Contribution of mycorrhiza and phosphate-solubilizing fungi in coffee seedling growth in four soils with different fertility conditionsABSTRACT
Phosphorus (P) is a limiting nutrient for coffee seedlings. To meet this requirement, coffee growers usually apply di-ammonium phosphate (DAP), which is highly sensitive to local price fluctuations. The use of arbuscular mycorrhizal fungi (AMF) and phosphate-solubilizing fungi (PSF) has been recommended, but the results derived from their application are inconsistent and uncertain, depending on soil fertility status. The response of AMF and PSF application in the plant growth of coffee seedlings during the nursery stage was evaluated in four non-sterile soils, which represent the most abundant type of soils in the coffee regions of Colombia: Eutropept, Dystropept, Fulvudand, and Ultisol. The treatments included a commercial AMF inoculum, PSF-Phlebia subserialis-CH4, and a consortium of AMF+PSF, at four P levels (0, 0.5, 1, and 2 g.plant-1 P2O5) using DAP fertilizer. Shoot dry weight (SDW) was affected by P applications in Fulvudand. In the other soils, a P-response occurred with 0.5 g.plant-1 , whereas 1 and 2 g.plant-1 of P2O5 caused a significant reduction in SDW. AMF increased SDW by 40% in Eutropept. The negative effect of higher P amounts was mitigated (> 70%) through PSF and AMF+PSF in Ultisol and Eutropept, respectively. In plants in which microorganisms increased SDW, the P concentration was 0.17 to 0.22%. The plant growth promotion of coffee seedlings during the nursery stage with AMF and/or PSF applications varied according to soil type and P amounts applied.
Key words
Coffea arabica
; di-ammonium phosphate; mycorrhizal colonization; P-fertilization; P-solubilizing
Introduction
Phosphorus (P) is a limiting nutrient for coffee during the nursery stage (Avila-Reyes et al. 2007). Plant requirements are usually met by soluble P fertilizers such as di-ammonium phosphate (DAP) or mono-ammonium phosphate (MAP), generating effective and reproducible results in promoting plant growth (Sadeghian 2008). Despite their recognized effectiveness in coffee, new alternatives are necessary to promote P fertilization as a cost-effective and environmentally friendly option (Bindraban et al. 2015), due to these fertilizers have shown high sensitivity to the international market in the short term (Alewell et al. 2020). Moreover, the use of strong acids in their industrial production, coupled with the negative effects derived from the excessive use of P fertilizers, can cause serious environmental problems (Belboom et al. 2015, Micha et al. 2023).
According to the last situation, the substitution of synthetic P-fertilizers with biotechnological alternatives has been an ongoing exploration. In this context, phosphate-solubilizing microorganisms, particularly fungi (PSF), may be part of this strategy, as they are naturally found in coffee soil conditions in Colombia (González-Osorio et al. 2020). Unlike bacteria, which lost their ability to solubilize P on serial subculturing, fungi have long-term P solubilization capabilities, and their hyphae can cover a large contact area and soil volume, while bacteria do not (Whitelaw 2000). Additionally, the effectiveness of fungi increases, particularly when organic matter conditions are high (Zhang et al. 2020). As a result of their oxidative respiration and fermentation of soil carbonaceous compounds (Wyciszkiewicz et al. 2016), these organisms can generate low molecular weight organic anions, which can release P bound in the soil solid phase, increasing its availability in the soil solution (González-Osorio 2018)1. On the other hand, the hyphae of arbuscular mycorrhizal fungi (AMF) establish symbiosis with coffee (Beenhouwer et al. 2015, Bolaños et al. 2000, França et al. 2014, Lebrón et al. 2012, Sewnet and Tuju 2013, Suparno et al. 2023) and work as an extension of plant roots (Andrade et al. 2009, Hernández-Acosta et al. 2021), allowing coffee to acquire different resources beyond the reach of roots without AMF (Silveira et al. 2023, Zhang et al. 2017). This perspective reveals that an adequate use of these microorganisms can promote the nutrition and growth of coffee plants.
Despite this approach, it is well known that the dual or individual applications of PSF or AMF to substitute or complement synthetic P-fertilizers have sometimes generated promising results in greenhouses or in-vitro conditions, but there are controversial and inconsistent outcomes when applied in agricultural production systems (Roth and Paszkowski 2017, Wang et al. 2017). This behavior could be associated with the low quality of inoculants (Díaz-Urbano et al. 2023) and soil fertility status, specifically the limited availability of carbon and P, both essential for the PSF and AMF metabolic processes (González-Osorio et al. 2020, Moreira et al. 2019, Mortier et al. 2023). Additionally, in a biological context, microbial formulations usually develop different levels of effectiveness due to their competition with native soil biota (Blažková et al. 2021, Sarkar et al. 2021).
