Skip to main content

Advertisement

Log in

Clavulina-Membranomyces is the most important lineage within the highly diverse ectomycorrhizal fungal community of Abies religiosa

  • Original Article
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Abies religiosa is an endemic conifer of Mexico, where its monodominant forests are the winter refuge of the monarch butterfly. Due to climate change, it has been estimated that by 2090, A. religiosa populations will decline by 96.5 %. To achieve success, reforestation programs should consider its ectomycorrhizal (ECM) fungi. We used ITS nrDNA sequences to identify the ECM fungi associated with A. religiosa and, based on its abundance and frequency, determined the diversity and community structure in a pure A. religiosa forest near Mexico City. Using sequence metadata, we inferred the species geographic distribution and host preferences. We conducted phylogenetic analyses of the Clavulinaceae (the most important family). The ECM community held 83 species, among which the richest genera were Inocybe (21 species), Tomentella (10 species), and Russula (8 species). Besides its low species richness, the Clavulina-Membranomyces lineage was the most dominant family. Clavulina cf. cinerea and Membranomyces sp. exhibited the highest relative abundance and relative frequency values. Phylogenetic analyses placed the Clavulinaceae genotypes in three different clades: one within Membranomyces and two within Clavulina. A meta-analysis showed that the majority of the ECM fungi (45.78 %) associated with A. religiosa in Mexico have also been sequenced from North America and are shared by Pinaceae and Fagaceae. In contrast, because they have not been sequenced previously, 32.2 % of the species have a restricted distribution. Here, we highlight the emerging pattern that the Clavulina-Membranomyces lineage is dominant in several ECM communities in the Neotropics, including Aldinia and Dicymbe legume tropical forests in the Guyana Shield, the Alnus acuminata subtropical communities, and the A. religiosa temperate forests in Mexico.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ángeles-Argáiz RE, Flores-García A, Ulloa M, Garibay-Orijel R (2016) Commercial Sphagnum peat moss is a vector for exotic ectomycorrhizal mushrooms. Biol Invasions 18:89–101. doi:10.1007/s10530-015-0992-2

    Article  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic alignment search tool. J Mol Ecol 215:403–410. doi:10.1016/S0022-2836(05)80360-2

    CAS  Google Scholar 

  • Avis PG (2012) Ectomycorrhizal iconoclasts: the ITS rDNA diversity and nitrophilic tendencies of fetid Russula. Mycologia 104:998–1007. doi:10.3852/11-399

    Article  CAS  PubMed  Google Scholar 

  • Bahram M, Kõljalg U, Courty PE et al (2013) The distance decay of similarity in communities of ectomycorrhizal fungi in different ecosystems and scales. J Ecol 101:1335–1344. doi:10.1111/1365-2745.12120

    Article  Google Scholar 

  • Bonito GM, Gryganskyi AP, Trappe JM, Vilgalys R (2010) Global meta-analysis of Tuber ITS rDNA sequences: species diversity, host associations and long-distance dispersal. Mol Ecol 19:4994–5008

    Article  CAS  PubMed  Google Scholar 

  • Bringham MA, Simard S (2011) Ectomycorrhizal networks of Pseudotsuga menziesii var. glauca trees facilitate establishment of conspecific seedlings under drought. Ecosystems 15:188–199. doi:10.1007/s10021-011-9502-2

    Article  Google Scholar 

  • 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. Agrofor Syst 87:1101–1115. doi:10.1007/s10457-013-9623-z

    Article  Google Scholar 

  • Eckenwalder JE (2009) Conifers of the world: the complete reference. Timber press, London

    Google Scholar 

  • Fa JE, Morales LM (1998) Patrones de diversidad de mamíferos de México. In: Ramamoorthy TP, Bye R, Lot A, Fa JE (eds) Diversidad biológica de México: orígenes y distribución. Instituto de Biología. UNAM, México, pp 315–352

    Google Scholar 

  • García-Palomo A, Zamorano JJ, López-Miguel C, Galván-García A, Carlos-Valerio V, Ortega R, Macías JL (2008) El arreglo morfoestructural de la Sierra de Las Cruces, México central. Rev Mex Cienc Geol 25:158–178

    Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. doi:10.1111/j.1365-294X.1993.tb00005.x

    Article  CAS  PubMed  Google Scholar 

  • Garibay-Orijel R, Morales-Marañón E, Domínguez-Gutiérrez M, Flores-García A (2013) Caracterización morfológica y genética de las ectomicorrizas formadas entre Pinus montezumae y los hongos presentes en los bancos de esporas en la Faja Volcánica Transmexicana. Rev Mex Biodivers 84:153–169. doi:10.7550/rmb.29839

