ARTÍCULOS DE REVISIÓN

Experiences on the propagation and efficacy of arbuscular mycorrhizal fungi in Latin America

Experiencias sobre la propagación y efectividad de los hongos micorrizógenos arbusculares en Latinoamérica

Esquivel-Quispe, Roberta; Quispe-Ochoa, Josue Olser; Hernández-Cuevas, Laura Verónica

Esquivel-Quispe, Roberta

roberta.esquivel@unsch.edu.pe

National University of San Cristobal de Huamanga Perú

Quispe-Ochoa, Josue Olser

National University of San Cristobal de Huamanga Perú

Hernández-Cuevas, Laura Verónica

Autonomous University of Tlaxcala México

Journal of the Selva Andina Biosphere

Selva Andina Research Society, Bolivia

ISSN: 2308-3867

Periodicity: Bianual

vol. 9, no. 2, 2021

directoreditorbiosphere@gmail.com

Received: 01 May 2021

Accepted: 01 October 2021

Published: 01 November 2021

URL: http://portal.amelica.org/ameli/journal/71/712918712918008/

DOI: https://doi.org/10.36610/j.jsab.2021.090200099x

Selva Andina Research Society

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Abstract: Arbuscular mycorrhizal fungi (AMF) have great potential to contribute to the solution of multiple problems in agriculture, they are used in agricultural production in the form of bioprotectors, bioregulators, restoratives and other benefits. Mycorrhizal plants present higher values in height, biomass and performance; because the mycelial network is more efficient to avoid nutrient deficiency. AMF propagate in host plants that have the greatest capacity to establish arbuscular mycorrhizal symbiosis; among them it is mainly from the Poacea family and legumes. The host plants are planted in pots containing sterilized substrates of pH 5.2 to 7 and a low phosphorous source, conducted under greenhouse, laboratory or nursery conditions for an average period of six months. The study of mycorrhizae is scanty, the objective of this review compiles experiences on the effect of types of substrates, and hosts that favours the propagation of AMF, which can be used by researchers who are interested in recovering the deteriorated agroecosystem, mitigating pollution and contributing to quality food.

Keywords: Substrates, hosts, propagation of arbuscular mycorrhizal fungi, effectiveness, bioinoculants.

Resumen: Los hongos micorrizógenos arbusculares (HMA) tienen gran potencial para contribuir a la solución de múltiples problemas de la agricultura, son utilizados en la producción agrícola en forma de bioprotectores, biorreguladores, restablecedores y otros beneficios. Las plantas micorrizadas presentan mayores valores en altura, biomasa y rendimiento, porque la red micelial es más eficiente para evitar la deficiencia de nutrientes. Los HMA, se propagan en las plantas hospederas que tienen mayor capacidad de establecer la simbiosis micorrizógena arbuscular, entre ellas es principalmente de la familia Poacea y leguminosas. Las plantas hospederas se siembran en macetas que contienen sustratos esterilizados de pH 5.2 a 7 y fuente de fósforo bajo, conducidos en condiciones de invernadero, laboratorio o vivero, por un tiempo promedio de seis meses. El estudio de las micorrizas es poco, más aún sobre la propagación es muy escasa, motivo por la cual, el objetivo de esta revisión es recopilar experiencias sobre tipos de sustratos y hospederos que permiten la propagación de HMA, la cual puede ser útil y empleada por los investigadores que se interesan por recuperar el agroecosistema deteriorado, mitigar la contaminación y contribuir a la alimentación de calidad.

Palabras clave: Sustratos, hospederos, propagación hongos micorrizógenos arbusculares, efectividad, bioinoculantes.

Introduction

Agronomic production face overuse of chemical fertilizers which conducts to environmental pollution 1-4 , degradation of soils, in addition to increasing production costs. This leads to search sustainable production systems through use of beneficial microorganisms also known as biofertilizers 2- ⁴ , such as arbuscular mycorrhizal fungi (AMF). These fungi improve the soil productivity decreasing the use of synthetic fertilizers alleviating the environmental damage 1,5-9 .

AMF belong to the Phylum Glomeromycota, which establish arbuscular mycorrhizae with diverse plants groups 5,10 , forming mutualistic associations with most families of plants 5,11-13 .

Unlike helpful bacteria that could be isolated and propagated on artificial culture media, the AMF cannot, needing live plants which constitutes the most important limitation for using them. The scarce information about the more favorable substrates and hosts plants for propagation of spores and other propagules in Latin America, was the principal incentive to do this review. The objective is to compilate the experiences about the propagation of AMF with different substrata, and hosts, and the effectiveness of them in Latin America, to provide useful information to researchers interested in the recovery of degraded agroecosystems, alleviation of environmental pollution, and achievement of quality food.

Development

AMF form arbuscular mycorrhiza into the roots of more than 80 % of plants 5-7,11,12 , fungi get carbohydrates, plus an appropriate habitat to accomplish their life cycle thanks to the association, contributing to improve nutrimental status and hydration of hosts plants, phytopathogens protection, besides solubilization and easy absorption of soil nutrients, contributing to ecosystems stability 5-7,14 .

