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Revista Chapingo serie ciencias forestales y del ambiente

On-line version ISSN 2007-4018Print version ISSN 2007-3828

Rev. Chapingo ser. cienc. for. ambient vol.23 n.3 Chapingo Sep./Dec. 2017

http://dx.doi.org/10.5154/r.rchscfa.2016.11.060 

Review article

Ectomycorrhizal ecology, biotechnology and taxonomy for the conservation and use of Abies religiosa in temperate areas of Mexico

Iván Oros-Ortega1  * 

Antonio Andrade-Torres2 

Luis A. Lara-Pérez3 

Rubén F. Guzmán-Olmos2 

Fernando Casanova-Lugo1 

Luis A. Sáenz-Carbonell3 

Iván Córdova-Lara3 

1Instituto Tecnológico de la Zona Maya. Carretera Chetumal-Escárcega km 21.5, Ejido Juan Sarabia, Othón P. Blanco, C. P. 77960, Quintana Roo, México.

2Universidad Veracruzana, Instituto de Biotecnología y Ecología Aplicada, Ecología y manejo de la biodiversidad CA-UVER173. Av. de las Culturas Veracruzanas núm. 101, Campus para la Cultura, las Artes y el Deporte, col. Emiliano Zapata, C. P. 91090, Xalapa, Veracruz, México.

3 Centro de Investigación Científica de Yucatán, A.C. CICY, Unidad de Biotecnología. Calle 43 núm. 130, col. Chuburná de Hidalgo, C. P. 97205, Mérida, Yucatán, México.

Abstract

Endemic populations of Abies religiosa (fir, oyamel) have great economic, ecological and social importance; in addition, they form different interactions with edaphic microorganisms, mainly with ectomycorrhizal fungi. Currently, isolated populations (i. e. fir) are threatened by deforestation, agricultural expansion and global warming; therefore, it is urgent to understand the ecological and evolutionary interactions with ectomycorrhizal fungi. The objective of the present research was to analyze the use of molecular ecology, taxonomy and biology of ectomycorrhizal fungi to understand the role that these fungi play in A. religiosa trees in Mexico. Areas of research are presented as well as the main information gaps in the morphological/molecular characterization, taxonomy and evolution of the ectomycorrhizal symbiosis in A. religiosa. For the above, we collected information of 108 taxa of potentially ectomycorrhizal fungi obtained from different fir populations. The taxa with high potential to inoculate A. religiosa are Sebacina dimitica, Clavulina cf. cinerea, Membranomyces sp., Thelephoraceae, Russula spp., Ramaria spp., Lactarius spp. e Inocybe spp. Finally, we discuss issues that remain unresolved to determine their potential for use, management and conservation of A. religiosa in temperate areas of Mexico. This problem can be solved by combining molecular tools with the morphological and histological description of ectomycorrhizal morphotypes. In addition, methodologies are required to standardize results to come to more robust conclusions about mycorrhizal interactions.

Keywords: Temperate forests; mycorrhizal status; forest; ITS

Introduction

Abies religiosa (known in Mexico as oyamel) is the most abundant fir species in this country (Challenger, 1998). It has endemic populations along the Trans-Mexican Volcanic Belt, between 2 800 and 3 500 m of altitude, in the mountainous and temperate areas of Mexico (Jaramillo-Correa et al., 2008; Pérez-Miranda, Moreno-Sánchez, González-Hernandez, & Arriola-Padilla, 2015). Fir trees are highly economically, ecologically and socially relevant, providing fundamental ecosystem services such as carbon and water sequestration (Avendaño-Hernandez, Acosta-Mireles, Carrillo-Anzures, & Etchevers-Barra, 2009). In addition, they are a reservoir of biodiversity and host a variety of bird species, insects (i. e. monarch butterfly: Danaus plexippus) and plants, as well as a wealth of edible fungi, saprophytes and ectomycorrhizal fungi (EcMF) (Andrade-Torres et al., 2015; Argüelles-Moyao, Garibay-Orijel, Márquez-Valdemar, & Arellano-Torres, 2017; Morales-Mávil & Aguilar-Rodríguez, 2000; Sáenz-Romero, Rehfeldt, Duval & Lindig-Cisneros, 2012).

Fir is used as Christmas tree and as raw material in various economic activities: construction of houses, fences, furniture, pulp production for paper and to obtain turpentine and firewood (Sánchez-Velásquez, Pineda-López, & Hernández- Martínez, 1991). From the social point of view, fir due to its natural beauty, represents a relevant cultural heritage. Its populations are an attraction for recreational activities in the field; as is the case of the forests around Mexico City.

Despite the importance of A. religiosa populations, they are now threatened by land-use change, generated by the expansion of agriculture (mainly potato cultivation in the region of Cofre de Perote), deforestation, illegal logging, population growth, air pollution and forest fires. This is due to the fact that models of projections of climate change estimate a decrease of populations between 60 and 80 % (Ángeles-Cervantes & López-Mata, 2009; Pérez-Miranda et al., 2015; Sáenz-Romero et al., 2012; Villers-Ruíz & Trejo-Vázquez, 1998). Therefore, it is urgent to focus research efforts to establish strategies for management and conservation of populations, one of which may be ecological interactions.

In this sense, ectomycorrhiza constitute the main ecological interaction between fir and symbiotic organisms of the soil, because it has a great diversity of functions as the decomposition of organic matter, reduction of nitrogen to ammonium, protection to water stress and prevention against pathogens (Brundrett, 2009; Smith & Read, 2008). This interaction allows the mobilization, translocation and absorption of mineral nutrients from plants. In contrast, the host translocates sources of carbon to fungi (Peterson, Massicotte, & Melville, 2004; Smith & Read, 2008). Due to the above, and because ectomycorrhizal fungi have a obligate interaction, it has a significant influence on the establishment, survival, growth of plant species and regulation of ecosystems.

