Skip to main content

Oscillations in Plants

  • Chapter
Book cover Communication in Plants

Abstract

Despite the fact that the rhythmical behaviour is a quintessential pattern of life itself, most researchers still treat oscillations in plants as some unwanted “physiological noise”. In this review, an attempt is made to summarise recent progress in this area and highlight the paramount role of oscillatory processes in plant life. First, diversity and hierarchy of oscillations in plants are examined, then a general overview of oscillatory phenomena is given, with the main emphasis on the physiological role of oscillatory processes in plants. The areas covered include leaf and stomata movement, nutations, nutrient acquisition, growth and differentiation, photosynthesis and osmotic adjustment. A possible role for ultradian rhythms in timekeeping is also briefly discussed. The importance of ultradian oscillations is further illustrated by discussing their involvement in the encoding mechanism, mediating plant-environment interaction. Finally, advantages and principles of oscillatory control are considered in the context of plant physiology, with a major emphasis on feedback control and self-sustained oscillations, as well as on deterministic chaos and “strange” behaviour in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Anderson-Bernadas C, Cornelissen G, Turner CM, Koukkari WL (1997) Rhythmic nature of thigmomorphogenesis and thermal stress of Phaseolus vulgaris L shoots. J Plant Physiol 151:575–580

    CAS  Google Scholar 

  • Antkowiak B, Engelmann W (1995) Oscillations of apoplasmic K+ and H+ activities in Desmodium motorium (Houtt.) Merril. pulvini in relation to the membrane potential of motor cells and leaflet movements. Planta 196:350–356

    Article  CAS  Google Scholar 

  • Ashoff J (1981) A survey on biological rhythms. Hand Behav Neurobiol 3–10

    Google Scholar 

  • Barlow PW, Parker JS, Brain P (1994) Oscillations of axial plant organs. Adv Space Res 14:149–158

    Article  PubMed  CAS  Google Scholar 

  • Barrio RA, Zhang LM, Maini PK (1997) Hierarchically coupled ultradian oscillators generating robust circadian rhythms. Bull Math Biol 59:517–532

    Article  PubMed  CAS  Google Scholar 

  • Barrs HD (1971) Cyclic variations in stomatal aperture, transpiration, and leaf water potential under constant environmental conditions. The phenomenon. Annu Rev Plant Physiol 22:223–236

    Article  Google Scholar 

  • Blatt MR (2000) Cellular signalling and volume control in stomatal movements in plants. Annu Rev Cell Dev Biol 16:221–241

    Article  PubMed  CAS  Google Scholar 

  • Buer CS, Masle J, Wasteneys GO (2000) Growth conditions modulate root-wave phenotypes in Arabidopsis. Plant Cell Physiol 41:1164–1170

    Article  PubMed  CAS  Google Scholar 

  • Cardon ZG, Mott KA, Berry JA (1994) Dynamics of patchy stomatal movements, and their contribution to steady-state and oscillating stomatal conductance calculated using gas-exchange techniques. Plant Cell Environ 17:995–1007

    Article  Google Scholar 

  • Chen JP, Engelmann W, Baier G (1995) Nonlinear dynamics in the ultradian rhythm of Desmodium motorium. Z Naturforsch 50:1113–1116

    Google Scholar 

  • Cowan IR (1972) Oscillations in stomatal conductance and plant functioning associated with stomatal conductance: observations and a model. Planta 106:185–219

    Article  Google Scholar 

  • Dolmetsch RE, Xu K, Lewis RS (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392:933–936

    Article  PubMed  CAS  Google Scholar 

  • Dunlap J (1998) An end in the beginning. Science 280:1548–1549

    Article  PubMed  CAS  Google Scholar 

  • Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to rhizobium nodulation signals. Cell 85:673–681

    Article  PubMed  CAS  Google Scholar 

  • Engelmann W, Antkowiak B (1998) Ultradian rhythms in Desmodium. Chronobiol Int 15:293–307

