Assessing root–soil interactions in wetland plants: root exudation and radial oxygen loss

Haviland, Katherine A.; Noyce, Genevieve L.

doi:10.5194/bg-21-5185-2024

Assessing root–soil interactions in wetland plants: root exudation and radial oxygen loss

Journal Article · Wed Nov 20 23:00:00 EST 2024 · Biogeosciences (Online)

DOI:https://doi.org/10.5194/bg-21-5185-2024· OSTI ID:2478313

;

Abstract. Plant rhizosphere processes, such as root exudation and root oxygen loss (ROL), could have significant impacts on the dynamics and magnitude of wetland methane fluxes and other biogeochemical processes but are rarely measured directly. Here, we measure root exudation and ROL from Schoenoplectus americanus and Spartina patens, two plants that have had opposite relationships between biomass and methane flux in field experiments (positive in S. patens, negative in S. americanus). We found contrasting rates of ROL in the two species, with S. americanus releasing orders of magnitude more oxygen (O2) to the soil than S. patens. At the same time, S. patens exuded high amounts of carbon to the soil, and much of the rhizosphere carbon pool was reduced compared to exudates from other wetland species. This work suggests that the relative inputs of O2 and carbon to the rhizosphere vary significantly between wetland plant species, potentially with major consequences on biogeochemical cycling, and highlights the importance of understanding how plant rhizosphere processes mediate soil biogeochemistry at a community level. As global change drivers continue to affect wetlands, future research should consider how feedbacks from plant rhizosphere processes may exacerbate or mitigate coastal wetland methane emissions.

View Journal Article

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0014413; SC0019110; SC0021112

OSTI ID:: 2478313

Alternate ID(s):: OSTI ID: 2482252

Journal Information:: Biogeosciences (Online), Journal Name: Biogeosciences (Online) Journal Issue: 22 Vol. 21; ISSN 1726-4189

Publisher:: Copernicus GmbHCopyright Statement

Country of Publication:: Germany

Language:: English

References (62)