The study of EcMF, through disciplines such as ecology and biotechnology, can generate strategies that contribute to the conservation of fir populations. The interaction mentioned above plays a fundamental role in the biology and ecology of temperate species, mainly among members of the Pinaceae family, such as fir; however, most species of EcMF associated with ectomycorrhizae are not known (Brundrett, Bougher, Dell, Grove, & Malajczuk, 1996; Smith & Read, 2008). This is due to the limited progress in its morphological, molecular, and taxonomical characterization, mainly due to the low availability of basidiomes in fir forests, the marked seasonality in their appearance (there are species with fructification hypogea) and the difficulty to use, isolate and identify the species associated in ectomycorrhiza (Andrade-Torres et al., 2006; Brundrett, 2009). This difficulty is also due to the lack of use of molecular tools, as well as the still small number of researchers who integrate tools of ecology, taxonomy and molecular biology when analyzing these interactions.

Although it is true that the combination of techniques is gradually developing in Mexico (Argüelles-Moyao et al., 2017; Baeza-Guzmán, Medel-Ortiz, & Garibay-Orijel, 2017; Montoya, Bandala, & Garay-Serrano, 2015; Reverchon, Ortega-Larrocea, Bonilla-Rosso, & Pérez-Moreno, 2012), it is essential to increase the study of this type of interactions. Therefore, the objective of the present study is to analyze the use of molecular ecology, taxonomy and biology of ectomycorrhizal fungi to understand the role these fungi play in trees of A. religiosa. This information will make it possible to lead ectomycorrhizal interactions in populations of A. religiosa to promote the management and conservation of temperate forests in Mexico.

Evolution and diversity of ectomycorrhizal fungi

The coevolution between mycorrhizal fungi and host roots dates back to the Paleozoic era (more than 400 million years ago), when plants began to develop in terrestrial environments (Redecker, Kodner, & Graham, 2002). It is important to mention that their interaction is a mutualistic and functional association (Smith & Read, 2008). The classification of mycorrhizal fungi depends on the fungal and plant species that establish the association, in addition to the nutritional strategy that allows an intracellular penetration, or not, by the fungi inside the cortical cells of the root of the plants (Honrubia, 2009). The main benefits of these fungi are: to provide nutrients (phosphorus, zinc, nitrogen, calcium, sodium and potassium), to release hormones and increase tolerance to salinity, soil acidity, drought and toxicity of certain metals in plants (Smith & Read, 2008).

This interaction occurs in approximately 90 % of plants; so it is found in most of the world's ecosystems (Smith & Read, 2008). Some authors recognized seven types of mycorrhizal fungi: ectomycorrhiza, ectendomycorrhiza, arbuscular mycorrhiza, orchid mycorrhiza, ericoid mycorrhiza, arbutoid mycorrhiza and monotropoid mycorrhiza. Currently, mycorrhizal fungi have been defined by its mutualistic association, characterized by its structures and physiological contribution of fungi to plants; for this reason, only four types are recognized: ectomycorrhiza, arbuscular mycorrhiza, orchid mycorrhiza and ericoid mycorrhiza (van der Heijden, Martin, Selosse, & Sanders, 2015). In view of this, the mycorrhizal fungi are separated from other root-fungus associations, and by not revealing the functionality of the individuals involved they will be referred to as "endophytes” (Brundrett, 2009).

According to the morphological, functional and evolutionary characteristics, ectomycorrhizal fungi shows one of the most relevant interactions associated with the development of different plant species (such as those of the Pinaceae family). Regarding the fossil evidence, fungi and ectomycorrhizal plants have co-evolved for at least 88 million years (Bidartondo, 2005; LePage et al., 2003). Therefore, there is a high diversity of fungi associated with this type of plants. Comandini, Rinaldi, and Kuyper (2012) mention that there are about 7 950 EcMF species grouped in 234 genera, and estimated a potential richness of between 20 000 and 25 000 species; however, this data may be underestimated, because the criterion for inferring ectomycorrhizal status is still not consistent. Most of these EcMF have a wide variety of hosts, for example: Amanita muscaria, Cenococcum geophilum, Hebeloma crustuliniforme, Laccaria laccata, Pisolithus tinctorius and Thelephora terrestris (Smith & Read, 2008). Also the function of ectomycorrhizal fungi has great relevance due to the high diversity of plants where they are present; as they are found in some 7 750 to 10 000 forest plant species and the following stand out: family Betulaceae, Fagaceae, Pinaceae and Myrtaceae (Brundrett, 2009).

Molecular biology and ecology of ectomycorrhizal fungi

At present, molecular techniques are one of the main pathways of taxonomic, ecological and physiological studies of mycorrhizal symbiosis. However, these studies have been developed mainly with plants in mountainous areas of North America and Europe, with only some research on morphological and genetic characterization of EcMF in Mexico (Argüelles-Moyao et al., 2017; Baeza-Guzmán et al., 2017; Montoya et al., 2015). For the specific case of mountain ecosystems in Mexico, there are still many information gaps regarding the study of mycorrhizal symbiosis, both morpho-anatomical descriptions and characterization with the use of molecular biology techniques. These techniques are performed from the amplification of specific and conserved regions of DNA. This has been shown to be of great utility to identify EcMF through polymerase chain reaction (PCR; Bruns & Gardes, 1993).

In these specific regions there are multicopy genes, such as Internal Transcribed Spacer (ITS); which is located within the ribosomal DNA, replicated between the highly conserved genes 18S, 5.8S and 28S. ITS is a non-coding variable region and has two types: ITS1 and ITS2; which are used extensively as species-specific markers (Anderson & Cairney, 2004). These genes are amplified from a small DNA fragment, even if it is diluted or degraded in mixtures of DNA from plant and fungus, where in most cases the fungus may account for less than 1 % of the total extracted (Bruns & Gardes, 1993). The sequences of these regions represent a genetic fingerprint for each species; so they are the main marker in the taxonomic identification of EcMF (Montoya et al., 2015; Schoch et al., 2012).

