Sympatric species develop more efficient ectomycorrhizae in the Pinus-Laccaria symbiosis

Autores/as

  • Ibeth Rodríguez-Gutiérrez
  • Daniel Ramírez-Martínez
  • Roberto Garibay-Orijel Instituto de Biología, UNAM http://orcid.org/0000-0002-6977-7550
  • Virginia Jacob-Cervantes
  • Jesús Pérez-Moreno
  • María del Pilar Ortega-Larrocea
  • Elsa Arellano-Torres

DOI:

https://doi.org/10.22201/ib.20078706e.2019.90.2868

Palabras clave:

Ectomycorrhizal inoculum, Exotic, Laccaria laccata, Laccaria trichodermophora, Laccaria vinaceobrunnea, Laccaria bicolor, Pseudomonas fluorescens, Pinus montezumae

Resumen

The mycorrhizal symbiosis is optimal when the plant and the fungi are sympatric. However, in forest plantations the inoculum typically belongs to exotic or allopatric fungi. In this paper, the efficiency of mycorrhization was determined by evaluating the effect of 2 sympatric fungi species (Laccaria trichodermophora and L. bicolor s.l.) and 2 allopatric (L. laccata var. laccata and L. vinaceobrunnea) on the growth and nutrient contents of Pinus montezumae. We also tested the effect of the mycorrhizal helper bacteria Pseudomonas fluorescens (Pf_Ag001). After 1 year of growth, we evaluated the mycorrhization percentage, plant height, diameter at root collar, dry weight and nutrient contents (N, P, K) of aerial part and roots. The mycorrhization percentage varied from 93.5% to 98.5%. The treatments that showed higher efficiency (biomass accumulation and K contents) were those inoculated with sympatric species. All Laccaria treatments, either in the presence or absence of the bacteria, showed a better response compared to not inoculated controls. This work demonstrates the significance of using inocula of sympatric species as  these are genetically predisposed to associate with their hosts, naturally adapted to the local environmental and edaphic conditions compared with those of allopatric origin.

Citas

Agerer, R. (Ur. 1987-2002). Color Atlas of Ectomycorrhiza. Germany Einhorn-Verlag, Schwäbisch Gmünd.

Ángeles-Argáiz, R. E., Flores-García, A., Ulloa, M. & Garibay-Orijel, R. (2016). Commercial Sphagnum peat moss is a vector for exotic ectomycorrhizal mushrooms. Biological Invasions, 18: 89-101. doi.org/10.1007/S10530-015-0992-2

Aspray, T. J., Jones, E. E., Davies, M. W., Shipman, M. & Bending, G. D. (2013). Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus bay the helper bacterium Paenibacillus sp. Mycorrhiza, 23: 403-410. doi.org/10.1007/s00572-013-0483-1

Barroetaveña, C. & Rajchenberg, M. (2003). Las micorrizas y la producción de plántulas de Pinus ponderosa Dougl. ex Laws. en la Patagonia, Argentina. Bosque (Valdivia), 24: 17-33. doi.org/ 10.4067/S0717-92002003000100002

Barroetaveña, C., Bassani, V. N., Monges, J. I. & Rajchenberg, M. (2016). Field performance of Pinus ponderosa seedlings inoculated with ectomycorrhizal fungi planted in steppe-grasslands of Andean Patagonia, Argentina. Bosque (Valdivia), 37: 307-316. doi.org/10.4067/S0717-92002016000200009

Bois, G. & Coughlan, A. P. (2009). Ectomycorrhizal inoculation for boreal forest ecosystem restoration following oil sand extraction: the need for an initial three-step screening process. In D. Khasa, Y. Piché & A.P. Coughlan (Eds.), Advances in Mycorrhizal Science and Technology (pp. 129-137). Ottawa: NRC Research Press.

Bonfante, P. & Genre, A. (2010). Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nature Communications, 1: 1-11. doi.org/10.1038/ncomms1046

Bremner, J. M. (1975). Total nitrogen. In C.A. Black (Ed.), Methods of soil analysis (pp. 9: 1149-1178). American Society of Agronomy Madison.

Carrasco-Hernández, V., Pérez-Moreno, J., Espinosa-Hernández, V., Almaraz-Suárez, J. J., Quintero-Lizoala, R. & Torres-Aquino, M, (2010). Caracterización de micorrizas establecidas entre dos hongos comestibles silvestres y pinos nativos de México. Revista Mexicana de Ciencias Agrícolas, 4: 657-577.

