, Volume 238, Issue 3, pp 599–614 | Cite as

Emerging technologies for non-invasive quantification of physiological oxygen transport in plants

  • P. Chaturvedi
  • M. Taguchi
  • S. L. Burrs
  • B. A. Hauser
  • W. W. A. W. Salim
  • J. C. Claussen
  • E. S. McLamoreEmail author
Emerging Technologies


Oxygen plays a critical role in plant metabolism, stress response/signaling, and adaptation to environmental changes (Lambers and Colmer, Plant Soil 274:7–15, 2005; Pitzschke et al., Antioxid Redox Signal 8:1757–1764, 2006; Van Breusegem et al., Plant Sci 161:405–414, 2001). Reactive oxygen species (ROS), by-products of various metabolic pathways in which oxygen is a key molecule, are produced during adaptation responses to environmental stress. While much is known about plant adaptation to stress (e.g., detoxifying enzymes, antioxidant production), the link between ROS metabolism, O2 transport, and stress response mechanisms is unknown. Thus, non-invasive technologies for measuring O2 are critical for understanding the link between physiological O2 transport and ROS signaling. New non-invasive technologies allow real-time measurement of O2 at the single cell and even organelle levels. This review briefly summarizes currently available (i.e., mainstream) technologies for measuring O2 and then introduces emerging technologies for measuring O2. Advanced techniques that provide the ability to non-invasively (i.e., non-destructively) measure O2 are highlighted. In the near future, these non-invasive sensors will facilitate novel experimentation that will allow plant physiologists to ask new hypothesis-driven research questions aimed at improving our understanding of physiological O2 transport.


Oxygen Reactive oxygen species Sensor Non-invasive 



The authors also acknowledge the UF Excellence Award and the IFAS Early Career Award (CRIS No. 005062) for funding (McLamore). A special thanks to PIKL (Baltimore, MD) for help with graphic images.


  1. Abe Y, Sakairi T, Kajiyama H, Shrivastav S, Beeson C, Kopp JB (2010) Bioenergetic characterization of mouse podocytes. Am J Physiol Cell Physiol 299:C464–C476PubMedCrossRefGoogle Scholar
  2. Ahmad R, Kuppusamy P (2010) Theory, instrumentation, and applications of electron paramagnetic resonance oximetry. Chem Rev 110:3212–3236PubMedCrossRefGoogle Scholar
  3. Ahn CH, Choi JW, Beaucage G, Nevin JH, Lee JB, Puntambekar A, Lee JY (2004) Disposable smart lab on a chip for point-of-care clinical diagnostics. Proc IEEE 92:154–173CrossRefGoogle Scholar
  4. Alderman J, Hynes J, Floyd SM, Krüger J, O’Connor R, Papkovsky DB (2004) A low-volume platform for cell-respirometric screening based on quenched-luminescence oxygen sensing. Biosens Bioelectron 19:1529–1535PubMedCrossRefGoogle Scholar
  5. Alimohammadi M, Xu Y, Wang D, Biris AS, Khodakovskaya MV (2011) Physiological responses induced in tomato plants by a two-component nanostructural system composed of carbon nanotubes conjugated with quantum dots and its in vivo multimodal detection. Nanotechnology 22(29):295101PubMedCrossRefGoogle Scholar
  6. Alivisatos P (2004) The use of nanocrystals in biological detection. Nat Biotechnol 22:47–52PubMedCrossRefGoogle Scholar
  7. Anker JN, Kopelman R (2003) Magnetically modulated optical nanoprobes. Appl Phys Lett 82:1102–1104CrossRefGoogle Scholar
  8. Armstrong W, Webb T, Darwent M, Beckett PM (2009) Measuring and interpreting respiratory critical oxygen pressures in roots. Ann Bot 103:281–293PubMedCrossRefGoogle Scholar
