The impact of mechanical stress on anatomy, morphology, and gene expression in Urtica dioica L.

MAIN CONCLUSION: Mechanical stress induces distinct anatomical, molecular, and morphological changes in Urtica dioica, affecting trichome development, gene expression, and leaf morphology under controlled conditions The experiments were performed on common nettle, a widely known plant characterized by high variability of leaf morphology and responsiveness to mechanical touch. A specially constructed experimental device was used to study the impact of mechanical stress on Urtica dioica plants under strictly controlled parameters of the mechanical stimulus (touching) and environment in the growth chamber. The general anatomical structure of the plants that were touched was similar to that of control plants, but the shape of the internodes' cross section was different. Stress-treated plants showed a distinct four-ribbed structure. However, as the internodes progressed, the shape gradually approached a rectangular form. The epidermis of control plants included stinging, glandular and simple setulose trichomes, but plants that were touched had no stinging trichomes, and setulose trichomes accumulated more callose. Cell wall lignification occurred in the older internodes of the control plants compared to stress-treated ones. Gene analysis revealed upregulation of the expression of the UdTCH1 gene in touched plants compared to control plants. Conversely, the expression of UdERF4 and UdTCH4 was downregulated in stressed plants. These data indicate that the nettle's response to mechanical stress reaches the level of regulatory networks of gene expression. Image analysis revealed reduced leaf area, increased asymmetry and altered contours in touched leaves, especially in advanced growth stages, compared to control plants. Our results indicate that mechanical stress triggers various anatomical, molecular, and morphological changes in nettle; however, further interdisciplinary research is needed to better understand the underlying physiological mechanisms.

Flexure wood formation via growth reprogramming in hybrid aspen involves jasmonates and polyamines and transcriptional changes resembling tension wood development.

Stem bending in trees induces flexure wood but its properties and development are poorly understood. Here, we investigated the effects of low-intensity multidirectional stem flexing on growth and wood properties of hybrid aspen, and on its transcriptomic and hormonal responses. Glasshouse-grown trees were either kept stationary or subjected to several daily shakes for 5 wk, after which the transcriptomes and hormones were analyzed in the cambial region and developing wood tissues, and the wood properties were analyzed by physical, chemical and microscopy techniques. Shaking increased primary and secondary growth and altered wood differentiation by stimulating gelatinous-fiber formation, reducing secondary wall thickness, changing matrix polysaccharides and increasing cellulose, G- and H-lignin contents, cell wall porosity and saccharification yields. Wood-forming tissues exhibited elevated jasmonate, polyamine, ethylene and brassinosteroids and reduced abscisic acid and gibberellin signaling. Transcriptional responses resembled those during tension wood formation but not opposite wood formation and revealed several thigmomorphogenesis-related genes as well as novel gene networks including FLA and XTH genes encoding plasma membrane-bound proteins. Low-intensity stem flexing stimulates growth and induces wood having improved biorefinery properties through molecular and hormonal pathways similar to thigmomorphogenesis in herbaceous plants and largely overlapping with the tension wood program of hardwoods.

Nutrient Solution Flowing Environment Affects Metabolite Synthesis Inducing Root Thigmomorphogenesis of Lettuce (Lactuca sativa L.) in Hydroponics.

The principal difference between hydroponics and other substrate cultivation methods is the flowing liquid hydroponic cultivation substrate. Our previous studies have revealed that a suitable flowing environment of nutrient solution promoted root development and plant growth, while an excess flow environment was unfavorable for plants. To explain the thigmomorphogenetic response of excess flow-induced metabolic changes, six groups of lettuce (Lactuca sativa L.), including two flow conditions and three time periods, were grown. Compared with the plants without flow, the plants with flow showed decreased root fresh weight, total root length, root surface area, and root volume but increased average root diameter and root density. The roots with flow had more upregulated metabolites than those without flow, suggesting that the flow may trigger metabolic synthesis and activity. Seventy-nine common differential metabolites among six groups were screened, and enrichment analysis showed the most significant enrichment in the arginine biosynthesis pathway. Arginine was present in all the groups and exhibited greater concentrations in roots with flow than without flow. It can be speculated from the results that a high-flowing environment of nutrient solution promotes arginine synthesis, resulting in changes in root morphology. The findings provide insights on root thigmomorphogenesis affected by its growing conditions and help understand how plants respond to environmental mechanical forces.

