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Invited Special Paper |
Boyce Thompson Institute, Cornell University, Tower Road, Ithaca, New York 14853 USA
Received for publication August 21, 2001. Accepted for publication October 30, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONTHIGMOTACTIC,...THIGMO SECRETIONSTHIGMO TRAPSTHIGMO PROJECTILESNATURE OF THE THIGMO...A PROPOSAL FOR A...LITERATURE CITED |
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Key Words: mechanosensor • sensing • thigmomorphogenesis • thigmotactic • thigmotropism
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONTHIGMOTACTIC,...THIGMO SECRETIONSTHIGMO TRAPSTHIGMO PROJECTILESNATURE OF THE THIGMO...A PROPOSAL FOR A...LITERATURE CITED |
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A thigmo stimulus may be quite subtle. For example, in handling experimental plant materials, just the act of moving a potted plant from the greenhouse to the laboratory may expose the plant to sufficient mechanical perturbation to cause changes in the morphology and growth rate of the plant (Jaffe, 1985
). Indeed, moving the plant can result in inhibition of growth rate, and touching the plant can result both in alterations of phloem cell structure (Jaffe and Leopold, 1984
) and differentiation of stem pith (Jaffe and Lineberry, 1988
).
Responses to mechanical perturbation can occur with impressive rapidity; for example, touching the leaf of Mimosa will cause leaf folding beginning within 1 s (Jaffe, 1985
); disturbing the trigger hairs on a Venus flytrap leaf will cause the trap to close within 1 s; and touching the trigger hairs in a Utricularia bladder cause the trap to close within an estimated 0.01 s (Jaffe, 1985
; Simons, 1992
).
Although the initial thigmo stimulus is received by the cell wall, the magnitude of the deformation may be very slight indeed. For example, localized pressure can elicit the translocation of the nucleus and cytoplasm, the intracellular generation of reactive oxygen species, and the transcription of defense-related genes (Gus-Mayer et al., 1998
). Furthermore, these tiny perturbations can be transduced into enormous changes in morphology, growth rates, and metabolic products, as for example in thigmo growth and tropistic responses, thigmo secretions, thigmo traps, and thigmo projectiles as reviewed below.
We expected there to be commonalities among the thigmo responses with regard to perception, transduction, and response mechanisms. The evidence for such commonalties is scattered at the present time, but an overview of some repeating themes from relevant experimental studies may be helpful in developing a general scheme for thigmo-regulated mechanisms. We have undertaken this review to point out the commonalities and to offer at the end a unifying mechanism.
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THIGMOTACTIC, THIGMOMORPHOGENETIC, AND THIGMOTROPISTIC RESPONSES |
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TOPABSTRACTINTRODUCTIONTHIGMOTACTIC,...THIGMO SECRETIONSTHIGMO TRAPSTHIGMO PROJECTILESNATURE OF THE THIGMO...A PROPOSAL FOR A...LITERATURE CITED |
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). Similar movement adaptations occur with swimming Chilomonas and Cryptomonas cells (Nageli, 1860
) and in the motile spores of many algae (Strasburger, 1878
).
Changes in both growth rates and morphological differentiation, due to thigmomorphogenesis, are illustrated by thigmo responses of numerous fungi. The ridge pattern on the surface of a leaf can induce a directional orientation of mycelial growth (thigmotropism) (Johnson, 1934
; Hoch et al., 1987
). In another example, in certain species of the rust fungi, sensing the stomatal ridge will actually induce an alteration of cell differentiation (thigmomorphogenesis). Thus germ tube growth over a stomatal ridge can alter growth rates and induce appressorium differentiation in various species of rust fungi, as in Puccinia or Uromyces (Allen, 1923
; Wynn, 1976
), or bring about encystment of hop downy mildew zoospores (Deacon and Donaldson, 1993
). Again, in the bean rust fungus (Uromyces appendiculatus), the stimulus for appressorium differentiation is induced when the germ tube grows over a tiny stomatal ridge on the epidermis of the host plant, causing a termination of elongation of the sporeling germ tube, followed by activation of cell division and development of the appressorium (Allen, 1923
; Maheshwari, Hildebrandt, and Allen, 1967
). The mechanical nature of the thigmo stimulus is evident in the fact that cellular differentiation can be stimulated by contact of the germ tube with a plastic impression of the leaf stomatal surface. In some other cases, differentiation of zoospores at stomatal locations may also involve a cooperative action with some chemical signals emerging from the leaf stoma (Royle and Thomas, 1973
).
A dramatic example of thigmomorphogenesis is observed in the growth of a Monstera vine. On the ground, the seedling grows initially in a tropistic manner toward a dark object (skototropism); when it touches a tree, the thigmo stimulus changes from skototropic to phototropic, and it climbs the tree adhering to the tree's bark. At the same time the leaf form is thigmomorphogenetically altered from small nearly circular leaves to large finely divided leaves as it climbs the tree (Bussman, 1939
).
Thigmomorphogenesis is involved in numerous types of adaptation to stress. These include adaptation to wind, drought, frost, and infection (Aist, 1977
; Pressman et al., 1983
; Telewski and Jaffe, 1986a, b
; Gilroy, Read, and Trewavas, 1990
; Coops and Van der Velde, 1996
). However, thigmomorphogenetic responses may involve different regulatory systems. For example, suppressed elongation in response to touch may involve an inhibition of auxin effects in Bryonia dioica (Boyer, 1967
), or by an increase in abscisic acid content in Phaseolus vulgaris (Erner and Jaffe, 1982
), or a biosynthesis of ethylene in Pinus taeda (Telewski and Jaffe, 1986c
).