Carrasco-Hernández, V., Pérez-Moreno, J., Espinosa-Hernández, V., Almaraz-Suárez, J., Quintero-Lizaola, R. & Torres-Aquino, M. (2011). Contenido de nutrientes e inoculación con hongos ectomicorrízicos comestibles en dos pinos neotropicales. Revista Chilena de Historia Natural, 83: 83-96.

Carrera-Nieve, A. & López-Ríos, G. F. (2004). Manejo y evaluación de ectomicorrizas en especies forestales. Revista Chapingo Serie Ciencias Forestales y del Ambiente, 10: 93-98.

Castillo-Guevara, C., Lara, C. & Pérez, G. (2012). Mycophagy by rodents in a temperate forest of Central Mexico. Revista Mexicana de Biodiversidad, 83: 772-777. doi.org/rmb.27445

Chapela, I. H., Osher, L. J., Horton, T.R. & Henn, M.R. (2001). Ectomycorrhizal fungi introduced with exotic pine plantations induce soil carbon depletion. Soil Biology & Biochemistry, 33: 1733-1740. doi.org/10.1016/S0038-0717(01)00098-0

Chapman, H.D. & Parker, F.P. (1986). Métodos de análisis para suelos, plantas y agua. México. Trillas.

Cuevas-Rangel, R.A. (1979). Prueba de inoculación con el hongo micorrízico Pisolithus tinctorius (Pers.) Coker and Couch en plantas de Pinus montezumae Lamb. en suelos de vivero. Ciencia Forestal, 4: 46-62.

Deveau, A., Brulé, C., Palin, B., Champmartin, D., Rubini, O., Garbaye, J., Sarniguet, A. & Frey-Klett, P. (2010). Role of fungal trehalose and bacterial thiamine in the improved survival and growth of the ectomycorrhizal fungus Laccaria bicolor S238N and the helper bacterium Pseudomonas fluorescens BBc6r8. Environmental Microbiology Reports, 2: 560-568. doi.org/10.1111/j.1758-2229.2010.00145.x

Deveau, A., Palin, B., Delaruelle, C., Peter, M., Kohler, A., Pierrat, J. C., Sarniguet, A., Garbaye, J., Martin, F. & Frey-Klett, P. (2007). The mycorrhiza helper Pseudomonas fluorescens BBc6r8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytologist, 175: 743-755. doi.org/10.1111/j.1469-8137.2007.02148.x

Dixon, R. K. & Johnson, P.S. (1992). Synthesis of ectomycorrhizae on Northern red oak seedlings in a Michigan nursery. Journal of Arboriculture, 18: 266-272.

Duponnois, R. & Garbaye, J. (1991). Effect of dual inoculation of Douglas fir with the ectomycorrhizal fungus Laccaria laccata and mycorrhization helper bacteria (MHB) in two bare-root forest nurseries. Plant and Soil, 138: 169-176.

Farjon, A. (1996). Biodiversity of Pinus (Pinaceae) in Mexico: speciation and paleoendemism. Botanical Journal of the Linnean Society, 121: 365-384.

Farjon, A. & Styles, B. T. (1997). Pinus (Pinaceae). Flora Neotropical Monograph V75. New York: The New York Botanical Garden.

Flores-Villela, O. & Canseco-Márquez, L. (2007). Riqueza de la herpetofauna. In I. Luna-Vega, J. J. Morrone & D. Espinosa (Eds.), Biodiversidad de la Faja Volcánica Transmexicana (pp. 407-420). México: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad / Universidad Nacional Autónoma de México.

Fortin, J. A. & Lamhamedi, M. S. (2009). Ecophysiology of sporocarp development of ectomycorrhizal basidiomycetes associated with boreal forest gymnosperms. In D. Khasa, Y. Piché, A. P. Coughlan (Eds.), Advances in Mycorrhizal Science and Technology (pp. 161-173). Ottawa: NRC Research Press.

Frey-Klett, P., Churin, J.L., Pierrat, J.C. & Garbaye, J. (1999). Dose effect in the dual inoculation of an ectomycorrhizal fungus and a mycorrhiza helper bacterium in two forest nurseries. Soil Biology and Biochemistry, 31: 1555-1562. doi.org/10.1016/S0038-0717(99)00079-6

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. Botanical Sciences, 93: 1-9. doi.org/10.17129/botsci.200

Garbaye, J. (1994). Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytologist, 128:197-210. doi.org/10.1111/j.1469-8137.1994.tb04003.x

Garibay-Orijel, R., Martínez-Ramos, M. & Cifuentes, J. (2009). Disponibilidad de hongos comestibles en los bosques de pino-encino de Ixtlán de Juárez, Oaxaca. Revista Mexicana de Biodiversidad, 80: 521-534.

