ACORN Review: NPK fertilizer use in loblolly pine plantations: Who are we really feeding?

Hackman, Jacob J.; Rose, Benjamin D.; Frank, Hannah E. R.; Vilgalys, Rytas; Cook, Rachel L.; Garcia, Kevin

doi:10.1016/j.foreco.2022.120393

ACORN Review: NPK fertilizer use in loblolly pine plantations: Who are we really feeding?

Journal Article · Wed Jul 06 00:00:00 EDT 2022 · Forest Ecology and Management

DOI:https://doi.org/10.1016/j.foreco.2022.120393· OSTI ID:1981613

Hackman, Jacob J. ^[1]; Rose, Benjamin D. ^[1]; Frank, Hannah E. R. ^[1]; Vilgalys, Rytas ^[2]; Cook, Rachel L. ^[1]; ^[1]

North Carolina State University, Raleigh, NC (United States)
Duke Univ., Durham, NC (United States)

Optimizing loblolly pine (Pinus taeda L.) productivity using fertilizers and various site management practices has been a goal of foresters for decades. Nitrogen (N), phosphorus (P), and potassium (K) are the three most operationally applied fertilizers to loblolly pine silviculture and are of primary importance to their total productivity. Fertilizer recommendations for N, P, and K in loblolly pine are primarily made on abiotic factors such as site and soil characteristics, while the biological factors controlling nutrient uptake are typically overlooked in the production and optimization of these stands. Arguably the most important of these biological factors are the diverse ectomycorrhizal fungal (ECM) communities that colonize the fine roots of almost all loblolly pine trees. The mantle formed by ECM fungi on short-root tips presents a barrier for direct apoplastic uptake of N, P, and K from soil solution by pine roots. In well-colonized roots, the tree is dependent on symplastic fungal transport of N, P, and K foraged from the soil by the extraradical hyphal network. This raises the question: Who are we really feeding if the ECM fungi are the ones assimilating most of the tree's total nutritional requirements? Considering multiple species of ECM fungi can inhabit a single root system, many questions remain regarding the drivers of colonization, why some species are more efficient at taking up and exchanging nutrients with their hosts than others, and why certain fertilizers directly affect the morphology of ECM growth. The purposes of this review here are (1) to explore how the most commonly commercially applied macronutrients, N, P, and K, affect the relationship between loblolly pine and ECM communities, and (2) to propose future directions to investigate, preserve, and manipulate these interactions in pine plantations to optimize productivity.

View Accepted Manuscript (DOE)

Research Organization:: North Carolina State University, Raleigh, NC (United States)

Sponsoring Organization:: USDA Agriculture and Food Research Initiative (AFRI); USDOE

OSTI ID:: 1981613

Journal Information:: Forest Ecology and Management, Journal Name: Forest Ecology and Management Journal Issue: C Vol. 520; ISSN 0378-1127

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (68)

