Download thigmo responses in plants and fungi1

American Journal of Botany 89(3): 375–382. 2002.
INVITED SPECIAL PAPER
THIGMO
RESPONSES IN PLANTS AND FUNGI1
MORDECAI J. JAFFE, A. CARL LEOPOLD,2
AND
RICHARD C. STAPLES
Boyce Thompson Institute, Cornell University, Tower Road, Ithaca, New York 14853 USA
Thigmo mechanisms are adaptations that permit a plant to alter growth rates, change morphology, produce tropisms, avoid barriers,
control germination, cling to supporting structures, infect a host plant, facilitate pollination, expedite the movement of pollen, spores,
or seeds, and capture prey. Through these varied functions, plant thigmo systems have evolved impressive controls of cell differentiation, localized growth rates, regulated synthesis of novel products, and some elegant traps and projectile systems. For most thigmo
events, there will be a dependence upon transmission of a signal from the cell wall through the plasmalemma and into the cytoplasm.
We propose the possible involvement of integrin-like proteins, Hechtian strands, and cytoskeletal structures as possible transduction
components. Many thigmo mechanisms may use some modification of the calcium/calmodulin signal transduction system, though the
details of transduction systems are still poorly understood. While transmission of thigmo signals to remote parts of a plant is associated
with the development of action potentials, hormones may also play a role. Thigmo mechanisms have facilitated an enormous array of
plant and fungal adaptations that make major contributions to their success despite their relatively sessile or immobile states.
Key words:
mechanosensor; sensing; thigmomorphogenesis; thigmotactic; thigmotropism.
The relative immobility of plants as compared with animals
has naturally provoked a dependence upon their ability to
sense and respond to subtle environmental signals. Among
these, the adaptations of plants to touch, i.e., thigmo responses,
have become an elaborate and often elegant series of mechanical signalling systems. Thigmo responses are found over the
entire range of the plant kingdom, from fungi to algae, mosses,
ferns, and higher plants. In this review we attempt to bring
together an assemblage of thigmo responses under four categories and then consider the mechanisms that may initiate
them.
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.
1
2
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.
THIGMOTACTIC, THIGMOMORPHOGENETIC, AND
THIGMOTROPISTIC RESPONSES
In many instances, a thigmo stimulus leads to changes in
plant movement. For example, swimming movements reverse
direction of the alga Euglena when it runs into an obstacle
(Jennings, 1906). 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
Manuscript received 21 August 2001; revision accepted 30 October 2001.
Author for reprint requests (e-mail: [email protected]).
375
376
AMERICAN JOURNAL
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
OF
BOTANY
[Vol. 89
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).
THIGMO SECRETIONS
Many plant adaptations to physical perturbations involve the
synthesis or secretion of adhesives. Examples among the fungi
are the spores of Magnaporthe, which respond to the sensing
of landing on a surface by secreting an adhesive that holds the
spore at the landing site while the spore germinates (Hamer et
al., 1988). 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).
THIGMO TRAPS
Insect traps occur principally in sunny, moist environments
of extreme nitrogen deficiency (Givnish et al., 1984), 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
March 2002]
JAFFE
ET AL.—THIGMO RESPONSES
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).
THIGMO PROJECTILES
A number of species in the plant kingdom have developed
thigmo-triggered projectiles. Mention has already been made
that Sphagnum spores are thrown in response to thigmo stimulation by rain. A mechanism reminiscent of the Haptoglossa
injection device has been developed by stinging nettles (Urtica). The stinging device is located in a series of glands
around the edges of the leaf with a sting mechanism inside
(Esau, 1965). 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 (Im-
377
patiens) 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).
NATURE OF THE THIGMO STIMULUS
The perturbation needed for thigmo stimuli varies considerably, although the range is frequently in the vicinity of 1 g
or less (Darwin, 1891; Simons, 1992). During the sensing of
leaf-surface irregularities by pathogenic fungi, a ridge of 0.2
mm 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 0.5mm 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
378
AMERICAN JOURNAL
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.
