Enhancing morphophysiological traits by inoculating a neotropical pine (Pinus teocote) with edible ectomycorrhizal mushrooms grown in environmentally friendly substrates
Abstract
Aim of study: To evaluate the effect of inoculating Pinus teocote Schiede ex Schltdl. & Cham. plants, a neotropical pine species highly resilient to stress conditions, with two edible ectomycorrhizal mushrooms, Laccaria proxima (Boud.) Pat. and Suillus pungens Thiers & A.H.Sm., on their growth and physiological quality. The plants were grown in different environmentally friendly substrate combinations. Area of study: Bioassays were conducted in the greenhouses of the Colegio de Postgraduados in Texcoco, Mexico. Material and methods: The influence of L. proxima and S. pungens on P. teocote was assessed through growth and physiological parameters using three distinct substrate formulations, two of which incorporated mixtures of sawdust and compost. The evaluated variables included plant biomass, photosynthesis, transpiration, chlorophyll a, b, and total chlorophyll content, as well as carotenoids and ectomycorrhizal colonization, measured 570 days after sowing. Main results: High ectomycorrhizal colonization, exceeding 84%, was recorded in the plants grown in sawdust and compost mixtures. Additionally, increases in biomass and physiological quality were observed in these plants compared to non-inoculated plants. Depending on the substrate mixtures evaluated, the inoculation with S. pungens produced higher transpiration and chlorophyll a, b, total chlorophyll, and carotenoid content than that with L. proxima. Research highlights: It was demonstrated that the production of ectomycorrhizal Pinus teocote plants in greenhouse, with high morphophysiological quality and elevated mycorrhization rates, is feasible when using environmentally friendly substrates.
Downloads
References
Agerer R, Rambold G, 2009. DEEMY. An information system for characterization and determination of ectomycorrhizae. München, Germany.
Aguilera-Rodríguez M, Aldrete A, Martínez-Trinidad T, Ordaz-Chaparro VM, 2016a. Producción de Pinus pseudostrobus Lindl. con sustratos de serrín y fertilizantes de liberación controlada. Rev Mex Cien For 7, 7-20.
Aguilera-Rodríguez M, Aldrete A, Martínez-Trinidad T, Ordaz-Chaparro VM, 2016b. Producción de Pinus montezumae Lamb. con diferentes sustratos y fertilizantes de liberación controlada. Agrociencia 50, 107-118.
Atzori G, Pane C, Zaccardelli M, Cacini S, Massa D, 2021. The Role of Peat-Free Organic Substrates in the Sustainable Management of Soilless Cultivations. Agronomy 11, 1236. https://doi.org/10.3390/agronomy11061236
Barragán-Soriano JL, Perez-Moreno J, Almaraz-Suárez JJ, Carcaño-Montiel MC, Delgadillo-Martínez J, Cetina-Alcalá M, Mata G, 2022. Coinoculación de Pinus montezumae (Pinaceae) con un hongo comestible ectomicorrízico y bacterias promotoras de crecimiento vegetal. Acta Bot Mex 129, 1-17. https://doi.org/10.21829/abm129.2022.2024
Barragán-Soriano JL, Pérez-Moreno J, Almaraz-Suárez JJ, Carcaño-Montiel MG, Medrano-Ortiz KI, 2018. Inoculation with an edible ectomycorrhizal fungus and bacteria increases growth and improves the physiological quality of Pinus montezumae Lamb. Rev Chapingo Ser Hortic 24. https://doi.org/10.5154/r.rchscfa.2017.01.010
Barroetaveña C, Bassani VN, Rajchenberg M, 2012. Inoculación micorrízica de Pinus ponderosa en la Patagonia Argentina: colonización de las raíces, descripción de morfotipos y crecimiento de las plántulas en vivero. Bosque 33, 163-169. http://dx.doi.org/10.4067/S0717-92002012000200006
Calisti R, Regni L, Pezzolla D, Cucina M, Gigliotti G, Proietti P, 2023. Evaluating Compost from Digestate as a Peat Substitute in Nursery for Olive and Hazelnut Trees. Sustainability, 15, 282. https://doi.org/10.3390/su15010282
Carrasco-Hernández V, Pérez-Moreno J, Espinosa-Hernández V, Almaraz-Suárez JJ, Quintero-Lizaola R, Torres-Aquino M, 2010. Caracterización de micorrizas establecidas entre dos hongos comestibles silvestres y pinos nativos de México. Rev Mex Cienc Agríc 567-577.