Mechanical Stimulation Decreases Auxin and Gibberellic Acid Synthesis but Does Not Affect Auxin Transport in Axillary Buds; It Also Stimulates Peroxidase Activity in Petunia × atkinsiana.

Thigmomorphogenesis (or mechanical stimulation-MS) is a term created by Jaffe and means plant response to natural stimuli such as the blow of the wind, strong rain, or touch, resulting in a decrease in length and an increase of branching as well as an increase in the activity of axillary buds. MS is very well known in plant morphology, but physiological processes controlling plant growth are not well discovered yet. In the current study, we tried to find an answer to the question if MS truly may affect auxin synthesis or transport in the early stage of plant growth, and which physiological factors may be responsible for growth arrest in petunia. According to the results of current research, we noticed that MS affects plant growth but does not block auxin transport from the apical bud. MS arrests IAA and GA3 synthesis in MS-treated plants over the longer term. The main factor responsible for the thickening of cell walls and the same strengthening of vascular tissues and growth arrestment, in this case, is peroxidase (POX) activity, but special attention should be also paid to AGPs as signaling molecules which also are directly involved in growth regulation as well as in cell wall modifications.

Environmental-biomechanical reciprocity and the evolution of plant material properties.

Abiotic-biotic interactions have shaped organic evolution since life first began. Abiotic factors influence growth, survival, and reproductive success, whereas biotic responses to abiotic factors have changed the physical environment (and indeed created new environments). This reciprocity is well illustrated by land plants who begin and end their existence in the same location while growing in size over the course of years or even millennia, during which environment factors change over many orders of magnitude. A biomechanical, ecological, and evolutionary perspective reveals that plants are (i) composed of materials (cells and tissues) that function as cellular solids (i.e. materials composed of one or more solid and fluid phases); (ii) that have evolved greater rigidity (as a consequence of chemical and structural changes in their solid phases); (iii) allowing for increases in body size and (iv) permitting acclimation to more physiologically and ecologically diverse and challenging habitats; which (v) have profoundly altered biotic as well as abiotic environmental factors (e.g. the creation of soils, carbon sequestration, and water cycles). A critical component of this evolutionary innovation is the extent to which mechanical perturbations have shaped plant form and function and how form and function have shaped ecological dynamics over the course of evolution.

Acclimation to wind loads and/or contact stimuli? A biomechanical study of peltate leaves of Pilea peperomioides.

Plants are exposed to various environmental stresses. Leaves immediately respond to mechano-stimulation, such as wind and touch, by bending and twisting or acclimate over a longer time period by thigmomorphogenetic changes of mechanical and geometrical properties. We selected the peltate leaves of Pilea peperomioides for a comparative analysis of mechano-induced effects on morphology, anatomy, and biomechanics of petiole and transition zone. The plants were cultivated for 6 weeks in a phytochamber divided into four treatment groups: control (no stimulus), touch stimulus (brushing every 30 s), wind stimulus (constant air flow of 4.6 m s-1), and a combination of touch and wind stimuli. Comparing the four treatment groups, neither the petiole nor the transition zone showed significant thigmomorphogenetic acclimations. However, comparing the petiole and the transition zone, the elastic modulus (E), the torsional modulus (G), the E/G ratio, and the axial rigidity (EA) differed significantly, whereas no significant difference was found for the torsional rigidity (GK). The twist-to-bend ratios (EI/GK) of all petioles ranged between 4.33 and 5.99, and of all transition zones between 0.67 and 0.78. Based on the twist-to-bend ratios, we hypothesize that bending loads are accommodated by the petiole, while torsional loads are shared between the transition zone and petiole.

Mechanostimulation: a promising alternative for sustainable agriculture practices.

