SpringerLink
Log in

Synergistic effects of Amanita stranella and Suillus decipiens inoculation on morphological features and phenolic compounds of Pinus pseudostrobus var. coatepecensis, a narrow endemic Mexican variety

  • Published:
New Forests Aims and scope Submit manuscript

Abstract

The effect of an inoculum composed of Amanita stranella and Suillus decipiens was evaluated on morphological features and total phenolic compounds in seedlings of Pinus pseudostrobus var. coatepecensis – a narrow endemic Mexican variety. The treatments were used: (1) A. stranella; (2) S. decipiens; (3) combined inoculum and (4) control, using a completely randomized design with 12 seedlings per treatment. The morphotype descriptions of both fungi significantly facilitate their identification in the field. The results showed significant differences in plant growth among the treatment groups. Seedlings treated with the combined treatment exhibited remarkable increases in height, surpassing the A. stranella, S. decipiens treatments, and the control group by 21.81%, 28.83%, and 59%, respectively. Moreover, the root collar diameter in the combined treatment group measured 2.53 cm, contrasting with the control group, 1.05 cm. Additionally, the shoot height/root length ratio and Dickson’s index were both close to 1 in the combined treatment, suggesting a well-developed root system in relation to the above-ground part of the plant. The percentage of ectomycorrhizal root colonization showed no significant differences among the inoculated treatments. Furthermore, the combined treatment significantly increased the total phenolic content in plants (39.2 mg GAE g− 1). Therefore, the combined inoculation of P. pseudostrobus var. coatepecensis seedlings with A. stranella and S. decipiens is recommended during the nursery stage for reforestation practices.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Agerer R, Rambold G. (2004–2021) DEEMY - an information system for characterization and determination of ectomycorrhizae. München, Germany. Retrieved January 2023, from http://www.deemy.de

  • Aragón-Peralta RD (2019) Eficiencia reproductiva y calidad de progenie de Pinus pseudostrobus Lindl var oaxacana en Oaxaca. Dissertation. Instituto Tecnológico de Valle de Oaxaca

  • Ávila-Flores IJ, Prieto-Ruíz JA, Hernández-Díaz JC, Whehenkel CA, Corral-Rivas JJ (2014) Preacondicionamiento De Pinus engelmannii Carr mediante déficit de riego en vivero. Revista Cha**o Serie Ciencias Forestales Y Del Ambiente 20(3):237–245. https://doi.org/10.5154/r.rchscfa.2014.02.004

    Article  Google Scholar 

  • 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. Revista Cha**o Serie Ciencias Forestales Y Del Ambiente 24(1):3–16. https://doi.org/10.5154/r.rchscfa.2017.01.010

    Article  Google Scholar 

  • Bidartondo MI, Ek H, Wallander H, Söderström B (2001) Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytol 151(2):543–550. https://doi.org/10.1046/j.1469-8137.2001.00180.x

    Article  CAS  Google Scholar 

  • 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. Revista Mexicana De Ciencias Agrícolas 1(4):567–577

    Google Scholar 

  • 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. Revista Chil de Historia Nat 84(1):83–96. https://dx doi org/104067/S0716-078X2011000100006

    Article  Google Scholar 

  • Carrasco Hernández V, Rodríguez Trejo DA, Pérez Moreno J, Duarte Zaragoza VM, Navarro Sandoval JL, Quintero Lizaola R (2018) Evaluación Del costo de producción de inoculantes ectomicorrízicos neotropicales a base de esporas. Revista Mexicana De Ciencias Agrícolas 9(2):417–429. https://doi.org/10.29312/remexca.v9i2.1082

    Article  Google Scholar 

  • Castaño C, Suarez-Vidal E, Zas R, Bonet JA, Oliva J, Sampedro L (2023) Ectomycorrhizal fungi with hydrophobic mycelia and rhizomorphs dominate in young pine trees surviving experimental drought stress. Soil Biol Biochem 178:108932. https://doi.org/10.1016/j.soilbio.2022.108932

    Article  CAS  Google Scholar 

  • Castrillón M, León JD, 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(2):169–179. https://doi.org/10.1080/00103624.2014.967856

    Article  CAS  Google Scholar 

  • Charya LS, Garr S (2019) Advances in methods and practices of ectomycorrhizal research In: Meena SN, Naik MM (ed) Advances in Biological Science Research: A Practical Approach. Academic Press, London, UK, pp 303–325. https://doi.org/10.1016/B978-0-12-817497-5.00019-7