Some of the most common thigmo responses are the tropistic responses. Thigmotropism most often involves unilateral growth inhibitions (Jaffe, 1976b
), as in the enhancement of tropistic bending of styles, flowers, or petals toward visiting pollinators (Jaffe, Gibson, and Biro, 1977
; Faegri and van der Pijl, 1979
). The flowers of the orchid Melampyrum sense vibrations of a visiting bee and respond by releasing a shower of pollen (Meidell, 1945
). Likewise, in the flowers of Pedicularis, a visiting bee may shake the stamens by wing vibrations and collect the falling pollen on its back (Macior, 1969
).
The thigmonastic coiling of tendrils following a mechanical perturbation occurs in at least two phases in pea, an initial rapid nastic bending, which is predominantly a hydraulic-driven contraction on the ventral side of the tendril (Jaffe and Galston, 1968
), and a subsequent growth on the dorsal side (Jaffe and Galston, 1966
). It has been suggested that the sensing of the touch by tendrils may be achieved by small tactile protuberances on the ventral side that have particularly thin epidermal walls (Tronchet, 1964
).
The thigmonastic twining of the stems or roots of strangler figs (Ficus costaricensis) deserves mention here. The seedling starts as an epiphyte on a host tree. As it develops, the root of the fig plant winds down around the target tree, and it imposes an increasing pressure on the tree through the differentiation of increasing amounts of cortical tissue on the side away from the target tree. As this pressure against the tree increases, the twining fig ultimately kills the host tree and the fig becomes free-standing (Putz and Holbrook, 1989
).
Perhaps the most heralded thigmo responses are the nastic leaf-folding movements in response to touch. A mechanical perturbation of Mimosa pudica leaves results in the dramatic folding and lowering of the leaves. Such nastic leaf movements occur also in Cassia sensitivum and some species of Oxalis (Umrath, 1958
). While this thigmo response is very dramatic, its physiological function is very much in doubt. The leaf-folding movements in sensitive plants have both structural and physiological similarities to the diurnal folding of leaves that occurs commonly in legumes. Both movements involve hydraulic shifts in glandular organs, the pulvini, at the base of leaves or leaflets. Structurally, the folding movement involves water loss from one side of the pulvinus, and closing of the leaf, a constriction in the vascular strand serving as a hinge (Esau, 1965
). The thigmo stimulation of Mimosa leaf movement involves an action potential, which occurs first in the stimulated leaflet and then advances to each of the other pulvini above and below it (Sibaoka, 1966
; Pickard, 1971
). The movement of the signal has been suggested to involve the movement of a water-soluble substance (Ricca, 1916
), which could be hormonal (Umrath and Thaler, 1980
).
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THIGMO SECRETIONS |
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TOPABSTRACTINTRODUCTIONTHIGMOTACTIC,...THIGMO SECRETIONSTHIGMO TRAPSTHIGMO PROJECTILESNATURE OF THE THIGMO...A PROPOSAL FOR A...LITERATURE CITED |
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). In some instances the secretion of the adhesive is necessary for spore germination (Shaw and Hoch, 1999
). A variant of this requirement occurs in spores of Chochliobolus, which secrete adhesive only after experiencing both the contact and a wetting (Braun and Howard, 1994
). A parallel instance is the secretion of vitronectin-like molecules by Fucus zygotes in attaching to a solid surface (Wagner, Brian, and Quatrano, 1992
).
In higher plants, the secretion of adhesives provides for attachment to trees or rocks by epiphytes, lichens, and some climbing vines and roots. The attachment of vines to walls involves the formation of stunted roots, which become holdfasts, secreting strong adhesive substances (Darwin, 1881
; Dyer, 1979
). Such adhesive, vitronectin-like proteins are formed at areas where the cell wall contacts a solid surface.
Proteinaceous adhesives are involved in the sticking of pollen to the stigma of some flowers (Lolle and Pruitt, 1999
). When compatible pollen touches the stigma of flowers of bean and several other legumes, and flowers of Arabidopsis, the stigma secretes an adhesive substance that binds the pollen. The stigma then creates a channel of lipidic substances that facilitate the growth of the pollen tube (Sanders et al., 1991
; Lolle and Pruitt, 1999
). Another instance of thigmo-secretory activity is the case of formation of mucilage on the leaf-hairs of insect-trapping plants such as sundews and butterworts. As an insect enters the leaf-trap, its movements constitute the thigmo stimulus causing the trap to produce more mucilage, increasing the immobilization of the insect (Lloyd, 1942
).
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THIGMO TRAPS |
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TOPABSTRACTINTRODUCTIONTHIGMOTACTIC,...THIGMO SECRETIONSTHIGMO TRAPSTHIGMO PROJECTILESNATURE OF THE THIGMO...A PROPOSAL FOR A...LITERATURE CITED |
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), such as in sphagnum bogs where the acidic pH limits the degradation of organic matter. Among carnivorous plants there are five types of thigmo traps. The sundews (Drosera) form rosettes of green or red spoon-shaped leaves with tentacles on the upper surface. Each tentacle secretes globules of mucilage, which glisten in the sunshine and attract small insects. The thigmo stimulus generated by an insect landing and struggling with the sticky mucilage results in several responses: a bending of the tentacles toward the captured prey, an increased secretion of mucilage, a closure movement of the leaf, and subsequently the secretion of digesting enzymes by the leaf (Lloyd, 1942
).
The butterworts (Pinguicula) generate an insect trap involving the formation of two types of glandular tentacles: stalked glands that produce mucilage and sessile glands that produce digestive juices. The thigmo stimulus of an insect landing results in a gradual rolling of the leaf serving to engulf the insect as it is digested (Darwin, 1881
; Lloyd, 1942
). An impressive adaptation of the butterworts is that during the winter season when insects would not be expected to visit, the secretions do not occur, even if given a thigmo stimulation (M. J. Jaffe, personal observation).
