Mechanism of the Pulvinus-Driven Leaf Movement: An Overview.

Leaf movement is a manifestation of plant response to the changing internal and external environment, aiming to optimize plant growth and development. Leaf movement is usually driven by a specialized motor organ, the pulvinus, and this movement is associated with different changes in volume and expansion on the two sides of the pulvinus. Blue light, auxin, GA, H+-ATPase, K+, Cl-, Ca2+, actin, and aquaporin collectively influence the changes in water flux in the tissue of the extensor and flexor of the pulvinus to establish a turgor pressure difference, thereby controlling leaf movement. However, how these factors regulate the multicellular motility of the pulvinus tissues in a species remains obscure. In addition, model plants such as Medicago truncatula, Mimosa pudica, and Samanea saman have been used to study pulvinus-driven leaf movement, showing a similarity in their pulvinus movement mechanisms. In this review, we summarize past research findings from the three model plants, and using Medicago truncatula as an example, suggest that genes regulating pulvinus movement are also involved in regulating plant growth and development. We also propose a model in which the variation of ion flux and water flux are critical steps to pulvinus movement and highlight questions for future research.

A touchy subject: Ca2+ signaling during leaf movements in Mimosa.

Mimosa pudica, the sensitive plant, responds to stimuli such as touch and wounding with leaf movements that propagate throughout the plant. The motion is driven by changes in the turgor of specialized cells in a set of motor organs called pulvinae. By imaging cellular Ca2+ levels as the wave of movement propagates through the leaf, Hagihara and colleagues now show that Ca2+ signals precede and predict the pulvinar movements. These results provide compelling support for a model where Mimosa uses a Ca2+-related response system to trigger its leaf movements. These researchers then used CRISPR to delete a critical genetic regulator of pulvinar development, producing plants with immobile leaves. These plants experienced more herbivory than wild type, suggesting that the Ca2+-triggered leaf movements are an adaptation to deter herbivory.

Calcium-mediated rapid movements defend against herbivorous insects in Mimosa pudica.

Animals possess specialized systems, e.g., neuromuscular systems, to sense the environment and then move their bodies quickly in response. Mimosa pudica, the sensitive plant, moves its leaves within seconds in response to external stimuli; e.g., touch or wounding. However, neither the plant-wide signaling network that triggers these rapid movements nor the physiological roles of the movements themselves have been determined. Here by simultaneous recording of cytosolic Ca2+ and electrical signals, we show that rapid changes in Ca2+ coupled with action and variation potentials trigger rapid movements in wounded M. pudica. Furthermore, pharmacological manipulation of cytosolic Ca2+ dynamics and CRISPR-Cas9 genome editing technology revealed that an immotile M. pudica is more vulnerable to attacks by herbivorous insects. Our findings provide evidence that rapid movements based on propagating Ca2+ and electrical signals protect this plant from insect attacks.

Feedback-controlled hydrogels with homeostatic oscillations and dissipative signal transduction.

Driving systems out of equilibrium under feedback control is characteristic for living systems, where homeostasis and dissipative signal transduction facilitate complex responses. This feature not only inspires dissipative dynamic functionalities in synthetic systems but also poses great challenges in designing novel pathways. Here we report feedback-controlled systems comprising two coupled hydrogels driven by constant light, where the system can be tuned to undergo stable homeostatic self-oscillations or damped steady states of temperature. We demonstrate that stable temperature oscillations can be utilized for dynamic colours and cargo transport, whereas damped steady states enable signal transduction pathways. Here mechanical triggers cause temperature changes that lead to responses such as bending motions inspired by the single-touch mechanoresponse in Mimosa pudica and the frequency-gated snapping motion inspired by the plant arithmetic in the Venus flytrap. The proposed concepts suggest generalizable feedback pathways for dissipative dynamic materials and interactive soft robotics.

Mechanosensitive ion channels contribute to mechanically evoked rapid leaflet movement in Mimosa pudica.

Mechanoperception, the ability to perceive and respond to mechanical stimuli, is a common and fundamental property of all forms of life. Vascular plants such as Mimosa pudica use this function to protect themselves against herbivory. The mechanical stimulus caused by a landing insect triggers a rapid closing of the leaflets that drives the potential pest away. While this thigmonastic movement is caused by ion fluxes accompanied by a rapid change of volume in the pulvini, the mechanism responsible for the detection of the mechanical stimulus remains poorly understood. Here, we examined the role of mechanosensitive ion channels in the first step of this evolutionarily conserved defense mechanism: the mechanically evoked closing of the leaflet. Our results demonstrate that the key site of mechanosensation in the Mimosa leaflets is the pulvinule, which expresses a stretch-activated chloride-permeable mechanosensitive ion channel. Blocking these channels partially prevents the closure of the leaflets following mechanical stimulation. These results demonstrate a direct relation between the activity of mechanosensitive ion channels and a central defense mechanism of M. pudica.