    Chapter  Google Scholar 

  • Chen YL, Liu RJ, Bi YL, Feng G (2014) Use of mycorrhizal fungi for forest plantations and minisite rehabilitation. Mycorrhizal fungi: use in sustainable agriculture and land restoration. Springer, Berlin Heidelberg, pp 325–355

    Chapter  Google Scholar 

  • Chávez-García AS, Hernández-Ramos J, Muñoz-Flores HJ, García-Magaña JJ, Gómez-Cárdenas M, Gutiérrez-Contreras M (2022) Plasticidad fenotípica De progenies de árboles de Pinus Pseudostrobus Lindl superiores en producción de resina en vivero. Madera y Bosques 28(1):e2812381. https://doi.org/10.21829/myb.2022.2812381

    Article  Google Scholar 

  • Crane S, Dighton J, Barkay T (2010) Growth responses to and accumulation of mercury by ectomycorrhizal fungi. Fungal Biology 114(10):873–880. https://doi.org/10.1016/j.funbio.2010.08.004

    Article  CAS  PubMed  Google Scholar 

  • De la Fuente J, Ayala-Vásquez O, Garza-Ocañas F, López CY, García-Jiménez J (2018) Some interesting Boletales (Basidiomycota) from Quintana Roo. Mexico Scientia Fungorum 48:77–86. https://doi.org/10.33885/sf.2018.48.1201

    Article  Google Scholar 

  • Domínguez-Núñez A, Albanesi A (2020) Ectomycorrhizal Fungi as Biofertilizers in Forestry. Biostimulants in Plant Science. https://doi.org/10.5772/intechopen.88585

    Article  Google Scholar 

  • Duran Manual F, Geada López G, Martínez Becerra LW, Pérez Pereda E, Massó Matos J (2017) Diagnose of species of ectomycorrhizal mushrooms in a natural forest of Pinus cubensis Griseb affected for the fire. Revista Cubana de Ciencias Forestales 5(2): 61–171

  • Escobar-Alonso S, Rodríguez Trejo DA (2019) Estado Del arte en la investigación sobre calidad de planta del género Pinus en México. Revista Mexicana De Ciencias Forestales 10(55):4–38. https://doi.org/10.29298/rmcf.v10i55.558

    Article  Google Scholar 

  • Estrada-Valdés G, Endara Agramont AR, Vazquez-Lozada S, Todd FS (2021) Forest harvesting impacts on the structure and composition of coniferous forests in Mexico. Forests 12:1068. https://doi.org/10.3390/f12081068

    Article  Google Scholar 

  • Flores-Rentería D, Barradas VL, Álvarez-Sánchez J (2018) Ectomycorrhizal pre-inoculation of Pinus Hartwegii and Abies religiosa is replaced by native fungi in a temperate forest of. Cent Mexico Symbiosis 74(2):131–144. https://doi.org/10.1007/s13199-017-0498-z

    Article  CAS  Google Scholar 

  • Galindo-García F, Valdés RC, Sanchez Peña S, Gonzalez Morales S, Mendoza Villarreal R (2019) Improved parameters of Pinus greggii seedling growth and health after inoculation with ectomycorrhizal fungi. Southern Forests: a Journal of Forest Science, 81(1), 23–30: https://hdl.handle.net/10520/EJC-178acc24b9

  • García-Valencia LE, Pérez-García J, Vallejo-Reyna MÁ, Reynoso-Santos R, Vargas-Hernández J, García-Campusano F (2022) cpSSR and high-resolution melting analysis (HRM) for Pinus Pseudostrobus Lindl Variety Genoty** and discrimination. Forests 13(2):200. https://doi.org/10.3390/f13020200

    Article  Google Scholar 

  • Gómez-Romero M, Villegas J, Sáenz-Romero C, Lindig-Cisneros R (2013) Efecto De La micorrización en El establecimiento de Pinus pseudostrobus en cárcavas. Madera y Bosques 19(3):51–63

    Article  Google Scholar 

  • Herrera-Hernández R (2022) Producción y calidad de semilla de Pinus montezumae Lambert de ocho poblaciones en el centro de México. Thesis. Colegio de Postgraduados, Estado de México

  • Jörgensen K, Clemmensen KE, Wallander H, Lindahl BD (2023) Do ectomycorrhizal exploration types reflect mycelial foraging strategies? New Phytol 237:576–584. https://doi.org/10.1111/nph.18566

