ScienceWeek

PLANT BIOLOGY: ON MOVEMENT IN THE VENUS FLYTRAP

Notes by ScienceWeek:

The term "nastic motion" refers to a plant movement in response to an external stimulus, for example the opening or closing of flowers in response to temperature change.

The following points are made by Y. Forterre et al (Nature 2005 433:421):

1) The rapid closure of the Venus flytrap (Dionaea muscipula) leaf in about 100 ms is one of the fastest movements in the plant kingdom. This led Darwin to describe the plant as "one of the most wonderful in the world"[1]. The trap closure is initiated by the mechanical stimulation of trigger hairs.

2) Plants are not known for their ability to move quickly. Nevertheless, rapid plant movements are involved in essential functions such as seed and pollen dispersal (exploding fruits in Impatiens, squirting cucumber and trigger plants), defense (sensitive mimosa) and nutrition (Venus flytrap, Aldrovanda vesiculosa, bladderwort). Of these spectacular examples that have long fascinated scientists, the leaves of the Venus flytrap, which snap together in a fraction of second to capture insects, have long been a paradigm for study; however, the mechanism by which this engine works remains poorly understood[1,5]. The most frequently proposed explanations are an irreversible, acid-induced wall loosening, and a rapid loss of turgor pressure in "motor cells". However, the validity of both mechanisms has recently been questioned[5] on the grounds that these cellular mechanisms alone cannot explain the rapidity of closure of the entire leaf on a macroscopic scale; this has led to the suggestion[5] that elastic deformations might be important.

3) Previous studies[2-5] have focused on the biochemical response of the trigger hairs to stimuli and quantified the propagation of action potentials in the leaves. The authors complemented these studies by considering the post-stimulation mechanical aspects of Venus flytrap closure. Using high-speed video imaging, non-invasive microscopy techniques and a simple theoretical model, the authors demonstrate that the fast closure of the trap results from a snap-buckling instability, the onset of which is controlled actively by the plant. The study identifies a solution to scaling up movements in non-muscular engines and provides a general framework for understanding nastic motion in plants.

References (abridged):

1. Darwin, C. Insectivorous Plants (Murray, London, 1875)

2. Burdon-Sanderson, J. On the electromotive properties of the leaf of dionaea in the excited and unexcited states. Phil. Trans. R. Soc. Lond. 173, 1-55 (1882)

3. Stuhlman, O. Jr & Darder, E. B. The action potentials obtained from Venus's-flytrap. Science 111, 491-492 (1950)

4. Hodick, D. & Sievers, A. The action potential of Dionaea muscipula Ellis. Planta 174, 8-18 (1988)

5. Hodick, D. & Sievers, A. On the mechanism of trap closure of Venus flytrap (Dionaea muscipula Ellis). Planta 179, 32-42 (1989)

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Related Material:

MOLECULAR BASIS OF MECHANOSENSORY TRANSDUCTION

The following points are made by P.G. Gillespie and R.G. Walker (Nature 2001 413:194):

1) Mechanical forces impinge on us from all directions, transmitting valuable information about the external environment. Mechanosensory cells transduce these mechanical forces and transmit this sensory information to the brain. Hearing, touch, sense of acceleration -- each informs us about what is nearby and how we are moving relative to our surroundings. An organism detects sensory information with a variety of cells that respond to force. Although different structurally, hair cells within our ear, cutaneous mechanoreceptors of our skin, and invertebrate mechanoreceptors share many mechanistic features; whether mutual molecular mechanisms underlie these similar transduction mechanisms remains to be determined.

2) As with most sensory systems, mechanosensory cells place a premium on speed and sensitivity. A common theme is for mechanical forces to be directed to specific ion channels, which can open rapidly and amplify the signal by permitting entry of large numbers of ions. Mechanical forces can also affect intracellular events in cells -- such as gene transcription --directly through the cell surface and cytoskeleton, although such mechanisms typically are not used for rapid sensory transduction.

3) Speed requires that mechanical forces be funneled directly to transduction channels, without intervening second messengers. Sensitivity requires that the maximal amount of stimulus energy be directed to the transduction channel. A general model --borrowed from worm touch receptors(1,2) and hair cells(3) --applies to many mechanosensory transduction systems: its key feature is a transduction channel that detects deflection of an external structure relative to an internal structure, such as the cytoskeleton. Such a deflection could take the form of deformation of the skin, oscillation of a hair cell's hair bundle, or vibration of a fly's bristle. Deflection changes tension in all elements of the system, and the transduction channel responds by changing its open probability.

4) In summary: Mechanotransduction -- a cell's conversion of a mechanical stimulus into an electrical signal -- reveals vital features of an organism's environment. From hair cells and skin mechanoreceptors in vertebrates, to bristle receptors in flies and touch receptors in worms, mechanically sensitive cells are essential in the life of an organism. The scarcity of these cells and the uniqueness of their transduction mechanisms have conspired to slow molecular characterization of the ensembles that carry out mechanotransduction. But recent progress in both invertebrates and vertebrates is beginning to reveal the identities of proteins essential for transduction.(4,5)

References (abridged):

1. Chalfie, M. A molecular model for mechanosensation in Caenorhabditis elegans. Biol. Bull. 192, 125-130 (1997)

2. Tavernarakis, N. & Driscoll, M. Molecular modeling of mechanotransduction in the nematode Caenorhabditis elegans. Annu. Rev. Physiol. 59, 659-689 (1997)

3. Hudspeth, A. J. Hair-bundle mechanics and a model for mechanoelectrical transduction by hair cells. Soc. Gen. Physiol. Ser. 47, 357-370 (1992)

4. Narins, P. M. & Lewis, E. R. The vertebrate ear as an exquisite seismic sensor. J. Acoust. Soc. Am. 76, 1384-1387 (1984)

5. Sukharev, S. I., Blount, P., Martinac, B., Blattner, F. R. & Kung, C. A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 368, 265-268 (1994)

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