Carrasco-Hernández V, Pérez-Moreno J, Espinosa-Hernández V, Almaraz-Suárez JJ, Quintero-Lizaola R, Torres-Aquino M, 2011. Contenido de nutrientes e inoculación con hongos ectomicorrízicos comestibles en dos pinos neotropicales. Rev Chil Hist Nat 84, 83-96. http://dx.doi.org/10.4067/S0716-078X2011000100006
Carrillo-Saucedo SM, Puente-Rivera J, Montes-Recinas S, Cruz-Ortega R, 2022. Lasmicorrizascomo una herramienta para la restauración ecológica. Acta Bot Mex 129. https://doi.org/10.21829/abm129.2022.1932
Castrillón M, de León J, Carvajal D, Osorio NW, 2015. Effectiveness of single and combined ectomycorrhizal inocula on three species of Pinus at Nursery. Commun Soil Sci Plant Anal 46, 169-179. https://doi.org/10.1080/00103624.2014.967856
Cherlet M, Hutchinson C, Reynolds J, Hill J, Sommer S, von Maltitz G, 2018. (Eds.) World Atlas of Desertification, Publication Office of the European Union, Luxembourg.
Choi DS, Quoreshi AM, Maruyama Y, Jin HO, Koike T, 2005. Effect of ectomycorrhizal infection on growth and photosynthetic characteristics of Pinus densiflora seedlings grown under elevated CO2 concentrations. Photosynthetica 43, 223-229.
Chu H, Wang C, Li Z, Wang H, Xiao Y, Chen J, Tang M, 2019. The dark septate endophytes and ectomycorrhizal fungi effect on Pinus tabulaeformis carr. seedling growth and their potential effects to pine wilt disease resistance. Forests 10, 140. https://doi.org/10.3390/f10020140
Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finaly RD, Wardle DA, Lindahl BD, 2013. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339 (6127): 1615-1618. https://doi.org/10.1126/science.1231923
CONAFOR, Comisión Nacional Forestal, 2023. Pinus teocote Schiede ex Schltdl. Secretaría del Medio Ambiente y Recursos Naturales. Mexico City: Comisión Nacional Forestal. http://www.conafor.gob.mx:8080/documentos/docs/13/983Pinus%20teocote.pdf [01 December 2023].
DEEMY, 2020. An information system for characterization and determination of ectomycorrhizae. http://www.deemy.de/ [19 December 2020].
Dick LA, Gardner TG, Frene JP, Heitman JL, Sucre EB, Leggett ZH, 2022. Forest floor manipulation effects on the relationship between aggregate stability and ectomycorrhizal fungi. For Ecol Manage 505: 119873. https://doi.org/10.1016/j.foreco.2021.119873
Erlandson SR, Margis R, Ramirez A, Nguyen N, Lofgren LA, Liao HL, Vilgalys R, Kennedy PG, Peay KG, 2022. Transcriptional acclimation and spatial differentiation characterize drought response by the ectomycorrhizal fungus Suillus pungens. New Phytol, 234: 1910-1913. https://doi.org/10.1111/nph.17816
Escobar-Alonso S, Rodríguez-Trejo DA, 2021. Pinus teocote Schiede ex Schlechtendal & Chamisso (Pinaceae). In: Semillas de especies forestales; Rodríguez-Trejo DA (ed.). pp: 271-274.
FAO. Food and Agriculture Organization of the Unites Nations, 2025. International Day of Forest 21 March.