    Article  CAS  PubMed  Google Scholar 

  • Jurado Teixeira B, Aparcana Ataurima IM, Villarreal Inca LS, Ramos Llica E, Calixto Cotos MR, Hurtado Manrique PE, Acosta Alfaro KM (2016) Evaluación Del contenido de polifenoles totales Y La Capacidad Antioxidante De Los Extractos etanólicos De Los frutos de aguaymanto (Physalis peruviana L.) de diferentes lugares del Perú. Revista De La Sociedad química Del Perú 82(3):272–279

    Article  Google Scholar 

  • López-Gutiérrez A, Pérez-Moreno J, Hernández-Santiago F, Uscanga-Mortera E, García-Esteva A, Cetina-Alcalá VM, Cardoso-Villanueva MR, Xoconostle-Cázares B (2018) Nutrient mobilization growth and field survival of Pinus pringlei inoculated with three ectomycorrhizal mushrooms. Bot Sci 96(2):286–304. https://doi.org/10.17129/botsci.1239

    Article  Google Scholar 

  • Lu J, Aronen T, Pappinen A, Asiegbu FO (2011) Response of somatic embryos of Scots pine to fungal cell wall elicitors Summary Forest Pathology 41(1):75–82. https://doi.org/10.1111/efp.2011.41.issue-1https://doi.org/10.1111/j.1439-0329.2010.00641.x

  • Martignoni MM, Garnier J, Zhang X, Rosa D, Kokkoris V, Tyson RC, Hart MM (2021) Co-inoculation with arbuscular mycorrhizal fungi differing in carbon sink strength induces a synergistic effect in plant growth. J Theor Biol 531:110859. https://doi.org/10.1016/j.jtbi.2021.110859

    Article  CAS  PubMed  Google Scholar 

  • Moser B, Bachofen C, Müller JD, Metslaid M, Wohlgemuth T (2016) Root architecture might account for contrasting establishment success of Pseudotsuga menziesii var. menziesii and Pinus sylvestris in Central Europe under dry conditions. Ann for Sci 73:959–970. https://doi.org/10.1007/s13595-016-0574-1

    Article  Google Scholar 

  • Napierała-Filipiak A, Werner Piotr A, Karolewski P (2002) Content of phenolics in mycorrhizal roots of Pinus sylvestris seedlings grown in vitro Acta Physiologiae Plantarum 24(3):243–247. https://doi.org/10.1007/s11738-002-0047-z

  • Nguyen NH, Vellinga EC, Bruns TD, Kennedy PG (2016) Phylogenetic assessment of global suillus ITS sequences support morphologically defined species and reveals synonymous and undescribed taxa. Mycologia 108(6):1216–1228. https://doi.org/10.3852/16-106

    Article  PubMed  Google Scholar 

  • Niemi K, Julkunen-Tiitto R, Häggman H, Sarjala T (2007) Suillus Variegatus causes significant changes in the content of individual polyamines and flavonoids in scots pine seedlings during mycorrhiza formation in vitro. J Exp Bot 58(3):391–401. https://doi.org/10.1093/jxb/erl209

    Article  CAS  PubMed  Google Scholar 

  • Nisca A, Ștefănescu R, Stegăruș DI, Mare AD, Farczadi L, Tanase C (2021) Phytochemical profile and biological effects of spruce (Picea abies) bark subjected to Ultrasound assisted and microwave-assisted extractions. Plants 10(5):870. https://doi.org/10.3390/plants10050870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reis FS, Ferreira IC, Martins A (2012) Effect of the mycorrhizal symbiosis time in the antioxidant activity of fungi and Pinus pinaster roots stems and leaves. Ind Crops Prod 35(1):211–216. https://doi.org/10.1016/j.indcrop.2011.06.038

    Article  Google Scholar 

  • Restrepo-Llano MF, Osorio-Vega NW, León-Peláez JD (2018) Plant growth response of Pinus patula and P. Maximinoi seedlings at nursery to three types of ectomycorrhizal inocula. Appl Environ Soil Sci 1–8. https://doi.org/10.1155/2018/6027351

  • Rodríguez-Gutiérrez I, Ramírez-Martínez D, Garibay-Orijel R, Jacob-Cervantes V, Pérez-Moreno J, Ortega-Larrocea MP, Arellano-Torres Elsa (2019) Sympatric species develop more efficient ectomycorrhizae in the Pinus-Laccaria symbiosis. Revista Mexicana De Biodiversidad 90, e902868

  • Rodríguez-Ortiz G, Aragón-Peralta RD, Enríquez-del Valle JR, Hernández-Hernández A, Santiago-García W, Campos-Angeles GV (2020) Calidad De plántula de progenies selectas de Pinus Pseudostrobus Lindl. Var oaxacana del sur de México. Interciencia 45(2):96–101

