Plant-sediment interactions in salt marshes – An optode imaging study of O2, pH, and CO2 gradients in the rhizosphere

Frontiers in Plant Science

Volumn 9, Issue , 2018, Pages

  Koop Jakobsen, Ketil ^a   Mueller, Peter ^b   Meier, Robert J ^c   Liebsch, Gregor ^c   Jensen, Kai ^b  

^a UNIVERSITY OF BREMEN   (Germany)

^b UNIVERSITY OF HAMBURG   (Germany)

^c PRESENS PRECISION SENSING GMBH   (Germany)

Author keywords

Imaging methods; Planar optode; Plant soil interactions; Roots; Salt marsh; Sediment oxygenation; Soil chemistry; Spartina

Indexed keywords

EID: 85046899808     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2018.00541     Document Type: Article

References (50)

1. Armstrong, W. (1971). Radial oxygen losses from intact rice roots as affected by distance from the apex, respiration and waterlogging. Physiol. Plant. 25, 192–197. doi: 10.1111/j.1399-3054.1971.tb01427.x
2. Armstrong, W., Cousins, D., Armstrong, J., Turner, D. W., and Beckett, P. M. (2000). Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis. Ann. Bot. 86, 687–703. doi: 10.1006/anbo.2000. 1236
3. 2 optodes and membrane inlet mass spectrometry. Soil Biol. Biochem. 42, 2254–2265. doi: 10.1016/j.soilbio.2010.08.026
4. Begg, C. B. M., Kirk, G. J. D., Mackenzie, A. F., and Neue, H. U. (1994). Root-induced iron oxidation and pH changes in the lowland rice rhizosphere. New Phytol. 128, 469–477. doi: 10.1111/j.1469-8137.1994.tb02993.x
5. Bernal, B., Megonigal, J. P., and Mozdzer, T. J. (2017). An invasive wetland grass primes deep soil carbon pools. Glob. Change Biol. 23, 2104–2116. doi: 10.1111/gcb.13539
6. Bloom, A. J., Meyerhoff, P. A., Taylor, A. R., and Rost, T. L. (2002). Root development and absorption of ammonium and nitrate from the rhizosphere. J. Plant Growth Regul. 21, 416–431. doi: 10.1007/s00344-003-0009-8
7. Blossfeld, S. (2013). Light for the dark side of plant life: –Planar optodes visualizing rhizosphere processes. Plant Soil 369, 29–32. doi: 10.1007/s11104-013-1767-0
8. Blossfeld, S., and Gansert, D. (2007). A novel non-invasive optical method for quantitative visualization of pH dynamics in the rhizosphere of plants. Plant Cell Environ. 30, 176–186. doi: 10.1111/j.1365-3040.2006.01616.x
9. Blossfeld, S., Gansert, D., Thiele, B., Kuhn, A. J., and Loesch, R. (2011). The dynamics of oxygen concentration, pH value, and organic acids in the rhizosphere of Juncus spp. Soil Biol. Biochem. 43, 1186–1197. doi: 10.1016/j. soilbio.2011.02.007
10. 2 dynamics with planar optodes. Ann. Bot. 112, 267–276. doi: 10.1093/aob/mct047
11. Bradley, P. M., and Morris, J. T. (1990). Influence of oxygen and sulfide concentration on nitrogen uptake kinetics in Spartina alterniflora. Ecology 71, 282–287. doi: 10.2307/1940267
12. + uptake in Spartina alterniflora. Oecologia 85, 375–380. doi: 10.1007/BF00320613
13. Bu, N., Qu, J., Li, Z., Li, G., Zhao, H., Zhao, B., et al. (2015). Effects of Spartina alterniflora invasion on soil respiration in the Yangtze River estuary, China. PLoS One 10:e0121571. doi: 10.1371/journal.pone.0121571
14. Ca çador, I., Vale, C., and Catarino, F. (1996). Accumulation of Zn, Pb, Cu, Cr and Ni in sediments between roots of the Tagus estuary salt marshes, Portugal. Estuar. Coast. Shelf Sci. 42, 393–403. doi: 10.1006/ecss.1996.0026
15. Catallo, W. J. (1999). Hourly and Daily Variation of Sediment Redox Potential in Tidal Wetland Sediments. Biological Division Science Report USGS/BRD/BSR-1999–1991. Reston, VA: U.S. Geological Survey.