Fregoso-Madueño JN, Goche-Télles JR, Rutiaga-Quiñones JG, González-Laredo RF, Bocanegra-Salazar M, Chávez-Simental JA, 2017. Alternative uses of sawmill industry waste. Rev Chapingo Ser Cienc For Ambient 23, 243-260. https://doi.org/10.5154/r.rchscfa.2016.06.040
Galindo-Flores G, Castillo-Guevara C, Campos-López A, Lara C, 2015. Caracterización de las ectomicorrizas formadas por Laccaria trichodermophora y Suillus tomentosus en Pinus montezumae. Bot Sci 93, 855-863. https://doi.org/10.17129/botsci.200
Gang Z, Li S, Meng Q, Niu Ch, Zhang X, Wa Q, 2023. A new type of highly efficient fir sawdust-based super adsorbent: Remove cationic dyes from wastewater. Surf Interfaces 36. https://doi.org/10.1016/j.surfin.2023.102637
Garibay-Orijel R, Morales-Marañon 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. https://doi.org/10.7550/rmb.29839
Kothe E, Bogdanova O, Abdulsalam OA, Ezediokpu MN, Krause K, 2025. Ectomycorrhizae for the rescue: ectomycorrhizosphere signaling in agroforestry and afforestation. In: The Mycota 16, Agricultural and Industrial Applications; Grüttner S, Kollath-Leiß K, Kempken F (eds.). Springer, Cham. https://doi.org/10.1007/978-3-031-81904-9_5
Kraj W, Grad B, 2013. Seasonal dynamics of photosynthetic pigment, protein and carbohydrate contents in Pinus sylvestris L. seedlings inoculated with Hebeloma crustuliniforme and Laccaria bicolor. J Plant Nutr 36, 633-650. https://doi.org/10.1080/01904167.2012.754035
Kuraishi S, Sakurai N, Tazaki K, Sadatoku K, 1992. A posible relationship between chlorophyll synthesis and endogenous cytokinin levels in whole seedlings and excised cotyledons of squash. In: Physiology and biochemistry of cytokinins in plants; Kaminek M, Mok DWS, Zažímalová E (ed.). pp: 283-288. SPB Academic Publishing, The Hague.
Li M, Wang H, Zhao X, Lu Z, Sun X, Ding G, 2021. Role of Suillus placidus in improving the drought tolerance of Masson pine (Pinus massoniana Lamb.) seedlings. Forests 12, 332. https://doi.org/10.3390/f12030332
Lichtenthaler HK, 1987. Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148, 350-382. https://doi.org/10.1016/0076-6879(87)48036-1
López-Gutiérrez A, Pérez-Moreno J, Hernández-Santiago F, Uscanga-Mortera E, García-Esteva A, Cetina-Alcalá VM, Xoconostle-Cázares B, 2018. Nutrient mobilization, growth and field survival of Pinus pringlei inoculated with three ectomycorrhizal. Bot sci 96 (2) https://doi.org/10.17129/botsci.1239
Martínez-Nevárez LE, Prieto-Ruíz JÁ, Sigala-Rodríguez JÁ, García-Rodríguez JL, Martínez-Reyes M, Carrillo-Parra A, Dominguez-Calleros PA, 2023. Growth and Ef ficiency in the Use of Nutrients of Pinus cooperi C. E. Blanco Seedlings Produced in Nurseries with a Controlled Release Fertilizer. Terra Latinoam 41, 1-12. https://doi.org/10.28940/terra.v41i0.1707
Martínez-Reyes M, Pérez-Moreno J, Villarreal-Ruiz L, Ferrera-Cerrato R, Xoconostle-Cázares B, Vargas-Hernández JJ, Honrubia-García M, 2012. Crecimiento y contenido nutrimental de Pinus greggii Engelm. inoculado con el hongo comestible ectomicorrízico Hebeloma mesophaeum (Pers.) Quél. Rev Chapingo Ser Cienc For Ambient 18, 183-192. https://doi.org/10.5154/r.rchscfa.2010.11.112
Massicotte HB, Melville LH, Peterson RL, 2005. Building a basidiocarp: a case study of Laccaria spp. fruitbodies in the extraradical mycelium of Pinus ectomycorrhizas. Mycologist 19, 141-149. https://doi.org/10.1017/S0269-915X(05)00402-7
Moctezuma LG, Flores A, 2020. Importancia económica del Pino (Pinus spp.) como recurso natural en México. Rev Mex Cienc Forestales 11(60). https://doi.org/10.29298/rmcf.v11i60.720
Pera J, Parladé J, 2005. Inoculación controlada con hongos ectomicorrícicos en la producción de planta destinada a repoblaciones forestales: estado actual en España. Investig Agrar Sist Recur For 14, 419-433.