Losses of fertilizer nitrogen after a winter fertilization in three managed pine plantations of the southeastern United States Raymond, Jay E.; Fox, Thomas R.; Cook, Rachel L. Soil Science Society of America Journal, Vol. 84, Issue 2 https://doi.org/10.1002/saj2.20017	journal	March 2020
Potassium Dynamics in Soils Sparks, Donald L. Advances in Soil Science https://doi.org/10.1007/978-1-4612-4682-4_1	book	January 1987
Mycorrhizal Fungi: Role in the Solubilization of Potassium Dominguez-Nuñez, Jose Alfonso; Benito, Begoña; Berrocal-Lobo, Marta Potassium Solubilizing Microorganisms for Sustainable Agriculture https://doi.org/10.1007/978-81-322-2776-2_6	book	January 2016
Biotrophic transportome in mutualistic plant–fungal interactions Casieri, Leonardo; Ait Lahmidi, Nassima; Doidy, Joan Mycorrhiza, Vol. 23, Issue 8 https://doi.org/10.1007/s00572-013-0496-9	journal	April 2013
Benefits provided by four ectomycorrhizal fungi to Pinus taeda under different external potassium availabilities Frank, Hannah E. R.; Garcia, Kevin Mycorrhiza, Vol. 31, Issue 6 https://doi.org/10.1007/s00572-021-01048-z	journal	August 2021
Ectomycorrhizal fungi: the symbiotic route to the root for phosphorus in forest soils Cairney, John W. G. Plant and Soil, Vol. 344, Issue 1-2 https://doi.org/10.1007/s11104-011-0731-0	journal	February 2011
Effects of long-term temperature and nutrient manipulation on Norway spruce fine roots and mycelia production Leppälammi-Kujansuu, J.; Ostonen, I.; Strömgren, M. Plant and Soil, Vol. 366, Issue 1-2 https://doi.org/10.1007/s11104-012-1431-0	journal	September 2012
Nitrogen leaching and ectomycorrhizal nitrogen retention capacity in a Norway spruce forest fertilized with nitrogen and phosphorus Bahr, Adam; Ellström, Magnus; Bergh, Johan Plant and Soil, Vol. 390, Issue 1-2 https://doi.org/10.1007/s11104-015-2408-6	journal	February 2015
The influence of nitrogen fertilisers on ectomycorrhizas and their fungal carpophores in young stands of Pinus sylvestris Termorshuizen, Aad J. Forest Ecology and Management, Vol. 57, Issue 1-4 https://doi.org/10.1016/0378-1127(93)90171-I	journal	March 1993
Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals Landeweert, Renske; Hoffland, Ellis; Finlay, Roger D. Trends in Ecology & Evolution, Vol. 16, Issue 5 https://doi.org/10.1016/S0169-5347(01)02122-X	journal	May 2001
Competition for nitrogen between plants and soil microorganisms Kaye, Jason P.; Hart, Stephen C. Trends in Ecology & Evolution, Vol. 12, Issue 4 https://doi.org/10.1016/S0169-5347(97)01001-X	journal	April 1997
Lineages of ectomycorrhizal fungi revisited: Foraging strategies and novel lineages revealed by sequences from belowground Tedersoo, Leho; Smith, Matthew E. Fungal Biology Reviews, Vol. 27, Issue 3-4 https://doi.org/10.1016/j.fbr.2013.09.001	journal	December 2013
Availability of residual phosphorus fertilizer for loblolly pine Everett, Charles J.; Palm-Leis, Hugo Forest Ecology and Management, Vol. 258, Issue 10 https://doi.org/10.1016/j.foreco.2008.11.029	journal	October 2009
Differences in the recovery of four different nitrogen containing fertilizers after two application seasons in pine plantations across the southeastern United States Raymond, Jay E.; Fox, Thomas R.; Strahm, Brian D. Forest Ecology and Management, Vol. 380 https://doi.org/10.1016/j.foreco.2016.08.044	journal	November 2016