The deterioration of agroecosystems produces the need to recover them. Biofertilizers such as AMF could be used to achieve that purpose, improving the efficiency of biological processes in soils and plants. However, information about the better substrates for propagation is scarce. This is crucial to achieve the production required for intensive and extensive use of bioinoculants. The organic and biological fertilization sources have important potential use, efficiently providing nutrients and contributing to diminish economic costs during agronomic management, this promotes synthetic fertilizers substitution, and positive impacts on economy, society and environment 15,16 . Provide information about the AMF propagation that favors and helps the development of strategies to improve this kind of bioinoculants propagation is vital. The use of AMF could be one of the most appropriate methods to greenhouse sustainable cultivation of guava 17 , and conservation of threat wild species such as Andean magnolias, key plants to recover naturally deteriorated Andean forests 18 . Also important is its use on seashores rehabilitation 19 . Those are examples of the ecologic and economic importance of these fungi 20 .

Effectiveness of the AMF. In Cuba, biofertilizers such as AMF have been effective to substitute mineral fertilizers ¹ , promoting its use in conjunction with organic manures with good results ¹ . The reduction or substitution of inorganic fertilization using AMF is a viable practice that favors profitability and ecologic conservation of production systems 21, ²² .

In Musa AAA cv. Gran Enano (banana) in Colombia, the use of 15 AMF inoculum from banana agroecosystems produced the highest foliar and radical weights ²³ . In mixed culture of Lolium multiflorum and Pisum sativum in Peru, greenhouse mycorrhization favored the highest foliar dry weigh and plant size. The use of EcoMic® and Quito Max bioinoculants, alone and together, increased the production of Zea mays versus that of not inoculated plants ²⁴ .

The role of arbuscular mycorrhiza to solve many agronomic problems at tropical environments show its great potential as biofertilizers. Nevertheless, it is important to know that the effects produced by arbuscular mycorrhiza are not the same for all the cultured plants or trees, neither for all climatic conditions, the interactions that these fungi establish with other microorganisms are in part responsible for that. AMF could be inoculated as bioprotectors and bioregulators at nursery or rooting of vitroplants, being for several plants an invaluable alternative to solve micropropagation, acclimatization and nutrition problems 14, ²² . The positive effect of AMF is evident on dry aerial biomass because the inoculated treatments mostly produce the better values, being significatively different from not mycorrhizated 16 . The production of AMF mycelial network starting from the roots of host plant seems the most efficient and less expensive strategy to get those responses, through hyphal network the fungus explored more soil volume than thinner roots, reaching the smaller spaces, in addition to the AMF efficient physiological mechanisms for nutrients assimilation.

The dual action of AMF that increase the absorption of soluble phosphates, along the role of solubilizing phosphate fungi (P) promotes the solubilization of insoluble phosphate complexes, benefiting the Lactuca sativa nutrition, on this species, the plants inoculated with the AMF fungi Rhizophagus intraradices (Glomeromycota) and not AMF Penicillium thomii (Ascomycota) were significantly higher than not inoculated plants, both fungi on substrata added with phosphoric rocks, in an eight treatments experiment 25 .

On traditional seedbeds of tobacco plants, with the purpose to determinate the influence of AMF and mineral fertilizer reduction 26 , the results showed that agronomic practices applied during two periods reduced the effectiveness of AMF ²⁷ .

Table 1

Effectiveness of the AMF on mycorrhized plants

Mycorrhized plant | Stem height (cm) | Peduncle length (cm) | Dry foliar biomass (g) | Dry root biomass (g) | Reference
Lactuca sativa | not |  | 1.27 |  | 25
Musa AAA cv. Gran Enano | not | not | 0.78-1.417 | 1.750-3.287 | 23
Anthurium andreanum | 4.2 - 4.70 | 18.3 - 23.7 | not | not | 28
Anthurium andreanum | 4.70 | 23.67 | not | not | 28
Zea mays | 23.2 - 35.6 | not | 0.73-1.87 | 0.13-0.29 | 29
Brachiaria decumbens | not | not | 40.8 (g/plant) | not | 30
Begonia sp var. Rex | not | 16 (leaves) | 5.00 | 0.80 | 16
Psidium guajava L (Guayaba) | 9.3-18.8 | not | 0.46-2.02 | 0.4-1.7 | 17

The AMF consortia from Coffea arabica var. Garnica submitted to moderate technological management produced significatively better height and development of plants in nursery and field conditions 31 . AMF inoculated plants of Amelanchier denticulata (tlaxistle) and Eysenhardtia polystachya (sweet stick) had better responses in diameter, height, aerial biomass (p<0.001) and phosphorus content 32 .

The addition of 310.50 g m⁻² (75 %) of mineral fertilizer and 0.50 kg of AMF m⁻² of soil, positively influenced diameter, stem length, fresh and dry biomass, foliar area, and performance of useful tobacco seedlings/m², and increase percentage of mycorrhizal colonization, producing positive economic and environmental effects 26 .