Pérez-Moreno J, Read JD, 2004. Los hongos ectomicorrízicos, lazos vivientes que conectan y nutren a los árboles en la naturaleza. Interciencia 29, 239-247.
Pérez-Moreno J, Martínez-Reyes M, Yesca-Pérez A, Delgado-Alvarado A, Xoconostle-Cázares B, 2008. Wild mushroom markets in central México and a case study at Ozumba. Econ Bot 3, 425-436. https://doi.org/10.1007/s12231-008-9043-6
Pérez-Moreno J, Martínez-Reyes M, 2014. Edible ectomycorrhizal mushrooms: biofactories for sustainable development. In: Biosystems engineering: Biofactories for food production in the century XXI. Guevara-Gonzalez R, Torres-Pacheco I (ed.). pp: 151-233. Springer International Publishing. https://doi.org/10.1007/978-3-319-03880-3_6
Pérez-Moreno J, Martínez-Reyes M, Hernández-Santiago F, Ortiz-Lopez I, 2020. Climate Change, Biotechnology, and Mexican Neotropical Edible Ectomycorrhizal Mushrooms In: Mushrooms, Humans and Nature in a Changing World Perspectives from Ecological, Agricultural and Social Sciences; Pérez-Moreno J, Guerin-Laguette A, Flores-Arzú R, Fu-Qiang Y (eds). pp: 61-69. Springer NatureSwitzerland. Suiza. https://doi.org/10.1007/978-3-030-37378-8_3
Pérez-Moreno J, Guerin-Laguette A, Rinaldi AC, Yu F, Verbeken A, Hernández-Santiago F, Martínez-Reyes M, 2021. Edible mycorrhizal fungi of the world: What is their role in forest sustainability, food security, biocultural conservation and climate change? Plants People Planet 3, 471–490. https://doi.org/10.1002/ppp3.10199
Pickles BJ, Simard SW, 2017. Mycorrhizal networks and forest resilience to drought. In: Mycorrhizal mediation of soil: Fertility, structure, and carbon storage; Johnson NC, Gehring C, Jansa J. (ed.). pp: 319-339. Elsevier, Amsterdam.
Prieto RJÁ, Goche TJR, 2016. Las reforestaciones en México: Problemática y alternativas de solución. Editorial de la Universidad Juárez del Estado de Durango. Dgo., México. 79 pp.
Rincon A, Parlade J, Perea, J, 2005. Effects of ectomycorrhizal inoculation and the type of substrate on mycorrhization, growth and nutrition of containerised Pinus pinea L. seedlings produced in a commercial nursery. Ann For Sci 62, 817-822.
Rodríguez-Gutiérrez I, Ramírez-Martínez D, Garibay-Orijel R, Jacob-Cervantes V, Pérez-Moreno J, Ortega-Larrocea MDP, Arellano-Torres E, 2019. Sympatric species develop more efficient ectomycorrhizae in the Pinus-Laccaria symbiosis. Rev Mex Biodivers 90, 1-11. https://doi.org/10.22201/ib.20078706e.2019.90.2868
Salazar-Alemán T, García-Rivas JL, Garcia GB, Martínez-Reyes M, Pérez-Moreno J, Cortés-Sarabia J, 2023. Lyophilized biopolymeric beads of chitosan-xanthan with edible fungus Laccaria laccata (Scop.) Cooke as forest ectomycorrhizal biofertilizers. Agro Productividad 16, 79-85. https://doi.org/10.32854/agrop.v15i4.2411
Sánchez MJJ, Capulín-Grande J, Santana AMR, Islas SA, Moreno MB, 2014. Crecimiento de Acacia retinodes Schltdl. en sustratos a base de serrín de pino y envases tratados con cobre. Rev Cub Cienc For 2, 1-19.