Plants memorize events associated with environmental fluctuations. The integration of environmental signals into molecular memory allows plants to cope with future stressors more efficiently-a phenomenon that is known as 'priming'. Primed plants are more resilient to environmental stresses than non-primed plants, as they are capable of triggering more robust and faster defence responses. Interestingly, exposure to various forms of mechanical stimuli (e.g. touch, wind, or sound vibration) enhances plants' basal defence responses and stress tolerance. Thus, mechanostimulation appears to be a potential priming method and a promising alternative to chemical-based priming for sustainable agriculture. According to the currently available method, mechanical treatment needs to be repeated over a month to alter plant growth and defence responses. Such a long treatment protocol restricts its applicability to fast-growing crops. To optimize the protocol for a broad range of crops, we need to understand the molecular mechanisms behind plant mechanoresponses, which are complex and depend on the frequency, intervals, and duration of the mechanical treatment. In this review, we synthesize the molecular underpinnings of plant mechanoperception and signal transduction to gain a mechanistic understanding of the process of mechanostimulated priming.

Wind-evoked anemotropism affects the morphology and mechanical properties of Arabidopsis.

Plants are known to exhibit a thigmomorphogenetic response to mechanical stimuli by altering their morphology and mechanical properties. Wind is widely perceived as mechanical stress and in many experiments its influence is simulated by applying mechanical perturbations. However, it is known that wind-induced effects on plants can differ and at times occur even in the opposite direction compared with those induced by mechanical perturbations. In the present study, the long-term response of Arabidopsis thaliana to a constant unidirectional wind was investigated. We found that exposure to wind resulted in a positive anemotropic response and in significant alterations to Arabidopsis morphology, mechanical properties, and anatomical tissue organization that were associated with the plant's strategy of acclimation to a windy environment. Overall, the observed response of Arabidopsis to wind differs significantly from previously reported responses of Arabidopsis to mechanical perturbations. The presented results suggest that the response of Arabidopsis is sensitive to the type of mechanical stimulus applied, and that it is not always straightforward to simulate one type of perturbation by another.

Mechanical stimulation in wheat triggers age- and dose-dependent alterations in growth, development and grain characteristics.

BACKGROUND AND AIMS: Wheat crops are exposed to a range of mechanical stimulations in their natural environment, yet we know very little about their response to such conditions. The aim of this study was to better understand the effect of mechanical stimulation on wheat growth and development, stem mechanical properties and grain measures. We focused on the following questions: (1) Does plant age affect the response to mechanical stimulation? (2) Is there a minimum threshold for the perception of mechanical stimuli? (3) Is the effect of manual brushing different to natural wind stimulation? METHODS: For age- and dose-response experiments, wheat plants were grown under controlled glasshouse conditions with brushing treatments applied using a purpose-built rig. The results of the controlled experiments are compared with those from an outside experiment where wheat plants were exposed to natural wind, with or without additional brushing. Detailed phenotypic measurements were conducted and treatment effects on grain characteristics were determined using micro-computed tomography imaging. KEY RESULTS: Two-week-old wheat plants were particularly sensitive to mechanical stimulation by controlled brushing treatments. Amongst others, plants exhibited a large reduction in height and grain yield, and an increase in tillers, above-ground biomass and stiffness of stem segments. Plants responded significantly to doses as small as one daily brushstroke. Outdoor experiments by and large confirmed results from controlled environment experiments. CONCLUSIONS: The morphological and developmental response to mechanical brushing treatment, in relation to vegetative above-ground biomass and grain yield, is dependent on plant age as well as the dose of the treatments. This study shows that mechanical stimulation of wheat impacts on a multitude of agriculturally relevant traits and provides a much needed advancement of our understanding of wheat thigmomorphogenesis and the potential applications of mechanical conditioning to control relevant traits.

Quantitative and functional posttranslational modification proteomics reveals that TREPH1 plays a role in plant touch-delayed bolting.