    Article  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology: peeking into the black box. Mol Ecol 10:1855–1871. doi:10.1046/j.0962-1083.2001.01333.x

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • INEGI. Instituto Nacional de Estadística, Geografía e Informática (2011) Anuario estadístico del Estado de México. http://inegi.mx/est/contenidos/espanol/sistemas/aee11/info/mex/mapas.pdf. Accessed 14 May 2013

  • Ishida TA, Kazuhide N, Hogetsu T (2007) Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer-broadleaf forests. New Phytol 174:430–472. doi:10.1111/j.1469-8137.2007.02016.x

    Article  CAS  PubMed  Google Scholar 

  • Izzo A, Agbowo J, Bruns TD (2005) Detection of plot-level changes in ectomycorrhizal communities across years in an old-growth mixed-conifer forest. New Phytol 166:619–630. doi:10.1111/j.1469-8137.2005.01354.x

    Article  PubMed  Google Scholar 

  • Jujnovsky J, González-Martínez TM, Cantoral-Uriza EA, Almeida-Leñero L (2012) Assessment of water supply as an ecosystem service in a rural-urban watershed in southwestern Mexico City. Environ Manag 49:690–702. doi:10.1007/s00267-011-9804-3

    Article  Google Scholar 

  • Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298. doi:10.1093/bib/bbn013

    Article  CAS  PubMed  Google Scholar 

  • Kennedy PG, Garibay-Orijel R, Higgins LM, Ángeles-Argáiz R (2011) Ectomycorrhizal fungi in Mexican Alnus forests support the host co- migration hypothesis and continental-scale patterns in phylogeography. Mycorrhiza 6:559–568. doi:10.1007/s00572-011-0366-2

    Article  Google Scholar 

  • Kennedy PG, Matheny PB, Ryberg KM et al (2012) Scaling up: examining the macroecology of ectomycorrhizal fungi. Mol Ecol 21:4151–4154. doi:10.1111/j.1365-294X.2012.05703.x

    Article  PubMed  Google Scholar 

  • Kong A, Cifuentes J, Estrada-Torres A, Guzmán-Dávalos L, Garibay-Orijel R, Buyck B (2015) Russulaceae associated with mycoheterotroph Monotropa uniflora (Ericaceae) in Tlaxcala, Mexico: a phylogenetic approach. Cryptogam Mycol 36(4):479–512. doi:10.7872/crym/v36.iss4.2015.479

    Article  Google Scholar 

  • Kranabetter JM, Durall DM, MacKenzie WH (2009) Diversity and species distribution of ectomycorrhizal fungi along productivity gradients of a southern boreal forest. Mycorrhiza 19:99–162. doi:10.1007/s00572-008-0208-z

    Article  CAS  PubMed  Google Scholar 

  • Krzywinski M, Schein J, Birol I et al (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645. doi:10.1101/gr.092759.109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Looney BP, Ryberg M, Hampe F, Sanchez-Garcia M, Matheny PB (2016) Into and out of the tropics: global diversification patterns in a hyperdiverse clade of ectomycorrhizal fungi. Mol Ecol 25:630–647

    Article  PubMed  Google Scholar 

  • Larsson KH, Larsson E, Kõljalg U (2004) High phylogenetic diversity among corticioid homobasidiomycetes. Mycol Res 108:983–1002. doi:10.1017/S0953756204000851

    Article  CAS  PubMed  Google Scholar 

  • Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75 http://mesquiteproject.org

  • Manzo-Delgado L, López-García J, Alcántara-Ayala I (2013) Role of forest conservation in lessening land degradation in a temperate region: the Monarch Butterfly Biosphere Reserve, Mexico. J Environ Manage. doi:10.1016/j.jenvman.2013.11.017

    PubMed  Google Scholar 

  • Matheny PB, Aime MC, Bougher NL, Buyck B, Desjardin DE, Horak E, Kropp BR, Lodge DJ, Soytong K, Trappe JM, Hibbett DS (2009) Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae. J Biogeogr 36:577–592

    Article  Google Scholar 

  • Meiser A, Balint M, Schmitt I (2014) Meta-analysis of deep-sequenced fungal communities indicates limited taxon sharing between studies and the presence of biogeographic patterns. New Phytol 201:623–635. doi:10.1111/nph.12532

    Article  CAS  PubMed  Google Scholar 

  • McAleece N, Lambsshead P, Paterson G, Gage I (1997) Biodiversity Professional V2.0. The Natural History Museum and the Scottish Association for Marine Science, Argyll, Scotland

