Re-examining the evidence for the mother tree hypothesis - resource sharing among trees via ectomycorrhizal networks.
carbon
common mycorrhizal network
ectomycorrhizal symbiosis
forest
mother tree
nitrogen
resource sharing
stable isotopes
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
received:
15
11
2022
accepted:
19
03
2023
medline:
2
6
2023
pubmed:
7
5
2023
entrez:
7
5
2023
Statut:
ppublish
Résumé
Seminal scientific papers positing that mycorrhizal fungal networks can distribute carbon (C) among plants have stimulated a popular narrative that overstory trees, or 'mother trees', support the growth of seedlings in this way. This narrative has far-reaching implications for our understanding of forest ecology and has been controversial in the scientific community. We review the current understanding of ectomycorrhizal C metabolism and observations on forest regeneration that make the mother tree narrative debatable. We then re-examine data and conclusions from publications that underlie the mother tree hypothesis. Isotopic labeling methods are uniquely suited for studying element fluxes through ecosystems, but the complexity of mycorrhizal symbiosis, low detection limits, and small carbon discrimination in biological processes can cause researchers to make important inferences based on miniscule shifts in isotopic abundance, which can be misleading. We conclude that evidence of a significant net C transfer via common mycorrhizal networks that benefits the recipients is still lacking. Furthermore, a role for fungi as a C pipeline between trees is difficult to reconcile with any adaptive advantages for the fungi. Finally, the hypothesis is neither supported by boreal forest regeneration patterns nor consistent with the understanding of physiological mechanisms controlling mycorrhizal symbiosis.
Substances chimiques
Carbon
7440-44-0
Types de publication
Review
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
19-28Informations de copyright
© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.
Références
Aaltonen VT. 1926. On the space and arrangement of trees and root competition. Journal of Forestry 24: 627-644.
Abuzinadah RA, Read DJ. 1989. Carbon transfer associated with assimilation of organic nitrogen sources by silver birch (Betula pendula Roth.). Trees 3: 17-23.
Agerer R. 2001. Exploration types of ectomycorrhizae. Mycorrhiza 11: 107-114.
Avital S, Rog I, Livne-Luzon S, Cahanovitc R, Klein T. 2022. Asymmetric belowground carbon transfer in a diverse tree community. Molecular Ecology 31: 3481-3495.
Axelsson EP, Lundmark T, Högberg P, Nordin A. 2014. Belowground competition directs spatial patterns of seedling growth in boreal pine forest in Fennoscandia. Forests 5: 2106-2121.
Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J. 2017. Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355: 181-184.
Bingham MA, Simard S. 2012. Ectomycorrhizal Networks of Pseudotsuga menziesii var. glauca trees facilitate establishment of conspecific seedlings under drought. Ecosystems 15: 188-199.
Bluhm SL, Potapov AM, Shrubovych J, Ammerschubert S, Polle A, Scheu S. 2019. Protura are unique: first evidence of specialized feeding on ectomycorrhizal fungi in soil invertebrates. BMC Ecology 19: 10.
Booth MG, Hoeksema JD. 2010. Mycorrhizal networks counteract competitive effects of canopy trees on seedling survival. Ecology 91: 2294-2302.
Cahanovitc R, Livne-Luzon S, Angel R, Klein T. 2022. Ectomycorrhizal fungi mediate belowground carbon transfer between pines and oaks. The ISME Journal 6: 1420-1429.
Cameron DD, Johnson I, Read DJ, Leake JR. 2008. Giving and receiving: measuring the carbon cost of mycorrhizas in the green orchid, Goodyera repens. New Phytologist 180: 176-184.
Connell JH. 1970. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: Den Boer PJ, Gradwell GR, eds. Dynamics of population. Wageningen, the Netherlands: Pudoc, 298-312.
Coomes DA, Grubb PJ. 2000. Impacts of root competition in forests and woodlands: a theoretical framework and review of experiments. Ecological Monographs 70: 171-207.
Deslippe JR, Simard SW. 2011. Below-ground carbon transfer among Betula nana may increase with warming in Arctic tundra. New Phytologist 192: 689-698.