Environmental mechanical forces, such as wind and touch, trigger gene-expression regulation and developmental changes, called "thigmomorphogenesis," in plants, demonstrating the ability of plants to perceive such stimuli. In Arabidopsis, a major thigmomorphogenetic response is delayed bolting, i.e., emergence of the flowering stem. The signaling components responsible for mechanotransduction of the touch response are largely unknown. Here, we performed a high-throughput SILIA (stable isotope labeling in Arabidopsis)-based quantitative phosphoproteomics analysis to profile changes in protein phosphorylation resulting from 40 seconds of force stimulation in Arabidopsis thaliana Of the 24 touch-responsive phosphopeptides identified, many were derived from kinases, phosphatases, cytoskeleton proteins, membrane proteins, and ion transporters. In addition, the previously uncharacterized protein TOUCH-REGULATED PHOSPHOPROTEIN1 (TREPH1) became rapidly phosphorylated in touch-stimulated plants, as confirmed by immunoblots. TREPH1 fractionates as a soluble protein and is shown to be required for the touch-induced delay of bolting and gene-expression changes. Furthermore, a nonphosphorylatable site-specific isoform of TREPH1 (S625A) failed to restore touch-induced flowering delay of treph1-1, indicating the necessity of S625 for TREPH1 function and providing evidence consistent with the possible functional relevance of the touch-regulated TREPH1 phosphorylation. Taken together, these findings identify a phosphoprotein player in Arabidopsis thigmomorphogenesis regulation and provide evidence that TREPH1 and its touch-induced phosphorylation may play a role in touch-induced bolting delay, a major component of thigmomorphogenesis.

Between Stress and Response: Function and Localization of Mechanosensitive Ca2+ Channels in Herbaceous and Perennial Plants.

Over the past three decades, how plants sense and respond to mechanical stress has become a flourishing field of research. The pivotal role of mechanosensing in organogenesis and acclimation was demonstrated in various plants, and links are emerging between gene regulatory networks and physical forces exerted on tissues. However, how plant cells convert physical signals into chemical signals remains unclear. Numerous studies have focused on the role played by mechanosensitive (MS) calcium ion channels MCA, Piezo and OSCA. To complement these data, we combined data mining and visualization approaches to compare the tissue-specific expression of these genes, taking advantage of recent single-cell RNA-sequencing data obtained in the root apex and the stem of Arabidopsis and the Populus stem. These analyses raise questions about the relationships between the localization of MS channels and the localization of stress and responses. Such tissue-specific expression studies could help to elucidate the functions of MS channels. Finally, we stress the need for a better understanding of such mechanisms in trees, which are facing mechanical challenges of much higher magnitudes and over much longer time scales than herbaceous plants, and we mention practical applications of plant responsiveness to mechanical stress in agriculture and forestry.

Auxin mediates the touch-induced mechanical stimulation of adventitious root formation under windy conditions in Brachypodium distachyon.

BACKGROUND: It is widely perceived that mechanical or thigmomorphogenic stimuli, such as rubbing and bending by passing animals, wind, raindrop, and flooding, broadly influence plant growth and developmental patterning. In particular, wind-driven mechanical stimulation is known to induce the incidence of radial expansion and shorter and stockier statue. Wind stimulation also affects the adaptive propagation of the root system in various plant species. However, it is unknown how plants sense and transmit the wind-derived mechanical signals to launch appropriate responses, leading to the wind-adaptive root growth. RESULTS: Here, we found that Brachypodium distachyon, a model grass widely used for studies on bioenergy crops and cereals, efficiently adapts to wind-mediated lodging stress by forming adventitious roots (ARs) from nonroot tissues. Experimental dissection of wind stimuli revealed that not bending of the mesocotyls but physical contact of the leaf nodes with soil particles triggers the transcriptional induction of a group of potential auxin-responsive genes encoding WUSCHEL RELATED HOMEOBOX and LATERAL ORGAN BOUNDARIES DOMAIN transcription factors, which are likely to be involved in the induction of AR formation. CONCLUSIONS: Our findings would contribute to further understanding molecular mechanisms governing the initiation and development of ARs, which will be applicable to crop agriculture in extreme wind climates.

Mechanical stimulation in Brachypodium distachyon: Implications for fitness, productivity, and cell wall properties.

Mechanical stimulation, including exposure to wind, is a common environmental variable for plants. However, knowledge about the morphogenetic response of the grasses (Poaceae) to mechanical stimulation and impact on relevant agronomic traits is very limited. Two natural accessions of Brachypodium distachyon were exposed to wind and mechanical treatments. We surveyed a wide range of stem-related traits to determine the effect of the two treatments on plant growth, development, and stem biomass properties. Both treatments induced significant quantitative changes across multiple scales, from the whole plant down to cellular level. The two treatments resulted in shorter stems, reduced biomass, increased tissue rigidity, delayed flowering, and reduced seed yield in both accessions. Among changes in cell wall-related features, a substantial increase in lignin content and pectin methylesterase activity was most notable. Mechanical stimulation also reduced the enzymatic sugar release from the cell wall, thus increasing biomass recalcitrance. Notably, treatments had a distinct and opposite effect on vascular bundle area in the two accessions, suggesting genetic variation in modulating these responses to mechanical stimulation. Our findings highlight that exposure of grasses to mechanical stimulation is a relevant environmental factor affecting multiple traits important for their utilization in food, feed, and bioenergy applications.

