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Pre-requisites Basic knowledge about plant growth and physiology
Objectives To make the students aware of the various types of growth movements seen in plants Keywords Darwin, circumnutation, phototropism, gravitropism, nastic movements
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Introduction Types of movements Circumnutations Tropic movements Phototropism Gravitropism Thigmotropism Nastic movements Thigmonasty and Nyctinasty Nastic movements in carnivorous plants Summary and conclusions References
PLANT MOVEMENTS
Introduction
Darwin in 1881 published a book called 'The Power of Movements in Plants,' in which movements are described as 'circumnutations' and the causes underlying such movements have been discussed as '.....increased growth, first on one side and then on another, is a secondary effect, and that the increased turgescence of the cells, together with the extensibility of their walls, is the primary cause of the movement of circumnutation.' Further, Darwin described how plants sense external stimuli such as light and gravity and are able to respond through directional growth- mediated movements. He mentioned that that perception of a stimulus and plant growth response do not necessarily happen in the same organ of the plant and hypothesized that a factor moves from the site of stimulus perception to the site of growth response. More than 100 years have passed since Darwin's observations and our understanding of the mechanisms underlying plant movements have also advanced. In this module we will study some of the advances made in our understanding of plant movements.
Types of movements Plant movements can be classified into two main categories, namely movements that are spontaneous and those that are induced in the presence of specific stimuli. Spontaneous
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movements are also called nutational (or circumnutational) movements, while the induced movements, consist of tropic movements if movement occurs in the direction of the stimulus, or nastic movements, if the movement is independent of the direction of stimulus.
Circumnutations These are autonomous movements mostly shown by young growing parts of a plant like hypocotyls, coleoptiles, shoots, tendrils, petioles etc. The tips of these organs outline a circular, elliptical or zigzag shape over time that may range from minutes to hours. Due to simultaneous elongation of the organ, circumnutations over a longer period are seen in the form of a helix.
a b
Fig 1. (a) Shoot tips of Phaseolus showing circumnutation. (b) A 3-D trace of circumnutations in shoot tips during day (lower part) and night (upper part) shows that they vary in amplitude, dependent on availability of light. (From: Stolarz, M., 2009)
Circumnutation movements are ultraradian movements, with a period of occurrence that is less than a day. These movements may change in amplitude, period or direction dependent on stimuli received from hormonal applications, morphological features, temperature, light or gravity. Hence external application of gibberellic acid led to an increase in amplitude of the circumnutations in Phaseolus shoots, while the dark period increased the circumnutation in sunflower seedlings (Fig 1). The period of circumnutations also varied from several minutes minutes to hours in Phaseolus epicotyls in a temperature-dependent manner. At lower temperature of 15oC, the period of circumnutation was 27 min, while at higher temperature of 27oC, low-amplitude oscillations were
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observed having a period of 12 min. Hence the period is seen to become shorter with an increase in temperature, with an increase in plant age or in response to a mechanical stimulus. Two types of circumnutation periods are generally recognized; short period nutations(20–60 min long) and long period nutations(1–8 hrs). Hence an ultraradian oscillator having a broad period range may be responsible for circumnutations. The direction of circumnutation may also differ, sometimes even in the same plant. For example in Arabidopsis seedlings, the short period nutations generally occur in a clockwise direction, while the long period nutations are counterclockwise. The change in direction of the circumnutation may be induced by stimuli like gravity or touch or they may be spontaneous. Circumnutations may therefore be considered as an outcome of growth and intercellular communication, which are regulated by an oscillator (a biological clock). A model for circumnutations ascribes the movements to asymmetric plasmodesmata development, due to which the symplastic transport of growth substances, especially auxins, is irregular. Besides this, asymmetric changes in turgor due to alterations in ion content may also be responsible for these movements. Changes in intracellular K+ and Ca2+ ion concentrations were shown to change the amplitude and period of circumnutation probably by altering the electric potential across the plasma membrane. The function of circumnutation is obvious in climbing plants, which seek mechanical support by nutations of the young shoots and tendrils. Circumnutations are also thought to stabilize hypocotyls during elongation and inhibition of circumnutations is thought to be the first response of plants subjected to stress (before growth ceases).
Tropic movements Tropic movements are not spontaneous like circumnutations, but are directional growth mediated movements in response to external stimuli like light, gravity, touch etc. They enable plants to perform better, for example by directing growth of shoots towards light, or directing root growth towards water. These movements are due to growth activity. The curvature movement is always directional, either towards the stimulus or away from the stimulus. Most of these are phytohormone mediated movements.