Gaussian-preserved, non-volatile shape morphing in three-dimensional microstructures for dual-functional electronic devices.

Motile plant structures such as Mimosa pudica leaves, Impatiens glandulifera seedpods, and Dionaea muscipula leaves exhibit fast nastic movements in a few seconds or less. This motion is stimuli-independent mechanical movement following theorema egregium rules. Artificial analogs of tropistic motion in plants are exemplified by shape-morphing systems, which are characterized by high functional robustness and resilience for creating 3D structures. However, all shape-morphing systems developed so far rely exclusively on continuous external stimuli and result in slow response. Here, we report a Gaussian-preserved shape-morphing system to realize ultrafast shape morphing and non-volatile reconfiguration. Relying on the Gaussian-preserved rules, the transformation can be triggered by mechanical or thermal stimuli within a microsecond. Moreover, as localized energy minima are encountered during shape morphing, non-volatile configuration is preserved by geometrically enhanced rigidity. Using this system, we demonstrate a suite of electronic devices that are reconfigurable, and therefore, expand functional diversification.

Bio-chemo-electro-mechanical modelling of the rapid movement of Mimosa pudica.

A remarkable feature of Mimosa pudica is its ability to deform in response to certain external stimuli. Here, a two-dimensional transient bio-chemo-electro-mechanical model of the rapid movement of the main pulvinus of Mimosa pudica is developed. Based on the laws of mass and momentum conservation, poroelasticity, and representative volume elements, a novel fluid pressure equation is proposed to characterize the cell elasticity. Experiments were conducted to measure the time and amplitude of the rapid movement. After examinations with the published experiments, it is confirmed that the model can predict well the ionic concentrations, petiole bending angle, and membrane potential. The simulation analysis of the biophysical properties provides insights to biomechanics: the hydrostatic pressure in the lowest extensor decreases from 0.35 to 0.05 MPa at t = 0.00 to 3.00 s; fluid pressure increases from 0.00 to 0.11 MPa at t = 0.00 to 0.14 s; and the peak bending angle increases from 57.0° to 70.9° when the reflection coefficient is assigned as 0.10 to 0.20 in the model. The results highlight the biochemical actuation mechanism of the Mimosa pudica movement, and they confirm the importance of ionic and water transports for causing changes in osmotic and hydrostatic pressures.

Communication in Plants: Comparison of Multiple Action Potential and Mechanosensitive Signals With Experiments.

Both action potentials and mechanosensitive signalling are an important communication mechanisms in plants. Considering an information-theoretic framework, this paper explores the effective range of multiple action potentials for a long chain of cells (i.e., up to 100) in different configurations, and introduces the study of multiple mechanosensitive activation signals (generated due to a mechanical stimulus) in plants. For both these signals, we find that the mutual information per cell and information propagation speed tends to increase up to a certain number of receiver cells. However, as the number of cells increase beyond 10 to 12, the mutual information per cell starts to decrease. To validate our model and results, we include an experimental verification of the theoretical model, using a PhytlSigns biosignal amplifier, allowing us to measure the magnitude of the voltage associated with the multiple AP's and mechanosensitive activation signals induced by different stimulus in plants. Experimental data is used to calculate the mutual information and information propagation speed, which is compared with corresponding numerical results. Since these signals are used for a variety of important tasks within the plant, understanding them may lead to new bioengineering methods for plants.

Insect-damaged Arabidopsis moves like wounded Mimosa pudica.

Slow wave potentials (SWPs) are damage-induced electrical signals which, based on experiments in which organs are burned, have been linked to rapid increases in leaf or stem thickness. The possibility that pressure surges in injured xylem underlie these events has been evoked frequently. We sought evidence for insect feeding-induced positive pressure changes in the petioles of Arabidopsis thaliana Instead, we found that petiole surfaces of leaves distal to insect-feeding sites subsided. We also found that insect damage induced longer-duration downward leaf movements in undamaged leaves. The transient petiole deformations were contemporary with and dependent on the SWP. We then investigated if mutants that affect the xylem, which has been implicated in SWP transmission, might modify SWP architecture. irregular xylem mutants strongly affected SWP velocity and kinetics and, in parallel, restructured insect damage-induced petiole deformations. Together, with force change measurements on the primary vein, the results suggest that extravascular water fluxes accompany the SWP. Moreover, petiole deformations in Arabidopsis mimic parts of the spectacular distal leaf collapse phase seen in wounded Mimosa pudica We genetically link electrical signals to organ movement and deformation and suggest an evolutionary origin of the large leaf movements seen in wounded Mimosa.