Duration of response to nitrogen and phosphorus applications in mid-rotation Pinus taeda Albaugh, Timothy J.; Albaugh, Janine M.; Carter, David R. Forest Ecology and Management, Vol. 498 https://doi.org/10.1016/j.foreco.2021.119578	journal	October 2021
Potassium in agriculture – Status and perspectives Zörb, Christian; Senbayram, Mehmet; Peiter, Edgar Journal of Plant Physiology, Vol. 171, Issue 9 https://doi.org/10.1016/j.jplph.2013.08.008	journal	May 2014
Evaluation of methods to estimate production, biomass and turnover of ectomycorrhizal mycelium in forests soils – A review Wallander, H.; Ekblad, A.; Godbold, D. L. Soil Biology and Biochemistry, Vol. 57 https://doi.org/10.1016/j.soilbio.2012.08.027	journal	February 2013
Long-term experimental warming and fertilization have opposing effects on ectomycorrhizal root enzyme activity and fungal community composition in Arctic tundra Dunleavy, Haley R.; Mack, Michelle C. Soil Biology and Biochemistry, Vol. 154 https://doi.org/10.1016/j.soilbio.2021.108151	journal	March 2021
Mineral weathering by bacteria: ecology, actors and mechanisms Uroz, Stéphane; Calvaruso, Christophe; Turpault, Marie-Pierre Trends in Microbiology, Vol. 17, Issue 8 https://doi.org/10.1016/j.tim.2009.05.004	journal	August 2009
Take a Trip Through the Plant and Fungal Transportome of Mycorrhiza Garcia, Kevin; Doidy, Joan; Zimmermann, Sabine D. Trends in Plant Science, Vol. 21, Issue 11 https://doi.org/10.1016/j.tplants.2016.07.010	journal	November 2016
Phosphorus Transport in Mycorrhiza: How Far Are We? Plassard, Claude; Becquer, Adeline; Garcia, Kevin Trends in Plant Science, Vol. 24, Issue 9 https://doi.org/10.1016/j.tplants.2019.06.004	journal	September 2019
Biological mobilization of potassium from clay minerals by ectomycorrhizal fungi and eucalypt seedling roots Yuan, Ling; Huang, Jianguo; Li, Xiaolin Plant and Soil, Vol. 262, Issue 1/2 https://doi.org/10.1023/B:PLSO.0000037055.67646.97	journal	May 2004
Unearthing the roots of ectomycorrhizal symbioses Martin, Francis; Kohler, Annegret; Murat, Claude Nature Reviews Microbiology, Vol. 14, Issue 12 https://doi.org/10.1038/nrmicro.2016.149	journal	October 2016
The soil organic matter decomposition mechanisms in ectomycorrhizal fungi are tuned for liberating soil organic nitrogen Nicolás, César; Martin-Bertelsen, Tomas; Floudas, Dimitrios The ISME Journal, Vol. 13, Issue 4 https://doi.org/10.1038/s41396-018-0331-6	journal	December 2018
The molecular revolution in ectomycorrhizal ecology: peeking into the black-box: MOLECULAR APPROACHES FOR STUDIES OF EM ECOLOGY Horton, Thomas R.; Bruns, Thomas D. Molecular Ecology, Vol. 10, Issue 8 https://doi.org/10.1046/j.0962-1083.2001.01333.x	journal	August 2001
Differential effects of mineral and organic N sources, and of ectomycorrhizal infection by Hebeloma cylindrosporum, on growth and N utilization in Pinus pinaster Plassard, C.; Bonafos, B.; Touraine, B. Plant, Cell and Environment, Vol. 23, Issue 11 https://doi.org/10.1046/j.1365-3040.2000.00630.x	journal	November 2000
Root colonization dynamics of two ectomycorrhizal fungi of contrasting life history strategies are mediated by addition of organic nutrient patches Lilleskov, Erik A.; Bruns, Thomas D. New Phytologist, Vol. 159, Issue 1 https://doi.org/10.1046/j.1469-8137.2003.00794.x	journal	July 2003
Effects of Mineral Structure and Microenvironment on K Release from Potassium Aluminosilicate Minerals by Cenococcum geophilum fr Xue, Xiaopeng; Zhang, Li; Peng, Yunxiang Geomicrobiology Journal, Vol. 36, Issue 1 https://doi.org/10.1080/01490451.2018.1485064	journal	November 2018