    Article  PubMed  CAS  Google Scholar 

  • Erdei L, Szegletes Z, Barabas KN, Pestenacz A, Fulop K, Kalmar L, Kovacs A, Toth B, Der A (1998) Environmental stress and the biological clock in plants — changes of rhythmic behavior of carbohydrates, antioxidant enzymes and stomatal resistance by salinity. J Plant Physiol 152:265–271

    CAS  Google Scholar 

  • Feijo JA, Sainhas J, Holdaway-Clarke T, Cordeiro MS, Kunkel JG, Hepler PK (2001) Cellular oscillations and the regulation of growth: the pollen tube paradigm. Bioassays 23:86–94

    Article  CAS  Google Scholar 

  • Giersch C (1994) Photosynthetic oscillations: observations and models. Comments Theor Biol 3:339–364

    Google Scholar 

  • Goldbeter A, Li YX, Dupont G (1990) Oscillatory dynamics in intercellular communication. Biomed Biochim Acta 49:935–940

    PubMed  CAS  Google Scholar 

  • Gradmann D, Boyd CM (1995) Membrane voltage of marine-phytoplankton, measured in the diatom Coscinodiscus radiatus. Marine Biol 123:645–650

    Article  Google Scholar 

  • Hejnowicz Z (1975) A model for morphogenetic map and clock. J Theor Biol 54:345–362

    Article  PubMed  CAS  Google Scholar 

  • Hejnowicz Z, Sievers A (1995) Proton efflux from the outer layer of the peduncle of tulip in gravitropism and circumnutation. Bot Acta 108:7–13

    CAS  Google Scholar 

  • Holdaway-Clarke TL, Hepler PK (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 159:539–563

    Article  CAS  Google Scholar 

  • Inoue N, Arase T, Hagiwara M, Amano T, Hayashi T, Ikeda R (1999) Ecological significance of root tip rotation for seedling establishment of Oryza sativa L. Ecol Res 14:31–38

    Article  Google Scholar 

  • Jaeger J, Goodwin BC (2001) A cellular oscillator model for periodic pattern formation. J Theor Biol 213:171–181

    Article  PubMed  CAS  Google Scholar 

  • Kellershohn N, Prat R, Ricard J (1996) Aperiodic (‘chaotic’) behaviour of plant cell wall extension. 1. Nonlinear chemical model of periodic and aperiodic oscillations of cell wall growth. Chaos Sol Fractals 7:1103–1117

    Article  CAS  Google Scholar 

  • Kharitonashvili EV, Lebedeva GV, Plyusnina TY, Riznichenko GY, Alekhina ND (1997) Empirical model of nitrate metabolism regulation in the roots of wheat seedlings. Russ J Plant Physiol 44:493–499

    CAS  Google Scholar 

  • Kim HY, Cote GG, Crain RC (1993) Potassium channels in Samanea saman protoplasts controlled by phytochrome and the biological clock. Science 260:960–962

    Article  CAS  PubMed  Google Scholar 

  • Kocks P, Ross J (1995) Kinetic-model for (damped) oscillations of transthylakoid pH in plants. J Phys Chem 99:16490–16497

    Article  CAS  Google Scholar 

  • Lakin-Thomas PL (1998) Choline depletion, frq mutations, and temperature compensation of the circadian rhythm in Neurospora crassa. J Biol Rhythms 13:268–277

    Article  PubMed  CAS  Google Scholar 

  • Lloyd D (1997) Chaos and ultradian rhythms. Biol Rhythms Res 28:134–143

    Article  Google Scholar 

  • Lloyd D, Kippert F (1993) Intracellular coordination by the ultradian clock. Cell Biol Int 17:1047–1052

    Article  PubMed  CAS  Google Scholar 

  • Lloyd D, Stupfel M (1991) The occurrence and functions of ultradian rhythms. Biol Rev Cambr Philos Soc 66:275–299

