inoculation of the CMgrp consortium gave as a result plants with greater height (Figure 1). For this variable, the effect among both inoculants was different, above all, with respect to the inoculated coffee variety. The inoculant R. aggregatus had a minimum effect in this variable in the varieties Garnica and Catuaí (Figure 1).Adriano-Anaya et al., 2011 inoculated the var. Bourbon with Rhizophagus intrarradices cultivated in transformed roots, but no effect was observed in this variable.

*Different letters in the same figure indicate significant differences (Tukey’s P ≤ 0.05) test. Consortium = CMgrp (Glomus claroides, Rhizophagus diaphanus, and Paraglomus albidum).

Figure 1: Plant height of coffee varieties (a) Garnica, b) Catimor, (c) Caturra, and (d) Catuaí inoculated with two mycorrhizal inoculants Rhizophagus aggregatus and the consortium compared with the control plants at 335 days after sowing (DDS).  

Ibarra-Puón et al. (2014) tested the same AMF but in Coffea canephora (Robusta), where plant height increased when compared to control at 140 days after inoculation. These results may indicate a certain preference of AMF species for coffee species although the influence in the form of the inoculant, production could be a factor to study in a near future. Furthermore, the time factor could also have an influence in the results observed.

The effect of the mycorrhizal inoculants on coffee with respect to height has been documented with different AMF consortia. Del Aguila et al., 2018, applied nine mycorrhizal consortia in coffee plants of the var. Caturra although the species in the consortia were not reported. The increase in this variable may be related to obtaining phosphorus by the inoculants.

Dry biomass

The dry biomass variable was also influenced by the mycorrhizal inoculation, above all, when it was inoculated with the CMgrp consortium with weight fluctuating from 1.4-5.45 g for all the varieties. The only one where the effect was lower, although significantly, was observed on the var. Catuaí (Figure 2).

*Different letters in the same figure indicate significant differences (Tukey’s P ≤ 0.05) test. Consortium = CMgrp (Glomus claroides, Rhizophagus diaphanus, and Paraglomus albidum).

Figure 2: Dry biomass in coffee plants varieties (a) Garnica, (b) Catimor, (c) Caturra, and (d) Catuaí with two mycorrhizal inoculations (1) Rhizofagus aggregatus and (2) the consortium, compared with the control plants at 335 days after sowing (DDS).  

Dry biomass is one of the most measured growth and development variables in coffee to analyze the mycorrhizal effect as biofertilizer (Ibarra-Puón et al., 2014) because it allows calculating the variation among genotypes, environment and management - factors that generate modifications in biomass accumulation (Di Benedetto and Tognetti, 2016).

Aguirre-Medina et al., 2011 observed that Rhizophagus intrarradices inoculation did not show variation in this variable in coffee plants var. Oro Azteca even when dry root, stem, and leaf dry weight were evaluated from 60-210 DAS.

On the other hand, Adriano-Anaya et al. (2011) assessed the effect of Rhizophagus intraradices in coffee plants var. Bourbon at 112 days after inoculation when they evaluated dry root weight and leaves, finding increments from 118-141% compared to the control plants. In both studies, mycorrhizal fungus efficiency as biofertilizer was observed in growth depending on the variety of coffee and mycorrhizal inoculant.

Leaf phosphorus content

Inoculation of the AMF had effect on increasing total phosphorus content, having differential results in function of the inoculant source and coffee variety. The values with greater phosphorus content were observed in the var. Catimor, which increased with the AMF inoculation with 0.16 mg kg-1 (R. aggregatus) and 0.15 mg kg-1 (CMgrp) even in the non-inoculated treatment (Figure 3).

*Different letters in the same figure indicate significant differences (Tukey’s P ≤ 0.05) test. Consortium = CMgrp (Glomus claroides, Rhizophagus diaphanus, and Paraglomus albidum).

Figure 3: Leaf phosphorus content of coffee varieties (a) Garnica, (b) Catimor, (c) Caturra, and (d) Catuaí inoculated with two mycorrhizal inoculants (1) Rhizophagus aggregatus and (2) the consortium compared with control at 335 days after sowing (DDS).  

Ibarra-Puón et al. (2014) reported that phosphorus concentration in coffee plants was 0.014% higher in the treatments inoculated with Rhizophagus intraradices (0.045%) at 140 days after transplant (DAT), compared with the control group (0.031%).

In papaya cultivation, Quiñones-Aguilar et al. (2012) mentioned that the AMF hyphae are capable of capturing and transporting soil phosphorus towards higher parts of the plants in poor soil or without fertilizer, which could explain the increase.