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Phototropism It is the directional curvature of organs in response to differential light and has been mainly observed in young shoots of seedlings. This response ensures that maximum light is available to the plant for photosynthesis. Roots are negatively phototropic, which means that they grow away from light and possibly meant to ensure that the roots grow into soil for water and nutrient absorption. The direction of phototropic curvature depends on the direction of light stimulus and occurs due to differential cell elongation rates, such that the side receiving less light show more elongation than the side facing the light source, hence causing bending of the stem towards light. This differential elongation was shown to arise due to differential accumulation of the plant hormone auxin on the two sides of the stem (Went and Thimann, 1937). This differential auxin accumulation is due to lateral movement of auxin from the illuminated side to the shaded side. PIN proteins, which are components of the auxin efflux carrier, play an important role in this lateral auxin transport.
Fig 2. Lateral movement of auxin due to directional exposure to blue light. (a) Differential auxin accumulation across stem during phototropic curvature (b) Lateral auxin transport in response to light exposure as in (a).
Hence directional light has to be perceived by the stem and the signal transduced to bring about lateral auxin transport. Phototropins are blue light photoreceptors and are coded for by two genes PHOT1 and PHOT2. The phototropins consist of two photosensory domains that show similarity to proteins responsive to light, oxygen or voltage (LOV domains) and a phosphorylating
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kinase domain. The chromophore is Flavin mononucleotide (FMN), which is bound non-covalently to the two LOV domains. In the presence of blue light of 447nm, FMN excitation brings about a covalent bond formation between FMN and the SH group of a cysteine present in the LOV2 domain to form the LOV 390 form. This brings about an activation of the kinase domain, which autophosphorylates the protein. LOV390 is the active form of phototropin which is reversed to LOV447 in dark.
Fig: 3(a) Phototropins consist of two photosensory (LOV) domains with FMN as the chromophore. (b) Activation of phototropin by blue light causes bond formation between FMN and the LOV protein, which activates the kinase leading to autophosphorylation. (From: Christie, 2007).
Phototropins are located in the plasma membrane in dark, but are rapidly internalized in the presence of blue light, indicating that the phosphorylated form of phototropins dissociates from the membrane. This leads to a reduction in blue light sensing ability of cells. Phototropins are thought to play a role in the formation of differential auxin gradients. Though the exact mechanism of transduction of the light signal to cause lateral auxin transport are not understood, a number of proteins involved in this process have been identified. For example phototropin is known to directly phosphorylate PKS4, which is a positive regulator of phototropism and NPH3, which is part of a Cullin3-based E3 ligase complex, SCFNPH3, that plays a role in relocalization of auxin transporters. ABCB19 is an ATP-binding cassette transporter that is also an auxin efflux protein like PIN and both are activated by phototropin, though the mechanism by which this happens is not known. In addition, phototropinregulates the activity of an H+ ATPase that acidifies the apoplast, leading to protonation of IAA and facilitating its entry into cells through the auxin import carrier AUX1. Phototropins are also known to bring about a reorientation of cortical
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microtubules upon phototropic stimulation and change cellulose deposition, leading to asymmetric growth. However the mechanism by which phototropins bring about asymmetric auxin distribution during phototropic responses requires further research.
Fig 4 (a) Variation in PHOT1 activity and auxin content in the stem during bending. (b) Activation of LOV domains L1 and L2 of phototropins by blue light leads to autophosphorylation as well as the activation of several proteins involved in auxin transport like PKS4, ABCB19, PIN, NPH3 and an H+ATPase. Phototropins also bring about reorientation of microtubules such that cellulose deposition alters, leading to asymmetrical growth.(From: Frankhauser and Christie, 2015).
Gravitropism Plants have a mechanism to sense gravity and respond to it. Hence growth of the radicle and plumule emerging from a germinating seed towards and away from soil respectively, occurs in response to the gravity vector and constitutes a tropic response called gravitropism. Shoots of a plant are said to exhibit a negative gravitropic while roots show a positive gravitropic response. In roots, specialized cells called statocytes present in columella tissue of root cap sense the gravity stimulus, while endodermal cells, which form the innermost cortical layer are the gravity sensing cells in shoots. These cells sense the direction of the gravity vector and this signal is transduced to other tissues, which show differential growth leading to curvature towards or away from the direction of gravity. In roots the curvature occurs in the elongation zone of the roots, while in shoots an interplay between light and gravity responses lead to curvature. The statocytes contain dense starch filled organelles called statoliths or amyloplasts. Their position in the statocyte is oriented in the direction of the gravity vector and when the root orientation is changed, the
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statoliths also get reoriented.