Review: Factors affecting rhizosphere priming effects Kuzyakov, Yakov Journal of Plant Nutrition and Soil Science, Vol. 165, Issue 4 https://doi.org/10.1002/1522-2624(200208)165:4<382::AID-JPLN382>3.0.CO;2-#	journal	August 2002
Methods of collection of plant root exudates in relation to plant metabolism and purpose: A review Vranova, Valerie; Rejsek, Klement; Skene, Keith R. Journal of Plant Nutrition and Soil Science, Vol. 176, Issue 2 https://doi.org/10.1002/jpln.201000360	journal	March 2013
Carbon Sequestration and Storage by Wetlands: Implications in the Climate Change Scenario Lolu, Afreen J.; Ahluwalia, Amrik S.; Sidhu, Malkiat C. Restoration of Wetland Ecosystem: A Trajectory Towards a Sustainable Environment https://doi.org/10.1007/978-981-13-7665-8_4	book	June 2019
Gas exchange responses of Chesapeake Bay tidal marsh species under field and laboratory conditions DeJong, T. M.; Drake, B. G.; Pearcy, R. W. Oecologia, Vol. 52, Issue 1 https://doi.org/10.1007/BF00349004	journal	January 1982
Elevated Atmospheric CO2 Increases Root Exudation of Carbon in Wetlands: Results from the First Free-Air CO2 Enrichment Facility (FACE) in a Marshland Sánchez-Carrillo, Salvador; Álvarez-Cobelas, Miguel; Angeler, David G. Ecosystems, Vol. 21, Issue 5 https://doi.org/10.1007/s10021-017-0189-x	journal	October 2017
Local and regional disturbances associated with the invasion of Chesapeake Bay marshes by the common reed Phragmites australis Sciance, M. Benjamin; Patrick, Christopher J.; Weller, Donald E. Biological Invasions, Vol. 18, Issue 9 https://doi.org/10.1007/s10530-016-1136-z	journal	April 2016
Plant root exudates increase methane emissions through direct and indirect pathways Waldo, Nicholas B.; Hunt, Brianna K.; Fadely, Eleanor C. Biogeochemistry, Vol. 145, Issue 1-2 https://doi.org/10.1007/s10533-019-00600-6	journal	September 2019
Wetlands, carbon, and climate change Mitsch, William J.; Bernal, Blanca; Nahlik, Amanda M. Landscape Ecology, Vol. 28, Issue 4 https://doi.org/10.1007/s10980-012-9758-8	journal	June 2012
Biochemical cycling in the rhizosphere having an impact on global change Philippot, L.; Hallin, S.; Börjesson, G. Plant and Soil, Vol. 321, Issue 1-2 https://doi.org/10.1007/s11104-008-9796-9	journal	October 2008
Peatland vascular plant functional types affect dissolved organic matter chemistry Robroek, Bjorn J. M.; Albrecht, Remy J. H.; Hamard, Samuel Plant and Soil, Vol. 407, Issue 1-2 https://doi.org/10.1007/s11104-015-2710-3	journal	October 2015
Interactive regulation of root exudation and rhizosphere denitrification by plant metabolite content and soil properties Maurer, Daniel; Malique, François; Alfarraj, Salah Plant and Soil, Vol. 467, Issue 1-2 https://doi.org/10.1007/s11104-021-05069-7	journal	July 2021
A quick and simple spectrophotometric method to determine total carbon concentrations in root exudate samples of grass species Oburger, Eva; Staudinger, Christiana; Spiridon, Andreea Plant and Soil, Vol. 478, Issue 1-2 https://doi.org/10.1007/s11104-022-05519-w	journal	June 2022
The Dynamics of Plant-Mediated Sediment Oxygenation in Spartina anglica Rhizospheres—a Planar Optode Study Koop-Jakobsen, Ketil; Wenzhöfer, Frank Estuaries and Coasts, Vol. 38, Issue 3 https://doi.org/10.1007/s12237-014-9861-y	journal	August 2014
Soil organic matter mobilization by root exudates of three maize hybrids Nardi, S.; Reniero, F.; Concheri, G. Chemosphere, Vol. 35, Issue 10 https://doi.org/10.1016/S0045-6535(97)00302-0	journal	November 1997
Species and population variation to salinity stress in Panicum hemitomon, Spartina patens, and Spartina alterniflora: morphological and physiological constraints Hester, Mark W.; Mendelssohn, Irving A.; McKee, Karen L. Environmental and Experimental Botany, Vol. 46, Issue 3 https://doi.org/10.1016/S0098-8472(01)00100-9	journal	December 2001