Molecular biology techniques provide the possibility of identifying fungi species under laboratory conditions, to subsequently cultivate and inoculate them in host plants, evaluate whether they form mycorrhizal fungi and whether they prevail after transplantation; in addition, to study the extraradical mycelium formed in the field after a certain time of having established the host plant. By means of PCR, the genes of the large ribosomal subunit (LSU) of the ectomycorrhizal synthesized between Turbinellus floccosus with Abies religiosa have been successfully characterized (Lamus et al., 2015), as well as the ITS region of the ectomycorrhiza formed between seedlings of Pinus pinea and two strains of Lactarius deliciosus (Hortal, Pera, & Parladé, 2009). Molecular tools have also been used to determine the amount of fungal mycelium in different soil types (Landeweert et al., 2003) and the abundance of EcMF species (Kjøller et al., 2012).

Regarding the taxonomic status of EcMF, only a few species have been identified through the description of ectomycorrhizal fungi (de Román, Claveria, & de Miguel, 2005) and by molecular studies (Argüelles-Moyao et al., 2017), without having basidiomes that corroborate their identity with greater precision. The study of EcMF is complicated because there is no consistent taxonomic information, given the complexity of mycorrhizal fungi, and the difficulty of isolating and characterizing those (Read & Pérez-Moreno, 2003). Also, it has been discussed that traditional studies may be leaving aside information regarding species with hypogeal basidiomes (Dahlberg, 1997; Rodríguez-Tovar, Xoconostle-Cásares, & Valdés, 2004). These, according to studies in temperate forests of North America and Europe, are those of greater abundance (Gardes & Bruns, 1996). Therefore, it is necessary to generate information to determine the correct taxonomy of ectomycorrhizal fungi; which is fundamental to know different ecological attributes of EcMF communities and to understand their role in the establishment, survival and development of A. religiosa.

Molecular techniques have provided the study of ecological attributes; for example, alpha diversity, genetic diversity and functional diversity between fungi and host plants (García, Smith, Luoma, & Jones, 2016; Kjøller et al., 2012). Because of this, EcMF diversity has been accurately determined, even without the emergence of basidiomes (Aučina et al., 2011; Kjøller et al., 2012). The information generated with studies of molecular biology and traditional taxonomy (Montoya et al., 2015) represent the starting point for ecology studies (García et al., 2016).

On the other hand, due to recent molecular techniques, such as metagenomics studies, it has been possible to know microorganisms in a wide variety of environments (Tedersoo et al., 2014). Last generation sequencing is relatively inexpensive and produces thousands of sequences with which it is possible to identify and quantify individuals; which allows a better understanding of the ecology of fungal communities (Tedersoo et al., 2014). However, if one does not become aware of possible methodological errors, limiting markers and bioinformatic challenges, one can reach erroneous conclusions (Tedersoo et al., 2010). At present, this type of sequencing is becoming the primary tool for the study of mycorrhizal fungi (Taylor et al., 2016).

Molecular studies should aim to understand the factors that determine the structure of communities both in space and time (Garcia et al., 2016; Koide, Fernández, & Petprakob, 2011). Diversity should be considered simultaneously, both for basidiomas and for root tips. Another alternative is to determine the ectomycorrhizal status of EcMF species by comparing sequences between roots and basidiomas, properly classified (Montoya et al., 2015). This information is the basis for generating criteria in the selection of species of fungi to inoculate plants and thereby improve their development and growth. Due to the great wealth of species that exist in Mexico, it is likely that many of the specimens collected are new or not yet found in gene banks. Future studies of mycorrhizal ecology should, as far as possible, generate vouchers of both basidiomas and root tips to be deposited in herbaria and to improve storage techniques for subsequent comparative studies. The union of ecological, morphological and molecular data will help to have a better understanding of mycorrhizal interactions and their evolutionary history.

Ectomycorrhizal fungi in Abies religiosa forests in Mexico

Ectomycorrhizal fungi studies in A. religiosa forests are incipient; with a few exceptions, fungal diversity estimation it is known from mycological and listed taxonomic studies (Andrade-Torres et al., 2015; Burrola-Aguilar, Garibay-Orijel, & Argüelles-Moyao, 2013; García-Bastián, López-López, Velázquez-Martínez, & Pérez-Moreno, 1998; Valdés-Ramírez, 1972). Morphological research of ectomycorrhizal fungi in A. religiosa has been restricted to Cenococcum geophilum and Lactarius sp. (Appendix 1). However, Argüelles-Moyao et al. (2017) studied ectomycorrhizal fungi using molecular tools and pointed out that the Clavulinaceae family is the most dominant; in addition, they found 21 species of Inocybe, 10 of Tomentella and eight of Russula, and Clavulina cf. cinerea and Membranomyces sp. had the highest relative abundance.

At present, we identify 108 taxa of ectomycorrhizal fungi, collected in different populations of A. religiosa. Of these, 95 were classified as species and 13 in genera: Fischerula sp., Genabea sp., Genea sp., Hydnobolites sp., Lyophyllum sp., Membranomyces sp., Peziza sp., Phaeocollybia sp., Piloderma sp., Pseudotomentella sp., Tarzetta sp., Trychophaea sp. and Xerocomus sp. (Appendix 1).