  9. Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Ann Rev Plant Biol 59:313–339CrossRefGoogle Scholar
  10. Behrend CJ, Anker JN, McNaughton BH, Brasuel M, Philbert MA, Kopelman R (2004) Metal-capped brownian and magnetically modulated optical nanoprobes (MOONs): micromechanics in chemical and biological microenvironments. J Phys Chem B 108:10408–10414CrossRefGoogle Scholar
  11. Bewley JD (1994) Seeds: physiology of development and germination. Plenum Press, New YorkGoogle Scholar
  12. Borisjuk L, Rolletschek H (2009) The oxygen status of the developing seed. New Phytol 182:17–30PubMedCrossRefGoogle Scholar
  13. Borisjuk L, Macherel D, Benamar A, Wobus U, Rolletschek H (2007) Low oxygen sensing and balancing in plant seeds: a role for nitric oxide. New Phytol 176:813–823PubMedCrossRefGoogle Scholar
  14. Borisov SM, Klimant I (2007) Ultrabright oxygen optodes based on cyclometalated iridium(III) coumarin complexes. Anal Chem 79:7501–7509PubMedCrossRefGoogle Scholar
  15. Brand MD, Nicholls DG (2011) Assessing mitochondrial dysfunction in cells. Biochem J 435:297–312PubMedCrossRefGoogle Scholar
  16. Buck SM, Xu H, Brasuel M, Philbert MA, Kopelman R (2004) Nanoscale probes encapsulated by biologically localized embedding (PEBBLEs) for ion sensing and imaging in live cells. Talanta 63:41–59PubMedCrossRefGoogle Scholar
  17. Carraway ER, Demas JN, Degraff BA, Bacon JR (1991) Photophysics and photochemistry of oxygen sensors based on luminescent transition-metal complexes. Anal Chem 63:337–342CrossRefGoogle Scholar
  18. Chan WC, Maxwell DJ, Gao XH, Bailey RE, Han MY, Nie SM (2002) Luminescent quantum dots for multiplexed biological detection and imaging. Curr Opin Biotechnol 13:40–46PubMedCrossRefGoogle Scholar
  19. Chatni MR, Porterfield DM (2009) Self-referencing optrode technology for non-invasive real-time measurement of biophysical flux and physiological sensing. Analyst 134:2224–2232PubMedCrossRefGoogle Scholar
  20. Chatni MR, Li G, Porterfield DM (2009a) Frequency-domain fluorescence lifetime optrode system design and instrumentation without a concurrent reference light-emitting diode. Appl Opt 48:5528–5536PubMedCrossRefGoogle Scholar
  21. Chatni MR, Maier DE, Porterfield DM (2009b) Evaluation of microparticle materials for enhancing the performance of fluorescence lifetime based optrodes. Sens Actuators B Chem 141:471–477CrossRefGoogle Scholar
  22. Claussen JC, Franklin AD, ul Haque A, Porterfield DM, Fisher TS (2009) Electrochemical biosensor of nanocube-augmented carbon nanotube networks. ACS Nano 3:37–44PubMedCrossRefGoogle Scholar
  23. Claussen JC, Artiles MS, McLamore ES, Mohanty S, Shi J, Rickus JL, Fisher TS, Porterfield DM (2011) Electrochemical glutamate biosensing with nanocube and nanosphere augmented single-walled carbon nanotube networks: a comparative study. J Mater Chem 21:11224–11231CrossRefGoogle Scholar
  24. Claussen JC, Kumar A, Jaroch DB, Khawaja MH, Hibbard AB, Porterfield DM, Fisher TS (2012) Nanostructuring platinum nanoparticles on multilayered graphene petal nanosheets for electrochemical biosensing. Adv Funct Mater 22:3399–3405CrossRefGoogle Scholar
  25. Cloutier M, Chen J, Tatge F, McMurray-Beaulieu V, Perrier M, Jolicoeur M (2009) Kinetic metabolic modelling for the control of plant cells cytoplasmic phosphate. J Theor Biol 259:118–131PubMedCrossRefGoogle Scholar
  26. Collier BB, McShane MJ (2012) Dynamic windowing algorithm for the fast and accurate determination of luminescence lifetimes. Anal Chem 84(11):4725–4731PubMedCrossRefGoogle Scholar