16. Ehrenfeld, J. G., Ravit, B., and Elgersma, K. (2005). Feedback in the plant-soil system. Annu. Rev. Environ. Resour. 30, 75–115. doi: 10.1146/annurev.energy.30.050504.144212
17. Frederiksen, M. S., and Glud, R. N. (2006). Oxygen dynamics in the rhizosphere of Zostera marina: a two-dimensional planar optode study. Limnol. Oceanogr. 51, 1072–1083. doi: 10.4319/lo.2006.51.2.1072
18. Gribsholt, B., and Kristensen, E. (2002). Effects of bioturbation and plant roots on salt marsh biogeochemistry: a mesocosm study. Mar. Ecol. Prog. Ser. 241, 71–87. doi: 10.3354/meps241071
19. Hines, M. E., Banta, G. T., Giblin, A. E., and Hobbie, J. E. (1994). Acetate concentrations and oxidation in salt-marsh sediments. Limnol. Oceanogr. 39, 140–148. doi: 10.4319/lo.1994.39.1.0140
20. Hinsinger, P., Bengough, A. G., Vetterlein, D., and Young, I. M. (2009). Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321, 117–152. doi: 10.1007/s11104-008-9885-9
21. Hinsinger, P., Plassard, C., Tang, C., and Jaillard, B. (2003). Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248, 43–59. doi: 10.1023/A:102237113 0939
22. Howes, B. L., Dacey, J. W. H., and Teal, J. M. (1985). Annual carbon mineralization and belowground production of Spartina alterniflora in a New England salt marsh. Ecology 66, 595–605. doi: 10.2307/1940408
23. Howes, B. L., and Teal, J. M. (1994). Oxygen loss from Spartina alterniflora and its relationship to salt marsh oxygen balance. Oecologia 97, 431–438. doi: 10.1007/BF00325879
24. Koop-Jakobsen, K., Fischer, J., and Wenzhöfer, F. (2017). Survey of sediment oxygenation in rhizospheres of the saltmarsh grass - Spartina anglica. Sci. Total Environ. 589, 191–199. doi: 10.1016/j.scitotenv.2017.02.147
25. Koop-Jakobsen, K., and Wenzhöfer, F. (2015). The dynamics of plant-mediated sediment oxygenation in Spartina anglica rhizospheres—a planar optode study. Estuar. Coasts 38, 951–963. doi: 10.1007/s12237-014-9861-y
26. Koretsky, C. M., Haveman, M., Cuellar, A., Beuving, L., Shattuck, T., and Wagner, M. (2008). Influence of Spartina and Juncus on saltmarsh sediments. I. Pore water geochemistry. Chem. Geol. 255, 87–99. doi: 10.1007/s00248-015-0651-2
27. Lai, W.-L., Zhang, Y., and Chen, Z.-H. (2012). Radial oxygen loss, photosynthesis, and nutrient removal of 35 wetland plants. Ecol. Eng. 39, 24–30. doi: 10.1016/j.watres.2011.05.002
28. 2 dynamics in the rhizosphere of young rice plants (Oryza sativa L.) as studied by planar optodes. Plant Soil 390, 279–292. doi: 10.1007/s11104-015-2382-z
29. Lee, R. W. (1999). Oxidation of sulfide by Spartina alterniflora roots. Limnol. Oceanogr. 44, 1155–1159. doi: 10.4319/lo.1999.44.4.1155
30. Lenzewski, N., Mueller, P., Meier, R. J., Liebsch, G., Jensen, K., and Koop- Jakobsen, K. (2018). Dynamics of oxygen and carbon dioxide in rhizospheres of Lobelia dortmanna – a planar optode study of belowground gas exchange between plants and sediment. New Phytol. 218, 131–141. doi: 10.1111/nph. 14973
31. Megonigal, J. P., Hines, M. E., and Visscher, P. T. (2004). “Anaerobic metabolism: linkages to trace gases and aerobic processes,” in Biogeochemistry, ed. W. H. Schlesinger (Oxford: Elsevier-Pergamon).
32. Mendelssohn, I. A., and Morris, J. T. (2002). “Eco-physiological controls on the productivity of Spartina alterniflora Loisel,” in Concepts and Controversies in Tidal Marsh Ecology, eds M. P. Weinstein and D. A. Kreeger (Dordrecht: Kluwer Academic Publishers).
33. Millero, F. J., Graham, T. B., Huang, F., Bustos-Serrano, H., and Pierrot, D. (2006). Dissociation constants of carbonic acid in seawater as a function of salinity and temperature. Mar. Chem. 100, 80–94. doi: 10.1016/j.marchem.2005. 12.001