There are EcMF species, collected in forests of fir, whose interaction by morphology has not yet been verified, with A. religiosa and no records have been observed with any other plant species. These are considered to have potential to be associated, since others of the same genus of fungus have been determined as ectomycorrhizal; for example: Fischerula sp., Genabea sp., Genea sp., Lyophyllum sp., Hydnobolites sp., Membranomyces sp., Peziza sp., Piloderma sp., Pseudotomentella sp., Tarzetta sp., Tomentella sp. and species of the genus Amanita spp., Boletus spp., Clavulina spp., Cortinarius spp., Helvella spp., Hygrophorus spp., Inocybe spp., Lactarius spp., Ramaria spp., Russula spp., Suillus spp., Tricholoma spp., and in particular the following species Cantharellus floccosus, Chroogomphus vinicolor, Gomphus floccosus, Goutieria chilensis, Hebeloma albocolossum, Humaria hemisphaerica, Hydnotrya cerebriformis, Hydnum repandum, Hysterangium separabile, Leccinum aurantiacum, Sebacina dimitica, Tuber cf. separans and Xerocomus sp. (Appendix 1; Comandini et al., 2012; de Román et al., 2005; Rinaldi, Comandini, & Kuyper, 2008).

Argüelles-Moyao et al. (2017) used sequences from the ITS nrDNA to identify 83 species at seven study sites. These species represent 57 % of sampling efficiency; so it is estimated that EcMF associated with adult trees of A. religiosa would be about 145 species. This is a good approximation; since A. religiosa is located in the Neartic and Neotropical transition, a high diversity of EcMF species is expected.

There is still a lot of work to do, since there is a lack of information from populations in other regions of Mexico, considering that most EcMF associated with A. religiosa in Mexico have restricted distribution, have not been sequenced previously and the rankings that exist to compare them are from specimens of North America, associated with plant species of the family Pinaceae and Fagaceae (Argüelles-Moyao et al., 2017).

The morpho-anatomical description of ectomycorrhizae is missing, as well as the correct identification of the basidiomas. For this type of structures there is only information of molecular characteristics for A. muscaria, and Lactarius luculentus (Appendix 1). Argüelles-Moyao et al. (2017) consider that the taxa Sebacina dimitica, Russula acrifolia, Clavulina cf. cinerea, Membranomyces sp. and Thelephoraceae sp. (Appendix 1) have greater potential for inoculation programs. However, studies reviewed confirm that the most diverse genera are Russula spp., Ramaria spp., Lactarius spp. and Inocybe spp. These could have a strong potential to inoculate populations of fir in Mexico. However, new studies should be considered to know their diversity, distribution, feasibility and ease to spread, and to know if they are edible species.

The above information is essential, even for other temperate forest species in Mexico and in the world. For Abies spp. it represents a significant advance, since the potential diversity is high, regarding that it is home to about 48 species distributed in temperate, polar and subtropical areas (Xiang, Cao, & Zhou, 2007).

Future research

There are many gaps of information regarding the understanding of the mycorrhizal interaction in A. religiosa, which constitute an area of opportunity to generate lines of research. Some of these questions could be: What is the identity of the different morphotypes associated with A. religiosa? What is the evolutionary history of species of ectomycorrhizal fungi and how they established in fir forests? What is the distribution of fungi in fir populations? What are the factors that determine the diversity of EcMF in forest of A. religiosa? Does the diversity of EcMF change temporarily? Does the phenological state of the tree influence the EcMF species with which it is associated? In what way do other species of forest plants influence mycorrhizal interaction with A. religiosa?

Conclusions

The effort to elucidate the diversity of the communities of ectomycorrhizal fungi associated with A. religiosa must be greater, because the knowledge that one has is very incipient; without leaving out the important ecological and functional role of the ectomycorrhizal symbiosis in populations of this forest species. This problem can be solved by combining molecular tools with the morphological and histological description of ectomycorrhizal fungi; which, together with the traditional systematic method, are fundamental to know the diversity associated with the forests of A. religiosa.

Finally, a methodology is required to standardize results and reach more solid conclusions on mycorrhizal interactions. In this way, it will be possible to determine its potential of use or management, based on ecological studies that allow conservation, management and use of the forests of A. religiosa in temperate areas of Mexico.

Acknowledgements

The first author thanks the Consejo Nacional de Ciencia y Tecnología (CONACYT) for the grant (204524) given to undertake doctoral studies. We thank M. C. Julissa B. Perea-García and the reviewers for their valuable recommendations, comments, remarks and corrections to this manuscript.

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Koide, R. T., Fernandez, C., & Petprakob, K. (2011). General principles in the community ecology of ectomycorrhizal fungi. Annals of Forest Science, 68(1), 45-55. doi: 10.1007/s13595-010-0006-6 [ Links ]

Lamus, V., Franco, S., Montoya, L., Endara, A. R., Caballero, L. A., & Bandala., V. M. (2015). Mycorrhiza l synthesis of the edible mushroom Turbinellus floccosus with Abies religiosa from central Mexico. Mycoscience, 56, 622-626. doi: 10.1016/j.myc.2015.07.001 [ Links ]

Landeweert, R., Veenman, C., Kuyper, T. W., Fritze, H., Wernars, K., & Smit, E. (2003). Quantification of ectomycorrhizal mycelium in soil by real-time PCR compared to conventional quantification techniques. FEMS Microbiology Ecology, 45(3), 283-292. doi: 10.1016/S0168-6496(03)00163-6 [ Links ]

LePage, B. A. (2003). The evolution, biogeography and palaeoecology of the Pinaceae based on fossil and extant representatives. Acta Horticulturae, 615, 29-52. doi: 10.17660/ActaHortic.2003.615.1 [ Links ]

Montoya, L., Bandala, V. M., & Garay-Serrano, E. (2015). The ectomycorrhizas of Lactarius cuspidoaurantiacus and Lactarius herrerae associated with Alnus acuminata in Central Mexico. Mycorrhiza , 25(6), 457-467. doi: 10.1007/s00572-015-0625-8 [ Links ]

Morales-Mávil, J. E., & Aguilar-Rodríguez, S. H. (2000). Avifauna del Parque Nacional Cofre de Perote. Foresta Veracruzana, 2(1), 35-40. Retrieved from http://www.redalyc.org/articulo.oa?id=49720104Links ]