  27. Collier BB, Singh S, McShane M (2011) Microparticle ratiometric oxygen sensors utilizing near-infrared emitting quantum dots. Analyst 136:962–967PubMedCrossRefGoogle Scholar
  28. Criddle RS, Breidenbach RW, Rank DR, Hopkin MS, Hansen LD (1990) Simultaneous calorimetric and respirometric measurements on plant tissues. Thermochim Acta 172:213–221CrossRefGoogle Scholar
  29. Cywinski PJ, Moro AJ, Stanca SE, Biskup C, Mohr GJ (2009) Ratiometric porphyrin-based layers and nanoparticles for measuring oxygen in biosamples. Sens Actuators B Chem 135:472–477CrossRefGoogle Scholar
  30. Dmitriev RI, Zhdanov AV, Ponomarev GV, Yashunski DV, Papkovsky DB (2010) Intracellular oxygen-sensitive phosphorescent probes based on cell-penetrating peptides. Anal Biochem 398:24–33PubMedCrossRefGoogle Scholar
  31. Do J, Lee S, Han JY, Kai JH, Hong CC, Gao CA, Nevin JH, Beaucage G, Ahn CH (2008) Development of functional lab-on-a-chip on polymer for point-of-care testing of metabolic parameters. Lab Chip 8:2113–2120PubMedCrossRefGoogle Scholar
  32. Dodds WK, Biggs BJF, Lowe RL (1999) Photosynthesis-irradiance patterns in benthic microalgae: variations as a function of assemblage thickness and community structure. J Phycol 35:42–53CrossRefGoogle Scholar
  33. Eggenberger K, Frey N, Zienicke B, Siebenbrock J, Schunck T, Fischer R, Bräse S, Birtalan E, Nann T, Nick P (2010) Use of nanoparticles to study and manipulate plant cells. Adv Eng Mater 12:B406–B412CrossRefGoogle Scholar
  34. Etxeberria E, Gonzalez P, Baroja-Fernandez E, Romero JP (2006) Fluid phase endocytic uptake of artificial nano-spheres and fluorescent quantum dots by sycamore cultured cells: evidence for the distribution of solutes to different intracellular compartments. Plant Signal Behav 1:196–200PubMedCrossRefGoogle Scholar
  35. Fercher A, Borisov SM, Zhdanov AV, Klimant I, Papkovsky DB (2011) Intracellular O2 sensing probe based on cell-penetrating phosphorescent nanoparticles. ACS Nano 5:5499–5508PubMedCrossRefGoogle Scholar
  36. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422(6930):442–446PubMedCrossRefGoogle Scholar
  37. Gupta KJ, Zabalza A, Van Dongen JT (2009) Regulation of respiration when the oxygen availability changes. Physiol Plant 137:383–391PubMedCrossRefGoogle Scholar
  38. Gurumurthy S, Xie SZ, Alagesan B, Kim J, Yusuf RZ, Saez B, Tzatsos A, Ozsolak F, Milos P, Ferrari F, Park PJ, Shirihai OS, Scadden DT, Bardeesy N (2010) The Lkb1 metabolic sensor maintains haematopoietic stem cell survival. Nature 468:659–663PubMedCrossRefGoogle Scholar
  39. Hannah W, Thompson PB (2008) Nanotechnology, risk and the environment: a review. J Environ Monit 10:291PubMedCrossRefGoogle Scholar
  40. Hardin P (2000) From biological clock to biological rhythms. Genome Biol 1:1–5CrossRefGoogle Scholar
  41. Hardman R (2006) A toxicologic review of quantum dots: toxicity depends on physicochemical and environmental factors. Environ Health Perspect 114(2):165–172PubMedCrossRefGoogle Scholar
  42. Holdaway-Clarke TL, Hepler PK (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 159:539–563CrossRefGoogle Scholar
  43. Hoshino A, Hanada S, Yamamoto K (2011) Toxicity of nanocrystal quantum dots: the relevance of surface modifications. Arch Toxicol 85(7):707–720PubMedCrossRefGoogle Scholar
  44. Hu C, Bai X, Wang Y, Jin W, Zhang X, Hu S (2012) Inkjet printing of nanoporous gold electrode arrays on cellulose membranes for high-sensitive paper-like electrochemical oxygen sensors using ionic liquid electrolytes. Anal Chem 84(8):3745–3750PubMedCrossRefGoogle Scholar
