O2 dynamics in the rhizosphere of young rice plants (Oryza sativa L.) as studied by planar optodes

Plant and Soil

Volumn 390, Issue 1-2, 2015, Pages 279-292

  Larsen, Morten ^a,b,c   Santner, Jakob ^e   Oburger, Eva ^e   Wenzel, Walter W ^e   Glud, Ronnie N ^a,b,c,d  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b SCOTTISH MARINE INSTITUTE   (United Kingdom)

^c Greenland Climate Research Centre (CO Greenland Institute of National Resources)   (Greenland)

^d AARHUS UNIVERSITY   (Denmark)

^e UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

Oxygen; Planar optode; Plaques imaging; Radial oxygen loss; Rhizosphere; Rice (Oryza sativa L.)

Indexed keywords

EID: 84939993263     PISSN: 0032079X     EISSN: 15735036     Source Type: Journal    
DOI: 10.1007/s11104-015-2382-z     Document Type: Article

References (62)

1. Armstrong W (1980) Aeration in higher plants. In: Woolhouse HW (ed) Advances in Botanical Research. Academic Press
2. Armstrong W (1994) Polarographic oxygen eletrodes and their use in plant aeration studies. Proc R Soc Edinb B Biol Sci 102:511–527
3. Armstrong J, Armstrong W (2005) Rice: Sulfide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Ann Bot 96:625–638. doi:10.1093/aob/mci215
4. Badri DV, Loyola-Vargas VM, Broeckling CD, Vivanco JM (2010) Root secretion of phytochemicals in Arabidopsis is predominantly not influenced by diurnal rhythms. Mol Plant 3:491–498. doi:10.1093/mp/ssq004
5. Blossfeld S, Schreiber CM, Liebsch G, Kuhn AJ, Hinsinger P (2013) Quantitative imaging of rhizosphere pH and CO2 dynamics with planar optodes. Ann Bot 112:267–276. doi:10.1093/aob/mct047
6. Borisov SM, Klimant I (2007) Ultrabright oxygen optodes based on cyclometalated iridium(III) coumarin complexes. Anal Chem 79:7501–7509. doi:10.1021/ac0710836
7. Cheng H, Wang M, Wong M, Ye Z (2014) Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues? Plant and Soil 375:137–148. doi:10.1007/s11104-013-1945-0
8. Christensen KK, Sand-Jensen K (1998) Precipitated iron and manganese plaques restrict root uptake of phosphorus in Lobelia dortmanna. Can J Bot 76:2158–2163. doi:10.1139/b98-181
9. Colmer TD (2003) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Ann Bot 91:301–309. doi:10.1093/aob/mcf114
10. Colmer TD, Pedersen O (2008) Oxygen dynamics in submerged rice (Oryza sativa). New Phytol 178:326–334. doi:10.1111/j.1469-8137.2007.02364.x
11. Colmer TD, Gibberd MR, Wiengweera A, Tinh TK (1998) The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution. J Exp Bot 49:1431–1436. doi:10.1093/jxb/49.325.1431
12. Damgaard LR, Revsbech NP, Reichardt W (1998) Use of an oxygen-insensitive microscale biosensor for methane to measure methane concentration profiles in a rice paddy. Appl Environ Microbiol 64:864–870
13. Deng D, Wu S-C, Wu F-Y, Deng H, Wong M-H (2010) Effects of root anatomy and Fe plaque on arsenic uptake by rice seedlings grown in solution culture. Environ Pollut 158:2589–2595. doi:10.1016/j.envpol.2010.05.015
14. Estapa ML, Boss E, Mayer LM, Roesler CS (2012) Role of iron and organic carbon in mass-specific light absorption by particulate matter from Louisiana coastal waters. Limnol Oceanogr 57:97–112. doi:10.4319/lo.2012.57.1.0097
15. Faget M, Blossfeld S, Von Gillhaußen P, Schurr U, Temperton VM (2013) Disentangling who is who during rhizosphere acidification in root interactions: combining fluorescence with optode techniques. Front Plant Sci 4. doi: 10.3389/fpls.2013.00392
16. Fenchel T (1996) Worm burrows and oxic microniches in marine sediments. 1. Spatial and temporal scales. Mar Biol 127:289–295. doi:10.1007/bf00942114
17. Fischer JP, Wenzhofer F (2010) A novel planar optode setup for concurrent oxygen and light field imaging: Application to a benthic phototrophic community. Limnol Oceanogr Methods 8:254–268. doi:10.4319/lom.2010.8.254
18. Frederiksen MS, Glud RN (2006) Oxygen dynamics in the rhizosphere of Zostera marina: A two-dimensional planar optode study. Limnol Oceanogr 51:1072–1083
19. Frenzel P, Rothfuss F, Conrad R (1992) Oxygen profiles and methane turnover in a flooded rice microcosm. BFS 14:84–89