Pérez-Miranda, R., Moreno-Sánchez, F., González-Hernández, A., & Arriola-Padilla, V. J. (2015). Distribución de Abies religiosa (Kunth) Schltdl. et. Cham. y Pinus montezumae Lamb. ante el cambio climático. Revista Mexicana de Ciencias Forestales, 5(25), 18-33. Retrieved from http://cienciasforestales.inifap.gob.mx/editorial/index.php/Forestales/article/view/3892/3249. [ Links ]

Peterson, R. L., Massicotte, H. B., & Melville, L. H. (2004). Mycorrhizas: anatomy and cell biology. Ottawa: CABI Publishing. [ Links ]

Read, D. J., & Pérez-Moreno, J. (2003). Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytologist, 157(3), 475-492. doi: 10.1046/j.1469-8137.2003.00704.x [ Links ]

Redecker, D., Kodner, R., & Graham, L. E. (2002). Palaeoglonius grayi from the Ordovician. Mycotaxon, 84, 33-37. Retrieved from http://www.mycotaxon.com/vol/84.htmlLinks ]

Reverchon, F., Ortega‐Larrocea, M., Bonilla‐Rosso, G., & Pérez‐Moreno, J. (2012). Structure and species composition of ectomycorrhizal fungal communities colonizing seedlings and adult trees of Pinus montezumae in Mexican neotropical forests. FEMS microbiology ecology, 80(2), 479-487. doi: 10.1111/j.1574-6941.2012.01314.x [ Links ]

Rinaldi, A. C., Comandini, O., & Kuyper, T. W. (2008). Ectomycorrhizal fungal diversity: Separating the wheat from the chaff. Fungal Diversity, 33, 1-45. Retrieved from http://www.fungaldiversity.org/fdp/sfdp/33-1.pdfLinks ]

Rodríguez-Tovar, A., Xoconostle-Cásares, B., & Valdés, M. (2004). Ecología molecular de los hongos ectomicorrízicos. Revista Fitotecnia Mexicana , 27(3), 267-278. Retrieved from http://www.revistafitotecniamexicana.org/documentos/27-3/7a.pdfLinks ]

Sáenz-Romero, C., Rehfeldt, G. E., Duval, P., & Lindig-Cisneros, R. A. (2012). Abies religiosa habitat prediction in climatic change scenarios and implications for monarch butterfly conservation in Mexico. Forest Ecology and Management, 275, 98-106. doi: 10.1016/j.foreco.2012.03.004 [ Links ]

Sánchez-Velásquez, L. R., Pineda-López, M., & Hernández-Martínez, A. (1991). Distribución y estructura de la población de Abies religiosa (H. B. K.) Schl. et. Cham. en el Cofre de Perote, estado de Veracruz, México. Acta Botánica Mexicana, 16, 45-55. Retrieved from http://www.redalyc.org/articulo.oa?id=57401604Links ]

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Taylor, D. L., Walters, W. A., Lennon, N. J., Bochicchio, J., Krohn, A., Caporaso, J. G., & Pennanen, T. (2016). Accurate estimation of fungal diversity and abundance through Improved lineage-specific primers optimized for illumina amplicon sequencing. Applied and Environmental Microbiology, 82(24), 7217-7226. doi: 10.1128/AEM.02576-16 [ Links ]

Tedersoo, L., Nilsson, R. H., Abarenkov, K., Jairus, T., Sadam, A., Saar, I., Bahram, M., Bechem, E., Chuyon, G., & Kõljalg, U. (2010). 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytologist, 188(1), 291-301. doi: 10.1111/j.1469-8137.2010.03373.x [ Links ]

Tedersoo, L., Bahram, M., Põlme, S., Kõljalg, U., Yorou, N. S., Wijesundera, R., … Abarenkov, K. (2014). Global diversity and geography of soil fungi. Science, 346(6213), 1078. doi: 10.1126/science.1256688 [ Links ]

Valdés-Ramírez, M. (1972). Microflora of a coniferous forest of the mexican basin. Plant and Soil, 36(1-3), 31-38. doi: 10.1007/BF01373453 [ Links ]

Van der Heijden, M., Martin, F. M., Selosse, M. A., & Sanders, I. R. (2015). Mycorrhiza l ecology and evolution: the past, the present, and the future. New Phytologist, 205(4), 1406-1423. doi: 10.1111/nph.13288 [ Links ]

Villers-Ruíz, L., & Trejo-Vázquez, I. (1998). El impacto del cambio climático en los bosques y áreas naturales protegidas de México. Interciencia, 8(2), 141-157. Retrieved from https://www.researchgate.net/publication/287831828_Impacto_del_Cambio_Climatico_en_los_bosques_y_areas_naturales_protegidas_de_MexicoLinks ]

Xiang, X., Cao, M., & Zhou, Z. (2007). Fossil history and modern distribution of the genus Abies (Pinaceae). Frontiers of Forestry in China, 2(4), 355-365. doi: 10.1007/s11461-007-0058 [ Links ]

Appendix 1

Research studies on ectomycorrhizal fungi associated with populations of Abies religiosa in Mexico. 