Artificial root exudates excite bacterial nitrogen fixation in the subsurface of mine soils Li, Yang; Yuan, Liang; Xue, Sheng Applied Soil Ecology, Vol. 157 https://doi.org/10.1016/j.apsoil.2020.103774	journal	January 2021
Radial oxygen loss, photosynthesis, and nutrient removal of 35 wetland plants Lai, Wen-Ling; Zhang, Yang; Chen, Zhang-He Ecological Engineering, Vol. 39 https://doi.org/10.1016/j.ecoleng.2011.11.010	journal	February 2012
Can root exudates from emergent wetland plants fuel denitrification in subsurface flow constructed wetland systems? Zhai, Xu; Piwpuan, Narumol; Arias, Carlos A. Ecological Engineering, Vol. 61 https://doi.org/10.1016/j.ecoleng.2013.02.014	journal	December 2013
Effects of root organic exudates on rhizosphere microbes and nutrient removal in the constructed wetlands Chen, Zong-Jing; Tian, Yun-Hui; Zhang, Yang Ecological Engineering, Vol. 92 https://doi.org/10.1016/j.ecoleng.2016.04.001	journal	July 2016
Influences of plant species and radial oxygen loss on nitrous oxide fluxes in constructed wetlands Jiang, Xuyao; Tian, Yunfei; Ji, Xiyan Ecological Engineering, Vol. 142 https://doi.org/10.1016/j.ecoleng.2019.105644	journal	January 2020
Rhizosphere: A new frontier for soil biogeochemistry Hinsinger, Philippe; Plassard, Claude; Jaillard, Benoît Journal of Geochemical Exploration, Vol. 88, Issue 1-3 https://doi.org/10.1016/j.gexplo.2005.08.041	journal	January 2006
Effects of different amino acids and their configurations on methane yield and biotransformation of intermediate metabolites during anaerobic digestion Liu, Hui; Chen, Yinguang; Ye, Jianfeng Journal of Environmental Management, Vol. 296 https://doi.org/10.1016/j.jenvman.2021.113152	journal	October 2021
Elevated CO2 increases soil redox potential by promoting root radial oxygen loss in paddy field Li, Jie; Zhang, Han; Xie, Wenyi Journal of Environmental Sciences, Vol. 136 https://doi.org/10.1016/j.jes.2023.01.003	journal	February 2024
Sampling root exudates – Mission impossible? Oburger, Eva; Jones, David L. Rhizosphere, Vol. 6 https://doi.org/10.1016/j.rhisph.2018.06.004	journal	June 2018
The effects of warming on root exudation and associated soil N transformation depend on soil nutrient availability Wang, Qitong; Chen, Lanying; Xu, Hang Rhizosphere, Vol. 17 https://doi.org/10.1016/j.rhisph.2020.100263	journal	March 2021
Composition and concentration of root exudate analogues regulate greenhouse gas fluxes from tropical peat Girkin, N. T.; Turner, B. L.; Ostle, N. Soil Biology and Biochemistry, Vol. 127 https://doi.org/10.1016/j.soilbio.2018.09.033	journal	December 2018
Molecular changes of soil organic matter induced by root exudates in a rice paddy under CO2 enrichment and warming of canopy air Xiong, Li; Liu, Xiaoyu; Vinci, Giovanni Soil Biology and Biochemistry, Vol. 137 https://doi.org/10.1016/j.soilbio.2019.107544	journal	October 2019
Effects of increased atmospheric CO₂, temperature, and soil N availability on root exudation of dissolved organic carbon by a N-fixing tree (Robinia pseudoacacia L.) Uselman, Shauna M.; Qualls, Robert G.; Thomas, Richard B. Plant and Soil, Vol. 222, Issue 1/2, p. 191-202 https://doi.org/10.1023/A:1004705416108	journal	July 2000
Associations with rhizosphere bacteria can confer an adaptive advantage to plants Haney, Cara H.; Samuel, Buck S.; Bush, Jenifer Nature Plants, Vol. 1, Issue 6 https://doi.org/10.1038/nplants.2015.51	journal	May 2015
Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress Martin, Belinda C.; Bougoure, Jeremy; Ryan, Megan H. The ISME Journal, Vol. 13, Issue 3 https://doi.org/10.1038/s41396-018-0308-5	journal	October 2018