20. Glud RN (2008) Oxygen dynamics of marine sediments. Mar Biol Res 4:243–289. doi:10.1080/17451000801888726
21. Glud RN, Ramsing NB, Gundersen JK, Klimant I (1996) Planar optrodes: A new tool for fine scale measurements of two- dimensional O2 distribution in benthic communities. Mar Ecol Prog Ser 140:217–226
22. Greenway H, Armstrong W, Colmer TD (2006) Conditions leading to high CO2 (>5 kPa) in waterlogged-flooded soils and possible effects on root growth and metabolism. Ann Bot 98:9–32. doi:10.1093/aob/mcl076
23. Holst G, Grunwald B (2001) Luminescence lifetime imaging with transparent oxygen optodes. Sensors Actuators B Chem 74:78–90. doi:10.1016/s0925-4005(00)00715-2
24. Holst G, Kohls O, Klimant I, König B, Kühl M, Richter T (1998) A modular luminescence lifetime imaging system for mapping oxygen distribution in biological samples. Sens Actuators B 51:163–170. doi:10.1016/s0925-4005(98)00232-9
25. Insalud N, Bell RW, Colmer TD, Rerkasem B (2006) Morphological and physiological responses of rice (Oryza sativa) to limited phosphorus supply in aerated and stagnant solution culture. Ann Bot 98:995–1004. doi:10.1093/aob/mcl194
26. Jensen SI, Kuhl M, Glud RN, Jorgensen LB, Prieme A (2005) Oxic microzones and radial oxygen loss from roots of Zostera marina. Mar Ecol Prog Ser 293:49–58. doi:10.3354/meps293049
27. Jiang F, Chen X, Luo A (2009) “Iron plaque formation on wetland plants and its influence on phosphorus, calcium and metal uptake.” Aquat Ecol 43(4):879–890
28. Jovanovic Z, Pedersen MØ, Larsen M, Kristensen E, Glud RN (2015) Rhizosphere O2 dynamics in young Zostera marina and Ruppia maritime. Mar Ecol Prog Ser 518: 95–105. doi:10.3354/meps11041
29. Jørgensen BB, Revsbech NP (1985) Diffusive boundary-layers and the oxygen-uptake of sediments and detritus. Limnol Oceanogr 30:111–122
30. Kirk GJD (1993) Root ventilation, rhizosphere modification, and nutrient uptake by rice. In: Vries F, Teng P, Metselaar K (eds) Systems approaches for agricultural development. Springer, Netherlands
31. Kirk GJD (2003) Rice root properties for internal aeration and efficient nutrient acquisition in submerged soil. New Phytol 159:185–194. doi:10.1046/j.0028-646x.2003.00793.x
32. Kirk GJD, Du LV (1997) Changes in rice root architecture, porosity, and oxygen and proton release under phosphorus deficiency. New Phytol 135:191–200. doi:10.1046/j.1469-8137.1997.00640.x
33. Klimant I, Meyer V, Kuhl M (1995) Fiber-optic oxygen microsensors, a new tool in aquatic biology. Limnol Oceanogr 40:1159–1165
34. Kludze HK, Delaune RD, Patrick WH (1993) Aerenchyma formation and methane and oxygen-exchange in rice. Soil Sci Soc Am J 57:386–391
35. Kotula L, Ranathunge K, Schreiber L, Steudle E (2009) Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution. J Exp Bot 60:2155–2167. doi:10.1093/jxb/erp089
36. Larsen M, Borisov SM, Grunwald B, Klimant I, Glud RN (2011) A simple and inexpensive high resolution color ratiometric planar optode imaging approach: application to oxygen and pH sensing. Limnol Oceanogr Methods 9:348–360. doi:10.4319/lom.2011.9.348
37. Mayr T, Borisov SM, Abel T, Enko B, Waich K, Gn M, Klimant I (2009) Light harvesting as a simple and versatile way to enhance brightness of luminescent sensors. Anal Chem 81:6541–6545. doi:10.1021/ac900662x
38. Mendelssohn I, Kleiss B, Wakeley J (1995) Factors controlling the formation of oxidized root channels: a review. Wetlands 15:37–46. doi:10.1007/bf03160678
39. Meysman FJR, Galaktionov OS, Glud RN, Middelburg JJ (2010) Oxygen penetration around burrows and roots in aquatic sediments. J Mar Res 68:309–336. doi:10.1357/002224010793721406
40. Miyamoto N, Steudle E, Hirasawa T, Lafitte R (2001) Hydraulic conductivity of rice roots. J Exp Bot 52:1835–1846. doi:10.1093/jexbot/52.362.1835
41. Mongon J, Konnerup D, Colmer TD, Rerkasem B (2014) Responses of rice to Fe2+ in aerated and stagnant conditions: growth, root porosity and radial oxygen loss barrier. Funct Plant Biol. doi:10.1071/FP13359