Fungal species References Revised structure Type of sudie Ectomycorrhizal status quotation
Basidiomes Ectomycorrhizal Morphological Molecular
Amanita muscaria 1, 8, 11 x nda x x Ingleby, Mason, Last, and Fleming (1990) (Betula pendula)*
A. pantherina 1, 5 x nda x nda Ingleby et al. (1990)**
A. rubescens 3, 5 x nda x nda Ingleby et al. (1990)**
Boletus edulis 1, 5 x nda x nda Ceruti, Tozzi, y Reitano (1987) (Pinus silvestris)*
B. luridus 8 x nda x nda Brunner, Amiet, Zollinger, and Egli (1992) (Picea abies)*
B. pinophilus 5 x nda x nda Brunner et al. (1992)*
Boletellus projectellus 10 x nda x nda Determinado por filogenia (Binder & Hibbett, 2006).
Cantharellus cibarius 5, 3, 8, 6 x nda x nda Mleczko (2004) (Pinus sylvestris)*
C. floccosus 12, 3 x nda x nda Mleczko (2004)**
Cenococcum geophilum 12, 9 nda x x nda Valdés-Ramírez (1972) (Abies religiosa)*
Chroogomphus vinicolor 1, 5 x nda x nda Agerer (1990)*
Clavulina aff. rugosa 2 nda x nda x Tedersoo, Kõljalg, Hallenberg, and Larsson (2003)**
Clavulina cinerea 4 x nda x nda Tedersoo et al. (2003)**
Collybia dryophyla 3, 10 x nda x nda Undetermined
Cortinarius cf. ignipes 2 nda x nda x Agerer (1987)**
Cortinarius obtusus 2 nda x nda x Agerer (1987)**
Cortinarius vernus 2 nda x nda x Buée, Vairelles, and Garbaye (2005)**
Fischerula sp. 2 nda x nda x Buée et al. (2005)**
Genabea sp. 2 nda x nda x Buée et al. (2005)**
Genea sp. 2 nda x nda x Buée et al. (2005)**
Gomphus floccosus 1, 3, 4, 6, 8 x nda x nda Agerer, Beenken, and Christan (1998)**
Goutieria chilensis 5 x nda x nda Palfner (2001)**
Hebeloma albocolossum 2 nda x nda x Jakucs, Magyar, and Beenken (1999)**
Helvella sculenta 3 x nda x nda Tedersoo, Hansen, Perry and Kjøller (2006)**
H. crispa 3, 4, 6 x nda x nda Tedersoo et al. (2006)**
H. lacunosa 3, 6 x nda x nda Tedersoo et al. (2006)**
Helvellosebacina helveloides 2 nda x nda x Undetermined
Humaria hemisphaerica 2 nda x nda x Ingleby et al. (1990)**
Hydnobolites sp. 2 nda x nda x Molina, Massicotte, and Trappe (1992)**
Hydnotrya cerebriformis 2 nda x nda x Tedersoo et al. (2003)**
Hydnum repandum 5 x nda x nda Agerer, Kraigher, and Javornik (1996)**
Hygrophoropsis aurantiaca 10 x nda x nda Undetermined
Hygrophorus chrysodon 5, 8, 12 x nda x nda Treu (1990)**
H. hypothejus 5, 8 x nda x nda Treu (1990)**
H. nigrescens 5 X nda x nda Treu (1990)**
H. russula 10 X nda x nda Treu (1990)**
Hysterangium separabile 12 X nda x nda Raidl and Agerer (1998)**
Inocybe aff. fastigiata 6 x nda x nda Magyar, Beenken, and Jakucs (1999)**
I. aff. geophylla var. alba 6 x nda x nda Magyar et al. (1999)**
I. geophylla var. geophylla 5, 10 x nda x nda Magyar et al. (1999)**
I. griseovelata 2 nda x nda x Magyar et al. (1999)**
I. lanatodisca 2 nda x nda x Magyar et al. (1999)**
I. lilacina 2 nda x nda x Magyar et al. (1999)**
I. lutescens 10 x nda x nda Magyar et al. (1999)**
I. obscura 10 x nda x nda Magyar et al. (1999)**
Laccaria laccata 1, 4 x nda x nda Dickie, Guza, Krazewski, and Reich (2004) (Elianthemum bicknellii)*
Lactarius chelidonium var. chelidonioides 8 x nda x nda Eberhardt et al. (2000)**
L. chysorrheus 10 x nda x nda Eberhardt et al. (2000)**
L. deliciosus 1, 3 x nda x nda Kernaghan, Currah, and Bayer (1997) (Abies lasiocarpa)*
L. fennoscandicus 2 nda x nda x Eberhardt et al. (2000)**
L. luculentus 4, 9 x nda x x Eberhardt et al. (2000)*
L. mexicanus 1, 5, 7 x nda x nda Eberhardt et al. (2000)*
L. rubrilacteus 8 x nda x nda Eberhart and Luoma (1997) (Pseudotsuga menziesii)*
L. rufus 1, 5 x nda x nda Ingleby et al. (1990) (Picea sitchensis)*
L. salmonicolor 3, 5, 8 x nda x nda Eberhardt et al. (2000) (Abies alba)*
L. vietus 10 x nda Hagerman, Sakakibara, and Durall (2001) (Pseudotsuga menziesii)
Leccinum aurantiacum 8 x nda x nda Müller and Agerer (1990)**
Lyophyllum sp. 8 x nda x nda Agerer and Beenken (1998)**
Membranomyces sp. 2 nda x nda x Tedersoo et al. (2003)**
Peziza sp. 2 nda x nda x Tedersoo et al. (2006)**
Phaeocollybia sp. 2 nda x nda x Undetermined
Piloderma sp. 2 nda x nda x Hagerman et al. (2001)**
Pseudotomentella sp. 2 nda x nda x Agerer (1994)**
Ramaria bonii 8 x nda x nda Nouhra, Horton, Cazares, and Castellano (2005)**
R. botrytis var. botrytis 1, 3, 5 x nda x nda Nouhra et al. (2005)**
R. cystidiophora var. 8 x nda x nda Nouhra et al. (2005)**
R. stricta 3 x nda x nda Nouhra et al. (2005)**
R. flava var. sanguinea 1, 3 x nda x nda Nouhra et al. (2005)**
R. flavobrunnescens 8 x nda x nda Nouhra et al. (2005)**
R. rasilispora var. scatesiana 8 x nda x nda Nouhra et al. (2005)**
R. rubiginosa 8 x nda x nda Nouhra et al. (2005)**
R. rubricarnata 8 x nda x nda Nouhra et al. (2005)**
R. rubripermanens 8 x nda x nda Nouhra et al. (2005)**
Russula abietina 1, x nda x nda Kernaghan et al. (1997)**
R. acrifolia 8 x nda x nda Agerer et al. (1996) (Picea abies)*
R. americana 8 x nda x nda Kernaghan et al. (1997)**
R. brevipes 3, 4, 8 x nda x nda Kernaghan et al. 1997 (Abies lasiocarpa)*
R. cf. chloroides 2 nda x nda x Kernaghan et al. (1997)**
R. delica 1, 5, 12 x nda x nda Beenken (2001) (Fagus sylvatica)*
R. emetica 1, 5 x nda x nda Kernaghan et al. (1997)**
R. aff. firmula 2 nda x nda x Treu (1990) (Pinus mugo)*
R. foetens 6 x nda x nda Beenken (2001) (Fagus sylvatica)**
R. aff. lepida 6 x nda x nda Kernaghan et al. (1997)**
R. mexicana 6 x nda x nda Kernaghan et al. (1997)**
R. olivacea 1, 8 x nda x nda Kernaghan et al. (1997)**
R. puellaris 5 x nda x nda Kernaghan et al. (1997)**
R. romagnesiana 8 x nda x nda Kernaghan et al. (1997)**
R. sanguinaria 8 x nda x nda Kernaghan et al. (1997)**
Sarcodon imbricatus 1, 5 x nda x nda Agerer (1990) (Picea abies)*
S. escabrosus 4 x nda x nda Agerer (1990) (Picea abies)*
Sebacina dimitica 2 nda x nda x de Román, Claveria, and de Miguel, (2005)**
S. incrustans 2 nda x nda x Urban, Weiss, and Bauer (2003) (Picea abies)**
Suillus americanus 5 x nda x nda Treu (1990)
S. brevipes 5 x nda x nda Bradbury (1998) (Pinus contorta)**
S. granulatus 1, 5 x nda x nda Yamada, Ogura, and Ohmasa (2001) (Pinus densiflora)*
S. guzmanii 5 x nda x nda Treu (1990)**
S. tomentosus 8 x nda x nda Bradbury (1998) (Pinus contorta)*
Thelephora terrestris 5 x nda x nda Agerer and Weiss (1989) (Picea abies)*
Tarzetta sp. 2 nda x nda x Tedersoo et al. (2006)**
Tomentella lateritia 2 nda x nda x Bradbury (1998)**
T. pilosa 2 nda x nda x de Román et al. (2005) (Quercus ilex)*
Tremelloscypha dichroa 2 nda x nda x Undetermined, only by phylogenies (Weiß & Oberwinkler, 2001)
Tricholoma equestre 1, 8 x nda x nda Comandini, Haug, Rinaldi, and Kuyper (2004)**
T. imbricatum 5 x nda x nda Comandini et al. (2004)**
T. terreum 5 x nda x nda Comandini et al. (2004)**
Trychophaea sp. 2 nda x nda x Undetermined
Tuber cf. separans 2 nda x nda X Comandini and Pacioni (1997)**
Xerocomus sp. 2 nda x nda X Torres and Honrubia (1997)**