Characteristic early membrane effects induced by tryptophan in pulvinar motor cells.

Tryptophan at concentrations higher than 0.1 mM, triggered characteristic early physiological effects such as rapid (within 5 min) dose-dependent membrane hyperpolarization in Mimosa pudica motor cells and modification of the time course of the spontaneous proton efflux monitored in the incubation medium of pulvinar tissues. The rapid modifications of the leaf turgor-mediated movements seen on the primary pulvini of M. pudica following a shock and on Cassia fasciculata leaflets during a transition from light to darkness indicate that tryptophan disturbed the ionic migrations involved in the electrophysiological events and in the osmocontractile reaction of the motor cells. These reactions were specific to tryptophan compared to those induced by serine and 5-hydroxytryptophan. The tryptophan mode of action cannot be linked to a direct modification of the plasma membrane H+-ATPase activity as monitored on purified pulvinar plasma membrane vesicles. The tryptophan metabolism-linked products tryptamine and indole also inhibited the motile reactions, activated in a continuous manner the H+ secretion of pulvinar tissues and showed properties of a protonophore and an ATPase activity inhibitor on plasma membrane vesicles, respectively. The specific behavior of tryptophan in the reaction studies here is discussed in light of the previously reported action of phytohormones.

ACC deaminase plays a major role in Pseudomonas fluorescens YsS6 ability to promote the nodulation of Alpha- and Betaproteobacteria rhizobial strains.

Ethylene acts as a major regulator of the nodulation process of leguminous plants. Several rhizobial strains possess the ability to modulate plant ethylene levels through the expression of the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase; however, rhizobia present low enzymatic activities. One possible alternative to this problem resides on the use of free-living bacteria, such as Pseudomonas, presenting high levels of ACC deaminase activity that may be used as adjuvants in the nodulation process by decreasing inhibitory ethylene levels. Nevertheless, not much is understood about the specific role of ACC deaminase in the possible role of free-living bacteria as nodulation adjuvants. Therefore, this work aims to study the effect of ACC deaminase in the plant growth-promoting bacterium, Pseudomonas fluorescens YsS6, ability to facilitate alpha- and beta-rhizobia nodulation. The ACC deaminase-producing P. fluorescens YsS6 and its ACC deaminase mutant were used in co-inoculation assays to evaluate their impact in the nodulation process of alpha- (Rhizobium tropici CIAT899) and beta-rhizobia (Cupriavidus taiwanensis STM894) representatives, in Phaseolus vulgaris and Mimosa pudica plants, respectively. The results obtained indicate that the wild-type P. fluorescens YsS6, but not its mutant defective in ACC deaminase production, increase the nodulation abilities of both alpha- and beta-rhizobia, resulting in an increased leguminous plant growth. Moreover, this is the first report of the positive effect of free-living bacteria in the nodulation process of beta-rhizobia. The modulation of inhibitory ethylene levels by free-living ACC deaminase-producing bacteria plays an important role in facilitating the nodulation process of alpha- and beta-rhizobia.

Communication and Information Theory of Single Action Potential Signals in Plants.

Many plants, such as Mimosa pudica (the "sensitive plant"), employ electrochemical signals known as action potentials (APs) for rapid intercellular communication. In this paper, we consider a reaction-diffusion model of individual AP signals to analyze APs from a communication- and information-theoretic perspective. We use concepts from molecular communication to explain the underlying process of information transfer in a plant for a single AP pulse that is shared with one or more receiver cells. We also use the chemical Langevin equation to accommodate the deterministic as well as stochastic component of the system. Finally, we present an information-theoretic analysis of single action potentials, obtaining achievable information rates for these signals. We show that, in general, the presence of an AP signal can increase the mutual information and information propagation speed among neighboring cells with receivers in different settings.

A nurse plant benefits from facilitative interactions through mycorrhizae.