Gibson, F. & Deacon, J. W. (1988). Experimental study of the establishment of ectomycorrhizas in different regions of birch root systems. Transactions of the British Mycological Society, 91: 239-251. doi.org/10.1016/S0007-1536(88)80211-0

Hoeksema, J. D., Chaudhary, V. B., Gehrin, C. A., Johnson, N. C., Kars, J., Koide, R. T., Pringle, A., Zabinski, C., Bever, J. D., Moore, J. C., Klironomos, J. N. & Umbanhowar, J. (2010). A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters, 13: 394-407. doi.org/10.1111/j.1461-0248.2009.01430.x

Hynson, N. A., Merckx, V. S. F. T., Perry, B.A. & Treseder, K.K. (2013). Identities and distributions of the co-invading ectomycorrhizal fungal symbionts of exotic pines in the Hawaiian Islands. Biological Invasions, 15: 2373-2385. doi.org/10.1007/s10530-013-0458-3

Karst, J., Randall, M. J. & Gehring, C. A. (2014). Consequences for ectomycorrhizal fungi of the selective loss or gain of pine across landscapes. Botany, 92: 855-865. doi.org/10.1139/cjb-2014-0063

Khasa, D., Piché, Y. & Coughlan, A. P. (2009). Advances in Mycorrhizal Science and Technology. Ottawa: NRC-Research Press.

Klironomos, J. N. (2003). Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology, 84: 2292-2301. doi.org/10.1890/02-0413

Kornerup, A. & Wanscher, J. H. (1978). Methuen Handbook of Colour. London: E. Methuen.

Kumari, D., Sudhakara, R. & Ramseh, C.U. (2013). Diversity of cultivable bacteria associated with fruiting bodies of wild Himalayan Cantharellus spp. Annals of Mirobiology, 63:845-853. doi.org/10.1007/s13213-012-0535-3

Kropp, B. R. & Mueller, G. M. (1999). Laccaria. In J. W.G. Cairney , S. M. Chambers (Eds.), Ectomycorrhizal Fungi: key genera in profile (pp. 65-88). Berlin: Springer-Verlag.

Loper, J. E., Hassan, K. A., Mavrodi, D. V., Davis, I. I. E. W., Lim, C. K., Shaffer, B. T., et al. (2012). Comparative genomics of plant-associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genetics, 8(7): e1002784. doi.org/10.1371/journal.pgen.1002784

Martin, F. & Selosse, M. A. (2008). The Laccaria genome: a symbiont blueprint decoded. New Phytologist, 180: 296-310. doi.org/10.1111/j.1469-8137.2008.02613.x

Martínez-Reyes, M., Pérez-Moreno, J., Villarreal-Ruiz, L., Ferrera-Cerrato, R., Xoconostle-Cázarez, B., Vargas-Hernández, J. J. & Honrubia-García, M. (2012). Crecimiento y contenido nutrimental de Pinus greggii Engelm. inoculado con el hongo comestible ectomicorrízico Hebeloma mesophaeum (Pers.) Quél. Revista Chapingo Serie Forestales y del Ambiente, 18: 183-192. doi.org/10.5154/r.rchscfa.2010.11.112

Méndez-Neri, M., Pérez-Moreno, J., Quintero-Lizaola, R., Hernández-Acosta, E. & Lara-Herrera, A. (2011). Crecimiento y contenido nutrimental de Pinus greggii inoculado con tres hongos comestibles ectomicorrízicos. Terra Latinoamericana, 29: 73-81.

Molina, R., Massicotte, H. & Trappe, J. M. (1992). Specificity phenomena in mycorrhizal symbiosis: community-ecological consequences and practical implications. In M. R. Allen (Ed.), Mycorrhizal functioning: An integrative plant-fungal process (pp. 357-423). New York: Chapman & Hall.

Montoya, A., Kong, A., Estrada-Torres, A., Cifuentes, J. & Caballero, J. (2005). Useful wild fungi of La Malinche National Park, Mexico. Fungal Diversity, 17: 115-14.

Montoya, A., Torres-García, E., 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, 104: 826-834. doi.org/10.3852/11-347.