Morphological plasticity in the kelp Nereocystis luetkeana (Phaeophyceae) is sensitive to the magnitude, direction, and location of mechanical loading.

Nereocystis luetkeana is a canopy-forming kelp that exhibits morphological plasticity across hydrodynamic gradients, producing broad, undulate blades in slow flow and narrow, flattened blades in fast flow, enabling thalli to reduce drag while optimizing photosynthesis. While the functional significance of this phenomenon has been well studied, the developmental and physiological mechanisms that facilitate the plasticity remain poorly understood. In this study, we conducted three experiments to characterize how the (1) magnitude, (2) direction, and (3) location of plasticity-inducing mechanical stimuli affect the morphology of Nereocystis blades. We found that applying a gradient of tensile force caused blades to grow progressively longer, narrower, less ruffled, and heavier in a linear fashion, suggesting that Nereocystis is equally well adapted for all conditions within its hydrodynamic niche. We also found that applying tension transversely across blades caused the growth response to rotate 90°, indicating that there is no substantial separation between the sites of stimulus perception and response and suggesting that a long-distance signaling mechanism, such as a hormone, is unlikely to mediate this phenomenon. Meristoderm cells showed morphological changes that paralleled those of their respective blades in this experiment, implying that tissue-level morphology is influenced by cell growth. Finally, we found that plasticity was only induced when tension was applied directly to the growing tissue, reinforcing that long-distance signaling is probably not involved and possibly indicating that the mechanism on display generally requires an intercalary meristem to facilitate mechanoperception.

Sorghum tiller bud growth is repressed by contact with the overlying leaf.

Basal branching in grasses, or tillering, is an important trait determining both form and function of crops. Although similarities exist between eudicot and grass branching programs, one notable difference is that the tiller buds of grasses are covered by the subtending leaf, whereas eudicot buds are typically unconstrained. The current study shows that contact with the leaf sheath represses sorghum bud growth by providing a mechanical signal that cues the bud to refrain from rapid growth. Leaf removal resulted in massive reprogramming of the bud transcriptome that included signatures of epigenetic modifications and also implicated several hormones in the response. Bud abscisic acid transiently increased, then decreased following leaf removal relative to controls, and abscisic acid was necessary to repress bud growth in the presence of the leaf. Jasmonic acid (JA) levels and signalling increased in buds following leaf removal. Remarkably, application of JA to buds in situ promoted growth. The repression of bud growth by leaf contact shares characteristics of thigmomorphogenic responses in other systems, including the involvement of JA, though the JA effect is opposite. The repression of bud growth by leaf contact may represent a mechanism to time tillering to an appropriate developmental stage of the plant.

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.

Poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli.

BACKGROUND: Trees experience mechanical stimuli -like wind- that trigger thigmomorphogenetic syndrome, leading to modifications of plant growth and wood quality. This syndrome affects tree productivity but is also believed to improve tree acclimation to chronic wind. Wind is particularly challenging for trees, because of their stature and perenniality. Climate change forecasts are predicting that the occurrence of high wind will worsen, making it increasingly vital to understand the mechanisms regulating thigmomorphogenesis, especially in perennial plants. By extension, this also implies factoring in the recurring nature of wind episodes. However, data on the molecular processes underpinning mechanoperception and transduction of mechanical signals, and their dynamics, are still dramatically lacking in trees. RESULTS: Here we performed a genome-wide and time-series analysis of poplar transcriptional responsiveness to transitory and recurring controlled stem bending, mimicking wind. The study revealed that 6% of the poplar genome is differentially expressed after a single transient bending. The combination of clustering, Gene Ontology categorization and time-series expression approaches revealed the diversity of gene expression patterns and biological processes affected by stem bending. Short-term transcriptomic responses entailed a rapid stimulation of plant defence and abiotic stress signalling pathways, including ethylene and jasmonic acid signalling but also photosynthesis process regulation. Late transcriptomic responses affected genes involved in cell wall organization and/or wood development. An analysis of the molecular impact of recurring bending found that the vast majority (96%) of the genes differentially expressed after a first bending presented reduced or even net-zero amplitude regulation after the second exposure to bending. CONCLUSION: This study constitutes the first dynamic characterization of the molecular processes affected by single or repeated stem bending in poplar. Moreover, the global attenuation of the transcriptional responses, observed from as early as after a second bending, indicates the existence of a mechanism governing a fine tuning of plant responsiveness. This points toward several mechanistic pathways that can now be targeted to elucidate the complex dynamics of wind acclimation.

