Oscillations in plant membrane transport: model predictions, experimental validation, and physiological implications

• Published in: Journal of experimental botany Vol. 57; no. 1; pp. 171 - 184
• Main Authors: Shabala, Sergey, Shabala, Lana, Gradmann, Dietrich, Chen, Zhonghua, Newman, Ian, Mancuso, Stefano
• Format: Journal Article
• Language: English
• Published: Oxford Oxford University Press 01.01.2006; Oxford Publishing Limited (England)
• Subjects: Adaptation; Adaptation, Physiological; barley; Biological and medical sciences; Cell Membrane; Cell Membrane - physiology; Cell membranes; Cell physiology; Cell Size; cells; Control systems; corn; Electric potential; encoding; Environmental information; feedback; Feedback, Physiological; Fundamental and applied biological sciences. Psychology; Guard cells; Hordeum vulgare; Hypoxia; ion flux; Ion Pumps; Ion Pumps - physiology; ion transport; Ion Transport - physiology; Ions; leaves; membrane; metabolism; Modeling; Models, Biological; Oscillometry; Oxygen; Oxygen - metabolism; Physiology; Plant cells; Plant Physiological Phenomena; Plant physiology; Plant physiology and development; Plant roots; Plant species; Plant tissues; Plants; Plasma membrane and permeation; Potassium; Potassium - metabolism; potassium channels; proton pump; Proton Pumps; Proton Pumps - physiology; Pumps; Research Papers; rhythms; roots; Sodium Chloride; Sodium Chloride - metabolism; stress; Temperature; temporal variation; Zea mays; rhythms; Temperature; membrane; Root; Plant leaf; encoding; Stress; Salinity; feedback; Membrane transport; ion flux; Plasma membrane; Hypoxia; Adaptation
• ISSN: 0022-0957; 1460-2431; 1460-2431
• DOI: 10.1093/jxb/erj022

Although oscillations in membrane-transport activity are ubiquitous in plants, the ionic mechanisms of ultradian oscillations in plant cells remain largely unknown, despite much phenomenological data. The physiological role of such oscillations is also the subject of much speculation. Over the last decade, much experimental evidence showing oscillations in net ion fluxes across the plasma membrane of plant cells has been accumulated using the non-invasive MIFE technique. In this study, a recently proposed feedback-controlled oscillatory model was used. The model adequately describes the observed ion flux oscillations within the minute range of periods and predicts: (i) strong dependence of the period of oscillations on the rate constants for the H+ pump; (ii) a substantial phase shift between oscillations in net H+ and K+ fluxes; (iii) cessation of oscillations when H+ pump activity is suppressed; (iv) the existence of some ‘window’ of external temperatures and ionic concentrations, where non-damped oscillations are observed: outside this range, even small changes in external parameters lead to progressive damping and aperiodic behaviour; (v) frequency encoding of environmental information by oscillatory patterns; and (vi) strong dependence of oscillatory characteristics on cell size. All these predictions were successfully confirmed by direct experimental observations, when net ion fluxes were measured from root and leaf tissues of various plant species, or from single cells. Because oscillatory behaviour is inherent in feedback control systems having phase shifts, it is argued from this model that suitable conditions will allow oscillations in any cell or tissue. The possible physiological role of such oscillations is discussed in the context of plant adaptive responses to salinity, temperature, osmotic, hypoxia, and pH stresses.