Several results show that agricultural practices negatively affect the AMF, reducing their effectiveness. Then, a decreasing of chemical fertilizers and pesticides along with the AMF inoculation could be used to reduce the ecological deterioration of soil, while reducing production costs ²⁷ .

When evaluating the effect of different doses of the agronomic bioinoculant MicoFert on dry matter (DM) and foliar phosphorus content in Leucaena leucocephala in Cuba, it was found that inoculated plants produced higher content of foliar phosphorus 33 .

On Lolium multiflorum and P. sativum at greenhouse, the AMF positively affected the length and dry foliar biomass, the mycorrhized plants obtained from 21.8 to 30.4 cm, and 69.2 to 82.6 cm heigh, and 13.0 to 16.01 g of dry foliar biomass, respectively.

On tomato (hybrid HA 3108 Hazera), the effects on height, foliar dry matter, final performance and bromatological quality of the fruits, at different doses of AMF, Cubense strain applied through the commercial biofertilizer Ecomic®, and worm humus, alone and combined with the AMF, as mineral nutrition substitutes were evaluated ³⁴ . Only one treatment of inoculation was significant, although all treatments inoculated were numerically better than control. According to above results the application of AMF inoculant was more efficient than worm humus at 25 % of mineral fertilizer.

Substrates for the propagation of AMF. The type of substrate used depends on availability at each place. Next, experiences and results obtained per different searchers are described. Propagation pots were stablished in greenhouse, with 500 g of soil of interest as inoculum source, plus 500 g of the same soil sterilized as substratum 35 . On squash in greenhouse were evaluated the response of compost, vermicompost, tea compost, and vermicompost associated with mycorrhizae. The spores were used to determinate the propagation, using 1 kg of sterilized substratum, plus 200 g of soil sample containing AMF consortia.

On growth of Anthurium plants the influence of different pH values in the substrata, and the effects of biofertilization with AMF were evaluated. The mixture of acidic peat+” cachaza” +zeolite, 6.9 pH produced the better response on mycorrhized treatmens ²⁸ .

Six substrate combinations produced by the addition of banana soil with AMF natives from it, combined with three inert materials, sand, rice husk and vermiculite, at 70/30 and 50/50 volume proportions of each were prepared. pH 5.2, 4.7 % organic matter, 27 mg·kg⁻¹ P, and sandy loam texture were the soil features. The substrata S2 (sand 50-soil 50) and the S6 (vermiculite 50-soil 50) produced the significantly higher responses 23 .

Table 2

Substates and proportions that favor higher multiplication of AMF

Substrate | Proportion v/v | Proportion % or weight | pH | Phosphorus source | Reference
“Terrafertil”-volcanic ash | 1:1 | not | 5.7 | 22.7 mg RP/plant | 25
Soil-sand (S2) | 50 | 50 | 5.2 | 27 mg kg-1 | 23
Soil-vermiculite (S6) | 50 | 50 | 5.2 | 27 mg kg-1 | 23
A (agricultural soil-sand-black soil) | 3:3:2 | not | 6.5 | 0.1% NT | 36
C (uncultured soil) | not | 100 | 7.2 | 0.03% NT | 36
1 (acid peat-“cachaza”-soil) | not | 40:40:20 | 7.0 | 2930 pm | 28
2 (acid peat-“cachaza”-zeolite) | not | 40:40:20 | 6.9 | 3076 pm | 28
3 (acid peat-“cachaza”-rice husk) | not | 40:40:20 | 6.8 | 3028 pm | 28
Sand-soil | 1:1 | not | not | not | 17
SC (sugar cane bagasse)-sand-carbonized rice husk | 1:1:1 | not | 6.6 | 1.1 g k-1 | 37
Soil + rice husk | 2:1 | not |  | Foliar fertilization | 29
Red soil: agricultural soil | 3:1 | not | 4.12 | 10 | 30
Ferralitic leached soil-“cachaza”-rice straw | not | 62:28:10 | 7 | 289 mg.kg-1 | 16

On squash in greenhouse, the response of compost, vermicompost, tea compost and vermicompost associated with mycorrhiza were evaluated. The treatment 4 (75 % river sand+25 % compost+mycorrhizae+tea vermicompost) was set up on vegetative stage, while treatment 6 (75 % river sand+25 % vermicompost+mycorrhizae+tea vermicompost) was set up on reproductive stage ¹⁵ . The response in leaf length, leaves quantity, plant vigor, dry aerial biomass, and root biomass of Begonia var. Rex, and number of AMF spores were determined according to the substrata produced by the mixture of soil, “cachaza” and rice husk, plus AMF application (EcoMic®) ¹⁶ . To propose one substratum appropriate to produce L. sativa in pots, eight treatments were established, combining AMF and phosphate solubilizing fungi (S) plus different materials: 1) substratum, 2) substratum+AMF, 3) substratum+S, 4) substratum+AMF+S, 5) substratum: PR (phosphoric rock)+S, and, 8) substratum: PR+AMF+S. The substrate used had 5.7 pH, and 22.7 mg of PR per plant ²⁵ .

