Nitrogen and light regulate symbiotic nitrogen fixation by a temperate forest tree.
Disturbance
Nodule
Rhizobia
Robinia pseudoacacia (black locust)
Succession
Journal
Oecologia
ISSN: 1432-1939
Titre abrégé: Oecologia
Pays: Germany
ID NLM: 0150372
Informations de publication
Date de publication:
Feb 2023
Feb 2023
Historique:
received:
24
06
2022
accepted:
03
01
2023
pubmed:
14
1
2023
medline:
25
2
2023
entrez:
13
1
2023
Statut:
ppublish
Résumé
Symbiotic nitrogen fixation (SNF) is a critical mechanism of ecosystem recovery, and in forests of the eastern United States, the most common tree species that supports SNF is black locust (Robinia pseudoacacia L.). Despite its prevalence, black locust's fixation strategy-whether it maintains fixation at a constant rate (obligate fixation) or reduces its fixation rate (facultative fixation)-is unknown. Here, we examined how nitrogen and light control SNF by black locust, by growing seedlings under two nitrogen levels and across four levels of light. Seedlings were harvested after 12 weeks to determine biomass changes, nodule activity, and photosynthetic rates. Black locust seedlings increased biomass growth with increasing light, but only in the absence of nitrogen addition, while seedling root:shoot (biomass) modestly declined with increasing light regardless of nitrogen level. We found that black locust behaved like a facultative fixer, and regulated fixation by excising or maintaining nodules, and by controlling nodule biomass and activity. Specifically, nitrogen addition reduced seedling investment in nodule biomass (g g
Identifiants
pubmed: 36637524
doi: 10.1007/s00442-023-05313-0
pii: 10.1007/s00442-023-05313-0
doi:
Substances chimiques
Nitrogen
N762921K75
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
565-574Subventions
Organisme : Division of Environmental Biology
ID : 1440485
Organisme : Division of Environmental Biology
ID : 1637522
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Barron AR, Purves DW, Hedin LO (2011) Facultative nitrogen fixation by canopy legumes in a lowland tropical forest. Oecologia 165:511–520. https://doi.org/10.1007/s00442-010-1838-3
doi: 10.1007/s00442-010-1838-3
pubmed: 21110206
Batterman SA, Wurzburger N, Hedin LO (2013) Nitrogen and phosphorus interact to control tropical symbiotic N
doi: 10.1111/1365-2745.12138
Boring LR, Swank WT (1984a) The role of black locust (Robinia pseudoacacia) in forest succession. J Ecol 72:749. https://doi.org/10.2307/2259529
doi: 10.2307/2259529
Boring LR, Swank WT (1984b) Symbiotic nitrogen fixation in regenerating black locust (Robinia pseudoacacia L.) stands. Forest Science 30:528–537
Carpenter DO, Taylor MK, Callaham MA, Hiers JK, Loudermilk EL, O’Brien JJ, Wurzburger N (2021) Benefit or liability? The ectomycorrhizal association may undermine tree adaptations to fire after long-term fire exclusion. Ecosystems 24:1059–1074. https://doi.org/10.1007/s10021-020-00568-7
doi: 10.1007/s10021-020-00568-7
Dovrat G, Masci T, Bakhshian H, Mayzlish Gati E, Golan S, Sheffer E (2018) Drought-adapted plants dramatically downregulate dinitrogen fixation: evidences from mediterranean legume shrubs. J Ecol 106:1534–1544. https://doi.org/10.1111/1365-2745.12940
doi: 10.1111/1365-2745.12940
Elliott KJ, Caldwell PV, Brantley ST, Miniat CF, Vose JM, Swank WT (2017) Water yield following forest–grass–forest transitions. Hydrol Earth Syst Sci 21:981–997. https://doi.org/10.5194/hess-21-981-2017
doi: 10.5194/hess-21-981-2017
Evans JR, Jakobsen I, Ögren E (1993) Photosynthetic light-response curves: 2. Gradients of light absorption and photosynthetic capacity. Planta. https://doi.org/10.1007/BF00195076