Perea-Rojas et al. (2018) studied the importance of the AMF consortium in phosphorus transformation and absorption processes in coffee plants, finding greater leaf phosphorus concentration in the var. Garnica in treatments of plants inoculated with the mycorrhizal consortium and phosphorus solubilizing fungi. This study showed that despite the availability of this element in soil, the presence of the AMF was determinant to translocate phosphorus to the plant parts.

Aguirre-Medina et al. (2011) measured an increase in phosphorus at 150 DAS in coffee var. Oro Azteca inoculated with Rhizophagus intraradices although this effect was not constant throughout the measurements from 60-210 DAS.

Mycorrhizal colonization

The highest colonization percentages were obtained with the CMgrp consortium, which fluctuated from 15.44% (in var. Catuaí) to 34.32% (in var. Garnica); the latter was the variety that best responded to the inoculation with the CMgrp consortium. Although the colonization percentages were lower than those obtained with the mycorrhizal consortium, R. aggregatus originated significant values of 9.7% in the var. Garnica and 23.5% in the var. Catimor - the variety with the best response to inoculation with R. aggregatus (Table 2).

Table 2: Efficiency of Rhizophagus aggregatus mycorrhizal-coffee symbiosis and phosphorus availability. 


Mycorrhizal inoculant

Mycorrhizal colonization

Mycorrhizal efficiency

Available phosphorus by mycorrhization

- - - - - - - - - - - - - - - % - - - - - - - - - - - - - - -


R. aggregatus









R. aggregatus









R. aggregatus









R. aggregatus








Several studies have shown the mycorrhizal dependence on coffee plants, above all on less fertile soils. Tristão et al. (2006) mentioned that for these plants mycorrhizal symbiosis is extremely important, especially in soils where conditions are unfavorable - hydric stress, high salt content, degraded and contaminated soils.

Efficiency of the different inoculants is one of the parameters that should be considered when selecting them for their use in coffee plants, taking into account different examples, such as Gigaspora margarita (Tristão et al., 2006), Rhizophagus intraradices (Ibarra-Puón et al., 2014), and mycorrhizal consortia (Del Aguila et al., 2018).

Despite mycorrhizal colonization percentage is one of the most measured variables, it does not guarantee an increase in the plant morphological and physiological variables. An example that supports this argument may be observed in Aguirre-Medina et al. (2011) where at 90 DAS, the colonization percentage in the treatments with Glomus intraradices did not go beyond 18%; however, the increase in dry biomass compared with the control was 307 and 116% in phosphorus content.

Current data reported by Del Aguila et al. (2018) highlighted mycorrhizal colonization from 13-31.3% and increments with respect to the control for the dry biomass variable (root and leaf) 566%; whereas Adriano-Anaya et al. (2011) obtained colonization percentages from 6.6-16.3% in inoculated plants and increments of 41.3% (root) and 17.3% (leaves) compared to the control for the dry weight variable. The previous results are justified because growth, development, and yield of the cultivation depend on mycorrhizal efficiency. To this respect, Aguirre-Medina et al. (2011) quoted that the initial establishment of the AMF in coffee plants may be slow, which is why its effect on plant development promotion responds in the same manner.

Mycorrhizal efficiency

The CMgrp consortium promoted the greatest mycorrhizal efficiency percentage in the four coffee varieties with intervals from 333% in var. Catuaí to 1670% in var. Caturra, compared to non-treated plants (control). The fungus R. aggregatus, originated values from 13% (in var. Garnica) to 610% (in var. Caturra) (Table 2). The beneficial response of the AMF is defined as effectiveness; this capacity promotes plant growth and is determined by the species diversity used and origin of its isolation (Trejo et al., 2011). Coffee plants establish mycorrhizal symbiosis naturally; their efficiency depends on the fungus species, plant (variety), environment, substrate (Rivera, 2010), and soil (nutrient content, mainly phosphorus) (Gadea and Peña, 2013).

In this study, the var. Caturra obtained the greatest mycorrhizal percentage, which was reflected in the highest values for coffee plants for the variables plant height (4.79 cm), dry biomass (4.73 g) and average values in phosphorus content (0.13 mg kg-1) (Figures 1, 2, 3). With these results, we may conclude that the mycorrhizal CMgrp consortium promoted growth, development, and phosphorus absorption in plants.