The venus flytrap (Dionaea) operates on a different basis. Instead of secreting mucilage, the photosynthetic leaves develop a trap involving a row of spines on each margin and a cluster of trigger-hairs at the center of the leaf. Thigmo stimulation by a landing insect or spider causes a very rapid closure of the two lobes of the leaf; the spines then restrain the prey while digestive juices are secreted. An impressive feature of this thigmo trap is the rapidity of the trap closure, viz. shutting like a castle's portcullis, it closes within a second (Brown, 1916
).
Traps are not restricted to land plants. The aquatic Aldrovanda is a tiny aquatic version of the trap mechanism of Dionaea (Darwin, 1881
; Lloyd, 1942
). The hydrophyte bladderwort (Utricularia) presents an even more rapid trapping action. This aquatic plant forms a bladder, with long guide-hairs adjoining the small entrance. Swimming daphnia or crustaceans can be steered by the guide hairs into the entrance, where trigger hairs sense their presence. The thigmo stimulus on the trigger activates a rapid sucking of water (along with the prey) into the trap by an expanding action of the bladder, after which a trapdoor closes over the entrance. The rapidity of this trap action is impressive, estimated at <0.01 sec (Fineran, 1985
).
The soil fungus Haptoglossa has evolved another trap system. The fungus forms a trap as a circle of three cells, arranged in the manner of a lasso. Attracted by chemical pheromones, a nematode enters and touches the trap, and the three cells exercise a very rapid hydraulic swelling, trapping the prey in the lasso. After the trap has been sprung, movements by the nematode create a further thigmo stimulus for the actual firing of a needle-like gland that injects the fungus into the prey, starting the digestive process (Robb and Barron, 1982
). The fungus then grows further into the nematode body and completes the digestion of the trapped nematode (Lee, Vaughan, and Durschner-Pelz, 1992
). In at least some cases, the chemical sensing of the nematodes stimulates the fungus to form more traps (Robb and Barron, 1982
).
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THIGMO PROJECTILES |
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TOPABSTRACTINTRODUCTIONTHIGMOTACTIC,...THIGMO SECRETIONSTHIGMO TRAPSTHIGMO PROJECTILESNATURE OF THE THIGMO...A PROPOSAL FOR A...LITERATURE CITED |
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). The gland contains a pouch of toxin, a mixture of histamine and acetylcholine (Feldberg, 1950
), and a fine hollow needle, which points outward with a calcified seal at the extended end. Upon being touched, the calcified seal breaks off, and the bared needle readily penetrates the intruder's skin and introduces the sting, serving to repel herbivores or wandering humans.
A more dynamic projectile action is found in numerous ferns and higher plants that actually throw their spores or seeds into the air. The well-known jewel-weed or touch-me-not (Impatiens) is a common example. As the fruit matures, the outer shell develops lines of cell separation, which, when combined with a partial drying of the tissues, constitute a poised spring. Thigmo stimulation (touching) will cause the fruit to explode, and the seeds will be thrown for a meter or more from the mother plant. This type of seed projection is very common, occurring for example in Geranium, manioc, and in broom and gorse bushes (Simons, 1992
).
Exploding flowers are another type of thigmo system. In many legumes, such as alfalfa (Medicago), when a flower is being visited by a pollinating insect, its entry spreads some of the flower parts apart, causing the flower to "explode," suddenly exposing its anthers or stigmata (Faegri and van der Pijl, 1979
).
A more aggressive strategy is taken by some orchids such as the twayblade (Listera). As a bee enters the flower or hovers close to the flower, the thigmo perturbation of wing vibration causes the flower to fling a pollinium at the bee, along with a quick-drying adhesive that attaches the pollinium to the face of the bee (Faegri and van der Pijl, 1979
).
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NATURE OF THE THIGMO STIMULUS |
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TOPABSTRACTINTRODUCTIONTHIGMOTACTIC,...THIGMO SECRETIONSTHIGMO TRAPSTHIGMO PROJECTILESNATURE OF THE THIGMO...A PROPOSAL FOR A...LITERATURE CITED |
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; Simons, 1992
). During the sensing of leaf-surface irregularities by pathogenic fungi, a ridge of 0.2 µm is sufficient to reorient the growth direction of a urediospore germ tube (Hoch and Staples, 1987
; Hoch et al., 1993
). Phycomyces sporangiophores are stimulated to bend by a 0.5-µm movement (Dennison and Roth, 1967
). For a higher plant such as Drosera, the magnitude of touch perturbation needed for response is estimated to be 
0.3 mg (Darwin, 1881
). Such very low thresholds suggest that there must be sensitive systems to substantially amplify the signal. Environmental features may also be involved because the pea tendril is sensitive to pH, such that exposing it to a low-pH solution will enhance responsiveness to touch (Jaffe and Galston, 1966
), and blue light is a corequisite for tendril coiling (Jaffe and Galston, 1966
; Shotwell and Jaffe, 1979
).
For fungal spores, the hardness of the landing site influences the response in terms of secretion and/or germination. For example, anthracnose fungi are able to form appressoria on a hard glass surface, and spores of several species of anthracnose fungi germinate poorly or not at all when suspended in liquids. There is often a requirement also for the surface to be hydrophobic (Nicholson and Epstein, 1991
; Terhune and Hoch, 1993
; Hoch, Bojko, Comeau et al., 1995
). Thus hard surfaces such as polystyrene, Teflon, polycarbonate, collodion, or glass treated with organic silanes (compounds of carbon and silicone) will all serve to stimulate germination.