Fig 5. Gravitropic response of root. Reorientation of statoliths (amyloplasts) in specialized columella cells called statocytes occurs when the orientation of the root with respect to the direction of gravity vector changes.
The change in position of the statoliths within the statocytes initiates a gravitropic response in the root. Statoliths present in endodermal cells of the shoot also play a similar role in the antigravity orientation of the shoot. Characean algal species, which do not have amyloplasts were also seen to exhibit gravitropism. In these species sensing of the gravity vector was thought to arise by the differential weight exerted by the cytoplasm on top and bottom part of the plasma membrane (with reference to the gravity vector) and was called the protoplast -pressure hypothesis. Both, the statolith as well as protoplast pressure could constitute redundant mechanisms of sensing gravity in higher plants for eliciting a gravitropic response. Transmission of the gravity signal to the responding tissue is thought to involve the cytoskeleton of plant cells. According to the actin-tether hypothesis, the amyloplasts are thought to be physically associated with the actin microfilaments and reorientation of the former cause a tension in one part of the cytoskeleton and release of tension in the other part. This difference in tension is relayed to the plasma membrane and the signal is transduced further. An alternate hypothesis suggests that amyloplasts are not in contact with the cytoskeleton, but in the process of getting reoriented with respect to the gravity vector, they disrupt the actin microfilament network. Disruption of the cytoskeleton is thought to act as a signal that is transduced to the plasma membrane and leads to an increase in the cytoplasmic Ca2+ levels and a decrease in H+ levels. A change in H+ levels is thought to play a role in causing differential auxin distribution along
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the gravity vector, which causes bending or curvature of the root towards gravity. The gravity signal perceived by the root cap has to be transduced to the root elongation region for differential growth of the cells in the latter. The mechanism leading to asymmetric auxin distribution in the root elongation zone is thought to occur by regulation of the expression of genes involved in auxin transport (similar to those involved in the phototropic response). Localization of PIN proteins (auxin efflux) and AUX1 (auxin import) in the plasma membranes of columella or endodermis cells are thought to play a role in regulating auxin levels in the response tissue and bring about the differential growth response. Hence auxin is a key player in both, the gravitropic response and the phototropic response. Recent evidence suggests that gravitropic bending in roots is mediated by asymmetric nitric oxide (NO)accumulation that is triggered by auxin (Hu et al., 2005).
Thigmotropism This type of tropic movement is seen when tendrils contact an object and involves the coiling of the tendril around that object (directional and hence a tropic response). Differential growth that leads to coiling occurs due to osmotically driven contraction of the cells on the ventral side and expansion of cells on the dorsal side of the tendril. Like in the other tropic responses auxin plays a major role in bringing about differential growth. In the climber Bryoniadioica, the epidermal cells present at the tip of the tendril form tactile bleps, which are protrusions from the cell walls. Below these bleps the cytoplasm shows a unique arrangement of actin microfilaments and high levels of membrane associated Ca2+. These protrusions serve as mechano-receptors and signal transducers. In some tendrils, 5-6 layers of gelatinous type of fibres (G-fibres) exist between the vascular tissue and cortex, which can swell or desiccate rapidly due to their highly water absorptive polysaccharide composition. These fibres are important in bringing about rapid change in shape of cells during the coiling movements and also generate tensile strength in the tendril, which causes it to coil.
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c
Fig 6. Thigmotropic movement of a tendril showing that when the tendril touches a neighbouring stem (a), it starts contact coiling around it (b) due to differential growth. (c) Differential growth that leads to coiling is achieved by rapid contraction / expansion of xylan-rich gelatinous fibres present on the inner surface of the coiled tendril.
Nastic movements Thigmonasty and Nyctinasty Some plant movements that occur in response to a stimulus are independent of the direction of stimulus, unlike tropic movements. Such movements are called nastic movements and are seen in many leguminous as well as in carnivorous plants. The touch-me-not plant Mimosa pudica is known to fold its leaflets during night (nyctinastic movements) and also in response to touch (thigmonastic movements), the latter type of movement being faster than the former, which spreads to neighboring leaflets and leaves.
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Fig 7. Nyctinastic movements in Mimosa pudica that cause folding of leaflets in the absence of light.
Fig 8. Thigmonastic movements of leaflets in Mimosa pudica. Unfolded leaflets when touched (a) fold within in a few seconds (b). This movement is brought about by change in turgor in two regions of the pulvinus, composed of flexor and extensor cells respectively. In the unfolded state extensor cells are turgid (c) and during leaf folding they become flaccid (d).