AMF host plants. The AMF need a host plant to complete their development, until now there are not synthetic culture media to isolate and to multiply these fungi in absence of plant roots 30,38 .

Trap crops allow propagation of AMF spores with the morphological features needed to taxonomical identification, also to observe its ontogenetical stages ⁶ . Zea mays (corn) and Leucaena sp. (gourd) have been used as host plants in pots with field soil (500 g/pot) in greenhouse conditions, to obtain newly formed spores, by six months of propagation, watered every third day 10 .

The propagation of native AMF has been achieved using L. multiflorum and P. sativum as host plants. The infective potential of the propagation has been evaluated on corn (Z. mays L.) in greenhouse, through the most probable number (MPN) of infective propagules 27 . Pre-germinated Brachiaria decumbens (B), Pueraria phaseoloides (K), Sorghum vulgare (S) and Tagetes erecta (T) were used as trap crops, for five months plus 15 extra days to promote sporulation 23 .

By their capacity to establish the arbuscular mycorrhizal symbiosis seeds of corn (Z. mays L.), English grass (Lolium perenne L.), and tomato (Lycopersicum esculentum P. Mill.) were selected for propagation. The soil was collected to extract the AMF spores, after two culture cycles of four months each 39 .

Table 3

Main AMF host plant species

Species | Family | Number of plants/pot | Greenhouse/field | Country | Reference
Lactuca sativa | Asteraceae | not | greenhouse | Argentina | 25
Brachiaria decumbens (B) | Poaceae | not | greenhouse | Colombia | 23
Sorgum vulgare (S) | Poaceae | not | greenhouse | Colombia | 23
L. multiflorum | Poaceae | 1 | laboratory | Peru | 36
Zea mays | Poaceae | 1 | laboratory | Peru | 36
Anthurium andreanum | Araceae | 1 | nursery | Cuba | 28
Sorghum bicolor | Poaceae | 9 | field | Brazil | 37
Zea mays | Poaceae | 1 | nursery | Colombia | 29
Brachiaria decumbens | Poaceae | 10 | greenhouse | Honduras | 30
Begonia sp var. Rex | Begoniaceae | 1 | semi-controlled conditions | Cuba | 16
Psidium guajava L | Myrtaceae | 1 | nursery | Mexico | 17

Propagation of AMF species and consortia (spore quantity and colonization %). The AMF inocula are generally propagated using sterilized soil and greenhouse conditions 5, ⁴⁰ , and quantifying the spore number previous extraction through wet sieving 36, ⁴⁰ .

The AMF greenhouse propagation was performed in pots with 500 g, and 200 g of interest soil as inoculum source, plus 1300 g of the same soil, sterilized three days consecutively, for 1 to 1.5 h dairy, at 120 °C and 1.0 kg/cm² of pressure ³⁵ . Propagation pots were established with rhizospheric soil (500 g/pot) in greenhouse conditions, during six months, watered with distilled water every third day, the plants were not watered for 15 days to promote the sporulation at the end of the period 10, ³⁵ .

On Lolium multiflorum (“rye grass”) + P. sativum (“pea”) in greenhouse conditions there were 16 to 43 spores of AMF consortia/g of soil. Papaya cultured on very technical field conditions produced 10.9 spores as MPN of infective propagules 27 , and 8.04 to 12.62 % of colonization.

Contents of 30 and 60 ppm of P reduce the number of spores from 49.9 to 40, and 31 spores, respectively ³⁰ . However, the biomass increases with those doses of P. The P level must be kept low because high concentrations inhibit the development of the vesicular arbuscular mycorrhiza (MVA) 30 .

Table 4

Propagation of AMF species or consortia spore quantity and colonization %

AMF species or genus | AMF consortia | Spore number/100 g | MPN of propagules/cm³ | Colonization % | Direct inoculation/transplant | Reference
Rhizophagus intraradices-Penicillium thomii | R. intraradices – P. thomii | not | not | 26 | transplant | 25
Glomus, Acaulospora and Entrophospora | Glomus, Acaulospora and Entrophospora | 966 - 1618 | not | 49.0 ± 44.8 % | transplant | 23
Glomus sp. | not | 1050-1633 | not | 25-40 |  | 36
Glomus hoi like | not | not | not | not | 5 g per plant | 28
Experiment I Rhizophagus clarus |  | 162+-82.5 | 283 a 350 | not |  | 37
Experiment II Claroideoglomus etunicatum | not | 240 +- 169.7 | 233 a 283 | not |  | 37
Rhizophagus clarus | not | 11.6±10.0 | 28 | not | transplant | 37
Claroideoglomus etunicatum | not | 16.3±7.7 | 8 | not | transplant | 37
Dentiscutata heterogama | not | 0.3±0.5 | 0.3 | not | transplant | 37
Preinoculum of cacao culture 5 g/pot | Glomus, Acaulospora, Entrophospora, Gigaspora, Archaeospora and Scutellospora | 12 - 364/10g | not | 12.16 - 30.5 micelio | direct inoculation | 29
MYCORAL inoculant | Glomus, Acaulospora and Entrophospora | 49.9 (25 mL/100g suelo) | not | not | direct inoculation | 30
EcoMic® inoculant | EcoMic® inoculant | 50% | not | not | transplant | 16
Native AMF + INIFAP | Native AMF + INIFAP | 3-40/g | not | 70 |  | 17

One experiment in greenhouse conditions showed the negative effect of agronomic management, after six weeks, when the root system was collected and the colonization potential was evaluated, root samples collected in grassland had higher percentage of mycorrhizal colonization, while a drastic decline of infective propagules, proportional to management intensity was found at cultured plots. These results show that the agronomic practices decline the infectivity of AMF ²⁷ .