A PROPOSAL FOR A THIGMO RECEPTOR
MECHANISM
How is a touch stimulus to the cell wall transduced into
intracellular responses, and how may the signal bring about
responses at remote sites? Any thigmo event in plants and
fungi involves a perturbation at the cell wall. We know that
at least some thigmo signals are picked up through patches of
sensitized cells, in which the surfaces of exposed cell walls
are slightly corrugated (e.g., pea tendrils). In other instances
there are sensing hairs that serve as thigmo sensors (e.g., Utricularia, Dionaea) and in which the cell walls are presumably
bent by mechanical force (Lloyd, 1942; 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
OF
BOTANY
[Vol. 89
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 a-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 integrinlike 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 a-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 trans-
March 2002]
JAFFE
ET AL.—THIGMO RESPONSES
mission 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 Ca12 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 Ca12 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 Ca12 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 Ca12 may result from release of Ca12 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
379
Fig. 1. Proposed model of components of the thigmo transduction system
from cell wall into the cytoplasm. Pressure against the cell wall causes displacement of the plasma membrane via Hechtian strands and integrin-like
linkages, thus repositioning the microtubules. At the same time, ion channels
are opened, altering the intracellular Ca11 concentration and inducing action
potentials.
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.
LITERATURE CITED
AIST, J. R. 1977. Mechanically induced wall appositions of plant cells can
prevent penetration by a parasitic fungus. Science 197: 568–571.
ALLEN, R. F. 1923. A cytological study of infection of Baart and Kanred
380
AMERICAN JOURNAL
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, AND B. D.
KOHORN. 2001. WAKS: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Molecular Biology 47: 197–206.
ARGRAVES, W. S., S. SUZUKI, H. ARAI, K. THOMPSON, M. D. PIERSCHBACHER, AND E. RUOSLAHTI. 1995. Amino acid sequence of the human fibronectin receptor. Journal of Cell Biology 105: 1183–1190.
BACHEWICH, C., AND 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, AND G. ALIBERT. 1998.
RGD-mediated membrane-matrix adhesion triggers agarose-induced embryoid formation in sunflower protoplasts. Protoplasma 206: 143–151.
BERRIDGE, M. J., P. LIPP, AND M. D. BOOTMAN. 2000. The versatility and
universality of calcium signalling. Nature Reviews: Molecular Cell Biology 1: 11–21.
BÖGRE, L., W. LIGTERINK, E. HEBERLE-BORS, AND H. HIRT. 1996. Mechanosensors in plants. Nature 383: 489–490.
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., AND R. W. DAVIS. 1990. Rain-, Wind-, and touch-induced expression of calmodulin and calmodulin-related genes in arabidopsin. Cell
60: 357–364.
BRAUN, E. J., AND R. J. HOWARD. 1994. Adhesion of Cochliobolus heterostrophus conidia and germlings to leaves and artificial surfaces. Experimental Mycology 18: 211–220.
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.
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, AND M. H. GINSBERG. 2000. Integrins
and actin filaments: reciprocal regulation of cell adhesion and signaling.
Journal of Biological Chemistry 275: 22 607–22 610.
CANUT, H., A. CARRASCO, J. P. GALAUD, C. CASSAN, H. BOUYSSOU, N. VITA,
P. FERRARA, AND 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.
COOPS, H., AND 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.
CORRÊA, A., JR., AND H. C. HOCH. 1995. Identification of thigmoresponsive
loci for cell differentiation in Uromyces germlings. Protoplasma 186:
34–40.
CORRÊA, A., JR., R. C. STAPLES, AND H. C. HOCH. 1996. Inhibition of thigmostimulated cell differentiation with RGD-peptides in Uromyces germlings. Protoplasma 194: 91–102.
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., AND 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.
DENNISON, D. S., AND C. C. ROTH. 1967. Phycomyces sporangiophores: fungal stretch receptors. Science 156: 1386–1388.
DING, J. P., AND N. G. PICKARD. 1993. Mechanosensory calcium-selective
cation channels in epidermal cells. Plant Journal 3: 83–110.
DROBAK, B. K. 1993. Plant phosphoinosidides and intracellular signaling.