  45. Huh D, Hamilton GA, Ingber DE (2011) From 3D cell culture to organs-on-chips. Trends Cell Biol 21:745–754PubMedCrossRefGoogle Scholar
  46. Kader MA, Lindberg S (2010) Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal Behav 5:233–238PubMedCrossRefGoogle Scholar
  47. Kerchev PI, Fenton B, Foyer CH, Hancock RD (2012) Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant Cell Environ 35(2):441–453PubMedCrossRefGoogle Scholar
  48. Kim HK, Youn BS, Shin MS, Namkoong C, Park KH, Baik JH, Kim JB, Park J-Y, Lee KU, Kim Y-B, Kim MS (2010) Hypothalamic Angptl4/Fiaf is a novel regulator of food intake and body weight. Diabetes 59(11):2772–2780PubMedCrossRefGoogle Scholar
  49. Kochian LV, Shaff JE, Kühtreiber WM, Jaffe LF, Lucas WJ (1992) Use of an extracellular, ion-selective, vibrating microelectrode system for the quantification of K+, H+, and Ca2+ fluxes in maize roots and maize suspension cells. Planta 188:601–610CrossRefGoogle Scholar
  50. Kocincová AS, Nagl S, Arain S, Krause C, Borisov SM, Arnold M, Wolfbeis OS (2008) Multiplex bacterial growth monitoring in 24-well microplates using a dual optical sensor for dissolved oxygen and pH. Biotechnol Bioeng 100:430–438PubMedCrossRefGoogle Scholar
  51. Kratasyuk VA, Esimbekova EN, Gladyshev MI, Khromichek EB, Kuznetsov AM, Ivanova EA (2001) The use of bioluminescent biotests for study of natural and laboratory aquatic ecosystems. Chemosphere 42:909–915PubMedCrossRefGoogle Scholar
  52. Krihak MK, Shahriari MR (1996) Highly sensitive, all solid state fibre optic oxygen sensor based on the sol-gel coating technique. Electron Lett 32:240–242CrossRefGoogle Scholar
  53. Kuhl M, Jorgensen BB (1992) Spectral light measurements in microbenthic phototrophic communities with a fiber-optic microprobe coupled to a sensitive diode array detector. Limnol Oceanogr 37:1813–1823CrossRefGoogle Scholar
  54. Kuhl M, Polerecky L (2008) Functional and structural imaging of phototrophic microbial communities and symbioses. Aquat Microb Ecol 53:99–118CrossRefGoogle Scholar
  55. Küpper H, Šetlík I, Hlásek M (2004) A versatile chamber for simultaneous measurements of oxygen exchange and fluorescence in filamentous and thallous algae as well as higher plants. Photosynthetica 42:579–583CrossRefGoogle Scholar
  56. Lambers H, Colmer T (2005) Root physiology—from gene to function. Plant Soil 274:7–15CrossRefGoogle Scholar
  57. Lamboursain L, St-Onge F, Jolicoeur M (2002) A lab-built respirometer for plant and animal cell culture. Biotechnol Prog 18:1377–1386PubMedCrossRefGoogle Scholar
  58. Land SC, Porterfield DM, Sanger RH, Smith PJS (1999) The self-referencing oxygen-selective microelectrode: detection of transmembrane oxygen flux from single cells. J Exp Biol 202:211–218PubMedGoogle Scholar
  59. Lee S-K, Okura I (1997) Photostable optical oxygen sensing material: platinum tetrakis (pentafluorophenyl)porphyrin immobilized in polystyrene. Anal Commun 34:185–188CrossRefGoogle Scholar
  60. Lee S, They BL, Cote GL, Pishko MV (2008) Measurement of pH and dissolved oxygen within cell culture media using a hydrogel microarray sensor. Sens Actuators B Chem 128:388–398CrossRefGoogle Scholar
  61. Ligeza A, Wisniewska A, Subczynski WK, Tikhonov AN (1994) Oxygen production and consumption by chloroplasts in situ and in vitro as studied with microscopic spin label probes. Biochim Biophys Acta 1186:201–208PubMedCrossRefGoogle Scholar
  62. Lin S, Bhattacharya P, Rajapakse NC, Brune DE, Ke PC (2009) Effects of quantum dots adsorption on algal photosynthesis. J Phys Chem C 113:10962–10966CrossRefGoogle Scholar
