Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera

The nature and characteristics of the electrical response to wounding in the woody plant Vitis vinifera L. were examined. Following burning of a small area of a leaf, bioelectrical events spread throughout the shoot. The heat wound triggered stem deformations (widening–contraction), which preceded changes in biopotentials and that are interpreted as reflecting wound-induced hydraulic signals. It also caused marked decrease of extracellular resistance in stem tissues, starting about 15 s after stimulation, while intracellular resistance did not show any modification. Under an N2 atmosphere (hypoxic conditions), action potentials disappeared and the amplitude of variation potentials decreased approximately 50%. At saturating humidity variation potentials were completely eliminated, while action potentials were evident. Taken together, the results demonstrate that action and variation potentials differ both in their mechanism of propagation and electrogenic nature. Action potentials are ‘genuine’ self-propagating electrical signals travelling at a velocity of about 10 cm s-1, with a metabolic nature involving active components (electrogenic pumps). Variation potentials are a ‘local’ response to the passage of an hydraulic wave. Results support the hypothesis that both ion channels and pumps are involved in variation potential depolarisation.

[1]  J. Kourie.  Transient Cl- and K+ Currents during the Action Potential in Chara inflata (Effects of External Sorbitol, Cations, and Ion Channel Blockers) , 1994, Plant physiology.

[2]  M. Malone,et al.  Only xylem-borne factors can account for systemic wound signalling in the tomato plant , 1995, Planta.

[3]  M. Malone,et al.  Wound-Induced Hydraulic Signals: Survey of Occurrence in a Range of Species , 1993 .

[4]  T. Sibaoka.  Action potentials in plant organs. , 1966, Symposia of the Society for Experimental Biology.

[5]  T. Sibaoka,et al.  Physiology of Rapid Movements in Higher Plants , 1969 .

[6]  M. Malone,et al.  Rapid, Long-distance Signal Transmission in Higher Plants , 1996 .

[7]  A. L. Houwink,et al.  The conduction of excitation in Mimosa pudica , 1935 .

[8]  Gabriel Roblin,et al.  Analysis of the Variation Potential Induced by Wounding in Plants , 1985 .

[9]  M. Samejima,et al.  Identification of the Excitable Cells in the Petiole of Mimosa pudica by Intracellular Injection of Procion Yellow , 1983 .

[10]  D. Cosgrove,et al.  The Propagation of Slow Wave Potentials in Pea Epicotyls , 1997, Plant physiology.

[11]  E. Davies,et al.  Characteristics of action potentials in Helianthus annuus , 1991 .

[12]  J. Bonnemain,et al.  Propagation in Vicia faba Stem of a Potential Variation Induced by Wounding , 1985 .

[13]  Marvin Weintraub,et al.  LEAF MOVEMENTS IN MIMOSA PUDICA L. , 1952 .

[14]  P. Minchin,et al.  Electrical signalling and systemic proteinase inhibitor induction in the wounded plant , 1992, Nature.

[15]  Jörg Fromm,et al.  Characteristics of Action Potentials in Willow (Salix viminalis L.) , 1993 .

[16]  Stefano Mancuso,et al.  Seasonal dynamics of electrical impedance parameters in shoots and leaves related to rooting ability of olive (Olea europea) cuttings. , 1999, Tree physiology.

[17]  M. Tazawa,et al.  MEMBRANE CONTROL IN THE CHARACEAE , 1987 .

[18]  J. B. Hanson,et al.  Controls on Calcium Influx in Corn Root Cells , 1986 .

[19]  Takashi Shiina,et al.  Action Potential in Luffa cylindlica and its Effects on Elongation Growth , 1986 .

[20]  M. Malone,et al.  Wound-induced hydraulic signals and stimulus transmission in Mimosa pudica L. , 1994, The New phytologist.

[21]  Eric Davies,et al.  Action potentials as multifunctional signals in plants: a unifying hypothesis to explain apparently disparate wound responses , 1987 .

[22]  Bratislav Stankovic,et al.  Surface potentials and hydraulic signals in wheat leaves following localized wounding by heat , 1991 .

[23]  P. Minorsky.  An heuristic hypothesis of chilling injury in plants: a role for calcium as the primary physiological transducer of injury , 1985 .

[24]  J. Lassalles,et al.  Stretch activated channels in plant cells. A new model for osmoelastic coupling , 1996 .

[25]  D. Bush.  Proton-Coupled Sugar and Amino Acid Transporters in Plants , 1993 .

[26]  Extra- and intracellular measurements of action potentials in the liverwort Conocephalum conicum , 1985 .

[27]  S. Ries,et al.  Cation signals rapidly elicited in several different plant species by pinching the leaves , 1994 .

[28]  Dianna J. Bowles,et al.  Systemic responses arising from localized heat stimuli in tomato plants , 1989 .

[29]  JOHN W. Moore.  Membranes, ions, and impulses , 1976 .

[30]  I. Tasaki,et al.  Fractionation of Tracer Effluxes during Action Potential , 1961, Science.

[31]  Eric Davies,et al.  Characteristics of action potentials generated spontaneously in Helianthus annuus , 1995 .

[32]  K. Oda.  Simultaneous recording of potassium and chloride effluxes during an action potential in Chara corallina , 1976 .

[33]  A. Trewavas,et al.  Wind-induced plant motion immediately increases cytosolic calcium. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Barbara G. Pickard,et al.  Mediation of rapid electrical, metabolic, transpirational, and photosynthetic changes by factors released from wounds. I. Variation potentials and putative action potentials in intact plants , 1976 .

[35]  E. Davies,et al.  Characterization of the Variation Potential in Sunflower , 1997, Plant physiology.

[36]  T. Sibaoka.  Excitable Cells in Mimosa , 1962, Science.

[37]  L. Mullins,et al.  Ion fluxes during the action potential in Chara , 1958, The Journal of physiology.

[38]  J. Ding,et al.  Mechanosensory calcium-selective cation channels in epidermal cells. , 1993, The Plant journal : for cell and molecular biology.

[39]  M. Malone.  Kinetics of wound-induced hydraulic signals and variation potentials in wheat seedlings , 1992, Planta.

[40]  A. Campbell,et al.  Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium , 1991, Nature.