Plant facilitation promotes coexistence by maintaining differences in the regeneration niche because some nurse species recruit under arid conditions, whereas facilitated species recruit under more mesic conditions. In one Mexican community, 95% of species recruit through facilitation; Mimosa luisana being a keystone nurse for many of them. M. luisana individuals manifest greater fitness when growing in association with their facilitated plants than when growing in isolation. This observation suggests that nurses also benefit from their facilitated plants, a benefit thought to be mediated by mycorrhizal fungi. Under field conditions, we experimentally tested whether mycorrhizal fungi mediate the increased fitness that M. luisana experiences when growing in association with its facilitated plants. We applied fungicide to the soil for nurse plants growing alone and growing in association with their facilitated plants in order to reduce the mycorrhizal colonisation of roots. We then assessed the quantity and quality of seed production of M. luisana in four treatments (isolated-control, isolated-fungicide, associated-control and associated-fungicide). Fungicide application reduced the percentage root length colonised by mycorrhizae and reduced fitness of M. luisana when growing in association with their facilitated plants but not when growing in isolation. This reduction was reflected in the total number of seeds, number of seeds per pod, seed mass and seed viability. These results suggest that nurses benefit from the presence of their facilitated plants through links established by mycorrhizae, indicating that both plants and belowground mutualistic communities are all part of one system, coexisting by means of intrinsically linked interactions.

Photosynthetic opportunity cost and energetic cost of a rapid leaf closure behavior in Mimosa pudica.

PREMISE OF THE STUDY: The rapid leaf movement of Mimosa pudica is expected to be costly because of energetic trade-offs with other processes such as growth and reproduction. Here, we assess the photosynthetic opportunity cost and energetic cost of the unique leaf closing behavior of M. pudica. METHODS: In the greenhouse, we employed novel touch-stimulation machines to expose plants to one of three treatments: (1) untouched control plants; (2) plants touch-stimulated to close their leaves during the day to incur energetic costs associated with leaf movement and reduced photosynthesis; (3) plants touched at night to assess the effects of touch alone. M. pudica is nyctinastic and closes its leaves at night; thus, touching at night does not impart additional costs. We directly assessed costs by comparing physical traits. Leaf re-opening response was measured to assess the potential for plant behavioral plasticity to impact photosynthetic opportunity costs. KEY RESULTS: The cost of rapid leaf closure behavior was expressed as a 47% reduction in reproductive biomass accounting for the effect of touch. Touch itself changed physical traits such as biomass, with touched plants being generally bigger. Plants touched at night re-opened their leaflets 26% quicker than plants touched during the day. CONCLUSIONS: We reason that the reproductive allocation costs incurred by M. pudica can be attributed to a combination of photosynthetic opportunity cost and the energetic cost associated with increased stimulation of leaf movement and that behavioral plasticity has the potential to alter photosynthetic opportunity costs.

Cysteine: A multifaceted amino acid involved in signaling, plant resistance and antifungal development.

Early effects induced by cysteine were monitored using the model of Mimosa pudica pulvinar cells. Rapid dose-dependent membrane depolarization (within seconds) and modification of proton secretion (within minutes) were triggered at cysteine concentrations higher than 0.1 mM. These effects did not result from a modification of the plasma membrane H+-ATPase activity nor from a protonophore effect as shown by assays on plasma membrane vesicles isolated from pulvinar tissues. In a 0.5-10 mM range, cysteine inhibited the ion-driven turgor-mediated seismonastic reaction of Mimosa pudica primary pulvini and the dark-induced movement of Cassia fasciculata leaflets. At concentrations higher than 1 mM, it induced a long-lasting leaflet necrosis dependent on the concentration and treatment duration. Electron microscopy showed that cysteine induced important damage in the nucleus, mitochondria, endoplasmic reticulum and Golgi of the M. pudica motor cell. Cysteine inhibited in a concentration-dependent manner, from 0.5 to 20 mM, both the mycelial growth and the spore germination of the fungal pathogens Phaeomoniella chlamydospora and Phaeoacremonium minimum implicated in esca disease of grapevines. Using [35S] cysteine, we showed that the amino acid was absorbed following leaf spraying, translocated from leaves to other parts of grapevine cuttings and accumulated within trunks and roots. Therefore, cysteine showed relevant properties to be a candidate able to control fungal diseases either by acting as an early signal directing plant host reaction or/and by acting directly on fungal development.

Anaesthetics stop diverse plant organ movements, affect endocytic vesicle recycling and ROS homeostasis, and block action potentials in Venus flytraps.