SEMARNAT, 2025. Secretaría de Medio Ambiente y Recursos Naturales. Residuos sólidos urbanos: la otra cara de la basura. www.gob.mx 01/05/2025
SEMARNAT, 2021. Anuario Estadístico de la Producción Forestal. Secretaría del Medio Ambiente y Recursos Naturales. Mexico City.
Smaill SJ, Walbert K, 2013. Fertilizer and fungicide use increases the abundance of less beneficial ectomycorrhizal species in a seedling nursery. Appl Soil Ecol 65, 60-64. https://doi.org/10.1016/j.apsoil.2013.01.007
Smith SE. Read DJ, 2008. Mycorrhizal symbiosis. Third edition. Academic Press, UK. https://doi.org/10.1016/B978-0-12-370526-6.X5001-6
UNEP, 2024. Global Waste Management Outlook 2024. https://www.unep.org [01 May 2025] https://doi.org/10.59117/20.500.11822/44939
Vicente-Arbona JC, Carrasco-Hernández V, Rodríguez-Trejo DA, Villanueva-Morales A, 2019. Calidad de planta de Pinus greggii producida en sustratos a base de serrín. Madera Bosques 2, 1-14. https://doi.org/myb.2019.2521784
Villegas-Olivera JA, Pérez-Moreno J, Mata G, Almaraz-Suárez JJ, Ojeda-Trejo E, Espinosa-Hernández V, 2017. Type of light and formation of basidiomata of two species of edible ectomycorrhizal mushrooms associated with neo-tropical pines and the description of basidiomata development. Rev Fitotec Mex 40, 405-413. https://doi.org/10.35196/rfm.2017.4.405-413
Vodnik D, Gogala N, 1994. Seasonal fluctuations of photosynthesis and its pigments in 1-year mycorrhized spruce seedlings. Mycorrhiza 4, 277-281. https://doi.org/10.1007/BF00206777
Wang Y, Hall IR, 2004. Edible ectomycorrhizal mushrooms: challenges and achievements. Canad J Bot 82, 1063-1073. https://doi.org/10.1139/b04-051
Xu H, Kemppainen M, El Kayal W, Lee SH, Pardo AG, Cooke JE, Zwiazek JJ, 2015. Overexpression of Laccaria bicolor aquaporin JQ585595 alters root water transport properties in ectomycorrhizal white spruce (Picea glauca) seedlings. New Phytol 205, 757-770. https://doi.org/10.1111/nph.13098
Yin D, Deng X, Song R, 2016. Synergistic effects between Suilllus luteus and Trichoderma virens on growth of Korean spruce seedlings and drought resistance of scotch pine seedlings. J For Res 27, 193-201. https://doi.org/10.1007/s11676-015-0131-z
Yu SJ, Shen R, Lin DM, 2025. Research advances in the impacts of ectomycorrhizal fungi on the formation and decomposition of soil organic matter in forests. Ying Yong Sheng Tai Xue Bao 18; 36(3): 943-949. https://doi:10.13287/j.1001-9332.202503.034
Zhang ZX, 1986. Determination of chlorophyll content of plants - acetone and ethanol mixture method. Liaoning Agric Sci 3, 26-28
Zong K, Huang J, Nara K, Chen Y, Shen Z, Lian C, 2015. Inoculation of ectomycorrhizal fungi contributes to the survival of tree seedlings in a copper mine tailing. J For Res 20, 493-500. https://doi.org/10.1007/s10310-015-0506-1
Copyright (c) 2026 Consejo Superior de Investigaciones Científicas (CSIC)

This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the print and online versions of this journal are the property of the Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a Creative Commons Attribution 4.0 International (CC BY 4.0) licence. You may read the basic information and the legal text of the licence. The indication of the CC BY 4.0 licence must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the final version of the work produced by the publisher, is not allowed.