Taking into account the prominent role of P in coffee growth, the significant dependency on synthetic P-fertilizers, the need to reduce production costs, and the imperative to comply with international regulations on fertilizer use, which prescribe minimal pollution from both production and application of fertilizers (Chojnacka et al. 2020, Escribà-Gelonch et al. 2023), our research aimed to evaluate the response of coffee seedlings during the nursery stage to P-fertilization complemented by AMF and PSF. Thus, our hypothesis was that the effect of AMF and/or PSF on coffee growth promotion during the nursery stage varies according to soil type and the amount of P applied.
MATERIALS AND METHODS
The study was conducted at the soils laboratory and facilities of La Granja, part of the National Coffee Research Center (Cenicafé), Plan Alto district of Chinchiná, Colombia (5°15’34”N, 75°15’34”W, and altitude of 1,430 m). Four representative soils from the Colombian coffee-growing region were selected (Eutropept, Dystropept, Fulvudand, and Ultisol), characterized by varying levels of P and organic matter content (Table 1). The soils were left untreated to preserve their native biological diversity.
For each soil, 16 treatments were evaluated (Table 2), derived from different combinations of four P amounts (0, 0.5, 1, and 2 g.plant-1 of P2O5), the AMF commercial inoculum composed of Rhizoglomus sp., Acaulospora sp., Scutellospora sp., and Entrophospora sp.; the PSF Phlebia subserialis strain CH4 (Cenicafé collection); the AMF+PSF combination; and a control without P-fertilization, AMF, or PSF.
The experimental unit consisted of a coffee seedling (70 days after germination), planted in a black plastic bag (size 13 cm × 23 cm), filled with 1.24 dm3 of soil. Each treatment had 15 replicates in a factorial arrangement of 4 × 3 + 1 (four P dosages, three microorganisms including the AMF+PSF combination, and a control without P-fertilization, AMF, or PSF).
Procedure for applying all treatments
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AMF application: A commercial inoculum was applied at a rate of 10 g per plant into the planting hole, ensuring a minimum of 300 spores per gram of inoculant;
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PSF application: P. subserialis-CH4 was transferred aseptically into Petri dishes containing potato dextrose agar (PDA) medium. After verifying its macroscopic and microscopic characteristics, the fungal strain was cultivated in rice (at 1×108 spores.mL-1). Once the strain achieved over 95% germination of spores, a fungal suspension containing 1×108 spores.mL-1 in water was prepared. Each coffee plant received 10 mL of suspension, once the coffee plants had their first pair of fully expanded active photosynthetic leaves (15 days after transplanting). A second application was carried out after 60 days using the same PSF concentration;
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P-fertilization: DAP 18-46-0 fertilizer was applied to the surface of the soil on the 20th day after transplanting.
At harvest (five months, according to the recommendation for the Colombian coffee zone), mycorrhizal colonization in fine root fragments was determined using the grid-line intersection method by Giovannetti and Mosse (1980) on seven out of the experimental units. Shoot dry weight (SDW), the response variable, was evaluated for all plants (100%) after oven-drying the samples at 60°C for 96 hours. The soil P level was evaluated by Bray II methodology, at the end of the experiment, taking a compound sample of soils by each treatment. Additionally, P concentration in plant tissue was measured using the molybdenum blue method (Murphy & Riley 1962) for five out of 15 of the experimental units.
For each soil and treatment, data were analyzed using descriptive statistics to determine the average and variation of the response variable. The effects of microorganisms and P levels were evaluated using analysis of variance (ANOVA) based on a factorial 4 × 3 + 1 design for each soil type. Significant results at the 5% level in the ANOVA were further analyzed using Dunnett’s test to compare treatments with the control. All statistical analyses were performed using SAS version 9.4 (2016 by SAS Institute Inc., Cary, NC, United States of America).
RESULTS
Soil phosphorus level
P applications via fertilization resulted in varying soil concentrations depending on the soil type and amount of P fertilizer applied (Table 3). Across all soils evaluated, P soil levels ranged from 112 to 166 mg.kg-1 with applications of 0.5 g.plant-1 of P2O5, and averaged 353 mg.kg-1 with 2 g.plant-1 of P2O5.
The results are presented by soil type to measure the effect of microorganisms and P dosage on P fertilization, without focusing on comparing responses between different soils.