Vine tendrils use contact chemoreception to avoid conspecific leaves.

Movement and growth habit of climbing plants have attracted attention since the time of Charles Darwin; however, there are no reports on whether plants can choose suitable hosts or avoid unsuitable ones based on chemoreception. Here, I show that the tendrils of Cayratia japonica (Vitaceae) appear to avoid conspecific leaves using contact chemoreception for oxalates, which are highly concentrated in C. japonica leaves. The coiling experiments show that C. japonica has a flexible plastic response to avoid coiling around conspecific leaves. The coiling response is negatively correlated with the oxalate content in the contacted leaves. Experiments using laboratory chemicals indicate that the tendrils avoid oxalate-coated plastic sticks. These results indicate that the tendrils of C. japonica avoid coiling around a conspecific leaf based on contact chemoreception for oxalate compounds. The tendrils of climbing plants may function as a chemoreceptor system to detect the chemical cues of a contacted plant.

The RNA Polymerase-Associated Factor 1 Complex Is Required for Plant Touch Responses.

Thigmomorphogenesis is a stereotypical developmental alteration in the plant body plan that can be induced by repeatedly touching plant organs. To unravel how plants sense and record multiple touch stimuli we performed a novel forward genetic screen based on the development of a shorter stem in response to repetitive touch. The touch insensitive (ths1) mutant identified in this screen is defective in some aspects of shoot and root thigmomorphogenesis. The ths1 mutant is an intermediate loss-of-function allele of VERNALIZATION INDEPENDENCE 3 (VIP3), a previously characterized gene whose product is part of the RNA polymerase II-associated factor 1 (Paf1) complex. The Paf1 complex is found in yeast, plants and animals, and has been implicated in histone modification and RNA processing. Several components of the Paf1 complex are required for reduced stem height in response to touch and normal root slanting and coiling responses. Global levels of histone H3K36 trimethylation are reduced in VIP3 mutants. In addition, THS1/VIP3 is required for wild type histone H3K36 trimethylation at the TOUCH3 (TCH3) and TOUCH4 (TCH4) loci and for rapid touch-induced upregulation of TCH3 and TCH4 transcripts. Thus, an evolutionarily conserved chromatin-modifying complex is required for both short- and long-term responses to mechanical stimulation, providing insight into how plants record mechanical signals for thigmomorphogenesis.

Forest trees filter chronic wind-signals to acclimate to high winds.

Controlled experiments have shown that trees acclimate thigmomorphogenetically to wind-loads by sensing their deformation (strain). However, the strain regime in nature is exposed to a full spectrum of winds. We hypothesized that trees avoid overreacting by responding only to winds which bring information on local climate and/or wind exposure. Additionally, competition for light dependent on tree social status also likely affects thigmomorphogenesis. We monitored and manipulated quantitatively the strain regimes of 15 pairs of beech (Fagus sylvatica) trees of contrasting social status in an acclimated stand, and quantified the effects of these regimes on the radial growth over a vegetative season. Trees exposed to artificial bending, the intensity of which corresponds to the strongest wind-induced strains, enhanced their secondary growth by at least 80%. Surprisingly, this reaction was even greater - relatively - for suppressed trees than for dominant ones. Acclimated trees did not sense the different types of wind events in the same way. Daily wind speed peaks due to thermal winds were filtered out. Thigmomorphogenesis was therefore driven by intense storms. Thigmomorphogenesis is also likely to be involved in determining social status.