The colonization percentage has been quantifying removing the root pigments, through acid and basic solutions, the dye trypan blue could be substituted by Parker QuinK water washable ink, also the glycerin and lactic acid 41 . The roots are colored and cut off in 2 cm length pieces, and placed in slides to observe under microscopy, to quantify the AMF colonized and not colonized points.

Between 30 and 60 % of colonization was obtained on three mycorrhization treatments, on papaya cultured under high technification the AMF colonization fluctuated between 8.04 and 12.62 % 25 . AMF average colonization on trap plants was 37.76±21.86 %, the B plants (Brachiaria decumbens) and S (Sorghum vulgare) were the most favorable to AM symbiosis 23 . The extraction of AMF spores was performed in 100 g of dry soil by sample, through wet sieving and decantation procedures 10,42,43 .

The spores were separated from mineral and organic material by mechanical stir and 2500 r.p.m. centrifugation (revolutions per minute) with water, a second centrifugation with 60 % sucrose at 1200 r.p.m., and decantation over 44 µm pore size sieve. Isolation of spores from every extract was placed inside Petri dishes divided in fields (0.5 x 0.5 cm), only turgent and homogeneous colored spores were considered. The abundance of spores in 100 g of soil is established by direct quantification ³⁵ ,44 . Samples of 20 or 50 g of dry soil could be also considered ²⁶ . Also, 40 and 60 % sucrose solutions could be used to extract spores and separate them from organic and mineral soil material 10,41,44,45 , and even 50 % sucrose solution can be used for it 33 . Stereomicroscope is used to separate and to quantify spores 36,38,46,47 . Live and dead spores were quantified, those with cytoplasmatic content and without spore wall damage were alive spores, if these conditions were not meet the spores were dead 47 . The spores were placed in permanent slides with polyvinyl alcohol-lactoglycerol (PVLG) and PVLG + Melzer´s Reagent, 1:1 proportions 36,38,41, ⁴⁶ .

Glomus .G. aggregatum, G. geosporum, G. clarum), Acaulospora .A. morrowiae, A. mellea, A. gerdemannii), Scutellospora .S. calospora) and Entrophospora were the AMF species from banana agroecosystems, while Glomus sp., Acaulospora sp., Scutellospora sp., and Entrophospora were the AMF from commercial inoculum. From 966 to 1618 spores in 100 g of dry soil and 49.0±44.8 % colonization percentage were obtained 23 .

About the abundance, from 216.4±96.6 spores of AMF per 100 g of dry soil have been obtained 35 . Ten genera and 27 morphospecies 44 . The abundance of spores fluctuated from 55 to 198 in 100 g dry soil. Ambispora reticulata was a new record for Chiapas and Mexico. Acaulospora was the most frequent and diverse genus. Richness of AMF morphospecies, diversity, and evenness made “Chiquihuites” site stood out, low levels of organic matter and PO.⁻³ in the soil contributed to it 44 .

Conclusion

The improvement in the growth and resistance of mycorrhized plants against non-mycorrhized ones show the effectiveness of AMF as bioprotectors, bioregulators, biofertilizers, restorers of polluted soils, among other benefits for plants and soils.

Combinations of inert and organic substrates, slightly acid to neutral (pH 5.2 to 7) and low phosphorus content (20 to 30 ppm) seem the most suitable conditions to propagate AMF.

Plants of the family Poaceae, alone and combined with legumes are appropriate hosts for AMF propagation.

The substrates and the hosts plants influence the propagation of individual AMF species, species mixtures or consortia, therefore it is crucial to consider them for successful propagation.

Cited Literature

1. Perez A, Rojas J, Donicer V. Hongos forma dores de micorrizas arbusculares: una alternativa biologica para la sostenibilidad de los agroe cosistemas de praderas en el caribe colombiano. Rev Colombiana Cienc Anim 2011; 3(2):366-85. DOI: http://doi.org/10.24188/recia.v3.n2.2011.412

2. Vital-Vilchis I, Quiñones-Aguilar EE, Hernández-Cuevas LV, Rincón-Enríquez G. Growth of ornamental sunflower in pot at field level by effect of arbuscular mycorrhizal fungi. Terra Latinoam 2020;38(3):679-92. DOI: https://doi.org/10.28940/terra.v38i3.715