  63. Liszkay A, Kenk B, Schopfer P (2003) Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth. Planta 217:658–667PubMedCrossRefGoogle Scholar
  64. Liu Q, Chen B, Wang Q, Shi X, Xiao Z, Lin J, Fang X (2009) Carbon nanotubes as molecular transporters for walled plant cells. Nano Lett 9:1007PubMedCrossRefGoogle Scholar
  65. Malins C, Niggemann M, MacCraith BD (2000) Multi-analyte optical chemical sensor employing a plastic substrate. Meas Sci Technol 11:1105–1110CrossRefGoogle Scholar
  66. Mancuso S, Boselli M (2002) Characterisation of the oxygen fluxes in the division, elongation and mature zones of Vitis roots: influence of oxygen availability. Planta 214:767–774PubMedCrossRefGoogle Scholar
  67. Mancuso S, Papeschi G, Marras AM (2000) A polarographic, oxygen-selective, vibrating-microelectrode system for the spatial and temporal characterisation of transmembrane oxygen fluxes in plants. Planta 211:384–389PubMedCrossRefGoogle Scholar
  68. Martin-Ortigosa S, Valenstein JS, Lin VSY, Trewyn BG, Wang K (2012) Nanotechnology meets plant sciences: gold functionalized mesoporous silica nanoparticle mediated protein and DNA codelivery to plant cells via the biolistic method. Adv Funct Mater 22:3529CrossRefGoogle Scholar
  69. Masi E, Ciszak M, Stefano G, Renna L, Azzarello E, Pandolfi C, Mugnai S, Baluška F, Arecchi FT, Mancuso S (2009) Spatiotemporal dynamics of the electrical network activity in the root apex. Proc Natl Acad Sci 106:4048–4053PubMedCrossRefGoogle Scholar
  70. Matsui T, Tsuchiya T (2006) A method to estimate practical radial oxygen loss of wetland plant roots. Plant Soil 279:119–128CrossRefGoogle Scholar
  71. McEvoy AK, Von Bültzingslöwen C, McDonagh C, MacCraith BD, Klimant I, Wolfbeis OS (2003) Optical sensors for application in intelligent food packaging technology. Proc SPIE (The Society of Optical Engineering) 4876:806–815Google Scholar
  72. McLamore ES, Porterfield DM (2011) Non-invasive tools for measuring metabolism and biophysical analyte transport: self-referencing physiological sensing. Chem Soc Rev 40:5308–5320PubMedCrossRefGoogle Scholar
  73. McLamore ES, Jaroch D, Chatni MR, Porterfield DM (2010a) Self-referencing optrodes for measuring spatially resolved, real-time metabolic oxygen flux in plant systems. Planta 232:1087–1099PubMedCrossRefGoogle Scholar
  74. McLamore ES, Diggs A, Calvo Marzal P, Shi J, Blakeslee JJ, Peer WA, Murphy AS, Porterfield DM (2010b) Non-invasive quantification of endogenous root auxin transport using an integrated flux microsensor technique. Plant J 63:1004–1016PubMedCrossRefGoogle Scholar
  75. McLamore ES, Zhang W, Porterfield DM, Banks MK (2010c) Membrane-aerated biofilm proton and oxygen flux during chemical toxin exposure. Environ Sci Technol 44:7050–7057PubMedCrossRefGoogle Scholar
  76. Mojovic M, Spasojevic I, Vuletic M, Vucinic Z, Bacic G (2005) An EPR spin-probe and spin-trap study of the free radicals produced by plant plasma membranes. J Serb Chem Soc 70(2):177–186CrossRefGoogle Scholar
  77. Molter TW, McQuaide SC, Suchorolski MT, Strovas TJ, Burgess LW, Meldrum DR, Lidstrom ME (2009) A microwell array device capable of measuring single-cell oxygen consumption rates. Sens Actuators B Chem 135:678–686PubMedCrossRefGoogle Scholar
  78. Navarro E, Baun A, Behra R, Hartmann N, Filser J, Miao A-J, Quigg A, Santschi P, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17:372–386PubMedCrossRefGoogle Scholar
  79. Newman IA (2001) Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. Plant Cell Environ 24:1–14PubMedCrossRefGoogle Scholar