doi: 10.1007/BF00195076
Gei M, Rozendaal DMA, Poorter L, Bongers F, Sprent JI, Garner MD, Aide TM, Andrade JL et al (2018) Legume abundance along successional and rainfall gradients in neotropical forests. Nat Ecol Evol 2:1104–1111. https://doi.org/10.1038/s41559-018-0559-6
doi: 10.1038/s41559-018-0559-6
pubmed: 29807995
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Cal Agric Exp St Circ 347:32
Johnsen KH, Bongarten BC (1991) Allometry of acetylene reduction and nodule growth of Robinia pseudoacacia families subjected to varied root zone nitrate concentrations. Tree Physiol 9:507–522. https://doi.org/10.1093/treephys/9.4.507
doi: 10.1093/treephys/9.4.507
pubmed: 14972843
Knoepp JD, Vose JM, Swank WT (2008) Nitrogen deposition and cycling across an elevation and vegetation gradient in southern appalachian forests. Int J Environ Stud 65:391–410. https://doi.org/10.1080/00207230701862348
doi: 10.1080/00207230701862348
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379. https://doi.org/10.1890/06-2057.1
doi: 10.1890/06-2057.1
pubmed: 18409427
Lenth RV (2022) emmeans: estimated marginal means, aka Least-Squares Means.
Levy-Varon JH, Batterman SA, Medvigy D, Xu X, Hall JS, van Breugel M, Hedin LO (2019) Tropical carbon sink accelerated by symbiotic dinitrogen fixation. Nat Commun 10:5637. https://doi.org/10.1038/s41467-019-13656-7
doi: 10.1038/s41467-019-13656-7
pmcid: 6904724
pubmed: 31822758
Liao W, Menge DNL (2016) Demography of symbiotic nitrogen-fixing trees explains their rarity and successional decline in temperate forests in the United States. PLoS ONE 11:e0164522. https://doi.org/10.1371/journal.pone.0164522
doi: 10.1371/journal.pone.0164522
pmcid: 5079550
pubmed: 27780268
Lu M, Hedin LO (2019) Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modelling. Nat Ecol Evol 3:239–250. https://doi.org/10.1038/s41559-018-0759-0
doi: 10.1038/s41559-018-0759-0
pubmed: 30664701
Mangiafico S (2021) rcompanion: functions to support extension education program evaluation.
McCulloch LA, Porder S (2021) Light fuels while nitrogen suppresses symbiotic nitrogen fixation hotspots in neotropical canopy gap seedlings. New Phytol 231:1734–1745. https://doi.org/10.1111/nph.17519
doi: 10.1111/nph.17519
pubmed: 34058025
Menge DNL, Levin SA, Hedin LO (2008) Evolutionary tradeoffs can select against nitrogen fixation and thereby maintain nitrogen limitation. Proc Natl Acad Sci USA 105:1573–1578. https://doi.org/10.1073/pnas.0711411105
doi: 10.1073/pnas.0711411105
pmcid: 2234186
pubmed: 18223153
Menge DNL, Levin SA, Hedin LO (2009) Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences. Am Nat 174:465–477. https://doi.org/10.1086/605377
doi: 10.1086/605377
pubmed: 19694561
Menge DNL, Wolf AA, Funk JL (2015) Diversity of nitrogen fixation strategies in mediterranean legumes. Nature Plants 1:15064. https://doi.org/10.1038/nplants.2015.64
doi: 10.1038/nplants.2015.64
pubmed: 27250004
Minucci JM, Miniat CF, Wurzburger N (2019) Drought sensitivity of an N
doi: 10.1002/ecy.2862
Nowacki GJ, Abrams MD (2008) The demise of fire and “mesophication” of forests in the eastern United States. Bioscience 58:123–138. https://doi.org/10.1641/B580207
doi: 10.1641/B580207
Patriarca EJ, Tate R, Iaccarino M (2002) Key role of bacterial NH4+ metabolism in rhizobium-plant symbiosis. Microbiol Mol Biol Rev 66:203–222. https://doi.org/10.1128/MMBR.66.2.203-222.2002
doi: 10.1128/MMBR.66.2.203-222.2002
pmcid: 120787
pubmed: 12040124
R Core Team (2022) R: A language for statistical computer. R Foundation for Statistical Computing, Vienna, Austria.