42. Pedersen O, Rich SM, Colmer TD (2009) Surviving floods: leaf gas films improve O-2 and CO2 exchange, root aeration, and growth of completely submerged rice. Plant J 58:147–156. doi:10.1111/j.1365-313X.2008.03769.x
43. Polerecky L, Volkenborn N, Stief P (2006) High temporal resolution oxygen imaging in bioirrigated sediments. Environ Sci Tech 40:5763–5769
44. Precht E, Franke U, Polerecky L, Huettel M (2004) Oxygen dynamics in permeable sediments with wave-driven pore water exchange. Limnol Oceanogr 49:693–705. doi:10.2307/3597786
45. Reim A, Luke C, Krause S, Pratscher J, Frenzel P (2012) One millimetre makes the difference: high-resolution analysis of methane-oxidizing bacteria and their specific activity at the oxic-anoxic interface in a flooded paddy soil. ISME J 6: 2128–2139. doi: http://www.nature.com/ismej/journal/v6/n11/suppinfo/ismej201257s1.html
46. Revsbech NP, Pedersen O, Reichardt W, Briones A (1999) Microsensor analysis of oxygen and pH in the rice rhizosphere. Biol Fertil Soils 29:279–385
47. Roger PA, Zimmerman WJ, Lumpkin TA (1993) Microbiological management of wetland rice fields. Marcel Dekker, Inc., 270 Madison Avenue, New York, New York 10016, USA; Marcel Dekker, Inc., Basel, Switzerland
48. Rudolph N, Voss S, Moradi A, Nagl S, Oswald S (2013) Spatio-temporal mapping of local soil pH changes induced by roots of lupin and soft-rush. Plant and Soil 369:669–680. doi:10.1007/s11104-013-1775-0
49. Schreiber CM, Zeng B, Blossfeld S, Rascher U, Kazda M, Schurr U, Hoeltkemeier A, Kuhn AJ (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
50. Seyfferth AL, Webb SM, Andrews JC, Fendorf S (2010) Arsenic localization, speciation, and Co-occurrence with iron on rice (Oryza sativa L.) roots having variable Fe coatings. Environ Sci Technol 44:8108–8113. doi:10.1021/es101139z
51. Sherman DM, Waite TD (1985) Electronic-spectra of Fe-3+ oxides and oxide hydroxides in the near ir to near uv. Am Mineral 70:1262–1269
52. Shiono K, Ogawa S, Yamazaki S, Isoda H, Fujimura T, Nakazono M, Colmer TD (2011) Contrasting dynamics of radial O-2-loss barrier induction and aerenchyma formation in rice roots of two lengths. Ann Bot 107:89–99. doi:10.1093/aob/mcq221
53. Stahl H, Warnken KW, Sochaczewski L, Glud RN, Davison W, Zhang H (2012) A combined sensor for simultaneous high resolution 2-D imaging of oxygen and trace metals fluxes. Limnol Oceanogr Methods 10:389–401. doi:10.4319/lom.2012.10.389
54. Tschiersch H, Liebsch G, Stangelmayer A, Borisjuk L, Rolletschek H (2011) Planar Oxygen Sensors for Non Invasive Imaging in Experimental Biology
55. Waters I, Armstrong W, Thompson CJ, Setter TL, Adkins S, Gibbs J, Greenway H (1989) Diurnal changes in radial oxygen loss and ethanol metabolism in roots of submerged and Non-submerged rice seedlings. New Phytol 113:439–451
56. Watt M, Evans JR (1999) Linking development and determinacy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 concentration. Plant Physiol 120:705–716. doi:10.1104/pp. 120.3.705
57. Weiss JV, Emerson D, Megonigal JP (2005) Rhizosphere iron(III) deposition and reduction in a Juncus effusus L.-dominated wetland. Soil Sci Soc Am J 69:1861–1870. doi:10.2136/sssaj2005.0002
58. Wenzhofer F, Glud RN (2004) Small-scale spatial and temporal variability in coastal benthic O-2 dynamics: effects of fauna activity. Limnol Oceanogr 49:1471–1481
59. Williams PN, Santner J, Larsen M, Lehto N, Oburger E, Wenzel WW, Glud RN, Davison W, Zhang H (2014) Localised flux-maxima of arsenic, lead and iron around root apices in flooded lowland rice. Environ Sci Technol. doi:10.1021/es501127k
60. Wu C, Ye Z, Li H, Wu S, Deng D, Zhu Y, Wong M (2012) Do radial oxygen loss and external aeration affect iron plaque formation and arsenic accumulation and speciation in rice? J Exp Bot. doi:10.1093/jxb/ers017
61. Xu Z, Zheng X, Wang Y, Wang Y, Huang Y, Zhu J (2006) Effect of free-air atmospheric CO2 enrichment on dark respiration of rice plants (Oryza sativa L.). Agr Ecosyst Environ 115:105–112. doi:10.1016/j.agee.2005.12.017
62. Zhu Q, Aller RC, Fan Y (2006) Two-dimensional pH distributions and dynamics in bioturbated marine sediments. Geochim Cosmochim Acta 70:4933–4949. doi:10.1016/j.gca.2006