  80. Newman I, Chen SL, Porterfield DM, Sun J (2012) Non-invasive flux measurements using microsensors: theory, limitations, and systems. Methods Mol Biol 913:101–117PubMedGoogle Scholar
  81. O’Riordan TC, Buckley D, Ogurtsov V, O’Connor R, Papkovsky DB (2000) A cell viability assay based on monitoring respiration by optical oxygen sensing. Anal Biochem 278:221–227PubMedCrossRefGoogle Scholar
  82. O’Riordan TC, Zhdanov AV, Ponomarev GV, Papkovsky DB (2007) Analysis of intracellular oxygen and metabolic responses of mammalian cells by time-resolved fluorometry. Anal Chem 79:9414–9419PubMedCrossRefGoogle Scholar
  83. Ober ES, Sharp RE (1996) A microsensor for direct measurement of O2 partial pressure within plant tissues. J Exp Bot 47:447–454CrossRefGoogle Scholar
  84. Oppegard SC, Nam KH, Carr JR, Skaalure SC, Eddington DT (2009) Modulating temporal and spatial oxygenation over adherent cellular cultures. PLoS One 4(9):e6891. doi: 10.1371/journal.pone.0006891 PubMedCrossRefGoogle Scholar
  85. O’Riordan TC, Soini AE, Papkovsky DB (2002) Performance evaluation of the phosphorescent porphyrin label: solid-phase immunoassay of α-fetoprotein. Anal Chem 74:5845–5850PubMedCrossRefGoogle Scholar
  86. Paterson DM, Aspden RJ, Visscher PT, Consalvey M, Andres MS, Decho AW, Stolz J, Reid RP (2008) Light-dependant biostabilisation of sediments by stromatolite assemblages. PLoS One 3(9):e3176. doi: 10.1371/journal.pone.0003176 PubMedCrossRefGoogle Scholar
  87. Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Signal 8:1757–1764PubMedCrossRefGoogle Scholar
  88. Porterfield DM (2002) The biophysical limitations in physiological transport and exchange in plants grown in microgravity. J Plant Growth Regul 21:177–190PubMedCrossRefGoogle Scholar
  89. Porterfield DM (2007) Measuring metabolism and biophysical flux in the tissue, cellular and sub-cellular domains: recent developments in self-referencing amperometry for physiological sensing. Biosens Bioelectron 22:1186–1196PubMedCrossRefGoogle Scholar
  90. Porterfield DM, Smith PJ (2000) Single-cell, real-time measurements of extracellular oxygen and proton fluxes from Spirogyra grevilleana. Protoplasma 212:80–88CrossRefGoogle Scholar
  91. Porterfield DM, Kuang AX, Smith PJS, Crispi ML, Musgrave ME (1999) Oxygen-depleted zones inside reproductive structures of Brassicaceae: implications for oxygen control of seed development. Can J Bot 77:1439–1446PubMedCrossRefGoogle Scholar
  92. Presley T, Kuppusamy P, Zweier JL, Ilangovan G (2006) Electron paramagnetic resonance oximetry as a quantitative method to measure cellular respiration: a consideration of oxygen diffusion interference. Biophys J 91(12):4623–4631PubMedCrossRefGoogle Scholar
  93. Queval G, Noctor G (2007) A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development. Anal Biochem 363:58–69PubMedCrossRefGoogle Scholar
  94. Revsbech NP, Jorgensen BB (1986) Microelectrodes—their use in microbial ecology. Adv Microb Ecol 9:293–352CrossRefGoogle Scholar
  95. Rijnders JGHM, Armstrong W, Darwent MJ, Blom CWPM, Voesenek LACJ (2000) The role of oxygen in submergence-induced petiole elongation in Rumex palustris: in situ measurements of oxygen in petioles of intact plants using micro-electrodes. New Phytol 147:497–504CrossRefGoogle Scholar
  96. Rolletschek H, Stangelmayer A, Borisjuk L (2009) Methodology and significance of microsensor-based oxygen mapping in plant seeds—an overview. Sensors 9:3218–3227PubMedCrossRefGoogle Scholar