Forest Fertilizer Applications in the Southeastern United States from 1969 to 2016 Albaugh, Timothy J.; Fox, Thomas R.; Cook, Rachel L. Forest Science, Vol. 65, Issue 3 https://doi.org/10.1093/forsci/fxy058	journal	December 2018
Split down the middle: studying arbuscular mycorrhizal and ectomycorrhizal symbioses using split-root assays Kafle, Arjun; Frank, Hannah E. R.; Rose, Benjamin D. Journal of Experimental Botany, Vol. 73, Issue 5 https://doi.org/10.1093/jxb/erab489	journal	November 2021
Leaf chlorophyll, net gas exchange and chloroplast ultrastructure in citrus leaves of different nitrogen status Bondada, B. R.; Syvertsen, J. P. Tree Physiology, Vol. 23, Issue 8 https://doi.org/10.1093/treephys/23.8.553	journal	June 2003
Wood formation of trees in relation to potassium and calcium nutrition Fromm, J. Tree Physiology, Vol. 30, Issue 9 https://doi.org/10.1093/treephys/tpq024	journal	May 2010
Plant Nutrition: Root Transporters on the Move Zelazny, Enric; Vert, Grégory Plant Physiology, Vol. 166, Issue 2 https://doi.org/10.1104/pp.114.244475	journal	July 2014
Metatranscriptomic analysis of ectomycorrhizal roots reveals genes associated with P iloderma- P inus symbiosis: improved methodologies for assessing gene expression in situ : Metatranscriptomic analysis of ectomycorrhizae Liao, H. -L.; Chen, Y.; Bruns, T. D. Environmental Microbiology, Vol. 16, Issue 12 https://doi.org/10.1111/1462-2920.12619	journal	October 2014
Plant potassium nutrition in ectomycorrhizal symbiosis: properties and roles of the three fungal TOK potassium channels in Hebeloma cylindrosporum: TOK potassium channels of an ectomycorrhizal fungus Guerrero-Galán, Carmen; Delteil, Amandine; Garcia, Kevin Environmental Microbiology, Vol. 20, Issue 5 https://doi.org/10.1111/1462-2920.14122	journal	April 2018
Biological mobilization of potassium from soil by thirteen Suillus species and ectomycorrhizal Pinus massoniana Lamb. seedlings Peng, Liyuan; Huang, Jianguo; Yuan, Ling European Journal of Soil Science, Vol. 71, Issue 4 https://doi.org/10.1111/ejss.12898	journal	November 2019
A group of ectomycorrhizal fungi restricts organic matter accumulation in boreal forest Lindahl, Björn D.; Kyaschenko, Julia; Varenius, Kerstin Ecology Letters, Vol. 24, Issue 7 https://doi.org/10.1111/ele.13746	journal	May 2021
The “isohydric trap”: A proposed feedback between water shortage, stomatal regulation, and nutrient acquisition drives differential growth and survival of European pines under climatic dryness Salazar-Tortosa, Diego; Castro, Jorge; Villar-Salvador, Pedro Global Change Biology, Vol. 24, Issue 9 https://doi.org/10.1111/gcb.14311	journal	June 2018
Growth and phosphorus acquisition of karri (Eucalyptus diversicolor F. Muell.) seedlings inoculated with ectomycorrhizal fungi in relation to phosphorus supply Bougher, N. L.; Grove, T. S.; Malajczuk, N. New Phytologist, Vol. 114, Issue 1 https://doi.org/10.1111/j.1469-8137.1990.tb00376.x	journal	January 1990
Effects of excess nitrogen and phosphorus starvation on the extramatrical mycelium of ectomycorrhizas of Pinus sylvestris L. Wallander, H.; Nylund, J. -E. New Phytologist, Vol. 120, Issue 4 https://doi.org/10.1111/j.1469-8137.1992.tb01798.x	journal	April 1992
A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies Treseder, Kathleen K. New Phytologist, Vol. 164, Issue 2 https://doi.org/10.1111/j.1469-8137.2004.01159.x	journal	July 2004