Plant Physiology 102: 705–709.
DYER, A. F. 1979. The experimental biology of ferns. Academic Press, New
York, New York, USA.
ERNER, Y., AND 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., AND 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.
OF
BOTANY
[Vol. 89
FINERAN, B. A. 1985. Glandular trichomes in Utricularia: review of their
structure and function. Israel Journal of Botany 34: 295–330.
GALAUD, J. P., V. LAVAL, M. CARRIERE, A. BARRE, H. CANUT, P. ROUGE,
AND 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, AND 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, AND 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, AND 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.
GARRILL, A., S. L. JACKSON, R. R. LEW, AND I. B. HEATH. 2001. Ion channel
activity and tip growth: tip-localized stretch-activated channels generate
an essential Ca21 gradient in the oomycete Saprolegnia ferax. Journal of
Cell Biology 60: 358–365.
GARRILL, A., R. R. LEW, AND I. B. HEATH. 1992. Stretch-activated Ca21 and
Ca21-activated K1 channels in the hyphal tip plasma membrane of the
oomycete Saprolegnia ferax. Journal of Cell Science 101: 721–730.
GILROY, S., N. D. READ, AND A. J. TREWAVAS. 1990. Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates
stomatal closure. Nature 346: 769–771.
GIVNISH, T. J., E. L. K. BURKHARDT, R. E. HAPPEL, AND 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.
GLASS, N. L., D. J. JACOBSON, AND P. K. T. SHIU. 2000. The genetics of
hyphal fusion and vegetative incompatibility in filamentous ascomycete
fungi. Annual Review of Genetics 34: 165–186.
GOW, N. A. R. 1994. Growth and guidance of the fungal hypha. Microbiology
140: 3193–3205.
GUS-MAYER, S., B. NATON, K. HAHLBROCK, AND 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, AND 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, AND E. A. ALLEN. 1993. Integrating microfabrication and biology. Circuits and Devices 9: 17–22.
HOCH, H. C., R. J. BOJKO, G. L. COMEAU, AND 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., AND R. C. STAPLES. 1987. Structural and chemical changes
among the rust fungi during appressorium development. Annual Review
of Phytopathology 25: 231–247.
HOCH, H. C., R. C. STAPLES, B. WHITEHEAD, J. COMEAU, AND 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, AND K. E. KENDRICK. 1995. Antigenic and functional conservation of an integrin I-domain in Saccharomyces cerevisiae. Biochemical and Molecular Medicine 55: 122–130.
HYNES, R. O. 1987. Integrins: a family of cell surface receptors. Cell 48:
549–554.
HYNES, R. O. 1992. Integrins: versatility, modulation, and signaling in cell
adhesion. Cell 69: 11–25.
HYNES, R. O. 1999. Cell adhesion: old and new questions. Trends in Cell
Biology 9: M33–M37.
HYNES, R. O., AND 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 me-
March 2002]
JAFFE
ET AL.—THIGMO RESPONSES
chanical 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., AND A. W. GALSTON. 1966. Physiological studies on plant
tendrils, I. Plant Physiology 41: 1014–1025.
JAFFE, M. J., AND 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, AND 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.
JAFFE, M. J., AND A. C. LEOPOLD. 1984. Callose deposition during gravitropism of Zea mays and Pisum sativum. Planta 161: 20–26.
JAFFE, M. J., AND L. LINEBERRY. 1988. Pithiness in plants. Israel Journal of
Botany 37: 93–106.
JELITTO, T. C., H. A. PAGE, AND 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.
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.
JONES, R. S., AND C. A. MITCHELL. 1989. Calcium ion involvement in growth
inhibition of mechanically stressed soybean Glycine max seedlings. Physiologia Plantarum 76: 598–602.
KAMINSKYJ, S. G. W., AND I. B. HEATH. 1994. Integrin and spectrin homologues, and cytoplasm-wall adhesion in tip growth. Journal of Cell Science 108: 849–856.
KIBA, A., M. SUGIMOTO, K. TOYODA, Y. ICHINOSE, T. YAMADA, AND 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, AND 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.