Moreno-Martínez, E. (1984). Análisis físico y biológico de semillas agrícolas. Universidad Nacional Autónoma de México, Mexico.

Morrone, J. J. (2005). Hacia una síntesis biogeográfica de México. Revista Mexicana de Biodiversidad, 76: 207-252.

Morrone, J. J. (2010). Fundamental biogeographic patterns across the Mexican Transition Zone: an evolutionary approach. Ecography, 33: 355-361. doi.org/10.1111/j.1600-0587.2010.06266.x.

Morrone, J. J. & Escalante, T. (2002). Parsimony Analysis of Endemicity (PAE) of Mexican terrestrial mammals at different area units: when size matters. Journal of Biogeography, 29: 1095-1104. doi.org/10.1046/j365-2699.2002.00753.x.

Mortier, F., Le Tacon, F. & Garbaye, J. (1988). Effect of inoculum type and inoculation dose on ectomycorrhizal development, root necrosis, and growth of Douglas fir seedlings inoculated with Laccaria laccata in a nursery. Annals of Forest Science, 45: 301-310. doi.org/10.1051/forest:19880401.

Onwuchekwa, N. E., Zwuiazek, J. J., Quoreshi, A. & Khasa, D. P. (2014). Growth of mycorrhizal Jack pine (Pinus banksiana) and White spruce (Picea glauca) seedling planted in oil sands. Mycorrhiza, 24: 431-441. doi.org/10.1007/s00572.

Parent, S. & Moutoglis, P. (2009). Industrial perspective of applied mycorrhizal research in Canada. In D. Khasa, Y. Piché & A. P. Coughlan (Eds.), Advances in Mycorrhizal Science and Technology (pp. 105-113). Ottawa: NRC Research Press.

Parladé, J. & Álvarez, I. F. (1993). Coinoculation of aseptically grown Douglas fir with pairs of ectomycorrhizal fungi. Mycorrhiza, 3: 93-96.

Pera, J. & Parladé, J. (2005). Inoculación controlada con hongos ectomicorrízicos en la producción de plantas destinadas a repoblaciones forestales: estado actual en España. Investigación Agraria, Sistemas y Recursos Forestales, 14: 419-433.

Perea-Estrada, V. M., Pérez-Moreno, J., Villarreal-Ruíz, L., Trinidad-Santos, A., De la I de Bauer, M. L., Cetina-Alcalá, V. M. & Tijerina-Chávez, L. (2009). Humedad edáfica, nitrógeno y hongos ectomicorrízicos comestibles en el crecimiento de pino. Revista Fitotecnia Mexicana, 32: 93-102.

Pérez-Moreno, J. & Read, D. J. (2000). Mobilization and transfer of nutrients from litter to tree seedlings via the vegetative mycelium of ectomycorrhizal plants. New Phytologist, 145: 301-309. doi.org/10.1046/j.1469-8137.2000.00569.x.

Pérez-Moreno, J. & Read, D. J. (2004). Los hongos ectomicorrízicos, lazos vivientes que conectan y nutren a los árboles en la naturaleza. Interciencia, 29: 239-247.

Perrin, E., Parladé, X. & Pera, J. (1997). Receptiveness of forest soils to ectomycorrhizal association: concept and method as applied to the symbiosis between Laccaria bicolor (Maire) Orton and Pinus pinaster Art or Pseudotsuga menziesii (Mirb.) Franco. Mycorrhiza, 6: 469-476.

Programa de manejo forestal para el aprovechamiento persistente de los recursos forestales maderables. (2012). Comunidad de Ixtlán de Juárez.

Quoreshi, A.M., Kernaghan, G. & Hynt, G. A. (2009). Mycorrhizal fungi in Canadian forest nurseries and field performance of inoculated seedlings. In D. Khasa, Y. Piché & A. P. Coughlan (Eds.), Advances in Mycorrhizal Science and Technology (pp. 115-127). Ottawa: NRC Research Press.

Quoreshi, A. M., Piché, Y. & Khasa, D. (2008). Field performance of conifer and hardwood species 5 years after nursery inoculation in the Canadian Prairie provinces. New Forests, 35: 235-253. doi.org/10.1007/s11056-007-9074-3.

Read, D.J. & Pérez-Moreno, J. (2003). Mycorrhizas and nutrient cycling in ecosystems. New Phytologist, 157: 475-492. doi.org/10.1046/j.1469-8137.2003.00704.x.