In Eutropept, P concentration in the control was 32 mg.kg-1. Applications of 0.5 and 1 g.plant-1 of P2O5 raised soil P levels to 166 and 232 mg.kg-1, respectively. The highest P application (2 g.plant-1) increased soil P to around 307 mg.kg-1 (Table 3). In Dystropept without P fertilization (control), P concentration was 5 mg.kg-1. Applications of 0.5 g.plant-1 of P2O5 increased soil P to 146 mg.kg-1, while 1 and 2 g.plant-1 of P2O5 raised soil P concentrations to 206 and 227 mg.kg-1, respectively. For Fulvudand, the average soil P concentrations were 112, 205, and 571 mg.kg-1 in response to P dosages of 0.5, 1, and 2 g.plant-1 of P2O5. Finally, the Ultisol initially had 1 mg.kg-1 of P in soil without P fertilization, and, then, significant increases were observed with P applications, resulting in soil P concentrations of 129, 201, and 306 mg.kg-1, respectively.
Coffee growth
In Eutropept, Dystropept, and Fulvudand, coffee growth, in terms of SDW, responded variably to AMF and/or PSF depending on the P supply. This interaction was significant (p < 0.001). In Ultisol, the interaction was also significant at p = 0.046. Effects and interactions were analyzed using a generalized linear model with a gamma response distribution and log link function. Model assumptions were tested and verified at a 95% confidence level.
In Eutropept with a P level of 32 mg.kg-1 in the control, AMF applications increased SDW by an average of 40%. At 0.5 and 1 g.plant-1 of P2O5, microorganisms did not show an additive effect on SDW, while the highest P dosage (2 g.plant-1) caused reduction in SDW, which was mitigated by 77% when AMF+PSF were applied (Fig. 1). Under Dystropept conditions, SDW increased in response to P fertilization, but no additive effect from the microorganisms was evident (Fig. 1). Conversely, all biotechnological alternatives tested reduced SDW by 47% at 0.5 g.plant-1 of P2O5; and at 1 and 2 g.plant-1 of P2O5, SDW was lower compared to P fertilization alone.
In Fulvudand, applications of PSF and AMF+PSF without P fertilization reduced SDW by 40%. Similar responses were observed with 1g.plant-1 of P2O5, complemented with PSF. In Ultisol, SDW was only improved with the lowest P amount applied, while applications above 1 g.plant-1 of P2O5 decreased SDW. In this soil, negative effects from higher P doses were mitigated by PSF applications (Fig. 1).
These findings indicated that the response of biotechnological alternatives to promote coffee seedling growth during the nursery stage varies according to soil type and the amount of P applied via fertilization.
Shoot dry weight (SDW) of coffee seedlings in response to AMF, PSF and AMF+PSF applications, at different P-soil levels in Eutropept (a), Dystropept (b), Fulvudand (c), and Ultisol (d). Bars indicate standard error. The asterisk indicates highly significant differences compared the control, according to the Dunnett’s test (p<0.0001)
Arbuscular mycorrhizal fungi colonization
AMF colonization in plant roots was assessed across different soils and treatments. In the control (native colonization), average colonization rates were 49, 23, 22, and 9% for Eutropept, Ultisol, Dystropept, and Fulvudand, respectively (Fig. 2). Overall, native colonization improved by 28–41% with 1 g.plant-1 of P2O5 in Eutropept and Ultisol. In Dystropept, native colonization was consistent across different P amounts applied.
In Fulvudand, where native colonization was absent in the control, it ranged from 10–16% at 0.5 g.plant-1 of P2O5. Conversely, when AMF commercial inoculum was applied alone or combined with PSF, colonization rates were lower than native levels in Eutropept, Ultisol, and Dystropept, especially in treatments with P fertilization (Figs. 2a, 2b, and 2d). In Fulvudand, where all treatments resulted in lower plant growth responses, native colonization rates were also lower and ranged two to four-fold compared to other soils, particularly at lower P amounts (Fig. 2c).
Plant phosphorus concentration
The P concentration in plants exceeded 0.15% in all treatments and soils evaluated (Table 4). Due to the plant P concentration could not be fully explained by the treatments, several trends emerged.
AMF colonization in roots of coffee seedlings at different P-soil levels in Eutropept (a), Dystropept (b), Fulvudand (c) and Ultisol (d). Bars represent strandard error
For Eutropept, plants grown with AMF without P fertilization averaged 0.18% P concentration. Similarly, plants treated with the highest P fertilization dosage (g.plant-1 P2O5) supplemented with AMF+ PSF had a P concentration of 0.17%. For all other treatments, the average P concentration was 0.22%. In Ultisol, plants averaged a P concentration of 0.19%, but, in treatments in which P fertilization combined with PSF achieved the best response in SDW, P concentration was 0.17%. Finally, while in Dystropept, P concentration in plants ranged from 0.21 to 0.31% (Table 4). In Fulvudand, soil showed the lowest response magnitude in SDW due to the treatments, P concentration in plants ranged from 0.18% (without P fertilization) to 0.29% in the treatment (HMA+PSF).