Organic anion exudation by ectomycorrhizal fungi and Pinus sylvestris in response to nutrient deficiencies van Scholl, Laura; Hoffland, Ellis; van Breemen, Nico New Phytologist, Vol. 170, Issue 1 https://doi.org/10.1111/j.1469-8137.2006.01649.x	journal	March 2006
Measuring external mycelia production of ectomycorrhizal fungi in the field: the soil matrix matters Hendricks, Joseph J.; Mitchell, Robert J.; Kuehn, Kevin A. New Phytologist, Vol. 171, Issue 1 https://doi.org/10.1111/j.1469-8137.2006.01742.x	journal	July 2006
Biomass and compositional responses of ectomycorrhizal fungal hyphae to elevated CO ₂ and nitrogen fertilization Parrent, Jeri Lynn; Vilgalys, Rytas New Phytologist, Vol. 176, Issue 1 https://doi.org/10.1111/j.1469-8137.2007.02155.x	journal	October 2007
Recovery of ectomycorrhiza after ‘nitrogen saturation’ of a conifer forest Högberg, Peter; Johannisson, Christian; Yarwood, Stephanie New Phytologist, Vol. 189, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03485.x	journal	September 2010
Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? Näsholm, Torgny; Högberg, Peter; Franklin, Oskar New Phytologist, Vol. 198, Issue 1 https://doi.org/10.1111/nph.12139	journal	January 2013
Potassium nutrition of ectomycorrhizal Pinus pinaster : overexpression of the Hebeloma cylindrosporum Hc Trk1 transporter affects the translocation of both K ⁺ and phosphorus in the host plant Garcia, Kevin; Delteil, Amandine; Conéjéro, Geneviève New Phytologist, Vol. 201, Issue 3 https://doi.org/10.1111/nph.12603	journal	November 2013
A continental view of pine-associated ectomycorrhizal fungal spore banks: a quiescent functional guild with a strong biogeographic pattern Glassman, Sydney I.; Peay, Kabir G.; Talbot, Jennifer M. New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13240	journal	January 2015
Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses Garcia, Kevin; Delaux, Pierre‐Marc; Cope, Kevin R. New Phytologist, Vol. 208, Issue 1 https://doi.org/10.1111/nph.13423	journal	April 2015
Production and turnover of ectomycorrhizal extramatrical mycelial biomass and necromass under elevated CO ₂ and nitrogen fertilization Ekblad, Alf; Mikusinska, Anna; Ågren, Göran I. New Phytologist, Vol. 211, Issue 3 https://doi.org/10.1111/nph.13961	journal	April 2016
Recently photoassimilated carbon and fungus‐delivered nitrogen are spatially correlated in the ectomycorrhizal tissue of Fagus sylvatica Mayerhofer, Werner; Schintlmeister, Arno; Dietrich, Marlies New Phytologist, Vol. 232, Issue 6 https://doi.org/10.1111/nph.17591	journal	August 2021
Carbon–nitrogen relations of ectomycorrhizal mycelium across a natural nitrogen supply gradient in boreal forest Högberg, Mona N.; Högberg, Peter; Wallander, Håkan New Phytologist, Vol. 232, Issue 4 https://doi.org/10.1111/nph.17701	journal	September 2021
Suppressor T Cells: Role in Immune Regulation Marx, Jean L. Science, Vol. 188, Issue 4185 https://doi.org/10.1126/science.188.4185.245	journal	April 1975
Transcriptome Analysis Provides Novel Insights into the Capacity of the Ectomycorrhizal Fungus Amanita pantherina To Weather K-Containing Feldspar and Apatite Sun, Qibiao; Fu, Ziyu; Finlay, Roger Applied and Environmental Microbiology, Vol. 85, Issue 15 https://doi.org/10.1128/AEM.00719-19	journal	May 2019
Acid phosphatase, alkaline phosphatase, and nitrate reductase activity of selected ectomycorrhizal fungi Ho, Iwan Canadian Journal of Botany, Vol. 67, Issue 3 https://doi.org/10.1139/b89-101	journal	March 1989