  97. Sanchez BC, Ochoa-Acuna H, Porterfield DM, Sepulveda MS (2008) Oxygen flux as an indicator of physiological stress in fathead minnow (Pimephales promelas) embryos: a real-time biomonitoring system of water quality. Environ Sci Technol 42:7010–7017PubMedCrossRefGoogle Scholar
  98. Schmälzlin E, van Dongen JT, Klimant I, Marmodée B, Steup M, Fisahn J, Geigenberger P, Löhmannsröben H-G (2005) An optical multifrequency phase-modulation method using microbeads for measuring intracellular oxygen concentrations in plants. Biophys J 89:1339–1345PubMedCrossRefGoogle Scholar
  99. Serrano M, Robatzek S, Torres M, Kombrink E, Somssich IE, Robinson M, Schulze-Lefert P (2007) Chemical interference of pathogen-associated molecular pattern-triggered immune responses in Arabidopsis reveals a potential role for fatty-acid synthase type ii complex-derived lipid signals. J Biol Chem 282:6803–6811PubMedCrossRefGoogle Scholar
  100. Shabala L, Ross T, McMeekin T, Shabala S (2006a) Non-invasive microelectrode ion flux measurements to study adaptive responses of microorganisms to the environment. FEMS Microbiol Rev 30:472–486PubMedCrossRefGoogle Scholar
  101. Shabala S, Shabala L, Gradmann D, Chen Z, Newman I, Mancuso S (2006b) Oscillations in plant membrane transport: model predictions, experimental validation, and physiological implications. J Exp Bot 57:171–184PubMedCrossRefGoogle Scholar
  102. Shabala S, Shabala L, Newman I (2012) Studying membrane transport processes by non-invasive microelectrodes basic principles and methods. In: Volkov AG (ed) Plant electrophysiology: methods and cell electrophysiology. Springer-Verlag, Berlin, Heidelberg, New York, pp 167–186CrossRefGoogle Scholar
  103. Shi K, Hu WH, Dong DK, Zhou YH, Yu JQ (2007) Low O2 supply is involved in the poor growth in root-restricted plants of tomato (Lycopersicon esculentum Mill.). Environ Exp Bot 61:181–189CrossRefGoogle Scholar
  104. Shimamura S, Yamamoto R, Nakamura T, Shimada S, Komatsu S (2010) Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil. Ann Bot 106:277–284PubMedCrossRefGoogle Scholar
  105. Steffens B, Steffen-Heins A, Sauter M (2013) Reactive oxygen species mediate growth and death in submerged plants. Front Plant Sci 4:179. doi: 10.3389/fpls.2013.00179 PubMedCrossRefGoogle Scholar
  106. Sud D, Zhong W, Mycek M (2005) Measurement of intracellular oxygen levels using fluorescence lifetime imaging microscopy (FLIM). In: Licha K, Cubeddu R (eds) Photon migration and diffuse-light imaging II, vol 5859. Proc SPIEGoogle Scholar
  107. Tschiersch H, Liebsch G, Stangelmayer A, Borisjuk L, Rolletschek H (2011) Planar oxygen sensors for non invasive imaging in experimental biology, microsensors. In: Minin I (ed). InTech. doi: 10.5772/17893, ISBN: 978-953-307-170-1
  108. Tschiersch H, Liebsch G, Borisjuk L, Stangelmayer A, Rolletschek H (2012) An imaging method for oxygen distribution, respiration and photosynthesis at a microscopic level of resolution. New Phytol 196:926–936PubMedCrossRefGoogle Scholar
  109. Tsoi KM, Dai Q, Alman BA, Chan WC (2013) Are quantum dots toxic? Exploring the discrepancy between cell culture and animal studies. Acc Chem Res 46(3):662–671CrossRefGoogle Scholar
  110. Tyystjärvi E, Karunen J, Lemmetyinen H (1998) Measurement of photosynthetic oxygen evolution with a new type of oxygen sensor. Photosynth Res 56:223–227CrossRefGoogle Scholar
  111. ul Haque A, Chatni MR, Li G, Porterfield DM (2007) Biochips and other microtechnologies for physiomics. Expert Rev Proteomics 4:553–563PubMedCrossRefGoogle Scholar
