Export file:

Format

  • RIS(for EndNote,Reference Manager,ProCite)
  • BibTex
  • Text

Content

  • Citation Only
  • Citation and Abstract

Physics and the molecular revolution in plant biology: union needed for managing the future

Department of Biology, Technical University of Darmstadt, Schnittspahnstr. 3-5, 64287 Darmstadt, Germany

Special Issues: BIOPHYSICS OF ION TRANSPORT IN PLANTS

The question was asked if there is still a prominent role of biophysics in plant biology in an age when molecular biology appears to be dominating. Mathematical formation of theory is essential in systems biology, and mathematics is more inherent in biophysics than in molecular biology. A survey is made identifying and briefly characterizing fields of plant biology where approaches of biophysics remain essential. In transport at membranes electrophysiology and thermodynamics are biophysical topics. Water is a special molecule. Its transport follows the physical laws of osmosis and gradients of water potential on the background of physics of hydraulic architecture. Photobiology needs understanding of the physics of electro-magnetic radiation of quantitative nature in photosynthesis and of qualitative nature in perception by the photo-sensors cryptochromes, phototropins and phytochrome in environmental responses and development. Biophysical oscillators can play a role in biological timing by the circadian clock. Integration in the self-organization of modules, such as roots, stems and leaves, for the emergence of whole plants as unitary organisms needs storage and transport of information where physical modes of signaling are essential with cross talks between electrical and hydraulic signals and with chemical signals. Examples are gravitropism and root-shoot interactions in water relations. All of these facets of plant biophysics overlie plant molecular biology and exchange with it. It is advocated that a union of approaches of plant molecular biology and biophysics needs to be cultivated. In many cases it is already operative. In bionics biophysics is producing output for practical applications linking biology with technology. Biomimetic engineering intrinsically uses physical approaches. An extreme biophysical perspective is looking out for life in space. Sustained and increased practice of biophysics with teaching and research deserves strong encouragement
  Figure/Table
  Supplementary
  Article Metrics

Keywords bionics; clock; development; electro-physiology; photobiology; photosynthesis; self-organization; signaling; water relations

Citation: Ulrich Lüttge. Physics and the molecular revolution in plant biology: union needed for managing the future. AIMS Biophysics, 2016, 3(4): 501-521. doi: 10.3934/biophy.2016.4.501