    Google Scholar 

  • Miranda-Aragón L, Treviño-Garza EJ, Jiménez-Pérez J et al (2012) Modeling susceptibility to deforestation of remaining ecosystems in North Central Mexico with logistic regression. J For Res 23:345–354. doi:10.1007/s11676-012-0230-z

    Article  Google Scholar 

  • Montoya A, Kong A, Estrada-Torres A, Cifuentes J, Caballero J (2005) Useful wild fungi of La Malinche National Park, Mexico. Fungal Divers 17:115–143

    Google Scholar 

  • Montoya A, Torres-García EA, Kong A, Estrada-Torres A, Caballero J (2012) Gender differences and regionalization of the cultural significance of wild mushrooms around La Malinche volcano, Tlaxcala, Mexico. Mycologia 1004:826–834. doi:10.3852/11-347

    Article  Google Scholar 

  • Morris MH, Pérez-Pérez MA, Smith ME, Bledsoe CS (2009) Influence of host species on ectomycorrhizal communities associated with two co-occurring oaks (Quercus spp.) in a tropical cloud forest. FEMS Microbiol Ecol 69:274–287

    Article  CAS  PubMed  Google Scholar 

  • Nilsson R, Kristiansson E, Ryberg M, Hallenberg N, Larsson K-H (2008) Intraspecific ITS variability in the kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Bioinform Online 4:193–201

    PubMed  PubMed Central  Google Scholar 

  • Olariaga I, Jugo BM, García-Etxebarria K, Salcedo I (2009) Species delimitation in the European species of Clavulina (Cantharellales, Basidiomycota) inferred from phylogenetic analyses of ITS region and morphological data. Mycol Res 113:1261–1270. doi:10.1016/j.mycres.2009.08.008

    Article  CAS  PubMed  Google Scholar 

  • Oberwinkler F, Riess K, Bauer R, Garnica S (2014) Morphology and molecules: the Sebacinales, a case study. Mycol Prog 13:445–470. doi:10.1007/s11557-014-0983-1

    Article  Google Scholar 

  • Pacheco-Cobos L, Rosetti M, Cuatianquiz C, Hudson R (2010) Sex differences in mushroom gathering: men expend more energy to obtain equivalent benefits. Evol Hum Behav 31:289–297. doi:10.1016/j.evolhumbehav.2009.12.008

    Article  Google Scholar 

  • Peay KG, Kennedy PG, Bruns TD (2008) Fungal community ecology: a hybrid beast with a molecular master. Bioscience 58:799–810. doi:10.1641/B580907

    Article  Google Scholar 

  • Peay KG, Bidartondo MI, Arnold AE (2010) Not every fungus is everywhere: scaling to the biogeography of fungal-plant interactions across roots, shoots and ecosystems. New Phytol 185:865–867

    Article  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. doi:10.1093/molbev/msn083

    Article  CAS  PubMed  Google Scholar 

  • Reverchon F, Ortega-Larrocea MP, Pérez-Moreno J, Peña-Ramirez VM, Siebe C (2010) Changes in community structure of ectomycorrhizal fungi associated with Pinus montezumae across a volcanic soil chronosequence at Sierra Chichinautzin, México. Can J For Res 40:1165–1174

    Article  CAS  Google Scholar 

  • Rudawska M, Pietras M, Smutek I et al (2016) Ectomycorrhizal fungal assemblages of Abies alba Mill. outside its native range in Poland. Mycorrhiza 26(1):57–65. doi:10.1007/s00572-015-0646-3

    Article  PubMed  Google Scholar 

  • Ryberg M, Nilsson RH, Kristiansson E, Töpel M, Jacobsson S, Larsson E (2008) Mining metadata from unidentified ITS sequences in GenBank: a case study in Inocybe (Basidiomycota). BMC Evol Biol 8:50. doi:10.1186/1471-2148-8-50

    Article  PubMed  PubMed Central  Google Scholar 

  • Rzedowski J (1991) Diversidad y orígenes de la flora fanerogámica de México. Acta Bot Mex 14:3–21

    Google Scholar 

  • Rzedowski J (2006) Capítulo 17. Bosque de coníferas. In: Rzedowski J (2006) Vegetación de México. First digital edition. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Mexico, pp 295–327.