Devine WD, Harrington TB. 2008. Belowground competition influences growth of natural regeneration in thinned Douglas-fir stands. Canadian Journal of Forest Research 38: 3085-3097.
Finlay RD, Read DJ. 1986. The structure and function of the vegetative mycelium of ectomychorrhizal plants. New Phytologist 103: 143-156.
Franklin O, Näsholm T, Högberg P, Högberg MN. 2014. Forests trapped in nitrogen limitation - an ecological market perspective on ectomycorrhizal symbiosis. New Phytologist 203: 657-666.
Gorka S, Dietrich M, Mayerhofer W, Gabriel R, Wiesenbauer J, Martin V, Zheng Q, Imai B, Prommer J, Weidinger M et al. 2019. Rapid transfer of plant photosynthates to soil bacteria via ectomycorrhizal hyphae and its interaction with nitrogen availability. Frontiers in Microbiology 10: 168.
Göttlicher SG, Taylor AFS, Grip H, Betson NR, Valinger E, Högberg MN, Högberg P. 2008. The lateral spread of tree root systems in boreal forests: estimates based on 15N uptake and distribution of sporocarps of ectomycorrhizal fungi. Forest Ecology and Management 255: 75-81.
Hawkins B, Moran J. 2003. Growth responses of Abies amabilis advance regeneration to overstory removal, nitrogen fertilization and release from Vaccinium competition. Forest Science 59: 799-806.
He X, Xu M, Qiu GY, Zhou J. 2009. Use of 15N stable isotope to quantify nitrogen transfer between mycorrhizal plants. Journal of Plant Ecology 2: 107-118.
Henriksson N, Franklin O, Tarvainen L, Marshall J, Lundberg-Felten J, Eilertsen L, Näsholm T. 2021a. The mycorrhizal tragedy of the commons. Ecology Letters 24: 1215-1224.
Henriksson N, Lim H, Marshall J, Franklin O, McMurtrie RE, Lutter R, Magh R, Lundmark T, Näsholm T. 2021b. Tree water uptake enhances nitrogen acquisition in a fertilized boreal forest - but not under nitrogen-poor conditions. New Phytologist 232: 113-122.
Högberg MN, Briones MJI, Keel SG, Metcalfe DB, Campbell C, Midwood AJ, Thornton B, Hurry V, Linder S, Näsholm T et al. 2010. Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest. New Phytologist 187: 485-493.
Högberg P, Högberg MN. 2022. Does successful forest regeneration require the nursing of seedlings by nurse trees through mycorrhizal interconnections? Forest Ecology and Management 516: 120252.
Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg M, Nyberg G, Ottosson-Löfvenius M, Read DJ. 2001. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411: 789-792.
Hughes JW, Bechtel DA. 1997. Effect of distance from forest edge on regeneration of Red spruce and Balsam fir in clearcuts. Canadian Journal of Forest Research 27: 2088-2096.
Jackson WA, Coleman NT. 1959. Fixation of carbon dioxide by plant roots through phosphoenolpyruvate carboxylase. Plant and Soil 11: 1-16.
Jakobsson R. 2005. Effect of retained trees on the development of young Scots pine stands in Southern Finland. Doctoral thesis, Acta Universitatis Agriculturae Sueciae.
Janzen DH. 1970. Herbivores and the number of tree species in tropical forests. The American Naturalist 104: 940.
Johnson NC, Graham JH, Smith FA. 1997. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytologist 135: 575-585.
Karst J, Jones MD, Hoeksema JD. 2023. Positive citation bias and overinterpreted results lead to misinformation on common mycorrhizal networks in forests. Nature Ecology & Evolution 7: 501-511.
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333: 880-882.
Klein T, Siegwolf RTW, Körner C. 2016. Belowground carbon trade among tall trees in a temperate forest. Science 352: 342-344.
Leake J. 2005. Plants parasitic on fungi: unearthing the fungi in myco-heterotrophs and debunking the ‘saprophytic’ plant myth. Mycologist 19: 113-122.
Nara K. 2006. Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytologist 169: 169-178.
Näsholm T, Högberg P, Franklin O, Metcalfe D, Keel SG, Campbell C, Hurry V, Linder S, Högberg MN. 2013. Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? New Phytologist 198: 214-221.