It is common for calcium ions to play a role in the mediation of thigmo signals (Hoch and Staples, 1987
; van der Luit et al., 1999
). For example, pretreatment of the surface with calcium ions induces both attachment and germination of pycnidiospores of Phyllosticta ampelicida (Shaw and Hoch, 2000
), and Royle and Thomas (1973)
have suggested that calcium signals are involved in the encystment of the downy mildew fungi.
Some higher plants have developed receptors for thigmo signals. For example, the pea tendril has a specialized surface on the concave side, and when one draws a fiber across the sensing pad, one can feel that there are ridges present (M. J. Jaffe, personal observation). Grape tendrils have specialized epidermal cells in which the surface cell walls are very thin, a quality that may increase the sensitivity for thigmo stimuli. The tendrils of Eccromonocarpus have surface cells that bulge out hemispherically, and Tronchet (1964)
has claimed to be able to see plasma membrane invagination in these surface cells after thigmo stimulation.
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A PROPOSAL FOR A THIGMO RECEPTOR MECHANISM |
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TOPABSTRACTINTRODUCTIONTHIGMOTACTIC,...THIGMO SECRETIONSTHIGMO TRAPSTHIGMO PROJECTILESNATURE OF THE THIGMO...A PROPOSAL FOR A...LITERATURE CITED |
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; Simons, 1992
). In the thigmo systems of filamentous fungi, the hyphal growing points usually serve as sensors (Hoch et al., 1987
; Gow, 1994
; Corrêa and Hoch, 1995
; Jelitto, Page, and Read, 1995
). Whereas perception of thigmo stimuli can be presumed to originate at the exposed cell wall, a basic uncertainty is how the signal is transmitted to the interior of a cell.
Peptides containing the integrin-binding sequence, RGD (Arg-Gly-Asp), applied to walled cells interfere with a wide range of physiological events including gravisensing (Wayne, Staves, and Leopold, 1992
), development of sunflower protoplasts (Barthou et al., 1998
), expression of plant defense responses during host penetration by a rust fungus (Mellersh and Heath, 2001
), and accumulation of an antimicrobial phytoalexin in pea epicotyls (Kiba et al., 1998
). In a preliminary experiment, RGD peptides were found to retard the rate of leaflet closure involved by touch in Mimosa pedica to about one-third of the control rate (M. J. Jaffe, personal observation). Among the fungi, treatment with RGD peptides interferes with the association of the cell wall and plasmalemma in Saprolegnia ferax (Kaminskyj and Heath, 1994
), and in the bean rust fungus, Uromyces appendiculatus, RGD peptides interfere with development of the appressorium (Corrêa, Staples, and Hoch, 1996
). As demonstrated for onion and Arabidopsis (Canut et al., 1998
; Laval et al., 1999
; Nagpal and Quatrano, 1999
), bean (Garcia-Gómez et al., 2000
), Saprolegnia ferax (Kaminskyj and Heath, 1994
), and Candida albicans (Gale et al., 1996
), proteins that bind the RGD sequence are located in the plasmalemma of both fungi and higher plants. Such evidence strongly suggests a role for integrin-like proteins in the communication of a thigmo signal from the wall to the protoplasm.
Knowledge of integrins in animal cells is extensive now, and integrins have been recognized as a widely expressed family of cell surface adhesion receptors since 1987 (Hynes, 1987
). These proteins bind RGD sequences. They transfer external signals from the extra-cellular matrix (ECM), across the plasmalemma to the cytoplasm, and have important roles in cell-cell adhesion events (Hynes, 1992
). Recent reviews include those by Hynes (1999)
, Hynes and Zhao (2000)
, and Calderwood, Shattil, and Ginsberg (2000)
.
Proteins apparently related to the integrins have been demonstrated in the plasma membranes of fungi, e.g., Candida albicans (Gale et al., 1996
) and Saprolegnia ferax (Kaminskyj and Heath, 1994
), and higher plants, e.g., Arabidopsis (Canut et al., 1998
; Galaud et al., 1998
). Indeed, genes have been cloned from Saccharomyces cerevisiae (Hostetter et al., 1995
), Candida albicans (Gale et al., 1996
), and Arabidopsis thaliana (Galaud et al., 1998
; Laval et al., 1999
; Nagpal and Quatrano, 1999
) that have partial sequence similarity to the animal integrins.
Animal integrins mediate signalling as well as anchorage (Hynes, 1992
; Sastry and Horwitz, 1993
), and in the fungus Saprolegnia ferax, the distribution of an integrin-like protein correlates with stretch-activated calcium channels (Garrill, Lew, and Heath, 1992
; Garrill et al., 2001
; Levina, Lew, and Heath, 2001
). Channel function (Garrill et al., 2001
) and an integrin–extracellular matrix interaction (Bachewich and Heath, 1993
) are both required for growth in Saprolegnia, suggesting that they may be interdependent. In characean internode cells of the alga Chara, stretch-activated calcium channels and an integrin-like protein are co-distributed, both are required for gravisensing (Wayne, Staves, and Leopold, 1992
; Staves, Wayne, and Leopold, 1992
), and again the signal transduction chain linking the cell wall to the plasmalemma of the cells apparently consists of integrin-like proteins. These numerous reports of integrin-like proteins being involved in stretch regulation of calcium channels may well relate to the transduction of thigmo events.