References

  • 1. Abbaspour N, Kaiser B, Tyerman S (2013) Chloride transport and compartmentation within main and lateral roots of two grapevine rootstocks differing in salt tolerance. Trees 27: 1317–1325.    
  • 2. Aloni R, Langhans M, Aloni E, et al. (2004) Role of cytokinin in the regulation of root gravitropism. Planta 220: 177–182.    
  • 3. Barthlott W, Neinhuis C (1997) Purity of the sacred lotus for escape from contamination in biological surfaces. Planta 202: 1–8.
  • 4. Barthlott W, Mail M, Neinhuis C (2016) Superhydrophobic hierarchically structured surfaces in biology: evolution, structural principles and biomimetic applications. Philos T Roy Soc A. DOI: 10.1098/rsta.2016.0191.
  • 5. Barthlott W, Schimmel T, Wiersch S, et al. (2010) The Salvinia paradox: Superhydrophobic surfaces with hydrophilic pins for air-retention under water. Adv Eng Mater 22: 1–4.    
  • 6. Behrens HM, Gradmann D, Sievers A (1985) Membrane potential responses following gravistimulation in roots of Lepidium sativum L. Planta 163: 463–472.    
  • 7. Bilger W, Schreiber U, Bock M (1995) Determination of the quantum efficiency of photosystem II and the non-photochemical quenching of chlorophyll fluorescence in the field. Oecologia 102: 425–432.
  • 8. Blüchel KG, Malik F (2006) Faszination Bionik: Die Intelligenz der Schöpfung. Mcb Verlag, St. Gallen
  • 9. Böhm J, Scherzer S, Krol E, et al. (2016) The Venus flytrap Dionea muscipula counts prey-induced action potentials to induce sodium uptake. Curr Biol 26: 286–295.
  • 10. Borland AM, Hartwell J, Jenkins GI, et al. (1999) Metabolite control overrides circadian regulation in phosphoenolpyruvate carboxylase kinase and CO2 fixation in Crassulacean acid metabolism. Plant Physiol 121: 889–896.    
  • 11. Boyden ES, Zhang F, Bamberg E, et al. (2005) Millisecond-timescale, genetically targeted optical control of neuronal activity. Nat Neurosci 8: 1263–1268.
  • 12. Brauner L, Bünning E (1930) Geoelektrischer Effekt und Elektrotropismus. Berichte der Deutschen Botanischen Gesellschaft 48: 470–476.
  • 13. Brickwede F, Erb R, Lefèvre J, et al. (2007) Bionik und Nachhaltigkeit-Lernen von der Natur. Erich Schmidt Verlag, Eds., Berlin.
  • 14. Britto DT, Ruth TJ, Lapis S, et al. (2004) Cellular and whole-plant chloride dynamics in barley: insights into chloride-nitrogen interactions and salinity responses. Planta 218: 615–622.
  • 15. Bucci SJ, Scholz FG, Goldstein G, et al. (2003) Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels. Plant Cell Environ 26: 1633–1645.    
  • 16. Burdon-Sanderson J (1872) Note on the electrical phenomena which accompany stimulation of the leaf of Dionaea muscipula Ellis. Philos Proc Roy Soc 21: 495–496.    
  • 17. Carter PJ, Nimmo HG, Fewson CA, et al. (1991) Circadian rhythms in the activity of a plant protein kinase. Embo J 10: 2063–2068.
  • 18. Cermak J, Matyssek R, Kucera J (1993) Rapid response of large, drought –stressed beech trees to irrigation. Tree Physiol 12: 281–290.    
  • 19. Chen ZH, Hills A, Bätz U, et al. (2012) Systems dynamic modeling of the stomatal guard cell predicts emergent behaviors in transport, signaling, and volume control. Plant Physiol 159: 1235–1251.    
  • 20. Comstock JP (2002) Hydraulic and chemical signaling in the control of stomatal conductance and transpiration. J Exp Bot 53: 195–200.    
  • 21. Domec JC, Scholz FG, Bucci SJ, et al. (2006) Diurnal and seasonal variation in root xylem embolism in neotropical savanna woody species: impact on stomatal control of plant water status. Plant Cell Environ 29: 26–35.    
  • 22. Etherton B, Higinbotham N (1960) Transmembrane potential measurements of cells of higher plants as related to salt uptake. Science 131: 409–410.    
  • 23. Farré EM (2012) The regulation of plant growth by the circadian clock. Plant Biology 14: 401–410.    
  • 24. Friso G, Giacomelli L, Ytterberg AJ, et al. (2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell 16: 478–499.
  • 25. Genty B, Briantais JM, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA 990: 87–92.