nda: no data available.

*Species from which its ectomycorrhizal status has been determined in species of phytobionts other than Abies religiosa.

**Species of ectomycorrhizal fungi without status, only in other species of the same genus.

The references of the research studies correspond to the following authors:

Andrade-Torres, A., Oros-Ortega, I., Solís-Ramos, L. Y., Guzmán-Olmos, R. F., Lara-Pérez, L. A., Sánchez-Velásquez, L. R., & Rodríguez, V. (2015). Simbiosis ectomicorrízica y diversidad de hongos ectomicorrízicos en dos estados sucesionales del bosque de Abies religiosa (H. B. K.) Schl. et Cham., del Parque Nacional Cofre de Perote, Veracruz. In: M. R. Pineda-López, L. R. Sánchez-Velásquez, & J. Noa-Carrazana (Eds), Ecología, biotecnología y conservación del género Abies en México, Estudios de Abies en México (pp 81-105). México: Editorial Académica Española.

Argüelles-Moyao, A., Garibay-Orijel, R., Márquez-Valdelamar, L. M., & Arellano-Torres, E. (2017). Clavulina-Membranomyces is the most important lineage within the highly diverse ectomycorrhizal fungal community of Abies religiosa. Mycorrhiza, 27(1), 53-65. doi: 10.1007/s00572-016-0724-1

Arteaga-Martínez, B., & Moreno-Zárate, B. (2006). Los hongos comestibles silvestres de Santa Catarina del Monte, Estado de México. Revista Chapingo Serie Ciencias Forestales y del Ambiente, 12(2), 125-131. Retrieved from https://chapingo.mx/revistas/forestales/contenido.php?id_articulo=457

Burrola-Aguilar, C., Garibay-Orijel, R., & Argüelles-Moyao, A. (2013). Abies religiosa forests harbor the highest species density and sporocarp productivity of wild edible mushrooms among five different vegetation types in a neotropical temperate forest region. Agroforestry Systems, 87(5), 1101-1115. doi: 10.1007/s10457-013-9623-z

Córdova-Chávez, O., Medel, R., Mata, G., Castillo, R., & Vázquez-Ramírez, J. (2014). Evaluación de hongos ectomicorrícicos del grupo de los basidiomicetos en la zona del Cofre de Perote, Veracruz. Madera y bosques, 20(1), 97-106. doi: 10.21829/myb.2014.201179

García-Bastian, R. M., López-López, M. A., Velázquez-Martínez, A., & Pérez-Moreno, J. (1998). Mycorrhizal and saprotrophic macrofungi in declining sacred-fir stands. Micología Neotropical Aplicada, 11, 9-21. Retrieved from http://www.cabi.org/ISC/abstract/19991003440

Kong, A., & Estrada-Torres, A. (1994). A new species of Lactarius from Mexico. Mycotaxon, 52(2), 443-466.