Effects of Hebeloma arenosa and phosphorus fertility on root acid phosphatase activity of red pine (Pinus resinosa) seedlings MacFall, Janet; Slack, Steven A.; Iyer, Jaya Canadian Journal of Botany, Vol. 69, Issue 2 https://doi.org/10.1139/b91-052	journal	February 1991
Effects of ammonium sulphate on the community structure and biomass of ectomycorrhizal fungi in a Norway spruce stand in southwestern Sweden Kårén, Ola; Nylund, Jan-Erik Canadian Journal of Botany, Vol. 75, Issue 10 https://doi.org/10.1139/b97-875	journal	October 1997
Fungal Shaker-like channels beyond cellular K+ homeostasis: A role in ectomycorrhizal symbiosis between Hebeloma cylindrosporum and Pinus pinaster Garcia, Kevin; Guerrero-Galán, Carmen; Frank, Hannah E. R. PLOS ONE, Vol. 15, Issue 11 https://doi.org/10.1371/journal.pone.0242739	journal	November 2020
CO ₂ -ENRICHMENT AND NUTRIENT AVAILABILITY ALTER ECTOMYCORRHIZAL FUNGAL COMMUNITIES Parrent, Jeri Lynn; Morris, William F.; Vilgalys, Rytas Ecology, Vol. 87, Issue 9 https://doi.org/10.1890/0012-9658(2006)87[2278:CANAAE]2.0.CO;2	journal	September 2006
The Mutualism–Parasitism Continuum in Ectomycorrhizas: a Quantitative Assessment Using Meta-Analysis Karst, Justine; Marczak, Laurie; Jones, Melanie D. Ecology, Vol. 89, Issue 4 https://doi.org/10.1890/07-0823.1	journal	April 2008
Ectomycorrhizal Plant-Fungal Co-invasions as Natural Experiments for Connecting Plant and Fungal Traits to Their Ecosystem Consequences Hoeksema, Jason D.; Averill, Colin; Bhatnagar, Jennifer M. Frontiers in Forests and Global Change, Vol. 3 https://doi.org/10.3389/ffgc.2020.00084	journal	July 2020
The role of mycorrhizal associations in plant potassium nutrition Garcia, Kevin; Zimmermann, Sabine D. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00337	journal	July 2014
Forest Soil Phosphorus Resources and Fertilization Affect Ectomycorrhizal Community Composition, Beech P Uptake Efficiency, and Photosynthesis Zavišić, Aljosa; Yang, Nan; Marhan, Sven Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00463	journal	April 2018
Effects of Soil Microbes on Functional Traits of Loblolly Pine (Pinus taeda) Seedling Families From Contrasting Climates Ulrich, Danielle E. M.; Sevanto, Sanna; Peterson, Samantha Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01643	journal	January 2020
Juvenile Southern Pine Response to Fertilization Is Influenced by Soil Drainage and Texture Albaugh, Timothy; Fox, Thomas; Allen, H. Forests, Vol. 6, Issue 12 https://doi.org/10.3390/f6082799	journal	August 2015
Humedad EdÁFica, NitrÓGeno y Hongos EctomicorrÍZicos Comestibles en el Crecimiento de pino Perea-Estrada, Víctor M.; Pérez-Moreno, Jesús; Villarreal-Ruiz, Luis Revista Fitotecnia Mexicana, Vol. 32, Issue 2 https://doi.org/10.35196/rfm.2009.2.93-102	journal	June 2009
Effect of Ectomycorrhizal Development on Growth in Pine Seedlings Jha, B. N.; Sharma, G. D.; Shukla, A. K. Journal of Plant Sciences, Vol. 3, Issue 1 https://doi.org/10.3923/jps.2008.77.84	journal	December 2007
Growth Responses of Loblolly Pine in the Southeast United States to Midrotation Applications of Nitrogen, Phosphorus, Potassium, and Micronutrients Carlson, Colleen A.; Fox, Thomas R.; Allen, H. Lee Forest Science, Vol. 60, Issue 1 https://doi.org/10.5849/forsci.12-158	journal	February 2014

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ACORN Review: NPK fertilizer use in loblolly pine plantations: Who are we really feeding?

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