3. Tuesta-Pinedo ÁL, Trigozo-Bartra E, Cayotopa-Torres JJ, Arévalo-Gardini E, Arévalo-Hernández CO, Zúñiga-Cernadez LB, et al. Optimización de la fertilización orgánica e inorgánica del cacao (Theobroma Cacao L.) con la inclusión de Trichoderma endófito y Micorrizas arbusculares. Tecnología en Marcha 2017;30(1):67-78. DOI: https://doi.org/10.18845/tm.v30i1.3086

4. Montoya-Martínez AC, Rincón-Enríquez G, Lobit P, López-Pérez L, Quiñones-Aguilar EE. Native arbuscular mycorrhizal fungi from the rhizosphere of Agave cupreata and their effect on Agave tequilana growth. Rev Fitotec Mex 2019;42(4):429-38. DOI: https://doi.org/10.35196/rfm.2019.4.429-438

5. Sieverding, E. Manual de métodos para la investigación de la micorriza vesículo-arbuscular en el laboratorio [Internet]. Cali: Centro Internacional de Agricultura Tropical; 1983 Sep [citado 15 de mayo de 2020]. 121 p. CIAT QR 604.S5 c.2. Recuperado a partir de: https://es.scribd.com/document/270011075/Manual-de-Metodos-Para-La-Investigacion-de-La-Micorriza-Vesiculo-Arbuscular-en-El-Laboratorio

6. Smith SE, Read D. Mycorrhizal Symbiosis [Internet]. Massachusetts: Academic Press; 2008. 787 p. DOI: https://doi.org/10.1016/B978-0-12-370526-6.X5001-6

7. Ferrera Cerrato R, Gonzales Chavez MCA, Rodriguez Mendoza MN. Manual de Agromicrobiología. 1ra Ed. México: Editorial Trillas; 2003.

8. Altiere M, Nicholis C. Diseños agroecológicos, Perú: Sociedad Científica Latinoamericana; 2013.

9. Gamundí de Amos IJ, Godeas AM, Cabello MN. La investigación micológica en la argentina: periodo 1978-2016. Darwiniana 2017;5(1):98-108. DOI: https://doi.org/10.14522/darwiniana.2017.51.711

10. Reyes-Jaramillo I, Chimal-Sánchez E, Salmerón-Castro JY, Vázquez-Pérez N, Varela-Fregoso L. Comunidad de hongos micorrizógenos arbusculares (Glomeromycota) asociada con agaves mezcaleros de Oaxaca y su relación con algunas propiedades edáficas. Rev Mex Biodiv 2019;90: e902 777. DOI: https://doi.org/10.22201/ib.20078706e.2019.90.2777

11. Lovato P. Micorrizas arbúsculares en agroecosistemas. En: VIII Congreso Latinoamericano de Micología-Actualidades Biológicas: 2014, Medellín, Colombia: Asociación Latinoameri cana de Micología; 2014.

12. Becerra A, Bartoloni N, Cofré N, Soteras F, Cabello M. Arbuscular mycorrhizal fungi in saline soils: vertical distribution at different soil depth. Braz J Microbiol 2014;45(2):585-94. DOI: https://doi.org/10.1590/S1517-83822014000200029

13. Lovato P. Micorrizas arbúsculares en agroec osistemas. En: VIII Congreso Latinoamericano de Micología-Actualidades Biológicas: 2014, Mede llín, Colombia: Asociación Latinoameri cana de Micología; 2014.

14. Restrepo Giraldo KJ, Montoya Correa MI, Henao Jaramillo P, Gutiérrez LA, Molina Guzmán LP. Caracterización de hongos micorrízicos arbusculares de suelos ganaderos del trópico alto y trópico bajo en Antioquia, Colombia. Idesia 2019;37(1): 35-44. DOI: https://doi.org/10.4067/S0718-34292019005000301

15. Hermosillo-Salazar J, Vega-Sotelo F, Marquez-Mendoza JI, Leos-Escobedo L, Hermosillo-Alba MC, González-Quirino JG. Micorrizas asociadas a compost, vermicompost y tés orgánicos en el cultivo de calabacita (Cucurbita pepo L.), bajo invernadero. En:. IX Simposio Nacional y VI Reunión Iberoamericana de la Simbiosis Micorrízica. Mexico: Sociedad Mexicana de la Simbiosis Micorrízica, AC (SOMESIMI); 2018.

16. Morales Alvero C, Calaña Naranjo JM, Corbera Gorotiza J, Rivera Espinosa R. Evaluación de sustratos y aplicación de hongos micorrízicos arbusculares en Begonia sp. CulTrop 2011;32(1):50-62.

17. Quiñones-Aguilar EE, Rincón-Enríquez G, López-Pérez L. Hongos micorrízicos nativos como promotores de crecimiento en plantas de guayaba (Psidium guajava L.). Terra Latinoam 2020;38 (3) :541-54. DOI: https://doi.org/10.28940/terra.v38i3.646

18. Serna-Gonzalez M, Urrego-Giraldo LE, Osorio WN, Valencia-Rios D. Mycorrhizae: a key interaction for conservation of two endangered Magnolias from Andean forests. Pl Ecol Evol 2019; 152(1):30-40. DOI: https://doi.org/10.5091/plecevo.2019.1398

19. González González S, Torrres-Arias Y, Ortega-Fors R, Furrazola Gomez E. Hongos micorrizógenos arbusculares (Glomeromycota) de la playa Santa María del Mar Cuba. Rev Jard Bot Nac 2016;37:81-4.