Despite the apparent presence of integrin-like proteins in the plasmalemma of some fungi and higher plants, the exact structure of these RGD-binding proteins in plants may differ from that of the animal integrins. The latter are responsible for communication with an entirely different kind of extracellular matrix than the rigid cell wall typical of plants and fungi. The integrin-like protein, Int1p, from Candida albicans has limited sequence similarity to the 
-integrins (Gale et al., 1998
), and the sequence of an Arabidopsis protein deduced from a cDNA clone (Laval et al., 1999
) had restricted similarity to integrin-like proteins from Drosophila (Yee and Hynes, 1993
) and humans (Argraves et al., 1995
). It seems quite possible that the thigmo receptor proteins of fungi and higher plants may belong to a family of signal receptors that are quite different in structure from the animal integrins, but which share the common feature of binding and responding to RGD ligands. Indeed, the genes -Int1, responsible for adhesion in C. albicans (Gale et al., 1996
), and AtELP1, a member of a multigenic family composed of at least six water-deficit-response genes in Arabidopsis (Laval, Chabannes, Carrière et al., 1999
), are plasma membrane receptors containing domains specific to animal integrins (Laval et al., 1999
). However, they are otherwise quite different in sequence from typical animal integrin genes.
Recently, Lang-Pauluzzi and Gunning (2000)
have described the existence of Hechtian strands, i.e., strands linking the cell wall to the plasmalemma. These strands, which become visible during plasmolysis (Hecht, 1912
), can contain actin microfilaments and microtubules (Lang-Pauluzzi and Gunning, 2000
). They have been proposed to have a role in cell–cell communication and signal transduction routes in plant cells (Zandomeni and Schopfer, 1994
; Reuzeau et al., 1997
; Reuzeau, McNally, and Pickard, 1997
; Canut et al., 1998
; Glass, Jacobson, and Shiu, 2000
), a proposal supported by the fact that exposure of walled cells to RGD-containing peptides causes a loss of Hechtian strands accompanied by loss of resistance to pathogens (Canut et al., 1998
; Kiba et al., 1998
; Mellersh and Heath, 2001
) and loss of the signal transmission pathway between the cell wall and plasmalemma (Kiba et al., 1998
). Both integrins and Hechtian strands are considered to be linked to cortical microtubules, which in turn can regulate numerous cellular functions including ATPase, metabolism, and growth itself (Nick, 1999
).
A number of proteins have been shown to bind to both cell wall and plasma membrane and have the potential to signal directly between the compartments. These proteins include the arabinogalactans, cellulose synthases, and wall-associated kinases (Anderson et al., 2001
). However, it has not been shown yet that RGD sequences can disrupt the association of the proteins with either the cell wall or plasmalemma as is true for Hechtian strands. It should be noted, however, that wall-associated kinases are induced by pathogen infection and wounding and have roles in cell growth and cell wall expansion (Anderson et al., 2001
).
The general occurrence of changes in calcium ions with signal stimulations has led to the appellation of Ca+2 as a signalling molecule in plants (Toriyama and Jaffe, 1972
; Trewavas and Knight, 1994
; Berridge, Lipp, and Bootman, 2000
). The role of calcium in thigmo responses has been widely noted and indicates a common role for calcium in the transduction of the signal in the cytoplasm or nucleus (Toriyama and Jaffe, 1972
; Trewavas and Knight, 1994
; Legué et al., 1997
). The intimate connection between Ca+2 and calmodulin has been noted in many instances, and Braam and Davis (1990)
have shown that three of four genes involved in thigmo responses in Arabidopsis that serve as calmodulin regulators are quickly induced by touch. The calmodulin involved in the thigmo response is principally located in the nucleus (van der Luit et al., 1999
). Indeed, inhibitors of calmodulin have been shown to suppress thigmo responses (Jones and Mitchell, 1989
), an effect that may be related to the dissociation or rearrangement of microtubules (Braam and Davis, 1990
).
The changes in cytoplasmic Ca+2 occur in some instances through opening of calcium channels in the plasma membrane (Ding and Pickard, 1993
), or in some instances the rise in cytoplasmic Ca+2 may result from release of Ca+2 from intracellular pools (Knight, Smith, and Trewavas, 1992
; Kluesener et al., 1995
), perhaps via phosphoinositides released at the plasma membrane (Drobak, 1993
). A signalling propagation mechanism that is common to all thigmo systems involves changes in electrical resistance associated with development of an electrical potential across the plasmalemma (Sibaoka, 1966
; Pickard, 1971
; Jaffe, 1976a
). The participation of an electrical potential in thigmo responses is most vividly evidenced in the leaf movement of Mimosa, where a perturbation leads to an action potential that moves from leaf to leaf, spreading the thigmo response systemically. The rise time for the bioelectrical potential relates to the particular thigmo response. Thus the carnivorous and sensitive plants may show an electric potential rise time averaging 0.9 sec, whereas the rise time for thigmomorphogenetic changes averages 25 sec (Jaffe, 1976a
). Action potentials change the ionic balance in the cytoplasm, have been shown to induce some gene transcription (Stankovic and Davies, 1998
), and have the capability of altering a broad range of cellular activities.
Mitogen-activated protein (MAP) kinases may also be involved in mechanosensing in plants. Bögre et al. (1996)
have reported that a protein, p44MMK4, was activated within 1 min after alfalfa leaves were mechanically stimulated for 2 sec. The activation was transient and disappeared after 10 min. The authors suggested that activation of the MMK4 pathway must be one of the cell's immediate responses to shaking, perhaps in conjunction with rapid fluxes of calcium ions (Braam and Davis, 1990
).
So, a tentative model for thigmo responses (Fig. 1) would begin with a perturbation of the cell wall followed by signal transduction to the plasmalemma via Hechtian strands involving integrin-like proteins that can be disrupted by the RGD motif. These proteins appear to form a continuum from the cell wall to the cytoskeleton (Wyatt and Carpita, 1993
). Clearly, thigmo signals received at the cell wall are transmitted through the plasma membrane, probably opening cation- and stretch-activated channels and may involve MAP kinases. The perturbation may thus alter both membrane and cytoskeletal structures and lead finally to alterations in gene expression. Whether the RGD-sensitive Hectian strands serve the function visualized here for the reception of touch signals and whether they would be the only means of communication that enable response to thigmo signals (Kohorn, 2000
) will remain ambiguous until a proper experimental foundation has been provided.