Background and Aims: Anaesthesia for medical purposes was introduced in the 19th century. However, the physiological mode of anaesthetic drug actions on the nervous system remains unclear. One of the remaining questions is how these different compounds, with no structural similarities and even chemically inert elements such as the noble gas xenon, act as anaesthetic agents inducing loss of consciousness. The main goal here was to determine if anaesthetics affect the same or similar processes in plants as in animals and humans. Methods: A single-lens reflex camera was used to follow organ movements in plants before, during and after recovery from exposure to diverse anaesthetics. Confocal microscopy was used to analyse endocytic vesicle trafficking. Electrical signals were recorded using a surface AgCl electrode. Key Results: Mimosa leaves, pea tendrils, Venus flytraps and sundew traps all lost both their autonomous and touch-induced movements after exposure to anaesthetics. In Venus flytrap, this was shown to be due to the loss of action potentials under diethyl ether anaesthesia. The same concentration of diethyl ether immobilized pea tendrils. Anaesthetics also impeded seed germination and chlorophyll accumulation in cress seedlings. Endocytic vesicle recycling and reactive oxygen species (ROS) balance, as observed in intact Arabidopsis root apex cells, were also affected by all anaesthetics tested. Conclusions: Plants are sensitive to several anaesthetics that have no structural similarities. As in animals and humans, anaesthetics used at appropriate concentrations block action potentials and immobilize organs via effects on action potentials, endocytic vesicle recycling and ROS homeostasis. Plants emerge as ideal model objects to study general questions related to anaesthesia, as well as to serve as a suitable test system for human anaesthesia.

Spatio-temporal control of mutualism in legumes helps spread symbiotic nitrogen fixation.

Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a central question. We addressed this issue for one of the most significant mutualistic interactions on Earth, which associates plants of the leguminosae family and hundreds of nitrogen (N2)-fixing bacterial species. Here we analyze the spatio-temporal dynamics of fixers and non-fixers along the symbiotic process in the Cupriavidus taiwanensis-Mimosa pudica system. N2-fixing symbionts progressively outcompete isogenic non-fixers within root nodules, where N2-fixation occurs, even when they share the same nodule. Numerical simulations, supported by experimental validation, predict that rare fixers will invade a population dominated by non-fixing bacteria during serial nodulation cycles with a probability that is function of initial inoculum, plant population size and nodulation cycle length. Our findings provide insights into the selective forces and ecological factors that may have driven the spread of the N2-fixation mutualistic trait.

Cold plasma interactions with plants: Morphing and movements of Venus flytrap and Mimosa pudica induced by argon plasma jet.

Low temperature (cold) plasma finds an increasing number of applications in biology, medicine and agriculture. In this paper, we report a new effect of plasma induced morphing and movements of Venus flytrap and Mimosa pudica. We have experimentally observed plasma activation of sensitive plant movements and morphing structures in these plants similar to stimulation of their mechanosensors in vivo. Application of an atmospheric pressure argon plasma jet to the inside or outside of a lobe, midrib, or cilia in Dionaea muscipula Ellis induces trap closing. Treatment of Mimosa pudica by plasma induces movements of pinnules and petioles similar to the effects of mechanical stimulation. We have conducted control experiments and simulations to illustrate that gas flow and UV radiation associated with plasma are not the primary reasons for the observed effects. Reactive oxygen and nitrogen species (RONS) produced by cold plasma in atmospheric air appear to be the primary reason of plasma-induced activation of phytoactuators in plants. Some of these RONS are known to be signaling molecules, which control plants' developmental processes. Understanding these mechanisms could promote plasma-based technology for plant developmental control and future use for plant protection from pathogens. Our work offers new insight into mechanisms which trigger plant morphing and movement.

Using atmospheric plasma to increase wettability, imbibition and germination of physically dormant seeds of Mimosa Caesalpiniafolia.

In this study, we analyzed seed wettability as well as imbibition and germination after treatment with atmospheric pressure cold plasma (APCP) using dielectric barrier discharge (DBD) in seeds that have very low germination rates. To aid industrial applications, several seeds were simultaneously treated with plasma within a space between two coaxial glass tubes sandwiched by two metal mesh screens that produced high-voltage pulses at 17.5kV with a frequency of 990Hz. Three treatment times (3min, 9min and 15min) as well as untreated seeds were used to conduct the wettability, imbibition and germination tests. The wettability and imbibition were found to be directly related to the treatment duration, but saturation of the imbibition was found for treatment durations greater than 9min. Plasma treatment was also effective in improving germination, but shorter treatment duration presented greater germination. This apparent contradiction is explained by the cell damage caused by the increased exposure to plasma, as observed in other studies. The results suggest that there must be an optimal wettability and imbibition condition that ensures that excessive moisture does not harm the germination process.