  • Sáenz-Romero C, Rehfeldt GE, Duval P, Lindig-Cisneros RA (2012) Abies religiosa habitat prediction in climatic change scenarios and implications for monarch butterfly conservation in Mexico. For Ecol Manag 275:98–106. doi:10.1016/j.foreco.2012.03.004

    Article  Google Scholar 

  • Setaro SD, Garnica S, Herrera PI, Suárez JP, Göker M (2012) A clustering optimization strategy to estimate species richness of Sebacinales in the tropical Andes based on molecular sequences from distinct DNA regions. Biodivers Conserv 21:2269–2285. doi:10.1007/s10531-011-0205-y

    Article  Google Scholar 

  • Schirkonyer U (2013) Ectomycorrhizal diversity at five different tree species in forests of the Taunus Mountains in Central Germany. Open J Ecol 3:66–81. doi:10.4236/oje.2013.31009

    Article  Google Scholar 

  • Sjökvist E, Pfeil BE, Larsson E, Larsson KH (2014) Stereopsidales—a new order of mushroom-forming fungi. PLoS One 9(4):e95227. doi:10.1371/journal.pone.0095227

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith ME, Henkel TW, Catherine-Aime M, Fremier AK, Vilgalys R (2011) Ectomycorrhizal fungal diversity and community structure on three co-occurring leguminous canopy tree species in a Neotropical rainforest. New Phytol 192:699–712. doi:10.1111/j.1469-8137.2011.03844.x

    Article  PubMed  Google Scholar 

  • Talbot JM, Bruns TD, Taylor JW, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Liaoc HL, Smith ME, Peay KG (2014) Endemism and functional convergence across the North American soil mycobiome. PNAS 111(17):6341–6346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tse-Laurence MA, Bidartondo MI (2011) Mapping fungi from below ground: online genetic resources and ectomycorrhizal geographic distributions. iForest 4:252–255. doi:10.3832/ifor0599-008

    Article  Google Scholar 

  • Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263. doi:10.1007/s00572-009-0274-x

    Article  PubMed  Google Scholar 

  • Tedersoo L, Abarenkov K, Nilsson RH, Schüssler A, Grelet WA, Kohout P, Oja J, Bonito GM, Veldre V, Jairus T, Ryberg M, Larsson KH, Kõljalg U (2011) Tidying up international nucleotide sequence databases: ecological, geographical and sequence quality annotation of ITS sequences of mycorrhizal fungi. PLoS One 6:e24940. doi:10.1371/journal.pone.0024940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tedersoo L, Bahram M, Põlme S et al (2014) Global diversity and geography of soil fungi. Science 346:1078. doi:10.1126/science.1256688

    Article  CAS  Google Scholar 

  • Uehling JK, Henkel TW, Vilgalys R, Smith ME (2012) Membranomyces species are common ectomycorrhizal symbionts in Northern Hemisphere forests. Mycorrhiza 22:577–581. doi:10.1007/s00572-012-0457-8

    Article  PubMed  Google Scholar 

  • Villela OF (1998) Herpetofauna de México: distribución y endemismo. In: Ramamoorthy TP, Bye R, Lot A, Fa JE (eds) Diversidad biológica de México: orígenes y distribución. Instituto de Biología. UNAM, México, pp 251–278

    Google Scholar 

  • Ważny R (2014) Ectomycorrhizal communities associated with silver fir seedlings (Abies alba Mill.) differ largely in mature silver fir stands and in Scots pine forecrops. Ann For Sci 71:801–810. doi:10.1007/s13595-014-0378-0

    Article  Google Scholar 

  • Weiß M, Waller F, Zuccaro A, Selosse M-A (2016) Sebacinales—one thousand and one interactions with land plants. New Phytol 211:20–40. doi:10.1111/nph.13977

    Article  PubMed  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR Protocols: a guide to methods and applications. Academic Press, CA, USA, pp 315–322

    Google Scholar 

  • Xiang Q, Xiang JQ, Guo Y, Zhang X (2009) Phylogeny of Abies (Pinaceae) inferred from nrITS sequence data. Taxon 58:141–152. doi:10.1046/j.0028-646x.2003.00792.x

    Google Scholar 

Download references

Acknowledgments

This research was funded by the Universidad Nacional Autónoma de México grant PAPIIT-IN218210 and by the Consejo Nacional de Ciencia y Tecnología grant CONACYT-239266. AAM received from Consejo Nacional de Ciencia y Tecnología (CONACYT) two fellowships for graduate studies 314537 and 374558. This article is a requisite for AAM to obtain the PhD degree by the Posgrado en Ciencias Biologicas, UNAM. AAM offers recognition to Julieta Alvarez Manjarrez for her invaluable help in the phylogenetic analyses. We thank the contribution of two anonymous reviewers and the editor.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roberto Garibay-Orijel.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 1581 kb)

Supplementary Table 1

(PDF 135 kb)

Supplementary Table 2

(PDF 165 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-016-0724-1

Keywords

Navigation