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FOOTNOTES |
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2 Author for reprint requests (ACL9{at}cornell.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONTHIGMOTACTIC,...THIGMO SECRETIONSTHIGMO TRAPSTHIGMO PROJECTILESNATURE OF THE THIGMO...A PROPOSAL FOR A...LITERATURE CITED |
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Allen R. F. 1923 A cytological study of infection of Baart and Kanred wheats by Puccinia graminis tritici. Journal of Agricultural Research 26: 571-604
Anderson C. M. T. A. Wagner M. Perret Z.-H. He D. He B. D. Kohorn 2001 WAKS: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Molecular Biology 47: 197-206[CrossRef][ISI][Medline]
Argraves W. S. S. Suzuki H. Arai K. Thompson M. D. Pierschbacher E. Ruoslahti 1995 Amino acid sequence of the human fibronectin receptor. Journal of Cell Biology 105: 1183-1190
Bachewich C. I. B. Heath 1993 Effects of cell wall-cytoskeleton linkage inhibition on growth and development in Saprolegnia ferax. Inoculum 44: 25.
Barthou H. M. Petitprez C. Brière A. Souvré G. Alibert 1998 RGD-mediated membrane-matrix adhesion triggers agarose-induced embryoid formation in sunflower protoplasts. Protoplasma 206: 143-151[CrossRef][ISI]
Berridge M. J. P. Lipp M. D. Bootman 2000 The versatility and universality of calcium signalling. Nature Reviews: Molecular Cell Biology 1: 11-21[CrossRef][ISI][Medline]
Bögre L. W. Ligterink E. Heberle-Bors H. Hirt 1996 Mechanosensors in plants. Nature 383: 489-490[CrossRef][Medline]
Boyer N. 1967 Modifications de la croissance de la tige de Bryone (Bryonia dioica) a la suite d'irritations tactiles. Comptes Rendus de l'Academie des Sciences (Paris) 264: 2114-2117
Braam J. R. W. Davis 1990 Rain-, Wind-, and touch-induced expression of calmodulin and calmodulin-related genes in arabidopsin. Cell 60: 357-364[CrossRef][ISI][Medline]
Braun E. J. R. J. Howard 1994 Adhesion of Cochliobolus heterostrophus conidia and germlings to leaves and artificial surfaces. Experimental Mycology 18: 211-220[CrossRef][ISI]
Brown W. H. 1916 The mechanism of movement and the duration of the effects of stimulation in the leaves of Dionaea. American Journal of Botany 3: 68-90[CrossRef][ISI]
Bussman K. 1939 Untersuchen uber die induktion der dorsiventralitat bei den farnprotallien. Jahrbucher für wissenschaftliche botanik 87: 565-624
Calderwood D. A. S. J. Shattil M. H. Ginsberg 2000 Integrins and actin filaments: reciprocal regulation of cell adhesion and signaling. Journal of Biological Chemistry 275: 22607-22610
Canut H. A. Carrasco J. P. Galaud C. Cassan H. Bouyssou N. Vita P. Ferrara L. R. Pont 1998 High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant Journal 16: 63-71[CrossRef][ISI][Medline]
Coops H. G. van der Velde 1996 Effects of waves on halophyte stands: mechanical characteristics of stems of Phragmites australis and Scirpus lacustris. Aquatic Botany 53: 175-185[CrossRef]
Corrêa A., Jr. H. C. Hoch 1995 Identification of thigmoresponsive loci for cell differentiation in Uromyces germlings. Protoplasma 186: 34-40[CrossRef][ISI]
Corrêa A., Jr. R. C. Staples H. C. Hoch 1996 Inhibition of thigmostimulated cell differentiation with RGD-peptides in Uromyces germlings. Protoplasma 194: 91-102[CrossRef][ISI]
Darwin C. 1881 The power of movement in plants. D. Appleton, New York, New York, USA
Darwin C. 1891 The movement and habits of climbing plants. John Murray, London, UK
Deacon J. W. S. P. Donaldson 1993 Molecular recognition in the homing responses of zoosporic fungi, with special reference to Pythium and Phytophthora. Mycological Research 97: 1153-1171[ISI]
Dennison D. S. C. C. Roth 1967 Phycomyces sporangiophores: fungal stretch receptors. Science 156: 1386-1388
Ding J. P. N. G. Pickard 1993 Mechanosensory calcium-selective cation channels in epidermal cells. Plant Journal 3: 83-110[CrossRef][ISI][Medline]
Drobak B. K. 1993 Plant phosphoinosidides and intracellular signaling. Plant Physiology 102: 705-709[CrossRef][ISI][Medline]
Dyer A. F. 1979 The experimental biology of ferns. Academic Press, New York, New York, USA
Erner Y. M. J. Jaffe 1982 Thigmomorphogenesis: the involvement of auxin and abscisic acid in growth retardation due to mechanical perturbation. Plant and Cell Physiology 23: 935-941
Esau K. 1965 Plant anatomy. John Wiley, New York, New York, USA
Faegri K. L. van der Pijl 1979 The principles of pollination ecology. Pergamon, Oxford, UK
Feldberg W. 1950 The mechanism of the sting of common nettle. British Scientific News 3: 745-747
Fineran B. A. 1985 Glandular trichomes in Utricularia: review of their structure and function. Israel Journal of Botany 34: 295-330[ISI]
Galaud J. P. V. Laval M. Carriere A. Barre H. Canut P. Rouge R. Pont-Lezica 1998 Osmotic stress activated expression of an arabidopsis plasma membrane-associated protein: sequence and predicted secondary structure. Biochimica et Biophysica Acta 1341: 79-86
