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Physiological implications of ultradian oscillations in plant roots

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Abstract

Oscillatory processes are ubiquitous in the Plant Kingdom. Surprisingly, many plant physiologists ignored these as physiologically unimportant unwanted `noise'. Based on the application of the non-invasive ion-selective flux measuring (the MIFE) technique, this paper provides experimental evidence that ultradian oscillations in roots are a widespread phenomenon and reviews some physiological implications of ultradian rhythms in root nutrient acquisition. It is shown that the rhythmical character of root nutrient uptake is a characteristic feature for all measured species (both monocots and dicots; C3 and C4 type of photosynthesis). These oscillations were present in all major functional root zones, including root meristem, elongation and mature zone, and root hair region. For the first time, ultradian ion flux oscillations have been reported from the developing root hairs and from vertically grown roots exhibiting circumnutations. Several types of ultradian oscillations were distinguished, including those associated with extension growth of root tissues, more slow oscillations associated with either root circumnutation or nutrient acquisition in the mature zone, and rhythmical fluctuation in nutrient acquisition, associated with root adaptive responses to environmental stresses. Some underlying ionic mechanisms are discussed. Overall, these results show a crucial role of the rhythmical membrane-transport processes in plant–soil environmental interaction.

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References

  • Amzallag G N 1997 Influence of periodic fluctuations in root environment on adaptation to salinity in Sorghum bicolor. Austral. J. Plant Physiol. 24, 579-586.

    Google Scholar 

  • Barlow P W, Parker J S and Brain P 1994 Oscillations of axial plant organs. Adv. Space Res. 14, 149-158.

    PubMed  Google Scholar 

  • Brown A H 1993 Circumnutations: from Darwin to space flights. Plant Physiol. 101, 345-348.

    PubMed  Google Scholar 

  • Brown A H, Chapman D K, Lewis R F and Venditti A L 1990 Circumnutation of sunflower hypocotyls in satellite orbit. Plant Physiol. 94, 233-238.

    PubMed  Google Scholar 

  • Cardenas-Navarro R, Adamowicz S, Robin P 1998 Diurnal nitrate uptake in young tomato (Lycopersicon esculentum Mill.) plants-test of a feedback-based model. J. Exp. Bot. 49, 721-730.

    Google Scholar 

  • Claire A, Frachisse J M and Desbiez M O 1985 Oscillatione électriques observées au cours du movement des tiges volubiles d'Ipomoea purpurea. Compt. Rend. Acad. Sci. Paris 300, 363-366.

    Google Scholar 

  • Cortes P M 1997 Cortical intracellular electrical potential in roots of unstressed and stressed sunflower seedlings. 2. Radial profiles and oscillations. Austral. J. Plant Physiol. 24, 651-660.

    Google Scholar 

  • Cosgrove D J 2000 Expansive growth of plant cell walls. Plant Physiol. Biochem. 38, 109-124.

    PubMed  Google Scholar 

  • Delhon P, Gojon A, Tillard P and Passama L 1995 Diurnal regulation of NO3 – uptake in soybean plants. 2. Relationship with accumulation of NO3 – and asparagine in the roots. J. Exp. Bot. 46, 1595-1602.

    Google Scholar 

  • Ehrhardt D W, Wais R and Long S R 1996 Calcium spiking in plant root hairs responding to rhizobium nodulation signals. Cell 85, 673-681.

    PubMed  Google Scholar 

  • Ensminger PA and Lipson E D 1992 Growth rate fluctuations in Phycomyces sporangiphores. Plant Physiol. 99, 1376-1380.

    Google Scholar 

  • Geitmann A and Cresti M 1998 Ca2+ channels control the rapid expansions in pulsating growth of Petunia hybrida pollen tubes. J. Plant Physiol. 152, 439-447.

    Google Scholar 

  • Gradmann D and Boyd C M 1995 Membrane voltage of marine phytoplankton, measured in the diatom Coscinodiscus radiatus. Mar. Biol. 123, 645-650.

    Google Scholar 

  • Gradmann D, Blatt M R and Thiel G 1993 Electrocoupling of ion transporters in plants. J. Membrane Biol. 136, 327-332.

    Google Scholar 

  • Hecks B, Hejnowicz Z, Sievers A 1992 Spontaneous oscillations of extracellular electrical potentials measured on Lepidium sativum L. roots. Plant Cell Environ. 15, 115-121.

    Google Scholar 

  • Hejnowicz Z and Sievers A 1994 Proton efflux from the outer layer of the peduncle of tulip in gravitropism and circumnutation. Bot. Acta 108, 7-13.

    Google Scholar 

  • Holdaway-Clarke T L, Feijo J A, Hacket G R, Kunkel J G and Hepler P K 1997 Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell 9, 1999-2010.

    PubMed  Google Scholar 

  • Jaffe L F and Nuccitelli R 1974 An ultrasensitive vibrating probe for measuring steady state extracellular currents. J. Cell Biol. 63, 614-628.

    PubMed  Google Scholar 

  • Jenkinson I S 1962 Bioelectric oscillations of bean roots: further evidence for a feedback oscillator. II. Intracellular plant root potentials. Austral. J. Biol. Sci. 15, 101-114.

    Google Scholar 

  • Jenkinson I S and Scott B I H 1961 Bioelectric oscillations of bean roots: further evidence for a feedback oscillator. I. Extracellular response to oscillations in osmotic pressure and auxin. Austral. J. Biol. Sci. 14, 231-236.