Plant species determine tidal wetland methane response to sea level rise Mueller, Peter; Mozdzer, Thomas J.; Langley, J. Adam Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-18763-4	journal	October 2020
The core metabolome and root exudation dynamics of three phylogenetically distinct plant species McLaughlin, Sarah; Zhalnina, Kateryna; Kosina, Suzanne Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-37164-x	journal	March 2023
Rapid expansion of northern peatlands and doubled estimate of carbon storage Nichols, Jonathan E.; Peteet, Dorothy M. Nature Geoscience, Vol. 12, Issue 11 https://doi.org/10.1038/s41561-019-0454-z	journal	October 2019
Oxygen priming induced by elevated CO2 reduces carbon accumulation and methane emissions in coastal wetlands Noyce, Genevieve L.; Smith, Alexander J.; Kirwan, Matthew L. Nature Geoscience, Vol. 16, Issue 1 https://doi.org/10.1038/s41561-022-01070-6	journal	January 2023
Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma Visser, E. J. W.; Colmer, T. D.; Blom, C. W. P. M. Plant, Cell and Environment, Vol. 23, Issue 11 https://doi.org/10.1046/j.1365-3040.2000.00628.x	journal	November 2000
Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots Colmer, T. D. Plant, Cell and Environment, Vol. 26, Issue 1 https://doi.org/10.1046/j.1365-3040.2003.00846.x	journal	January 2003
Characterization of Root Exudates at Different Growth Stages of Ten Rice (Oryza sativa L.) Cultivars Aulakh, M. S.; Wassmann, R.; Bueno, C. Plant Biology, Vol. 3, Issue 2 https://doi.org/10.1055/s-2001-12905	journal	March 2001
Elevated CO2 stimulates marsh elevation gain, counterbalancing sea-level rise Langley, J. A.; McKee, K. L.; Cahoon, D. R. Proceedings of the National Academy of Sciences, Vol. 106, Issue 15 https://doi.org/10.1073/pnas.0807695106	journal	March 2009
Root Exudates of Wetland Plants Influenced by Nutrient Status and Types of Plant Cultivation Wu, Fu Yong; Chung, Anna King Chuen; Tam, Nora Fung Yee International Journal of Phytoremediation, Vol. 14, Issue 6 https://doi.org/10.1080/15226514.2011.604691	journal	July 2012
Rice: Sulfide-induced Barriers to Root Radial Oxygen Loss, Fe2+ and Water Uptake, and Lateral Root Emergence Armstrong, Jean; Armstrong, William Annals of Botany, Vol. 96, Issue 4 https://doi.org/10.1093/aob/mci215	journal	August 2005
RefMetaPlant: a reference metabolome database for plants across five major phyla Shi, Han; Wu, Xueting; Zhu, Yan Nucleic Acids Research, Vol. 52, Issue D1 https://doi.org/10.1093/nar/gkad980	journal	November 2023
Radial oxygen loss is correlated with nitrogen nutrition in mangroves Cheng, Hao; Liu, Yong; Jiang, Zhao-Yu Tree Physiology, Vol. 40, Issue 11 https://doi.org/10.1093/treephys/tpaa089	journal	July 2020
From energy to (soil organic) matter Gunina, Anna; Kuzyakov, Yakov Global Change Biology, Vol. 28, Issue 7 https://doi.org/10.1111/gcb.16071	journal	January 2022
Phragmites australis - A preliminary study of soil-oxidizing sites and internal gas transport pathways Armstrong, J.; Armstrong, W. New Phytologist, Vol. 108, Issue 4 https://doi.org/10.1111/j.1469-8137.1988.tb04177.x	journal	April 1988
Molecular Phylogenetic and Biogeochemical Studies of Sulfate-Reducing Bacteria in the Rhizosphere of Spartina alterniflora Hines, Mark E.; Evans, Robert S.; Sharak Genthner, Barbara R. Applied and Environmental Microbiology, Vol. 65, Issue 5 https://doi.org/10.1128/AEM.65.5.2209-2216.1999	journal	May 1999
Nitrogen Fixation (Acetylene Reduction) in a Salt Marsh Amended with Sewage Sludge and Organic Carbon and Nitrogen Compounds Hanson, Roger B. Applied and Environmental Microbiology, Vol. 33, Issue 4 https://doi.org/10.1128/aem.33.4.846-852.1977	journal	April 1977
Root Growth and Metabolism Under Oxygen Deficiency Armstrong, William; Drew, Malcolm C. Plant Roots https://doi.org/10.1201/9780203909423-50	book	March 2002