Movement of the leaflets is controlled by an organ called pulvinus that is located at the base of leaflets and leaves. The pulvinus has two zones of motor cells arranged on the dorsal (extensor zone) and ventral (flexor zone) sides respectively. These motor cells can undergo a reversible change in turgor in response to touch or the absence of light. Turgor loss in extensor cells cause the leaflets to fold and the leaf to droop.
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Fig 9. Mechanism of folding of M.pudica leaves in response to touch. Motor cells in the pulvinus contain two types of vacuoles, namely the tannin-rich vacuole (TnV) and the aqueous vacuole (V). Both vacuoles change their shape and size in response to touch. Ion fluxes to and from the cells is shown. (From: Scorza and Dornelas, 2011)
The mechanism underlying these nastic movements involves the generation of an action potential due to membrane depolarisation caused at the site of touch, that is transmitted to the pulvinus. Membrane depolarisation triggers H+ influx due to the activity of an H+ ATPase, which generates an electrochemical gradient and brings about ion (K+, Cl-) efflux across the plasma membrane. Auxin has been shown to play a role in turgor regulation of the pulvinar cells by regulating activity of the H+ ATPase. Ca2+ levels are also reported to increase in the cytosol of the extensor cells and it is thought to play a role as a signaling factor for regulating ion channels and also regulating phosphorylation of actin microfibrils. Rearrangement of actin filaments has been observed during pulvinus movements. A decrease in ion concentration within the cell leads to rapid water loss from the extensor cells, probably facilitated by aquaporins or solute/water cotransporters. This leads to the folding of leaves in response to touch. Nyctinastic leaf movements also arise due to the opening and closing of ion channels in the pulvinar cells as mentioned for thigmonastic movements, but the triggering factors are light and circadian rhythm induced rather than action potential induced. Auxin, phytochrome as well as some circadian rhythm oscillators are thought to regulate nyctinastic movements. Leaf movement is also controlled by bioactive chemical substances known as leaf opening or leaf closing factors present on the surface of motor cells. Interconversion of these factors to their aglycone or
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glycoside forms by the activity of a β-glucosidase, which is under circadian control, is thought to regulate opening and closing of the leaves.
Nastic movements in carnivorous plants Carnivorous plants use leaf movements for trapping their prey. The modified leaves of Dionaea sp. (Venus fly trap) are divided into two parts, namely the upper and lower leaf. The upper leaf has two lobes, lined with spine like projections. When an insect touches the trigger hairs present in the centre of the upper leaf lobes, the mechanical sensitive ion-channels are activated and cause membrane depolarisation. This generates an action potential that activates the motor cells and cause leaves to snap shut within seconds. The upper and lower cell layers of the leaf have a turgor difference that is brought about by osmotic loss or gain of water in response to ion fluxes. This maintains the leaves in a curved form (open trap). On stimulation, this turgor difference is lost due to water movement between cells, which restores the cells to an equilibrium state and causes the trap to close. Besides mechanical stimulation, the traps are also seen to close in response to electrical stimulation.
Fig 10. Modified leaves of (a and c) Dionea (Venus fly trap) and (b and d) Drosera (Sundew) that show movements leading to prey capture.
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In Drosera (Sundew), glandular trichomes resembling tentacles are seen on the modified leaves used for capturing prey. An insect trapped in the tentacles is a mechanical stimulant that generates an action potential triggering leaf movement that leads to prey capture. This movement is in the form of rapid cell growth and is slower than that seen to occur due to osmotically driven water flux. Thigmonastic movements in carnivorous plants are brought about by rapid turgor changes or cell growth and auxins appears to play a key role in these movements.
Summary and Conclusions Plants show movements of various kinds, which are important for optimising resource availability and growth. For example, circumnutations and tropic movements help a seedling establish in the correct orientation in the soil and maximise water, nutrient and light uptake. Movements enable climbers to find support, so that they can grow taller and optimize light capture for photosynthesis, or carnivorous plants to capture their nitrogen rich prey. Some of these movements are slow (tropic movements) while others are rapid (thigmonastic movements). They are mostly based on differential growth brought about by turgor changes that lead to expansion or shrinkage of cells. Auxins are known to play an important role in regulating plant movements. Understanding the physiology of plant movements is central to our understanding of how plants respond to environmental stimuli. These non-muscular movements displayed by plants are also important in applications like biomimetic design in the field of engineering.
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