Montoya, A., Kong, A., Estrada-Torres, A., Cifuentes, J., & Caballero, J (2004). Useful wild fungi of La Malinche National Park, Mexico. Fung Divers, 17, 15-43. Retrieved from http://www.fungaldiversity.org/fdp/sfdp/17-8.pdf

Oros-Ortega, I. (2015). Estructura de la comunidad de hongos ectomicorrizógenos en bosque de Abies religiosa (H. B. K.) Schl. et Cham, a través de un gradiente altitudinal. (Tesis Doctoral). Universidad Veracruzana, Xalapa, Veracruz, México.

Pérez-Silva, E., Herrera, T., & Ocampo-López, A. (2011). Nuevos registros de macromicetos para el municipio de Temascaltepec, Estado de México. Revista Mexicana de Micología, 34, 23-30. Retrieved from http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S018731802011000200005&lng=es&tlng=es.

Ramos-Fernández, A., López-Ramírez, F., Flores-Estevez, N., Jiménez-Montaño, M. A., Sánchez-Velásquez, L., Pineda-López, M., & Noa-Carrazana, J. (2013). An approach to finding enzymatic restriction patterns for molecular characterization of Amanita muscaria. Journal of Food, Agriculture & Environment, 11(1), 1099-1102. Retrieved from http://world-food.net/download/journals/2013-issue_1/2013-issue_1-environment/86.pdf

Valdés-Ramírez, M. (1972). Microflora of a coniferous forest of the mexican basin. Plant and Soil, 36(1-3), 31-38. doi: 10.1007/BF01373453

The ectomycorrhizal status was determined from the following reviews:

Agerer, R. (1987). Studies on ectomycorrhizae. X. Mycorrhizae formed by Cortinarius obtusus and C. venetus on spruce. Mycologia, 79(4), 524-539. doi: 10.2307/3807591

Agerer, R. (1990). Studies of ectomycorrhizae. XXIV. Ectomycorrhizae of Chroogomphus helveticus and C. rutilus (Gomphidiaceae, Basidiomycetes) and their relationship to those of Suillus and Rhizopogon. Nova Hedwigia, 50(1-2), 1-63. Retrieved from https://www.cabdirect.org/cabdirect/abstract/19902302879

Agerer, R. (1994). Pseudotomentella tristis (Thelephoraceae). An analysis of fruitbody and ectomycorrhiza. Zeitschrift für Mykologie, 60(1), 143-158. Retrieved from https://www.dgfm-ev.de/publikationen/artikelsuche?start=300

Agerer, R., & Beenken, L. (1998). Lyophyllum decastes (Fr.) Sing. + Quercus robur L. Descriptions of Ectomycorrhizae, 3, 43-47. Retrieved from http://www.nhbs.com/series/185718/descriptions-of-ectomycorrhizae

Agerer, R., Beenken, L., & Christan, J. (1998). Gomphus clavatus (Pers.: Fr.) SF Gray + Picea abies (L.) Karst. Descriptions of Ectomycorrhizae, 3, 25-29. Retrieved from http://www.nhbs.com/series/185718/descriptions-of-ectomycorrhizae

Agerer, R., Kraigher, H., & Javornik, B. (1996). Identification of ectomycorrhizae of Hydnum rufescens on Norway spruce and the variability of the ITS region of H. rufescens and H. repandum (Basidiomycetes). Nova Hedwigia, 63(1), 183-194. Retrieved from http://www.schweizerbart.de/journals/nova_hedwigia

Agerer, R., & Weiss, M. (1989). Studies on ectomycorrhizae. XX. Mycorrhizae formed by Thelephora terrestris on Norway spruce. Mycologia, 81(3), 444-453. doi: 10.2307/3760081.

Beenken, L. (2001). Russula nothofaginea Sing. + Nothofagus dombeyi (Mirbel) Oersted. Descriptions of Ectomycorrhizae, 5, 175-179. Retrieved from http://www.nhbs.com/series/185718/descriptions-of-ectomycorrhizae

Binder, M., & Hibbett, D. S. (2006). Molecular systematics and biological diversification of Boletales. Mycologia, 98(6), 971-981. doi: 10.1080/15572536.2006.11832626

Bradbury, S. M. (1998). Ectomycorrhizas of lodgepole pine (Pinus contorta) seedlings originating from seed in southwestern Alberta cut blocks. Canadian Journal of Botany, 76(2), 213-217. doi: 10.1139/b97-171

Brunner, I., Amiet, R., Zollinger, M., & Egli, S. (1992). Ectomycorrhizal syntheses with Picea abies and three fungal species: a case study on the use of an in vitro technique to identify naturally occurring ectomycorrhizae. Mycorrhiza, 2(2), 89-96. doi: 10.1007/BF00203255

Buée, M., Vairelles, D., & Garbaye, J. (2005). Year-round monitoring of diversity and potential metabolic activity of the ectomycorrhizal community in a beech (Fagus sylvatica) forest subjected to two thinning regimes. Mycorrhiza, 15, 235-245. doi: 10.1007/s00572-004-0313-6

Ceruti, A., Tozzi, M., & Reitano, G. (1987). Micorrize di sintesi tra Boletus edulis, Pinus sylvestris e Picea excelsa. Allionia, 28, 117-124.

Comandini, O., & Pacioni, G. (1997). Mycorrhizae of Asian black truffles, Tuber himalayense and T. indicum. Mycotaxon, 63, 77-86. Retrieved from http://www.mycotaxon.com/vol/63.html

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Received: November 09, 2016; Accepted: July 24, 2017

*Correspondence author: ivanoros1109@hotmail.com, tel: 9831674915

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