Rincón, A., Álvarez, I. F. & Pera, J. (2001). Inoculation of containerized Pinus pinea L. seedlings with seven ectomycorrhizal fungi. Mycorrhiza, 11: 265-271. doi.org/10.1007/s005720100127.

Rúa, M. G., Antoninka, A., Antunes, P. M., Chaudhary, V. B., Gehring, C., Lamit, L. J., Piculell, B. .J, Bever, J. D., Zabinski, C., Meadow, J. F., Lajeunesse, M. J., Milligan, B. G., Karst, J. & Hoeksema, J. D. (2016). Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through mea-analysis. BMC Evolutionary Biology, 16: 122. doi.org/10.1186/s12862-016-0698-9.

Santiago-Martínez, G., Estrada-Torres, A., Varela, L. & Herrera, T. (2003). Crecimiento de siete medios nutritivos y síntesis in vitro de una cepa de Laccaria bicolor. Agrociencias, 37: 575-584.

Sudhakara, R. M. & Natarajan, K. (1997). Coinoculation efficacy of ectomycorrhizal fungi on Pinus patula seedlings in a nursery. Mycorrhiza, 7: 133-138.

Smith, S. E. & Read, D. J. (2008). Mycorrhizal Symbiosis. New York: Academic Press

Teramoto, M., Wu, B. & Hogetsu, T. (2012). Transfer of 14C-photosynthate to the sporocarp of an ectomycorrhizal fungus Laccaria amethystina. Mycorrhiza, 22: 219-225. doi.org/10.1007/s00572-011-0395-x.

Trappe, J. M. (1977). Selection of fungi for ectomycorrhizal inoculation in nurseries. Annual Review of Phytopathology, 15: 203-222. doi.org/10.1146/annurev.py.15.090177.001223

Umbanhowar, J. & McCann, K. (2005). Simple rules for the coexistence and competitive dominance of plants mediated by mycorrhizal fungi. Ecology Letters, 8: 247-252. doi.org/10.1111/j.1461-0248.2004.00714.x.

Valdés, M., Asbjornsen, H., Gómez-Cárdenas, M., Juárez, M. & Vogt, K. A. (2006). Drought effects on fine-root and ectomycorrhizal-root biomass in managed Pinus oaxacana Mirov stand in Oaxaca, Mexico. Mycorrhiza, 2: 117-124. doi.org/10.1007/s00572-005-0022-9.

Valdés, M., Pereda, V., Ramírez, P., Valenzuela, R. & Pineda, R. M. (2009). The ectomycorrhizal community in a Pinus oaxacana forest under different silvicultural treatments. Journal of Tropical Forest Science, 21: 88-97.

Valdés, M., Piña, F. & Grada, R. (1983). Inoculación micorrízica y crecimiento de plántulas de pino en suelo erosionado. Boletín de la Sociedad Mexicana de Micología, 18: 56-70.

Vik, U., Logares, R., Blaalid, R., Halvorsen, R., Carlsen, T., Bekke, I., Kolstø, A. B., Økstad, O. A. & Kauserud, H. (2013). Different bacterial communities in ectomycorrhizal and surrounding soil. Scientific Reports, 3: 1-8. doi.org/10.1038/srep03471.

Wadud, M. A., Lian, C. L., Nara, K., Reza, M. S. & Hogetsu, T. (2008). Below ground genet differences of an ectomycorrhizal fungus Laccaria laccata infecting Salix stands in primary successional stage. Journal of Agroforestry and Environment, 2: 1-6.

Wadud, M. A., Nara, K., Lian, C. L., Ishida, A. T. & Hogetsu, T. (2014). Genet dynamics and ecological functions of the pioneer ectomycorrhizal fungi Laccaria amethystina and Laccaria laccata in volcanic desert on Mount Fuji. Mycorrhiza, 24: 551-563. doi.org/10.1007/s00572-014-0571.x.

Wilson, A. W., Hosaka, K. & Mueller, G. M. (2017). Evolution of ectomycorrhizas as a driver of diversification and biogeographic patterns in the model mycorrhizal mushroom genus Laccaria. New Phytologist, 213: 1862-1873. doi.org/10.1111/nph.14270.

Zadworny, M., Werner, A. & Idzikowska, K. (2004). Behavior of the hyphae of Laccaria laccata in the presence of Trichoderma harzianum in vitro. Mycorrhiza, 14: 401-40. doi.org/10.1007/s00572-004-0323-4.

Descargas

Publicado

2019-12-11

Número

Sección

MANEJO Y APROVECHAMIENTO DE RECURSOS