34. Minett, D. A., Cook, P. L. M., Kessler, A. J., and Cavagnaro, T. R. (2013). Root effects on the spatial and temporal dynamics of oxygen in sand-based laboratory-scale constructed biofilters. Ecol. Eng. 58, 414–422. doi: 10.1016/j. ecoleng.2013.06.028
35. 2 on ammonium uptake and root respiration by Spartina alterniflora. Am. J. Bot. 71, 979–985. doi: 10.1002/j.1537-2197.1984.tb14164.x
36. Mozdzer, T. J., Langley, J. A., Mueller, P., and Megonigal, J. P. (2016). Deep rooting and global change facilitate spread of invasive grass. Biol. Invasions 18, 2619–2631. doi: 10.1007/s10530-016-1156-8
37. Mueller, P., Jensen, K., and Megonigal, J. P. (2016). Plants mediate soil organic matter decomposition in response to sea level rise. Glob. Change Biol. 22, 404–414. doi: 10.1111/gcb.13082
38. Neumann, G., George, T., and Plassard, C. (2009). Strategies and methods for studying the rhizosphere—the plant science toolbox. Plant Soil 321, 431–456. doi: 10.1007/s11104-009-9953-9
39. Parkin, T. B., and Kaspar, T. C. (2003). Temperature controls on diurnal carbon dioxide flux. Soil Sci. Soc. Am. J. 67, 1763–1772. doi: 10.2136/sssaj2003. 1763
40. Patrick, W. H., and Delaune, R. D. (1977). Chemical and biological redox systems affecting nutrient availability in the coastal wetlands. Geosci. Man 18, 131–137.
41. Pezeshki, S. R. (2001). Wetland plant responses to soil flooding. Environ. Exp. Bot. 46, 299–312. doi: 10.1016/S0098-8472(01)00107-1
42. Polerecky, L., Volkenborn, N., and Stief, P. (2006). High temporal resolution oxygen imaging in bioirrigated sediments. Environ. Sci. Technol. 40, 5763–5769. doi: 10.1021/es060494l
43. Rozema, J., Luppes, E., and Broekman, R. (1985). Differential response of saltmarsh species to variation of iron and manganese. Vegetatio 62, 293–301. doi: 10.1007/BF00044756
44. Santner, J., Larsen, M., Kreuzeder, A., and Glud, R. N. (2015). Two decades of chemical imaging of solutes in sediments and soils – a review. Anal. Chim. Acta 878, 9–42. doi: 10.1016/j.aca.2015.02.006
45. Schreiber, C. M., Zeng, B., Blossfeld, S., Rascher, U., Kazda, M., Schurr, U., et al. (2012). Monitoring rhizospheric pH, oxygen, and organic acid dynamics in two short-time flooded plant species. J. Plant Nutr. Soil Sci. 175, 761–768. doi: 10.1002/jpln.201000427
46. Tschiersch, H., Liebsch, G., Stangelmayer, A., Ljudmilla, B., and Rolletschek, H. (2011). “Planar oxygen sensors for non invasive imaging in experimental biology,” in Microsensors, ed. I. Minin (Rijeka: Intechopen), 281–294.
47. Wang, X. D., Meier, R. J., Link, M., and Wolfbeis, O. S. (2010). Photographing oxygen distribution. Angew. Chem. Int. Ed. Engl. 49, 4907–4909. doi: 10.1002/anie.201001305
48. Wießner, A., Kuschk, P., and Stottmeister, U. (2002). Oxygen release by roots of Typha latifolia and Juncus effusus in laboratory hydroponic systems. Eng. Life Sci. 22, 209–216. doi: 10.1002/1521-3846(200205)22:1/2<209::AID-ABIO209> 3.0.CO;2-O
49. Winkel, A., Colmer, T. D., and Pedersen, O. (2011). Leaf gas films of Spartina anglica enhance rhizome and root oxygen during tidal submergence. Plant Cell Environ. 34, 2083–2092. doi: 10.1111/j.1365-3040.2011.02405.x
50. Wolf, A. A., Drake, B. G., Erickson, J. E., and Megonigal, J. P. (2007). An oxygen-mediated positive feedback between elevated carbon dioxide and soil organic matter decomposition in a simulated anaerobic wetland. Glob. Change Biol. 13, 2036–2044. doi: 10.1111/j.1365-2486.2007.01407.x