20. Torrres-Arias Y, Ortega-Fors R, González González S, Furrazola Gómez E. Diversity of arbuscular mycorrhizal fungi (Glomeromycota) in semicaducifolius forest of Ciénaga de Zapata, Cuba. Rev Jard Bot Nac 2015;36:195-200.

21. Díaz Franco A, Espinosa Ramírez M, Ortiz Cháirez FE. Reducción de la fertilización inorgánica mediante micorriza arbuscular en sorgo. Rev Int Contam Ambie 2019:35(3):683-92. DOI: https://doi.org/10.20937/rica.2019.35.03.13

22. Molina M, Mahecha L, Medina M. Importancia del manejo de hongos micorrizógenos en el establecimiento de árboles en sistemas silvopastoriles. Rev Col Cienc Pec 2005;18(2):162-75.

23. Usuga Osorio CE. Castañeda Sánchez DA, Franco Molano AE. Multiplication of arbuscular mycorrhizae fungi (AMF) and mycorrhization effect in micropropagated plants of banana (Musa AAA cv.'Gran Enano') (Musaceae). Rev Fac Nac Agron Medellín 2008;61(1):4279-90.

24. Pérez-Madruga Y, Rosales-Jenquis PR, Menéndez DC, Falcón-Rodríguez A. Aplicación combinada de quitosano y HMA en el rendimiento de maíz. CulTrop 2019; 40(4): e06.

25. Velázquez MS, Cabello MN, Elíades LA, Russo ML, Allegrucci N, Schalamuk S. Combinación de hongos movilizadores y solubilizadores de fósforo con rocas fosfóricas y materiales volcánicos para la promoción del crecimiento de plantas de lechuga (Lactuca sativa L.). Rev Argent Microbiol 2017;49(4):347-55. DOI: https://doi.org/10.1016/j.ram.2016.07.005

26. Cruz Hernández Y, García Rubido M, León González Y, Acosta Aguiar Y. Influencia de la aplicación de micorrizas arbusculares y la reducción del fertilizante mineral en plántulas de tabaco. CulTrop 2014;35(1):21-4.

27. Sangabriel-Conde W, Trejo-Aguilar D, Soto-Estrada A, Ferrera-Cerrato R, Lara-Capistrán L. Potencial de colonización de hongos micorrícico-arbusculares en suelos cultivados con papayo bajo diferentes manejos de producción. Rev Mex Mic 2010;31:45-52.

28. Corbera J, Paneque VM, Calaña JM, Morales C. Evaluación de sustratos y aplicación de hongos micorrízicos arbusculares (HMA) en el cultivo de Anthurium andreanum en etapa de vivero. CulTrop 2008;29(4):27-33.

29. Davila L, Ramos J, Rosales C. Multiplicación de hongos micorrizicos arbusculares nativos de cultivo de cacao (Theobroma cacao) en maíz (Zea mays) bajo distintos tratamientos agronómico [tesis licenciatura]. Valledupar: Universidad Popular del Cesar; 2009.

30. Suárez Quimí DF. Evaluación de sustratos para la producción de inoculantes de micorriza vesículo-arbuscular [tesis licenciatura]. [Zamorano]: Universidad Zamorano; 2001 [citado 16 de mayo de 2021]. Recuperado a partir de: https://docplayer.es/31075008-Evaluacion-de-sustratos-inorganicos-para-la-exportacion-de-inoculante-de-micorriza-vesiculo-arbuscular.html

31. Trejo D, Ferrera-Cerrato R, García R, Varela L, Lara L, Alarcón A. Efectividad de siete consorcios nativos de hongos micorrízicos arbusculares en plantas de café en condiciones de invernadero y de campo. Rev Chil Hist Nat 2011;84(1):23-31. DOI: http://doi.org/10.4067/S0716-078X2011000100002

32. Hernández-Cuevas L, Guerra-De la Cruz V, Santiago-Martínez G, Cuatlal-Cuahutencos P. Propagación y micorrización de plantas nativas con potencial para restauración de suelos. Rev Mex Cienc Forestales 2011;2(7):87-96. DOI: http://doi.org/10.29298/rmcf.v2i7.566

33. Ojeda L, Furrazola E, Hernández C. Respuesta de Leucaena leucocephala cv. Perú a la aplicación de diferentes dosis de MicoFert agrícola. Pastos y Forrajes 2015;38(3):176-82.

34. Charles NJ, Martin Alonso NJ. Uso y manejo de hongos micorrízicos arbusculares (HMA) y humus de lombriz en tomate (Solanum lycopersicum L.), bajo sistema protegido. CulTrop 2015;36(1): 55-64.