    CAS  Google Scholar 

  • Lüttge U, Beck F (1992) Endogenous rhythms and chaos in crassulacean acid metabolism. Planta 188:28–38

    Article  Google Scholar 

  • Lüttge U, Hütt M-T (2004) High frequency or ultradian rhythms in plants. Prog Bot 65:235–263

    Google Scholar 

  • Macduff JH, Dhanoa MS (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

    Article  CAS  Google Scholar 

  • Markevich NI, Sel’kov EE (1986) Mathematical model of resonance amplification on external effects on the membranes. Biofizika 31:662–666

    CAS  Google Scholar 

  • McAinsh M, Hetherington A (1998) Encoding specificity in Ca2+ signalling systems. Trends Plant Sci 3:32–36

    Article  Google Scholar 

  • McAinsh MR, Webb AAR, Taylor JE, Hetherington AM (1995) Stimulus-induced oscillations in guard-cell cytosolic-free calcium. Plant Cell 7:1207–1219

    Article  PubMed  CAS  Google Scholar 

  • Messerli MA, Robinson KR (1998) Ionic and osmotic disruptions of the lily pollen tube oscillator: testing proposed models. Planta 217:147–157

    Google Scholar 

  • Mott KA, Buckley TN (1998) Stomata heterogenity. J Exp Bot 49:407–417

    Article  Google Scholar 

  • Pavlidis T (1971) Population of biochemical oscillators as circadian clocks. J Theor Biol 33:319–338

    Article  PubMed  CAS  Google Scholar 

  • Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41:421–453

    Article  CAS  Google Scholar 

  • Rand RH, Upadhyaya SK, Cooke JR, Storti DW (1981) Hopf bifurcation in a stomatal oscillator. J Math Biol 12:1–11

    Article  Google Scholar 

  • Rapp PE (1987) Why are so many biological systems periodic? Prog Neurobiol 29:261–273

    Article  PubMed  CAS  Google Scholar 

  • Rapp PE, Mees AI, Sparrow CT (1981) Frequency encoded biochemical regulation is more accurate than amplitude dependent control. J Theor Biol 90:531–544

    Article  PubMed  CAS  Google Scholar 

  • Raschke K (1975) Stomatal action. Annu Rev Plant Physiol 26:309–340

    Article  CAS  Google Scholar 

  • Richter P, Ross J (1981) Oscillations and efficiency in glycolysis. Biophys Chem 12:285–297

    Article  Google Scholar 

  • Schuster J, Engelmann W (1997) Circumnutations of Arabidopsis thaliana seedlings. Biol Rhythm Res 28:422–440

    Article  Google Scholar 

  • Shabala S (1986) Forced oscillations of higher plant biopotentials. Izv Timiryazev S-kh Akad 4:86–89 (in Russian)

    Google Scholar 

  • Shabala S (1989) Light-induced oscillations of plant bioelectric potentials and their relation to physiological processes in plants. PhD thesis. Institute of Experimental Botany, Minsk

    Google Scholar 

  • Shabala S (1997) Leaf bioelectric responses to rhythmical light: identification of the contribution from stomatal and mesophyll cells. Aust J Plant Physiol 24:741–749

    Google Scholar 

  • Shabala S (2003) Physiological implications of ultradian oscillations in plant roots. Plant Soil 255:217–226

    Article  CAS  Google Scholar 

  • Shabala S, Knowles A (2002) Rhythmic patterns of nutrient acquisition by wheat roots. Funct Plant Biol 29:595–605

    Article  CAS  Google Scholar 

  • Shabala S, Newman IA (1997) Proton and calcium flux oscillations in the elongation region correlate with root nutation. Physiol Plant 100:917–926

    Article  PubMed  CAS  Google Scholar 

  • Shabala S, Maslobrod SN, Zhakote AG (1989) Effects of periodic light, given at a resonance frequency of oscillations in leaf bioelectric potentials, on growth and development of plants. Fiziol Biokhim Kult Rast 21:27–31 (in Russian)