DISCUSSION
Soil phosphorus level
The highest P concentrations observed at harvest (five months) were attributed to two main factors. Firstly, the application of 1 to 4 g of DAP (18-46-0) was necessary to achieve the evaluated P2O5 levels, resulting in elevated P-fertilizer concentrations in the soil within the plastic bags. Secondly, Colombian coffee soils typically exhibit low P mobility within the soil profile, as discussed by Sadeghian et al. (2015).
This behavior was evident even at lower P applications (0.5 g.plant-1 P2O5), aimed at raising native soil P levels to approximately 30 mg.kg-1, a range suggested in the literature as adequate for effective AMF applications under Colombian soil conditions (González-Osorio et al. 2022). Therefore, according to our results for evaluating the relationship between microorganism applications (especially AMF) and P-fertilization, P levels below 0.5 g.plant-1P2O5 should be considered, particularly when working with bags containing 1.24 dm3 of soil.
Coffee growth
The optimal SDW response of coffee plants was achieved with a single dosage of 0.5 g.plant-1P2O5 (approximately 1 g of DAP). This finding suggests a potential new recommendation for an appropriate P dosage for coffee seedlings grown in bags filled with 1.24 dm3 of soil (size 13 cm × 23 cm). Conversely, higher P doses (2 g.plant-1) had a negative impact on SDW. Recommendations for coffee seedling fertilization have evolved over time to enhance resource efficiency for coffee growers. For example, Salazar-Arias (1977) recommended 4 g.plant-1 of P2O5 for coffee seedlings planted in bags with 2.1 dm3 of soil (size 17 cm × 23 cm), whereas Sadeghian and Ospina-Penagos (2021) recently suggested 1 g.plant-1 of P2O5 for bags with 1.7 dm3 of soil (size 15 cm × 22 cm).
The effects of P fertilization, combined with biotechnological alternatives, elicited varying responses in plant SDW: the positive response of AMF in Eutropept may be attributed to the initially low P concentration in the control (native P), which was 32 mg.kg-1. At this soil P level, the AMF-plant symbiosis promoted better growth of coffee seedlings (SDW). This observation contrasts with the lack of positive AMF response in other soils (P levels ranged from 1 to 8 mg.kg-1), indicating that a P soil status (P-Bray II) concentration < 8 mg.kg-1 represents a very low sufficiency level of P for both AMF and plant. Therefore, the effectiveness of AMF in promoting SDW in coffee seedlings may occur within P-available levels between 8 and 32 mg.kg-1. These results align with those of Jaramillo and Osorio (2009) and González-Osorio et al. (2022), in which effective coffee growth responses to AMF inoculation during the nursery stage were observed at soil solution P levels of > 0.1 and < 0.2 mg.L-1. These values, as reported by González-Osorio (2018), correlate (R2 > 98%) with P-Bray II levels ranging from 9 to 30 mg.kg-1 in different Colombian coffee zone soils.
Based on all the aspects that have been in consideration, it is possible to find controvertial in the results that using AMF formulations complemented with the current P-recommendation for coffee seedlings in Colombia. Sadeghian and Ospina-Penagos (2021) registered a low magnitude of response to a commercial AMF inoculum, applied at 0, 1, and 2 g.plant-1 of P2O5 in seedlings planted in plastic bags with 2.1 dm3.
Conversely, the positive responses of PSF in Ultisol, as well as PSF+AMF in Eutropept, highlight the role of this fungus in P solubilization, particularly in scenarios where 1 and 2 g.plant-1 of P2O5 applications resulted in soil P concentrations above 200 mg.kg-1. The favorable SDW results in plants may be attributed to two metabolic processes of PSF, as described in their dynamic growth by González-Osorio et al. (2022). According to these authors, P. subserialis-CH4 has demonstrated a significant ability to reduce culture medium pH (> 2.8 units) while simultaneously saturating it with organic anions, potentially replacing insoluble P anions and making them available to plants.
In environments where excess P from fertilization occurs, precipitation of P fertilizer may surpass its solubility limit. Consequently, P solubilized by PSF may precipitate rapidly, necessitating AMF hyphae to facilitate P acquisition by plant roots. This phenomenon explains the additive effect of the AMF-PSF consortium in SDW of plants in Eutropept under higher DAP applications. Moreover, SDW without AMF and/or PSF was negatively affected from P fertilization due to a possible saline effect, which can cause damage to coffee plant tissues (Sadeghian and Zapata 2014) or impeding calcium availability, which is essential for coffee seedlings inoculated with AMF (Orozco 1988).