    Google Scholar 

  • Salcido-Ruiz S, Prieto-Ruíz JA, García-Rodríguez JL, Santana-Aispuro E, Chávez-Simental JA (2020) Mycorrhiza and fertilization: effect on the production of Pinus engelmannii Carr in nursery. Revista Cha**o Serie Ciencias Forestales Y Del Ambiente 26(3):327–342. https://doi.org/10.5154/r.rchscfa.2019.11.080

    Article  Google Scholar 

  • Secretaría de Economía (2016) Norma Mexicana NMX-AA-170-SCFI-2016. Certificación de la operación de viveros forestales. http://sivicoff.cnf.gob.mx/ContenidoPublico/10 Material de Consulta/Normatividad Vigente/NMX-AA-170-SCFI-2016.pdf (12 nov 2022)

  • Sáenz-Reyes JT, Muñoz Flores H, Pérez C, Rueda Sánchez A, Hernández Ramos J (2014) Calidad De planta de tres especies de pino en El vivero Morelia Estado De Michoacán. Revista Mexicana De Ciencias Forestales 5(26):98–111

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. 3rd Edition Academic Press London

  • Tapwal A, Kapoor KS, Thakur Y (2022) Growth enhancement in containerized Pinus gerardiana seedlings inoculated with ectomycorrhizal fungi. Archives of Microbiology 204 (12):724 https://doi.org/10.1007/s00203-022-03328-4

  • Tulloss RE, Yang ZL (2015) Subsection Pantherinae. In: Tulloss RE, Yang ZL, eds. Amanitaceae studies. Available from: http://amanitaceae.org/?Amanita%20stranella

  • Valdés-Ramírez M, Ambriz-Parra E, Camacho-Vera A, Fierros González AM (2010) Inoculación De plántulas de pinos con diferentes hongos e identificación visual de la ectomicorriza. Revista Mexicana De Ciencias Forestales 1:53–63

    Article  Google Scholar 

  • Zhang R, Mueller GM, Shi X, Pei-gui L (2017) Two new species in the Suillus spraguei complex from China. Mycologia 109(2):296–307. https://doi.org/10.1080/00275514.2017.1305942

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are thankful to Universidad Autónoma Metropolitana (UAM) for supporting the project and Laboratorio de Organismos Benéficos at Universidad Veracruzana for providing equipment to carry out the experiment; also grateful to the anonymous reviewers for their valuable comments and suggestions to improve the manuscript for publication.

Funding

This research was supported by Universidad Autónoma Metropolitana (Divisional Project). The first author (YBG) acknowledges CONAHCYT-Mexico 753106 (Consejo Nacional de Ciencia y Tecnología) for the scholarship to pursue a doctoral degree in the Doctoral Program, Doctorado en Ciencias Biológicas y de la Salud at Universidad Autónoma Metropolitana-Mexico.

Author information

Authors and Affiliations

  1. Doctorado en Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana, 09310, Mexico City, Mexico

    Yajaira Baeza-Guzmán

  2. Facultad de Ciencias Agrícolas, Universidad Veracruzana, Circuito Gonzalo Aguirre Beltrán s/n, Zona Universitaria, 91090, Xalapa, Veracruz, Mexico

    Dora Trejo Aguilar

  3. Departamento de Biología, División de Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana, Unidad Iztapalapa, 09310, Mexico City, Mexico

    Noé Manuel Montaño & Sara Lucía Camargo-Ricalde

Authors
  1. Yajaira Baeza-Guzmán
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dora Trejo Aguilar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Noé Manuel Montaño
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sara Lucía Camargo-Ricalde
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the conception and design of the study. YBG collected the plant and fungal material. YBG carried out the experiment, material preparation and data collection, and the statistical analysis was carried out by NMM and YBG. The first draft of the manuscript was written by YBG, and all authors contributed to later versions of the manuscript. All authors approved the final manuscript.

Corresponding authors

Correspondence to Dora Trejo Aguilar or Sara Lucía Camargo-Ricalde.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baeza-Guzmán, Y., Trejo Aguilar, D., Montaño, N. et al. Synergistic effects of Amanita stranella and Suillus decipiens inoculation on morphological features and phenolic compounds of Pinus pseudostrobus var. coatepecensis, a narrow endemic Mexican variety. New Forests 55, 1033–1048 (2024). https://doi.org/10.1007/s11056-023-10018-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11056-023-10018-6

Keywords

Search

Navigation