KNIGHT, M. R., S. M. SMITH, AND 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., AND B. E. S. GUNNING. 2000. A plasmolytic cycle: the
fate of cytoskeletal elements. Protoplasma 212: 174–183.
LAVAL, V., M. CHABANNES, M. CARRIÈRE, H. CANUT, A. BARRE, P. ROUGÉ,
R. PONT-LEZICA, AND J. GALAUD. 1999. A family of Arabidopsis plasma
membrane receptors presenting animal b-integrin domains. Biochimica
et Biophysica Acta 1435: 61–70.
LEE, D. L., P. C. VAUGHAN, AND 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, AND S.
GILROY. 1997. Cytoplasmic-free Ca21 in Arabidopsin roots changes in
response to touch but not gravity. Plant Physiology 114: 789–800.
LEVINA, N. N., R. R. LEW, AND I. B. HEATH. 2001. Cytoskeleton regulation
of ion channel distribution in the tip-growing organism Saprolegnia ferax. Journal of Cell Science 107: 127–134.
LLOYD, F. E. 1942. The carniverous plants. Ronald Press, New York, New
York, USA.
LOLLE, S. J., AND 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.
MAHESHWARI, R., A. C. HILDEBRANDT, AND 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.
381
MEIDELL, O. 1945. Notes on the pollination of Melampyrom pratense and
honeystealing. Bergens museums Aarbog Raekke 11.
MELLERSH, D. G., AND 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., AND R. S. QUATRANO. 1999. Isolation and characterization of a
cDNA clone from Arabidopsis thaliana with partial sequence similarity
to integrins. Gene 230: 33–40.
NICHOLSON, R. L., AND 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.
PICKARD, B. G. 1971. Action potentials resulting from mechanical stimulation
of pea epicotyls. Planta 7: 106–115.
PRESSMAN, E., M. HUBERMAN, B. ALONI, AND 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., AND 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, AND 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.
REUZEAU, C., J. G. MCNALLY, AND B. G. PICKARD. 1997. The endomembrane sheath: a key structure for understanding the plant cell? Protoplasma 200: 1–9.
RICCA, U. 1916. Soluzion d’un probleme de physiologie: la propagation de
stimulo nella Mimosa. Nuovo Giornale Botanico Italiano 23: 51–170.
ROBB, E. J., AND G. BARRON. 1982. Nature’s ballistic missile. Science 218:
1221–1222.
ROYLE, D. J., AND G. G. THOMAS. 1973. Factors affecting zoospore responses
towards stomata in hop downy mildew (Pseudoperonospora humuli) including some comparisons with grapevine downy mildew (Plasmopara
viticola). Physiological Plant Pathology 3: 405–417.
SANDERS, L. C., C. S. WANG, L. L. WALLING, AND E. M. LORD. 1991.
Homolog of the substrate adhesion molecule vitronectin in plants. Plant
Cell 3: 629–635.
SASTRY, S. K., AND A. F. HORWITZ. 1993. Integrin cytoplasmic domains:
mediators of cytoskeletal linkages and extra- and intracellular initiated
transmembrane signalling. Current Opinion in Cell Biology 5: 819–831.
SHAW, B. D., AND H. C. HOCH. 1999. The pycnidiospore of Phyllosticta
ampelicida: surface properties involved in substratum attachment and
germination. Mycological Research 103: 915–924.
SHAW, B. D., AND H. C. HOCH. 2000. Ca21 regulation of Phyllosticta ampelicida pycnidiospore germination and appressorium formation. Fungal
Genetics and Biology 31: 43–53.
SHOTWELL, M., AND M. J. JAFFE. 1979. Physiological studies on pea tendrils.
X. Characterization of the light activation on contact coiling as a blue
light trigger. Photochemistry and Photobiology 29: 1153.
SIBAOKA, T. 1966. Action potentials in plant organs. Symposium of the Society
of Experimental Biology 20: 165–184.
SIMONS, P. 1992. The action plant. Blackwell, Oxford, UK.