  112. Van Breusegem F, Vranova E, Dat JF, Inze D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414CrossRefGoogle Scholar
  113. van Dongen JT, Schurr U, Pfister M, Geigenberger P (2003) Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol 131:1529–1543PubMedCrossRefGoogle Scholar
  114. Verslues PE, Ober ES, Sharp RE (1998) Root growth and oxygen relations at low water potentials. Impact of oxygen availability in polyethylene glycol solutions. Plant Physiol 116:1403–1412PubMedCrossRefGoogle Scholar
  115. Vigeolas H, van Dongen JT, Waldeck P, Huhn D, Geigenberger P (2003) Lipid storage metabolism is limited by the prevailing low oxygen concentrations oilseed rape. Plant Physiol 133:2048–2060PubMedCrossRefGoogle Scholar
  116. Visscher PT, Stolz JF (2005) Microbial mats as bioreactors: populations, processes, and products. Palaeogeogr Palaeoclimatol Palaeoecol 219:87–100CrossRefGoogle Scholar
  117. Visscher PT, Beukema J, van Gemerden H (1991) In situ characterization of sediments: measurements of oxygen and sulfide profiles with a novel combined needle electrode. Limnol Oceanogr 36:1476–1480CrossRefGoogle Scholar
  118. Wan Y, McLamore ES, Fan L, Hao H, Porterfield DM, Zhang Z, Wang W, Xu Y Lin J (2011) Non-invasive measurement of real-time oxygen flux in plant systems with a self-referencing optrode. Protocol Exc. doi: 10.1038/protex.2011.266 Google Scholar
  119. Wang L, Acosta MA, Leach J, Carrier R (2013) Spatially monitoring oxygen level in 3D microfabricated cell culture systems using optical oxygen sensing beads. Lab Chip 13:1586–1592PubMedCrossRefGoogle Scholar
  120. Wolfbeis OS (2004) Fiber-optic chemical sensors and biosensors. Anal Chem 76:3269–3284PubMedCrossRefGoogle Scholar
  121. Xu H, Buck SM, Kopelman R, Philbert MA, Brasuel M, Monson E, Behrend C, Ross B, Rehemtulla A, Koo Y-EL (2005) Fluorescent PEBBLE nanosensors and nanoexplorers for real-time intracellular and biomedical applications. In: Geddes CD, Lakowicz JR (eds) Topics in Fluorescence Spectroscopy, Vol. 10, Academic/Plenum Press, pp 69–126Google Scholar
  122. Xu Y, Sun T, Yin L-P (2006) Application of non-invasive microsensing system to simultaneously measure both H+ and O2 fluxes around the pollen tube. J Integr Plant Biol 48:823–831CrossRefGoogle Scholar
  123. Yi X, Hargett SR, Liu H, Frankel LK, Bricker TM (2007) The PsbP protein is required for photosystem II complex assembly/stability and photoautotrophy in arabidopsis thaliana. J Biol Chem 282:24833–24841PubMedCrossRefGoogle Scholar
  124. Zhu H, Han J, Xiao JQ, Jin Y (2008) Uptake, translocation, and accumulation of manufactured iron oxide nanoparticles by pumpkin plants. J Environ Monit 10:170–173CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • P. Chaturvedi
    • 1
  • M. Taguchi
    • 1
  • S. L. Burrs
    • 1
  • B. A. Hauser
    • 2
  • W. W. A. W. Salim
    • 3
    • 4
  • J. C. Claussen
    • 5
    • 6
  • E. S. McLamore
    • 1
    Email author
  1. 1.Agricultural and Biological Engineering DepartmentUniversity of FloridaGainesvilleUSA
  2. 2.Department of BiologyUniversity of FloridaGainesvilleUSA
  3. 3.Department of Agricultural and Biological EngineeringPurdue UniversityWest LafayetteUSA
  4. 4.Birck Nanotechnology Center/Bindley Bioscience Center Physiological Sensing FacilityPurdue UniversityWest LafayetteUSA
  5. 5.U.S. Naval Research Laboratory, Center for Bio/Molecular Science and EngineeringWashington, DCUSA
  6. 6.College of ScienceGeorge Mason UniversityFairfaxUSA

Personalised recommendations