Biology of Wetland Soils Craft, Christopher Wetland Soils https://doi.org/10.1201/9781420026238.ch5	book	September 2000
Role of root exudates on assimilation of phosphorus in young and old Arabidopsis thaliana plants Pantigoso, Hugo A.; Yuan, Jun; He, Yanhui PLOS ONE, Vol. 15, Issue 6 https://doi.org/10.1371/journal.pone.0234216	journal	June 2020
Productive wetlands restored for carbon sequestration quickly become net CO2 sinks with site-level factors driving uptake variability Valach, Alex C.; Kasak, Kuno; Hemes, Kyle S. PLOS ONE, Vol. 16, Issue 3 https://doi.org/10.1371/journal.pone.0248398	journal	March 2021
A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO ₂ Mcleod, Elizabeth; Chmura, Gail L.; Bouillon, Steven Frontiers in Ecology and the Environment, Vol. 9, Issue 10 https://doi.org/10.1890/110004	journal	January 2011
A Plant-Soil-Atmosphere Microcosm for Tracing Radiocarbon from Photosynthesis through Methanogenesis Megonigal, J. P.; Whalen, S. C.; Tissue, D. T. Soil Science Society of America Journal, Vol. 63, Issue 3 https://doi.org/10.2136/sssaj1999.03615995006300030033x	journal	January 1999
The thermodynamic ladder in geomicrobiology Bethke, C. M.; Sanford, R. A.; Kirk, M. F. American Journal of Science, Vol. 311, Issue 3 https://doi.org/10.2475/03.2011.01	journal	March 2011
Decomposition of Spartina anglica roots and rhizomes in a salt marsh of the Westerschelde Estuary Hemminga, Ma; Kok, Cj; de Munck, W. Marine Ecology Progress Series, Vol. 48 https://doi.org/10.3354/meps048175	journal	January 1988
Oxic microzones and radial oxygen loss from roots of Zostera marina Jensen, Si; Kühl, M.; Glud, Rn Marine Ecology Progress Series, Vol. 293 https://doi.org/10.3354/meps293049	journal	January 2005
Plant-Sediment Interactions in Salt Marshes – An Optode Imaging Study of O2, pH, and CO2 Gradients in the Rhizosphere Koop-Jakobsen, Ketil; Mueller, Peter; Meier, Robert J. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00541	journal	May 2018
Root Exudation of Primary Metabolites: Mechanisms and Their Roles in Plant Responses to Environmental Stimuli Canarini, Alberto; Kaiser, Christina; Merchant, Andrew Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00157	journal	February 2019
Plant-Mediated Rhizosphere Oxygenation in the Native Invasive Salt Marsh Grass Elymus athericus Koop-Jakobsen, Ketil; Meier, Robert J.; Mueller, Peter Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.669751	journal	June 2021
Radial Oxygen Loss from Plant Roots—Methods Jiménez, Juan de la Cruz; Pellegrini, Elisa; Pedersen, Ole Plants, Vol. 10, Issue 11 https://doi.org/10.3390/plants10112322	journal	October 2021
Root Exudates Mediate the Processes of Soil Organic Carbon Input and Efflux Lei, Xue; Shen, Yuting; Zhao, Jianing Plants, Vol. 12, Issue 3 https://doi.org/10.3390/plants12030630	journal	January 2023
Oxygen dynamics in the rhizosphere of Zostera marina: A two-dimensional planar optode study Frederiksen, Morten S.; Glud, Ronnie N. Limnology and Oceanography, Vol. 51, Issue 2 https://doi.org/10.4319/lo.2006.51.2.1072	journal	March 2006
Biogeochemical and plant trait mechanisms drive enhanced methane emissions in response to whole-ecosystem warming Noyce, Genevieve L.; Megonigal, J. Patrick Biogeosciences, Vol. 18, Issue 8 https://doi.org/10.5194/bg-18-2449-2021	journal	January 2021

Similar Records

Plant Root Exudates Increase Methane Emissions through Direct and Indirect Pathways

Journal Article · Tue Oct 01 00:00:00 EDT 2019 · Biogeochemistry · OSTI ID:1574469

Assessing root–soil interactions in wetland plants: root exudation and radial oxygen loss

Citation Formats

References (62)

Similar Records

Related Subjects