STANKOVIC, B., AND E. DAVIES. 1998. The wound response in tomato involves rapid growth and electrical responses, systemically up-regulated
transcription of proteinase inhibitor and calmodulin and down-regulated
translation. Plant and Cell Physiology 39: 268–274.
STAVES, M. P., R. WAYNE, AND A. C. LEOPOLD. 1992. Hydrostatic pressure
mimics gravitational pressure in characean cells. Protoplasma 168: 141–
152.
STRASBURGER, E. 1878. Wirkung des Lichtes und der Warme auf Schwarmssporen. Fischer, Jena, Germany.
TELEWSKI, F., AND M. J. JAFFE. 1986a. Thigmomorphogenesis: anatomical,
morphological and mechanical analysis of genetically different sibs of
Pinus taeda L. in response to mechanical perturbation. Physiologia Plantarum 66: 219–226.
TELEWSKI, F., AND M. J. JAFFE. 1986b. Thigmomorphogenesis: field and lab-
382
AMERICAN JOURNAL
oratory studies of Abies fraseri (Pursh) Poir. Physiologia Plantarum 66:
211–218.
TELEWSKI, F., AND M. J. JAFFE. 1986c. Thigmomorphogenesis: the role of
ethylene in the response of Pinus taeda L. and Abies fraseri (Porsh) Poir.
to mechanical perturbation. Physiologia Plantarum 66: 227–233.
TERHUNE, B. T., AND H. C. HOCH. 1993. Substrate hydrophobicity and adhesion of Uromyces urediospores and germlings. Experimental Mycology
17: 241–252.
TORIYAMA, H., AND M. J. JAFFE. 1972. Migration of calcium and its role in
the regulation of seismo nasty in the motor cell of Mimosa pudica D.
Plant Physiology 49: 72–81.
TREWAVAS, A., AND M. KNIGHT. 1994. Mechanical signaling, calcium and
plant form. Plant Molecular Biology 26: 1329–1341.
TRONCHET, A. 1964. Quelque aspects de la sensibilite de vrilles. ProcesVerbaux Memoirs de l’Academie des Sciences Belles Lettres, Bensancon
175: 23–39.
UMRATH, K. 1958. Beobachtungen an taglich mehrmals mechanische gereizter Neptunia plena. Berichte der Deutschen Botanischen Gesellschaft
Jahrgang 7: 315–320.
UMRATH, K., AND I. THALER. 1980. Initiation of leaf movements in Mimosa
OF
BOTANY
[Vol. 89
pudica and of bendings of Lupinus albus hypocotyls interpreted by liberation of the excitatory substance and of auxin. Phyton 20: 333–348.
VAN DER LUIT, A. H., C. OLIVARI, A. HALEY, M. R. KNIGHT, AND A. J.
TREWAVAS. 1999. Distinct calcium signaling pathways regulate calmodulin gene expression in tobacco. Plant Physiology 121: 705–714.
WAGNER, V. T., L. BRIAN, AND R. S. QUATRANO. 1992. Role of vitronectinlike molecules in embryo adhesion of Fucus. Proceedings of the National
Academy of Sciences, USA 89: 3644–3648.
WAYNE, R., M. P. STAVES, AND A. C. LEOPOLD. 1992. The contribution of
the extracellular matrix to gravisensing in characean cells. Journal of
Cell Science 101: 611–623.
WYATT, S. E., AND N. C. CARPITA. 1993. The plant cytoskeleton–cell-wall
continuum. Trends in Cell Biology 3: 413–417.
WYNN, W. K. 1976. Appressorium formation over stomates by the bean rust
fungus: response to a surface contact stimulus. Phytopathology 66: 136–
146.
YEE, G. H., AND R. O. HYNES. 1993. A novel, tissue-specific integrin subunit,
bv, expressed in the midgut of Drosophila melanogaster. Development
118: 845–858.
ZANDOMENI, K., AND P. SCHOPFER. 1994. Mechanosensory microtubule reorientation in the epidermis of maize coleoptiles subjected to bending
stress. Protoplasma 182: 96–101.