The interaction between AMF and PSF in promoting coffee growth has been underexplored. Notably, research by Perea Rojas et al. (2019) focused on promoting coffee growth in sterile soil using four PSF consortiums (Aspergillus niger and Penicillium brevicompactum) and AMF (native) + PSF, which similarly increased SDW in the studied plants. In contrast, the negative effects on SDW observed in Dystropept from microorganism applications may be associated with other physicochemical soil characteristics or soil pollutants, which were not analyzed in the current study, but are known to limit soil fertility and the efficacy of microorganisms applied to enhance plant nutrition (Díaz-Urbano et al. 2023, Jiang et al. 2023, Lara-Capistran et al. 2021).
Arbuscular mycorrhizal fungi colonization
The high percentage (between 15 and 42%) of native AMF colonization in the control (without commercial AMF) found in Eutropept, Dystropept and Ultisol evidences that coffee plants stablish a multi-specific and spontaneous association with these fungi, such is showed by Cogo et al. (2017) and Hernández-Acosta (2021). Nevertheless, not all of AMF species participate in the same physiological way within its host. It has demonstrated that some AMF work in process associated to growing and coffee nutrition (Orozco 1988), instead of other species, participates controlling pathogens like Black (Rosellinia) root rot, and nematodes, which cause damage to the roots system (Rivillas et al. 2019). In general, it was found, while in Fulvudand the native colonization of AMF was null and it was increasing by application of the treatments, in Eutropept, Dystropept and Ultisol, the native colonization was effected negatively by AMF commercial.
Based on the last considerations, an evaluation to AMF colonization focused on predominance of vesicles, spores, mycelium, and arbuscules on the roots colonized provides better arguments, considering those structures work in different metabolic ways and process (Facelli et al. 2010). Namely, while the mycelium and the arbuscules are recognized as structures for exchanging nutrients between AMF-host, the vesicles are storage bodies, that facility the symbiosis (Luginbuehl and Oldroyd 2017).
This functional difference in response to environmental conditions can explain the agronomic results using native or commercial AMF inoculum. Based on the last aspects, a development of biotechnological alternatives in the laboratory must be encouraged to maintain these similar soil conditions where the inoculum will be applied. In our case, to achieve the objectives, as a minimal condition, there must be a medium limited on P availability, such as occurred during PSF production, which had effectively solubilizing phosphoric rock in vitro, and it was equally effective solubilizing P accumulated by higher P amounts applied.
Plant phosphorus concentration
Phosphorus concentration in plants was between 0.17 and 0.2%, in those in which the biotechnological alternatives generated response. In the other treatments, the P concentration has a maximum average of 0.34%, indicating in this way a high level of sufficiency of this nutrient. Low P levels in those plants in which the microorganisms applied promoted SDW may be associated to the dilution effect, which the nutrient concentration could decrease for increasing on the plant biomass or specific plant tissue (Sadeghian et al. 2013). According to our results, and considering a positive response on SDW on plants derived from the microorganisms evaluated, it is possible that the biotechnological alternatives studied can ameliorate indirectly other process that explain the plant development, among them the photosynthesis rate, the stomatal conductance, and the efficient use of water (Cruz et al. 2020).
CONCLUSIONS
The effect of AMF and/or PSF to promote the growth of coffee seedlings during the nursery stage varied according to soil evaluated and its P-level content.
Plant growth promotion of coffee seedlings to AMF application may be at P-soil level (Bray II) between 8 and 32 mg.kg-1.
An excessive effect derived from P-fertilization, which affected negatively SDW of plants, was amended through of applications of PSF and AMF+PSF.
ACKNOWLEDGMENTS
The authors wish to thank the Colombian coffee growers – Federacion Nacional de Cafeteros de Colombia; and Centro Nacional de Investigaciones de Café.
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How to cite: González-Osorio, H., Sadeghian, S. and Mira, B. E. (2025). Contribution of mycorrhiza and phosphate-solubilizing fungi in coffee seedling growth in four soils with different fertility conditions. Bragantia, 84, e20240171. https://doi.org/10.1590/1678-4499.20240171
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FUNDING
Centro Nacional de Investigaciones de Café – Federación Nacional de Cafeteros de ColombiaGrant No.: SUE-104036
DATA AVAILABILITY STATEMENT
Data will be available from the corresponding author on reasonable request.
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