Gale C. D. Finkel N.-J. Tao M. Meinke M. McClellan J. Olson K. Kendrick M. Hostetter 1996 Cloning and expression of a gene encoding an integrin-like protein in Candida albicans. Proceedings of the National Academy of Sciences, USA 93: 357-361
Gale C. A. C. M. Bendel M. McClellan M. Hauser J. M. Becker J. Berman M. K. Hostetter 1998 Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, Int1. Science 279: 1355-1358
Garcia-Gómez B. I. F. Campos M. Hernández A. A. Covarrubias 2000 Two bean cell wall proteins more abundant during water deficit are high in proline and interact with a plasma membrane protein. Plant Journal 22: 277-288[CrossRef][ISI][Medline]
Garrill A. S. L. Jackson R. R. Lew I. B. Heath 2001 Ion channel activity and tip growth: tip-localized stretch-activated channels generate an essential Ca2+ gradient in the oomycete Saprolegnia ferax. Journal of Cell Biology 60: 358-365
Garrill A. R. R. Lew I. B. Heath 1992 Stretch-activated Ca2+ and Ca2+-activated K+ channels in the hyphal tip plasma membrane of the oomycete Saprolegnia ferax. Journal of Cell Science 101: 721-730
Gilroy S. N. D. Read A. J. Trewavas 1990 Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature 346: 769-771[CrossRef][Medline]
Givnish T. J. E. L. K. Burkhardt R. E. Happel J. D. Weintraub 1984 Carnivory in the bromeliad Brocchinia reducta with a cost benefit model for the general restriction of carnivorous plants to sunny moist nutrient-poor habitats. American Naturalist 124: 479-497[CrossRef][ISI]
Glass N. L. D. J. Jacobson P. K. T. Shiu 2000 The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annual Review of Genetics 34: 165-186[CrossRef][ISI][Medline]
Gow N. A. R. 1994 Growth and guidance of the fungal hypha. Microbiology 140: 3193-3205[ISI][Medline]
Gus-Mayer S. B. Naton K. Hahlbrock E. Schmelzer 1998 Local mechanical stimulation induces components of the pathogen defense response in parsley. Proceedings of the National Academy of Sciences, USA 95: 8398-8403
Hamer J. E. R. J. Howard F. G. Chumley B. Valent 1988 A mechanism for surface attachment in spores of a plant pathogenic fungus. Science 239: 288-290
Hecht K. 1912 Studien über den Vorgang der Plasmolyse. Beitrage zür Biologie der Pflanzen 11: 133-189
Hoch H. C. R. J. Bojko G. L. Comeau E. A. Allen 1993 Integrating microfabrication and biology. Circuits and Devices 9: 17-22
Hoch H. C. R. J. Bojko G. L. Comeau D. A. Lilienfeld 1995 Microfabricated surfaces in signaling for cell growth and differentiation in fungi. In H. C. Hoch, L. W. Jelinski, and H. Craighead [eds.], Nanofabrication and biosystems: integrating materials science, engineering, and biology, 315–334. Cambridge University Press, Cambridge, UK
Hoch H. C. R. C. Staples 1987 Structural and chemical changes among the rust fungi during appressorium development. Annual Review of Phytopathology 25: 231-247[CrossRef][ISI]
Hoch H. C. R. C. Staples B. Whitehead J. Comeau E. D. Wolf 1987 Signaling for growth orientation and cell differentiation by surface topography in Uromyces. Science 235: 1659-1662
Hostetter M. K. N.-J. Tao C. Gale D. J. Herman M. McClellan R. L. Sharp K. E. Kendrick 1995 Antigenic and functional conservation of an integrin I-domain in Saccharomyces cerevisiae. Biochemical and Molecular Medicine 55: 122-130[CrossRef][ISI][Medline]
Hynes R. O. 1987 Integrins: a family of cell surface receptors. Cell 48: 549-554[CrossRef][ISI][Medline]
Hynes R. O. 1992 Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69: 11-25[CrossRef][ISI][Medline]
Hynes R. O. 1999 Cell adhesion: old and new questions. Trends in Cell Biology 9: M33-M37[CrossRef][ISI][Medline]
Hynes R. O. Q. Zhao 2000 The evolution of cell adhesion. Journal of Cell Biology 150: F89-F95
Jaffe M. J. 1976a Thigmo morphogenesis electrical resistance and mechanical correlates of the early events of growth retardation due to mechanical stimulation in beans. Zeitschrift für Pflanzenphysiologie 78: 24-32
Jaffe M. J. 1976b Thigmomorphogenesis: characterization of the response of beans to mechanical stimulation. Zeitschrift für Pflanzenphysiologie 77: 437-453
Jaffe M. J. 1985 Wind and other mechanical effects in the development of plants. Encyclopedia of Plant Physiology 11: 444-484
Jaffe M. J. A. W. Galston 1966 Physiological studies on plant tendrils, I. Plant Physiology 41: 1014-1025
Jaffe M. J. A. W. Galston 1968 Physiological studies on pea tendrils. V. Membrane changes and water movement associated with contact coiling. Plant Physiology 43: 537-542
Jaffe M. J. C. Gibson R. Biro 1977 Physiological studies of mechanically stimulated motor responses of flower parts. Part 1. Characterization of the thigmo tropic stamens of Portulaca grandiflora. Botanical Gazette 138: 438-447[CrossRef]