    Google Scholar 

  • Johnson C H, Knight M R, Kondo T, Masson P. Sedbrook J, Haley A and Trewavas A 1995 Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 249, 1863-1865.

    Google Scholar 

  • Johnsson A and Heathcote D 1973 Experimental evidence and models on circumnutations. Z. Pflanz. 70, 371-405.

    Google Scholar 

  • Kharitonashvili E V, Lebedeva G V, Plyusnina T Y, Riznichenko G Y and Alekhina N D 1997 Empirical model of nitrate metabolism regulation in the roots of wheat seedlings. Russian J. Plant Physiol. 44, 493-499.

    Google Scholar 

  • Knight H, Trewavas A J and Knight M R 1996 Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8, 489-503.

    PubMed  Google Scholar 

  • Kochian L V, Shaff J E, Kuhtreiber W M, Jaffe L F and Lucas W J 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, 601-610.

    Google Scholar 

  • Kristie D N and Joliffe P A 1986 High-resolution studies of growth oscillations during stem elongation. Can. J. Bot. 64, 2399-2405.

    Google Scholar 

  • Lucas W J and Kochian L V 1986 Ion transport processes in corn roots: an approach utilizing microelectrode techniques. In Advanced Agricultural Instrumentation: Design and Use. W G Gensler, pp. 402-425. Martinus Nijhoff, Dordrecht.

    Google Scholar 

  • Macduff J H and Dhanoa M S 1996 Diurnal and ultradian rhythms in K+ uptake by Trifolium repens under natural light patterns-evidence for segmentation at different root temperatures. Physiol. Plant. 98, 298-308.

    Google Scholar 

  • Macduff J H, Bakken A K and Dhanoa M S 1997 An analysis of the physiological basis of commonality between diurnal patterns of NH4 +, NO3 – and K+ uptake by Phleum pratense and Festuca pratensis. J. Exp. Bot. 48, 1691-1701.

    Google Scholar 

  • McAinsh Mand Hetherington A 1998 Encoding specificity in Ca2+ signalling systems. Trend. Plant Sci. 3, 32-36.

    Google Scholar 

  • Newman I A 2001 Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. Plant Cell Environ. 24, 1-14.

    PubMed  Google Scholar 

  • Prat R, Kellershohn N and Ricard J 1996 Aperiodic ('chaotic') behaviour of plant cell wall extension. II. Periodic and aperiodic oscillations of the elongation rate of a system of plant cells. Chaos Solut. Fract. 7, 1119-1125.

    Google Scholar 

  • Rapp P E, Mees A I and Sparrow C T 1981 Frequency encoded biochemical regulation is more accurate than amplitude dependent control. J. Theor. Biol. 90, 531-544.

    PubMed  Google Scholar 

  • Schurr U and Schulze E D 1995 The concentration of xylem sap constituents in root exudate, and in sap from intact, transpiring castor bean plants (Ricinus communis L). Plant Cell Environ. 18, 409-420.

    Google Scholar 

  • Scott B I H 1957 Electrical oscillations generated by plant roots and a possible feedback mechanism responsible for them. Austral. J. Biol. Sci. 10, 164-179.

    Google Scholar 

  • Shabala S and Knowles A 2002 Rhythmic patterns of nutrient acquisition by wheat roots. Funct. Plant Biol. 29, 595-605.

    Google Scholar 

  • Shabala S N and Newman I A 1997a Proton and calcium flux oscillations in the elongation region correlate with root nutation. Physiol. Plant. 100, 917-926.

    PubMed  Google Scholar 

  • Shabala S N and Newman I A 1997b Root nutation modelled by two ion flux-linked growth waves around the root. Physiol. Plant. 101, 770-776.

    Google Scholar 

  • Shabala S N and Newman I A 1998 Osmotic sensitivity of Ca2+ and H+ transporters in corn roots: effect on fluxes and their oscillations in the elongation, region. J. Membrane Biol. 161, 45-54.

    Google Scholar 

  • Shabala S N, Newman I A and Morris J 1997 Oscillations in H+ and Ca2+ ion fluxes around the elongation region of corn roots and effects of external pH. Plant Physiol. 113, 111-118.

    PubMed  Google Scholar 

  • Shabala S, Babourina O and Newman I 2000 Ion-specific mechanisms of osmoregulation in bean mesophyll cells. J. Exp. Bot. 51, 1243-1253.

    PubMed  Google Scholar 

  • Souda M, Toko K, Hayashi K, Fujiyoshi T, Ezaki S and Yamafuji K 1990 Relationship between growth and electric oscillations in bean roots. Plant Physiol. 93, 532-536.

    Google Scholar 

  • Termonia Y and Ross J 1982 Entrainment and resonance in glycolysis. Proc. Natl. Acad. Sci. USA 79, 2878-2881.

    PubMed  Google Scholar 

  • Toko K, Souda M, Matsuno T and Yamafuji K 1990 Oscillations of electrical potential along a root of a higher plant. Biophys. J. 57, 269-279.

    Google Scholar 

  • Zachariassen E, Johnsson A, Brown AH, Chapman DK and Johnson-Glebe C 1987 Influence of the g-force on the circumnutations of sunflower hypocotyls. Physiol. Plant. 70, 447-452.

    PubMed  Google Scholar 

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  1. School of Agricultural Science, University of Tasmania, GPO Box 252-54, Hobart, TAS, 7001, Australia

    S. Shabala

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Shabala, S. Physiological implications of ultradian oscillations in plant roots. Plant and Soil 255, 217–226 (2003). https://doi.org/10.1023/A:1026198927712

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