Assessing mycorrhizal efficiency in this research study was relevant because the best symbiosis plant-fungus (Garnica-CMgrp and Caturra-CMgrp) was found between two mycorrhizal inoculants and four coffee varieties of economic importance for Mexico. To this respect, Tristão et al. (2006) mentioned that in coffee plant production, locating the mycorrhizal fungi that show elevated efficiency, greater competitiveness, and soil adaptation is a priority.

Available phosphorus by mycorrhization

The greatest available phosphorus percentages (260-1651%) by mycorrhization for the four coffee varieties were obtained with the CMgrp consortium. The inoculant R. aggregatus also originated important percentages (24-614%); both inoculants responded better in the var. Caturra (Table 2). The mycorrhizal inoculants used in this research study favored phosphorus translocation since the content of this element in leaves was greater than in the inoculated plants (Figure 3).

The available phosphorus percentage variable by mycorrhization was determined to find the most efficient fungi for a host to increase its efficiency in nutrient absorption, consequently reducing inorganic fertilizers in field. Balota et al. (2011) mentioned that inoculated plants with mycorrhizal fungi showed greater efficiency in the use of phosphorus in root, which means greater P capture and its transference. Rivera (2010) quoted that to achieve an effective mycorrhization in coffee plants and in soils, it was necessary to inoculate an efficient arbuscular mycorrhizal fungus. Therefore, searching for the best plant-fungus symbiosis is necessary to guarantee growth and develop healthy and vigorous plants.

Plant health

Table 3 shows the Em, Index and the varieties Garnica, Catimor, and Caturra with the lowest harm indices - showing values close to 0 according to the scale from 0.14 +/- 0.24 established - when they were inoculated with the CMgrp consortium. Although the var. Catuaí had values closer to 1 with the CMgrp, it showed differences when compared with the control. Evidently, the effect of a monospecific inoculant, as R. aggregatus, reported lower Em indices than the control. The Em indices for chlorosis did not report differences in the var. Catuaí, which showed a similar health tendency as the other varieties and the mycorrhizal inoculants.

Table 3 Index Em in four coffee varieties by the effect of two mycorrhizal inoculants. 


Mycorrhizal inoculant

Index Em




R. aggregatus










R. aggregatus










R. aggregatus










R. aggregatus









The subjective scales were used as a tool to assess some variables without destroying the plants; similar classes or scales have been adopted in mycorrhizal symbiosis studies (Sieverding, 1991; Rosendahl and Rosendahl, 1991; Raghavendra-Kumar et al., 2018; Ren et al., 2018).

This study normalized the data obtained in the subjective scale, which allowed developing the Em Index that demonstrated a similar tendency to quantitative data (Figures 1, 2, 3); the results showed that the production of coffee plants inoculated with the CMgrp consortium experienced less harm by P. costarrisensis, which has also been demonstrated by several authors who pointed out that the presence of mycorrhizal fungi granted plants tolerance or resistance to harm by pathogens (Plouznikoff et al., 2019; El-Sharkawy et al., 2018; Trejo Aguilar et al., 2018). The data obtained in this study show that not all the varieties responded to the mycorrhizal inoculation, so other coffee varieties should be assessed in future studies.


- The highest colonization percentage was obtained in the var. Garnica, but the greatest mycorrhizal efficiency and available phosphorus percentage were obtained in the var. Caturra. The Em, Index showed that the coffee plants inoculated with the CMgrp consortium showed the least damage.

- The use of the mycorrhizal consortium formed by the fungi Glomus claroides + Rhizophagus diaphanus + Paraglomus albidum (CMgrp) increased the variables plant height, dry biomass, and phosphorus content compared with the non-inoculated plants. The mycorrhizal efficiency in coffee plants should be taken into account when choosing an inoculant with respect to the plant variety. For the var. Caturra, the inoculant with the greatest efficiency with respect to available phosphorus was the CMgrp consortium. Therefore, the consortium should be used in the varieties Catimor, Garnica, Catuaí, and Caturra rather than the use of one inoculant only, as in the case of Rhizophagus aggregatus.


Authors want to thank H.F. Coronel-Brizio for his collaboration with the data analysis and his suggestion to use the Mycorrhization Efficiency Index.


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Recommended citation:

Hernández-Acosta, E., D. Trejo-Aguilar, A. Rivera-Fernández y R. Ferrera-Cerrato. 2020. La micorriza arbuscular como biofertilizante en cultivo de café. Terra Latinoamericana Número Especial 38-3: 613-628. DOI:

Received: October 14, 2019; Accepted: December 13, 2019

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