35. Chimal-Sánchez E, Reyes Jaramillo I, Salmerón-Castro JY, Vázquez-Pérez N, Varela-Fregoso L. Cuatro nuevos registros de hongos micorrizógenos arbusculares (Glomeromycota) asociados con Agave karwinskii y A. angustifolia (Agavaceae) de Oaxaca, México. Act Bot Mex 2018;(125): e1356. DOI: https://doi.org/10.21829/abm125.2018.1356

36. Gutiérrez J, Esquivel R, editores. Influencia de tipo de substrato y planta hospedera en la colonización de Glomus sp. Ayacucho 2013. VIII Simposio Nacional y V Reunión Iberoamericana de la Simbiosis Micorrícica; 2016. México: Sociedad Mexicana de la Simbiosis Micorrízica. Universidad Autónoma Metropolitana Oaxtepec; 2016.

37. Schlemper TR, Stürmer SL. On farm production of arbuscular mycorrhizal fungi inoculum using lignocellulosic agrowastes. Mycorrhiza 2014; 24(8):571-80. DOI: https://doi.org/10.1007/s00572-014-0576-5

38. Furrazola Gómez E, Rodríguez-Rodríguez R. Cuban collection of arbuscular mycorrhizal fungi: history, functioning and conservation. Acta Botánica Cubana 2017;216(1):4-11.

39. Chimal-Sánchez E, García-Sánchez R, Hernández-Cuevas LV. Great richness of arbuscular mycorrhizal fungi at the Mezquital Valley, Hidalgo, Mexico. Rev Mex Mic 2015;41:14-26.

40. Fernández Martín F. Avances en la producción de inoculantes micorrízicos arbusculares. En: Rivera R, Fernández K, editores. El Manejo eficiente de la simbiosis micorrízica, una vía hacia la agricultura sostenible. Estudio de caso [Internet]. La Habana: Ediciones INCA; 2003. p. 97-110. Recuperado a partir de: http://repositorio.geotech.cu/xmlui/handle/1234/3472?show=full

41. Rodríguez Yon J, Arias Pérez L, Medina Carmona A, Mujica Pérez Y, Medina García LR, Fernández Suárez K, et al. Alternativa de la técnica de tinción para determinar la colonización micorrízica.CulTrop 2015;36(2):18-21.

42. Gerdemann JW, Nicolson TH. Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Brit Mycol Soc 1963;46(2):235-44. DOI: https://doi.org/10.1016/S0007-1536(63)80079-0

43. Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N. Working with mycorrhizal in forestry and agriculture [Internet]. Canberra: Australian Centre for International Agricultural Research; 1996. 344 p. DOI: https://doi.org/10.13140/2.1.4880.5444

44. Bertolini Vincenzo Montaño NM, Salazar-Ortuño BL, Chimal-Sánchez E, Varela L. Diversidad de hongos micorrizógenos arbusculares en plantaciones de café (Coffea arabica) del volcán Tacaná, Chiapas, México. Act Bot Mex 2020;(127):e 1602 . DOI: http://doi.org/10.21829/abm127.2020.1602

45. The International Bank for the Glomeromycota [Internet]. West Virginia University; 1993. [citado 16 de mayo de 2021]. Recuperado a partir de: https://invam.wvu.edu/

46. Lara-Capistrán L, Hernández-Montiel LG, Reyes-Pérez JJ, Preciado Rangel P, Zulueta-Rodríguez R. Respuesta agronómica de Phaseolus vulgaris a la biofertilización en campo. Rev Mex Cienc Agríc 2019;10(5):1035-46. DOI: https://doi.org/10.29312/remexca.v10i5.936

47. Fabián D. Guadarrama P, Hernández-Cuevas L, Ramos-Zapata JA. Arbuscular mycorrhizal fungi in a costal wetland in Yucatan, México. Bot Sci 2018;96(1):24-34. DOI: https://doi.org/10.17129/botsci.1216

Notes

Funding source: Universidad Nacional de San Cristóbal de Huamanga (3500 new soles on average).

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Conflicts of interest: This review paper has no conflicts of interest.

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Acknowledgements: The authors thanks to Universidad Nacional de San Cristóbal de Huamanga, Peru, for funds, and Ing. Sc. M. Mike Anderson Corazón Guivín, Universidad Nacional de San Martín, Peru by suggestions to this paper.

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Ethical considerations: This is a review paper, the authors declare it was prepared using the cited literature and giving credits to respective papers and authors.

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Authors' contributions: Esquivel Quispe Roberta, planned the paper and wrote the base document including tables, made bibliographic search and catalogued it. Hernández Cuevas Laura Verónica, made bibliographic search, contributed with ideas to paper integration and collaborated with the revision and correction of the paper. Quispe Ochoa Josue Olser, collaborated with bibliographic search.

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Editor's Note: Journal of the Selva Andina Biophere (JSAB) remains neutral with respect to jurisdictional claims published on maps and institutional affiliations.

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Article ID: 102/JSAB/2021

Author notes

* Contact address: National University of San Cristobal de Huamanga. Research and Innovation Unit. Faculty of Agricultural Sciences. Independence Portal No. 57. Ayacucho Peru. Roberta Esquivel Quispe E-mail address: roberta.esquivel@unsch.edu.pe

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