  • 26. Grams TEE, Koziolek C, Lautner S, et al. (2007) Distinct roles of electric and hydraulic signals on the reaction of leaf gas exchange upon re-irrigation in Zea mays L. Plant Cell Environ 30, 79–84.
  • 27. Grams TEE, Lautner S, Felle HH, et al. (2009) Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf. Plant Cell Environ 32: 319–326.    
  • 28. Harmer SL, Kay SA (2005) Positive and negative factors confer phase-specific circadian regulation of transcription in Arabidopsis. Plant Cell 17: 1926–1940.    
  • 29. Hartwell J, Smith LH, Wilkins MB, et al. (1996) Higher plant phosphoenolpyruvate carboxylase kinase is regulated by the level of translatable mRNA in response to light or a circadian rhythm. Plant J 10: 101–108.
  • 30. Hedrich R (2012) Ion channels in plants. Physiol Rev 92: 1777–1811.    
  • 31. Hedrich R, Schroeder JI, Fernandez JM (1987) Patch-clamp studies on higher plant cells: a perspective. Trends Biochem Sci 12: 49–52.    
  • 32. Hedrich R, Barbier-Brygoo H, Felle H, et al. (1988) General mechanisms for solute transport across the tonoplast of plant vacuoles: a patch-clamp survey of ion channels and proton pumps. Bot Acta 101: 7–13.    
  • 33. Hegemann P (1997) Vision in microalgae. Planta 203: 265–274.    
  • 34. Hüsken D, Steudle E, Zimmermann U (1978) Pressure probe technique for measuring water relations of cells of higher plants. Plant Physiol 61: 158–163.    
  • 35. Hütt M-Th (2013) A network view on patterns of gene expression and metabolic activity. Nova Acta Leopoldina NF 114/391: 183–199.
  • 36. Hütt M-Th, Lüttge U (2002) Nonlinear dynamics as a tool for data analysis and modelling in plant physiology. Plant Biology 4: 281–297.    
  • 37. Hütt M-Th, Lüttge U (2004) Network dynamics in plant biology: Current progress in historical perspective. Prog Bot 66: 277–310.
  • 38. Kikis EA, Khanna R, Quail PH (2005) ELF4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY. Plant J 44: 300–313.    
  • 39. Koo J, Kim Y, Kim J, et al.(2007). A GUS/luciferase fusion reporter for plant gene trapping and for assay of promoter activity with luciferin-dependent control of the reporter protein stability. Plant Cell Physiol 48: 1121–1131.
  • 40. Koten O van, Snel JFH ( 1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25: 147–150.
  • 41. Kronzucker HJ, Siddiqi MY, Glass ADM, et al. (1999) Nitrate-ammonium synergism in rice. A subcellular flux analysis. Plant Physiol 119: 1041–1045.
  • 42. Laughlin RB (2005) A Different Universe—Reinventing Physics from the Bottom Down. Basic Books, New York.
  • 43. Lösch R (1998) Plant water relations. Prog Bot 60: 193–233.
  • 44. Lundegardh H (1950) The translocation of salts and water through wheat roots. Plant Physiol 2: 103–151.
  • 45. Lundegårdh H (1955) Mechanisms of absorption, transport, accumulation, and secretion of ions. Annu Rev Physiol 6: 1–24.
  • 46. Lundegårdh H, Burström H (1933) Untersuchungen über die Salzaufnahme der Pflanzen. III. Quantitative Beziehungen zwischen Atmung und Anionenaufnahme. Biochemische Z 261: 235–251.
  • 47. Lundeghårdh H, Burström H (1935) Untersuchungen über die Atmungsvorgänge in Pflanzenwurzeln. Biochemische Z 277: 223–249.
  • 48. Lüttge U (1986) Nocturnal water storage in plants having crassulacean acid metabolism. Planta 168: 287–289.
  • 49. Lüttge U (2000) The tonoplast functioning as the master switch for circadian regulation of crassulacean acid metabolism. Planta 211: 761–769.    
  • 50. Lüttge U (2003) Circadian rhythmicity: Is the “biological clock” hardware or software. Prog Bot 64: 277–319.
  • 51. Lüttge U (2012) Whole-plant physiology: Synergistic emergence rather than modularity. Prog Bot 74: 165–190.
  • 52. Lüttge U (2013) Modularity and emergence: biology’s challenge in understanding life. Plant Biology 14: 865–871.
  • 53. Lüttge U (2016) Transport processes—The key integrators in plant biology. Prog Bot 77: 3–65.    
  • 54. Lüttge U, Hütt MT (2009) Talking Patterns: Communication of organisms at different levels of organization—an alternative view of systems biology. Nova Acta Leopoldina NF 96/357: 161–174.