Jaffe M. J. A. C. Leopold 1984 Callose deposition during gravitropism of Zea mays and Pisum sativum. Planta 161: 20-26[CrossRef][ISI][Medline]
Jaffe M. J. L. Lineberry 1988 Pithiness in plants. Israel Journal of Botany 37: 93-106[ISI]
Jelitto T. C. H. A. Page N. D. Read 1995 Role of external signals in regulating the pre-penetration phase of infection by the rice blast fungus, Magnaporthe grisea. Planta 194: 471-477[CrossRef][ISI]
Jennings H. S. 1906 Behavior of the lower organisms. Columbia University Press, New York, New York, USA
Johnson T. 1934 A tropic response in germ tubes of urediospores of Puccinia graminis tritici. Phytopathology 24: 80-82[ISI]
Jones R. S. C. A. Mitchell 1989 Calcium ion involvement in growth inhibition of mechanically stressed soybean Glycine max seedlings. Physiologia Plantarum 76: 598-602[CrossRef][Medline]
Kaminskyj S. G. W. I. B. Heath 1994 Integrin and spectrin homologues, and cytoplasm-wall adhesion in tip growth. Journal of Cell Science 108: 849-856[Abstract]
Kiba A. M. Sugimoto K. Toyoda Y. Ichinose T. Yamada T. Shiraishi 1998 Interaction between cell wall and plasma membrane via RGD motif is implicated in plant defense responses. Plant and Cell Physiology 39: 1245-1249
Kluesener B. G. Boheim H. Liss J. Engelberth E. W. Weiler 1995 Gadolinium-sensitive, voltage-dependent calcium release channels in the endoplasmic reticulum of a higher plant mechanoreceptor organ. EMBO Journal 14: 2708-2714[ISI][Medline]
Knight M. R. S. M. Smith A. J. Trewavas 1992 Wind-induced plant motion immediately increases cytosolic calcium. Proceedings of the National Academy of Sciences, USA 89: 4967-4971
Kohorn B. D. 2000 Plasma membrane–cell wall contacts. Plant Physiology 124: 31-38
Lang-Pauluzzi I. B. E. S. Gunning 2000 A plasmolytic cycle: the fate of cytoskeletal elements. Protoplasma 212: 174-183[CrossRef][ISI]
Laval V. M. Chabannes M. Carrière H. Canut A. Barre P. Rougé R. Pont-Lezica J. Galaud 1999 A family of Arabidopsis plasma membrane receptors presenting animal ß-integrin domains. Biochimica et Biophysica Acta 1435: 61-70[CrossRef][Medline]
Lee D. L. P. C. Vaughan U. Durschner-Pelz 1992 Ultrastructure of the thallus and secondary spore of the nematophagous fungus Haptoglossa heterospora oomycetes. Journal of Invertebrate Pathology 59: 33-39
Legué V. E. Blancaflor C. Wymer G. Perbal D. Fantin S. Gilroy 1997 Cytoplasmic-free Ca2+ in Arabidopsin roots changes in response to touch but not gravity. Plant Physiology 114: 789-800[Abstract]
Levina N. N. R. R. Lew I. B. Heath 2001 Cytoskeleton regulation of ion channel distribution in the tip-growing organism Saprolegnia ferax. Journal of Cell Science 107: 127-134[Abstract]
Lloyd F. E. 1942 The carniverous plants. Ronald Press, New York, New York, USA
Lolle S. J. R. E. Pruitt 1999 Epidermal cell interactions. Trends in Plant Science 3: 14-17
Macior L. W. 1969 Pollination adaptation in Pedicularis lanceolata. American Journal of Botany 56: 853-859[CrossRef][ISI]
Maheshwari R. A. C. Hildebrandt P. J. Allen 1967 The cytology of infection structure development in uredospore germ tubes of Uromyces phaseoli var. typica (Pers.) Wint. Canadian Journal of Botany 45: 447-450
Meidell O. 1945 Notes on the pollination of Melampyrom pratense and honeystealing. Bergens museums Aarbog Raekke 11
Mellersh D. G. M. C. Heath 2001 Plasma membrane-cell wall adhesion is required for expression of plant defense responses during fungal penetration. Plant Cell 13: 413-424
Nageli C. 1860 Ortsbewegungen der Pflanzenzellen un ihr Thiele. Naegeli's Beitrage zur Wissenschafliche Botanik 2: 59-108
Nagpal P. R. S. Quatrano 1999 Isolation and characterization of a cDNA clone from Arabidopsis thaliana with partial sequence similarity to integrins. Gene 230: 33-40[CrossRef][ISI][Medline]
Nicholson R. L. L. Epstein 1991 Adhesion of fungi to the plant surface: prerequisite for pathogenesis. In G. T. Cole and H. C. Hoch [eds.], The fungal spore and disease initiation in plants and animals, 3–23. Plenum, New York, New York, USA
Nick P. 1999 Signals, motors, morphogenesis—the cytoskeleton in plant development. Plant Biology 1: 169-179[CrossRef][ISI]
Pickard B. G. 1971 Action potentials resulting from mechanical stimulation of pea epicotyls. Planta 7: 106-115
Pressman E. M. Huberman B. Aloni M. J. Jaffe 1983 Thigmomorphogenesis: the effect of mechanical perturbation and ethrel on stem pithiness in tomato (Lycopersicon esculentum (Mill.)) plants. Annals of Botany 52: 93-100
Putz F. E. N. M. Holbrook 1989 Strangler fig rooting habits and nutrient status. American Journal of Botany 76: 7781-7788
Reuzeau C. K. W. Doolittle J. G. McNally B. G. Pickard 1997 Covisualisation in living onion cells of putative integrin, putative spectrin, actin, putative intermediate filaments and other proteins at the cell membrane and in an endomembranous sheath. Protoplasma 199: 173-197
