Kinetics and Mechanism of Dionaea muscipula Trap Closing1[C][OA]

The Venus flytrap (Dionaea muscipula) possesses an active trapping mechanism to capture insects with one of the most rapid movements in the plant kingdom, as described by Darwin. This article presents a detailed experimental investigation of trap closure by mechanical and electrical stimuli and the mechanism of this process. Trap closure consists of three distinctive phases: a silent phase with no observable movement; an accelerated movement of the lobes; and the relaxation of the lobes in their closed state, resulting in a new equilibrium. Uncouplers and blockers of membrane channels were used to investigate the mechanisms of different phases of closing. Uncouplers increased trap closure delay and significantly decreased the speed of trap closure. Ion channel blockers and aquaporin inhibitors increased time of closing. Transmission of a single electrical charge between a lobe and the midrib causes closure of the trap and induces an electrical signal propagating between both lobes and midrib. The Venus flytrap can accumulate small subthreshold charges, and when the threshold value is reached, the trap closes. Repeated application of smaller charges demonstrates the summation of stimuli. The cumulative character of electrical stimuli points to the existence of electrical memory in the Venus flytrap. The observed fast movement can be explained by the hydroelastic curvature model without invoking buckling instability. The new hydroelastic curvature mechanism provides an accurate description of the authors' experimental data.

[1]  A. Bennett,et al.  Leaf Closure in the Venus Flytrap: An Acid Growth Response , 1982, Science.

[2]  A. Volkov Liquid interfaces in chemistry and biology , 1998 .

[3]  Alexander G. Volkov,et al.  Electrophysiology and Phototropism , 2006 .

[4]  Douglas G. Howe,et al.  A quantitative study of tissue dynamics in Venus's flytrap Dionaea muscipula (Droseraceae). II. Trap reopening , 1996 .

[5]  S. L. Jacobson Receptor Response in Venus's Fly-Trap , 1965, The Journal of general physiology.

[6]  L. Mahadevan,et al.  Physical Limits and Design Principles for Plant and Fungal Movements , 2005, Science.

[7]  Emil Jovanov,et al.  Closing of Venus Flytrap by Electrical Stimulation of Motor Cells , 2007, Plant signaling & behavior.

[8]  Volko Green plants : electrochemical interfaces , 2000 .

[9]  J. Dipalma,et al.  Touch Receptor of Venus Flytrap, Dionaea muscipula , 1966, Science.

[10]  J. Burdon Sanderson,et al.  On the Electromotive Properties of the Leaf of Dionaea in the Excited and Unexcited States. Second Paper , 1888 .

[11]  F. Sachs,et al.  Thermodynamics of mechanosensitivity , 2004, Physical biology.

[12]  D. Hodick,et al.  On the mechanism of trap closure of Venus flytrap (Dionaea muscipula Ellis) , 1989, Planta.

[13]  D. Hodick,et al.  The influence of Ca2+ on the action potential in mesophyll cells ofDionaea muscipula Ellis , 1986, Protoplasma.

[14]  F Sachs,et al.  Thermodynamics of mechanosensitivity , 2004, Physical biology.

[15]  C. Maurel AQUAPORINS AND WATER PERMEABILITY OF PLANT MEMBRANES. , 1997, Annual review of plant physiology and plant molecular biology.

[16]  J. Burdon-Sanderson,et al.  I. On the mechanical effects and on the electrical disturbance consequent on excitation of the leaf of Dionæa muscipula , 1877, Proceedings of the Royal Society of London.

[17]  S. Tyerman,et al.  Plant aquaporins: multifunctional water and solute channels with expanding roles. , 2002, Plant, cell & environment.

[18]  D. Hodick,et al.  The action potential of Dionaea muscipula Ellis , 1988, Planta.

[19]  František Baluška,et al.  Communication in plants : neuronal aspects of plant life , 2006 .

[20]  R. Morillon,et al.  Rapid movements of plants organs require solute-water cotransporters or contractile proteins. , 2001, Plant physiology.

[21]  H. W. Lea A muscle contracting substance from a plant's closing Fly-Trap , 2004, Planta.

[22]  R. M. Benolken,et al.  Response Properties of a Sensory Hair Excised from Venus's Flytrap , 1970, The Journal of general physiology.

[23]  H. Dziubinska,et al.  Effects of ion channel inhibitors on cold- and electrically-induced action potentials in Dionaea muscipula , 2006, Biologia Plantarum.

[24]  W. Best,et al.  Action Potential and Contraction of Dionaea muscipula (Venus Flytrap) , 1961, Science.

[25]  A. H. Green The Glacial Period , 1874, Nature.

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

[27]  C. Maurel,et al.  Aquaporins. A molecular entry into plant water relations. , 2001, Plant physiology.

[28]  Yi Wang,et al.  Structural mechanism of plant aquaporin gating , 2006, Nature.

[29]  A. Sievers,et al.  Action Potentials Evoked by Light in Traps of Dionaea muscipula Ellis , 1998 .

[30]  P. A. Rea,et al.  The dynamics of H+ efflux from the trap lobes of Dionaea muscipula Ellis (Venus's flytrap) , 1983 .

[31]  J. Scala,et al.  Digestive Secretion of Dionaea muscipula (Venus's Flytrap). , 1969, Plant physiology.

[32]  M. Jaffe,et al.  The Role of ATP in Mechanically Stimulated Rapid Closure of the Venus's Flytrap. , 1973, Plant physiology.

[33]  A. Volkov,et al.  Nanodevices in Nature , 2007 .

[34]  P. Mangan Springing the trap. , 1993, Nursing times.

[35]  A. Volkov,et al.  Electrochemistry of soybean: effects of uncouplers, pollutants, and pesticides , 2001 .

[36]  William H. Brown,et al.  The Closing Response in Dionaea , 1910, Botanical Gazette.

[37]  W. Fagerberg,et al.  A QUANTITATIVE STUDY OF TISSUE DYNAMICS DURING CLOSURE IN THE TRAPS OF VENUS'S FLYTRAP DIONAEA MUSCIPULA ELLIS , 1991 .

[38]  O STUHLMAN,et al.  The action potentials obtained from venus's-flytrap. , 1950, Science.

[39]  S. Roberts,et al.  Plasma membrane anion channels in higher plants and their putative functions in roots. , 2006, The New phytologist.

[40]  Courtney L. Brown,et al.  Electrochemistry of Plant Life , 2006 .

[41]  Janet Braam,et al.  In touch: plant responses to mechanical stimuli. , 2004, The New phytologist.

[42]  B. L. de Groot,et al.  Quaternary Ammonium Compounds as Water Channel Blockers , 2006, Journal of Biological Chemistry.

[43]  FRANCISCO GINEZ,et al.  Carnivorous Plants , 1877, Nature.

[44]  M. E. Williams,et al.  THE FINE STRUCTURE OF THE TRIGGER HAIR IN VENUS'S FLYTRAP , 1971 .

[45]  S. L. Jacobson,et al.  Effect of ionic environment on the response of the sensory hair of Venus's-flytrap , 1974 .

[46]  Schmitt Lm Outline of remarks on the role of the college or university in continuing education for staff nurses in the hospital setting. , 1966 .

[47]  L. Mahadevan,et al.  How the Venus flytrap snaps , 2005, Nature.

[48]  William H. Brown,et al.  THE MECHANISM OF MOVEMENT AND THE DURATION OF THE EFFECT OF STIMULATION IN THE LEAVES OF DIONAEA , 1916 .

[49]  A. Volkov,et al.  Insect-induced biolectrochemical signals in potato plants , 1995 .

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