    Google Scholar 

  • Shabala S, Shevchenko VA, Maslobrod SN, Tretyakov NN (1991) Endogenous oscillations and the resonant phenomena in plants under rhythmical changes of the root environmental parameters. Izv Timiryazev S-kh Akad 6:87–97 (in Russian)

    Google Scholar 

  • Shabala S, Newman IA, Morris J (1997a) 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  CAS  Google Scholar 

  • Shabala S, Delbourgo R, Newman I (1997b) Observations of bifurcation and chaos in plant physiological responses to light. Aust J Plant Physiol 24:91–96

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Shabala S, Schimanski LJ, Koutoulis A (2002) Heterogeneity in bean leaf mesophyll tissue and ion flux profiles: Leaf electrophysiological characteristics correlate with the anatomical structure. Ann Bot 89:221–226

    Article  PubMed  Google Scholar 

  • Sharma VK, Bardal TK, Johnsson A (2003) Light-dependent changes in the leaflet movement rhythm of the plant Desmodium gyrans. Z Naturforsch 58:81–86

    CAS  Google Scholar 

  • Siebke K, Weis E (1995) Assimilation images of leaves of Glechoma hederacea: analysis of non-synchronous stomata lelated oscillations. Planta 196:155–165

    Article  CAS  Google Scholar 

  • Siebke K, Yin ZH, Raghavendra AS, Heber U (1992) Vacuolar pH oscillations in mesophyll cells accompany oscillations of photosynthesis in leaves — interdependence of cellular compartments, and regulation of electron flow in photosynthesis. Planta 186:526–531

    Article  CAS  Google Scholar 

  • Stucki JW, Somogyi R (1994) A dialog on Ca2+ oscillations — an attempt to understand the essentials of mechanisms leading to hormone-induced intracellular Ca2+ oscillations in various kinds of cell on a theoretical level. Biochim Biophys Acta 1183:453–472

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tsien RW, Tsien RY (1990) Calcium channels, stores, and oscillations. Annu Rev Cell Biol 6:715–760

    Article  PubMed  CAS  Google Scholar 

  • Tsong TY (1990) Electrical modulation of membrane proteins: enforced conformational oscillations and biological energy and signal transductions. Annu Rev Biophys Biophys Chem 19:83–106

    Article  PubMed  CAS  Google Scholar 

  • Tyerman SD, Beilby M, Whittington J, Juswono U, Newman I, Shabala S (2001) Oscillations in proton transport revealed from simultaneous measurements of net current and net proton fluxes from isolated root protoplasts: MIFE meets patch-clamp. Aust J Plant Physiol 28:591–604

    CAS  Google Scholar 

  • Vanden Driessche T (2000) Nutations in shoots and in Desmodium lateral leaflets, nyctinastism and seismonastism in Mimosa pudica. Comparison and evolution of morphology and mechanism. Biol Rhythm Res 31:451–468

    Article  Google Scholar 

  • Wagner E, Deitzer GF, Fischer S, Frosh S, Kempf O, Stroebele L (1975) Endogenous oscillations in pathways of energy transduction as related to circadian rhythmicity and photoperiodic control. BioSystems 7:68–76

    Article  PubMed  CAS  Google Scholar 

  • Wagner E, Normann J, Albrechtova JTP (1998) Photoperiodic control of flowering: ‘Florigen’ — A frequency-coded electric signal? Endocyt Cell Res 12:204–204

    Google Scholar 

  • Webb AAR (2003) The physiology of circadian rhythms in plants. New Phytol 160:281–303

    Article  CAS  Google Scholar 

  • Willmer CM (1988) Stomatal sensing of the environment. Biol J Linn Soc 34:205–321

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Shabala, S. (2006). Oscillations in Plants. In: Baluška, F., Mancuso, S., Volkmann, D. (eds) Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-28516-8_18

Download citation

Publish with us

Policies and ethics