  • 55. Lüttge U, Kluge M, Ball E (1975) Effects of osmotic gradients on vacuolar malic acid storage. A basic principle in oscillatory behavior of crassulacean acid metabolism. Plant Physiol 56: 613–616.
  • 56. Lüttge U, Kluge M, Thiel G (2010) Botanik. Die umfassende Biologie der Pflanzen. Wiley-VCH.
  • 57. MacRobbie EAC (1965) The nature of the coupling between light energy and active ion transport in Nitella translucens. BBA 94: 64–73.
  • 58. Mattheck C (2006) Verborgene Gestaltgesetze in der Natur. Forschungszentrum Karlsruhe.
  • 59. Matyssek R, Maruyama S, Boyer JS (1991) Growth-induced water potentials may mobilize internal water for growth. Plant Cell Environ 14: 917–923.    
  • 60. Maurel C (1997) Aquaporins and water permeability of plant membranes. Annu Rev Plant Physiol Plant Mol Biol 48: 399–429.    
  • 61. Maurel C, Santoni V, Luu DT, et al. (2009) The cellular dynamics of plant aquaporin expression and functions. Curr Opin Plant Biol 12: 690–698.    
  • 62. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51: 659–668
  • 63. Mayr S, Améglio T (2016) Freezing stress in tree xylem. Prog Bot 77: 381–414.    
  • 64. McClung CR (2006) Plant circadian rhythms. Plant Cell 18: 792–803.    
  • 65. Melcher PJ, Meinzer FC, Yount DE, et al. (1998) Comparative measurements of xylem pressure in transpiring and non-transpiring leaves by means of the pressure chamber and the xylem pressure probe. J Exp Bot 49: 1757–1760.
  • 66. Moran N, Ehrenstein G, Iwasa K, et al. (1984) Ion channels in plasmalemma of wheat protoplasts. Science 226: 835–838.
  • 67. Nachtigall W (2010): Bionik als Wissenschaft: Erkennen―Abstrahieren―Umsetzen. Springer Verlag, Heidelberg.
  • 68. Nachtigall W, Blüchel KG (2000) Das große Buch der Bionik. Deutsche Verlagsanstalt, Stuttgart.
  • 69. Nagel G, Ollig D, Fuhrmann M, et al. (2002) Channelrhodopsin-1: A light-gated proton channel in green algae. Science 296: 2395–2398.
  • 70. Nakamichi N (2011) Molecular mechanisms underlying the Arabidopsis circadian clock. Plant Cell Physiol 52: 1709–1718.    
  • 71. Neher E, Sakmann B (1976) Single channel currents recorded from membrane of denervated frog muscle fibers. Nature 260: 799–802.
  • 72. Neher E, Sakmann B, Steinbach JH (1978) The extracellular patch clamp: A method for resolving currents through individual open channels in biological membranes. Pflüg Arch 375: 219–228.    
  • 73. Newman IA (2001) Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. Plant Cell Environ 24: 1–14.    
  • 74. Nimmo HG (2000) The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends Plant Sci 5: 75–80.
  • 75. Nobel PS (2009) Physicochemical and environmental plant physiology, 4Eds. Amsterdam: Academic Press.
  • 76. Nobel PS, Jordan PW (1983) Transpiration stream of desert species: resistances and capacitances for a C3, a C4 and a CAM plant. J Exp Bot 34: 1379–1391.
  • 77. O’Regan B, Grätzel M (1991) A low-cost, high-efficiency solar cell based on dye-sensitized colloidal TiO2 films. Nature 353: 737–740.    
  • 78. Pitman MG (1963) The determination of the salt relations of the cytoplasmic phase in cells of beetroot tissue. Aust J of Biol Sci 1: 647–668.
  • 79. Raven JA (1967) Light stimulation of active transport in Hydrodictyon africanum. J Gen Physiol 50: 1627–1640.    
  • 80. Raven JA (1976) Transport in algal cells. Encyclopedia Plant Physiology New Series 2A, Springer Berlin Heidelberg, 129–188.
  • 81. Sakmann B, Neher E (1984) Patch clamp techniques for studying ionic channels in excitable membranes. Annu Rev Physiol 46: 455–472.    
  • 82. Scholander P, Bradstreet E, Hemmingsen E, et al (1965) Sap pressure in vascular plants: Negative hydrostatic pressure can be measured in plants. Science 148: 339–346.    
  • 83. Schopfer P, Brennicke A (2010) Pflanzenphysiologie. 7Eds. Spektrum, Heidelberg.
  • 84. Schreiber U, Bilger W (1993) Progress in chlorophyll fluorescence research: major developments during the past years in retrospect. Prog Bot 54: 151–173.
  • 85. Schroeder JI, Hedrich R, Fernandez JM (1984) Potassium-selective single channels in guard cell protoplasts of Vicia faba. Nature 312: 361–362.    