Näsholm T, Kielland K, Ganeteg U. 2009. Uptake of organic nitrogen by plants. New Phytologist 182: 31-48.
Nehls U, Das A, Neb D. 2016. Carbohydrate metabolism in ectomycorrhizal symbiosis. In: Martin F, ed. Molecular mycorrhizal symbiosis. Hoboken, NJ, USA: John Wiley & Sons, 161, 177.
Offermann C, Ferrio JP, Holst J, Grote R, Siegwolf R, Kayler Z, Gessler A. 2011. The long way down - are carbon and oxygen isotope signals in the tree ring uncoupled from canopy physiological processes? Tree Physiology 31: 1088-1102.
Petritan IC, von Lüpke B, Petritan AM. 2011. Effects of root trenching of overstorey Norway spruce (Picea abies) on growth and biomass of underplanted beech (Fagus sylvatica) and Douglas fir (Pseudotsuga menziesii) saplings. European Journal of Forest Research 130: 813-828.
Pickles BJ, Wilhelm R, Asay AK, Hahn AS, Simard SW, Mohn WW. 2017. Transfer of 13C between paired Douglas-fir seedlings reveals plant kinship effects and uptake of exudates by ectomycorrhizas. New Phytologist 214: 400-411.
Robinson D, Fitter A. 1999. The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. Journal of Experimental Botany 50: 9-13.
Ruuska J, Sipilehto J, Valkonen S. 2008. Effect of edge stands on the development of young Pinus sylvestris stands in southern Finland. Scandinavian Journal of Forest Research 23: 214-226.
Schwartz MW, Hoeksema JD. 1998. Specialization and resource trade: biological markets as a model of mutualisms. Ecology 79: 1029-1038.
Selosse M-A, Bocayuva MF, Kasuya MCM, Courty P-E. 2016. Mixotrophy in mycorrhizal plants. In: Martin F, ed. Molecular mycorrhizal symbiosis. Hoboken, NJ, USA: John Wiley & Sons, 451-471.
Simard SW. 2018. Mycorrhizal networks facilitate tree communication, learning, and memory. In: Baluska F, Gagliano M, Witzany G, eds. Memory and learning in plants. Cham, Switzerland: Springer International Publishing AG, part of Springer Nature 2018, 501-560.
Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste FP. 2012. Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biology Reviews 26: 39-60.
Simard SW, Jones MD, Durall DM, Perry DA, Myrold DD, Molina R. 1997a. Reciprocal transfer of carbon isotopes between ectomycorrhizal Betula papyrifera and Pseudotsuga menziesii. New Phytologist 137: 529-542.
Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R. 1997b. Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388: 579-582.
Simard SW, Roach WJ, Beauregard J, Burkart J, Cook D, Law D, Murphy-Steed A, Schacter T, Zickmantel A, Armstrong G et al. 2021. Partial retention of legacy trees protect mycorrhizal inoculum potential, biodiversity, and soil resources while promoting natural regeneration of interior Douglas-fir. Frontiers in Forests and Global Change 3: 620436.
Smith SE, Read DJ. 2008. Mycorrhizal symbiosis, 3rd edn. London, UK: Academic Press, 300-320.
Teste FP, Simard SW, Durall DM, Guy RD, Jones MD, Schoonmaker AL. 2009. Access to mycorrhizal networks and roots of trees: importance for seedling survival and resource transfer. Ecology 90: 2808-2822.
Van Der Heijden MGA, Horton TR. 2009. Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. Journal of Ecology 97: 1139-1150.
Wagner S, Collet C, Madsen P, Nakashizuka T, Nyland RD, Sagheb-Talebi K. 2010. Beech regeneration research: from ecological to silvicultural aspects. Forest Ecology and Management 259: 2172-2182.
Walters MB, Lajzerowicz CC, Coates KD. 2006. Soil resources and the growth and nutrition of tree seedlings near harvest gap - forest edges in interior cedar-hemlock forests of British Columbia. Canadian Journal of Forest Research 36: 62-76.
Wu B, Nara K, Hogetsu T. 2001. Can 14C-labeled photosynthetic products move between Pinus densiflora seedlings linked by ectomycorrhizal mycelia? New Phytologist 149: 137-146.