Sheffer E, Batterman SA, Levin SA, Hedin LO (2015) Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle. Nature Plants 1:15182. https://doi.org/10.1038/nplants.2015.182
doi: 10.1038/nplants.2015.182
pubmed: 27251717
Staccone A, Liao W, Perakis S, Compton J, Clark CM, Menge D (2020) A spatially explicit, empirical estimate of tree-based biological nitrogen fixation in forests of the United States. Global Biogeochem Cycles. https://doi.org/10.1029/2019GB006241
doi: 10.1029/2019GB006241
pmcid: 7359885
pubmed: 32665747
Taylor BN, Menge DNL (2018) Light regulates tropical symbiotic nitrogen fixation more strongly than soil nitrogen. Nature Plants 4:655–661. https://doi.org/10.1038/s41477-018-0231-9
doi: 10.1038/s41477-018-0231-9
pubmed: 30127409
Truchet GL, Dazzo FB (1982) Morphogenesis of lucerne root nodules incited by Rhizobium meliloti in the presence of combined nitrogen. Planta 154:352–360. https://doi.org/10.1007/BF00393915
doi: 10.1007/BF00393915
pubmed: 24276164
Ursino DJ, Hunter DM, Laing RD, Keighley JLS (1982) Nitrate modification of photosynthesis and photoassimilate export in young nodulated soybean plants. Can J Bot 60:2665–2670. https://doi.org/10.1139/b82-323
doi: 10.1139/b82-323
Vítková M, Müllerová J, Sádlo J, Pergl J, Pyšek P (2017) Black locust (Robinia pseudoacacia) beloved and despised: a story of an invasive tree. For Ecol Manage 384:287–302. https://doi.org/10.1016/j.foreco.2016.10.057
doi: 10.1016/j.foreco.2016.10.057
pmcid: 6143167
pubmed: 30237654
Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Phil Trans R Soc B 368:20130119. https://doi.org/10.1098/rstb.2013.0119
doi: 10.1098/rstb.2013.0119
pmcid: 3682739
pubmed: 23713117
Walsh KB, Thorpe MR, Minchin PEH (1998) Photoassimilate partitioning in nodulated soybean II. The effect of changes in photoassimilate availability shows that nodule permeability to gases is not linked to the supply of solutes or water. J Exp Bot 49:1817–1825. https://doi.org/10.1093/jxb/49.328.1817
doi: 10.1093/jxb/49.328.1817
Wang X, Guo W, Du N, Guo W, Pang J (2020) Rapid nitrogen fixation contributes to similar growth and photosynthetic rate of Robinia pseudoacacia supplied with different levels of nitrogen. Tree Physiol 41:177–189. https://doi.org/10.1093/treephys/tpaa129
doi: 10.1093/treephys/tpaa129
Wurzburger N, Hedin LO (2016) Taxonomic identity determines N
doi: 10.1111/ele.12543
pubmed: 26584690
Wurzburger N, Miniat CF (2014) Drought enhances symbiotic dinitrogen fixation and competitive ability of a temperate forest tree. Oecologia 174:1117–1126. https://doi.org/10.1007/s00442-013-2851-0
doi: 10.1007/s00442-013-2851-0
pubmed: 24337710
Wurzburger N, Motes JI, Miniat CF (2022) A framework for scaling symbiotic nitrogen fixation using the most widespread nitrogen fixer in eastern deciduous forests of the United States. J Ecol 110:569–581. https://doi.org/10.1111/1365-2745.13819
doi: 10.1111/1365-2745.13819