  • 86. Shabala S, Pang J, Zhou M, et al. (2009) Electrical signalling and cytokinins mediate effects of light and root cutting on ion uptake in intact plants. Plant Cell Environ 32: 194–207.    
  • 87. Shabala S, White RC, Djordjevic MA, et al. (2016) Root-to-shoot signalling: integration of diverse molecules, pathways and functions. Funct Plant Biol 43: 87–104.    
  • 88. Siefritz F, Otto B, Bienert G, et al. (2004), The plasma membrane aquaporin NtAQP1 is a key component of the leaf unfolding mechanism in tobacco. Plant J 37: 147–155.
  • 89. Speck T, Speck O, Neinhuis C, et al. (2011) Was die Technik von Pflanzen lernen kann–Bionik in botanischen Gärten. Verband Botanischer Gärten, Freiburg, Dresden und Bayreuth.
  • 90. Speck T, Neinhuis C (2004) Bionik, Biomimetik–Ein interdisziplinäres Forschungsgebiet mit Zukunftspotential. Naturwissdenschaftliche Rundsch 57: 177–191.
  • 91. Stancović B, Zawadzki T, Davies E (1997) Characterization of the variation potential in sunflower. Plant Physiol 115: 1083–1088.    
  • 92. Stancović B, Witters DL, Zawadzki T, et al. (1998) Action potentials and variation potentials in sunflower: an analysis of their relation-ships and distinguishing characteristics. Physiol Plantarum 103: 51–58.    
  • 93. Stenz HG, Weisenseel MH (1991) DC-electric field affects the growth direction and statocyte polarity of root tips (Lepidium sativum). J Plant Physiol 138: 335–344.    
  • 94. Stenz HG, Weisenseel MH (1993) Electrotropism of maize (Zea mays L.) roots. Facts and artifacts. Plant Physiol 101: 1107–1111.
  • 95. Steudle E (2011) Hydraulic architecture of vascular plants. In: Lüttge U, Beck E, Bartels D, Plant desiccation tolerance, Springer-Heidelberg, 185–207.
  • 96. Steudle E, Smith JAC, Lüttge U (1980) Water relation parameters of individual mesophyll cells of the Crassulacean Acid Metabolism plant Kalanchoë daigremontiana. Plant Physiol 66: 1155–1163.    
  • 97. Tang AC, Boyer JS (2003) Root pressurization affects growth-induced water potentials and growth in dehydrated maize plants. J Exp Bot 54: 2479–2488.    
  • 98. Tyree MT (1997) The cohesion-tension theory of sap ascent: current controversies. J Exp Bot 48: 1753–1765.
  • 99. Tyree MT, Hammel HT (1972) The measurement of the turgor pressure and the water relations of plants by the pressure –bomb technique. J Exp Bot 23: 267–282.    
  • 100. Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, Berlin.
  • 101. Umrath K (1930) Untersuchungen über Plasma und Plasmaströmung an Characeen. IV. Potentialmessungen an Nitella mucronata mit besonderer Berücksichtigung der Erregungsleitung. Protoplasma 9: 576–597.
  • 102. Vogel S (2000) Von Grashalmen und Hochhäusern–Mechanische Schöpfungen in Natur und Technik. Wiley-VCH.
  • 103. Walker NA (1976) Membrane transport: Theoretical background. Encyclopedia of Plant Physiology New Series 2A, 36–52.
  • 104. Walker NA, Pitman MG (1976) Measurement of fluxes across membranes. Encyclopedia of Plant Physiology New Series 2A, 93–126.
  • 105. Wei J, Hongzhong L, Lei Y, et al. (2016) Enhanced photoelectric properties in dye-sensitized solar cells using TiO2 pyramid arrays. J Phys Chem 120: 9678–9684.
  • 106. Wei MC, Tyree MT, Steudle E (1999) Direct measurement of xylem pressure in leaves of intact maize plants. A test of the cohesion-tension theory taking hydraulic architecture into consideration. Plant Physiol 121: 1191–1205.
  • 107. Whitelegge JP (2003) Thylakoid proteomics. Photosynth Res 78: 265–277.    
  • 108. Zhu GL, Steudle E (1991) Water transport across maize roots: simultaneous measurements of flows at the cell and root level by double pressure probe technique. Plant Physiol 95: 305–315.    
  • 109. Zimmermann U, Meinzer FC, Benkert R, et al. (1994) Xylem water transport: is the available evidence consistent with the cohesion theory. Plant Cell Environ 17:1169–1181.

 

This article has been cited by

Reader Comments

your name: *   your email: *  

Copyright Info: 2016, Ulrich Lüttge, licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)

Download full text in PDF

Export Citation

Copyright © AIMS Press All Rights Reserved