Bruno Moulia

Posture control and skeletal mechanical acclimation in terrestrial plants : Implications for mechanical modeling of plant architecture

Self-supporting plant stems are slender, erect structures that remain standing while growing in highly variable mechanical environments. Such ability is not merely related to an adapted mechanical design in terms of material-specific stiffness and stem tapering. As many terrestrial standing animals do, plant stems regulate posture through active and coordinated control of motor systems and acclimate their skeletal growth to prevailing loads. This analogy probably results from mechanical challenges on standing organisms in an aerial environment with low buoyancy and high turbulence. But the continuous growth of plants submits them to a greater challenge. In response to these challenges, land plants implemented mixed skeletal and motor functions in the same anatomical elements. There are two types of kinematic design: (1) plants with localized active movement (arthrophytes) and (2) plants with continuously distributed active movements (contortionists). The control of these active supporting systems involves gravi- and mechanoperception, but little is known about their coordination at the whole plant level. This more active view of the control of plant growth and form has been insufficiently considered in the modeling of plant architecture. Progress in our understanding of plant posture and mechanical acclimation will require new biomechanical models of plant architectural development.

A scaling law for the effects of architecture and allometry on tree vibration modes suggests a biological tuning to modal compartmentalization

Wind is a major ecological factor for plants and a major economical factor for forestry. Mechanical analyses have revealed that the multimodal dynamic behavior of trees is central to wind-tree interactions. Moreover, the trunk and branches influence dynamic modes, both in frequency and location. Because of the complexity of tree architecture, finite element models (FEMs) have been used to analyze such dynamics. However, these models require detailed geometric and architectural data and are tree-specific-two major restraints for their use in most ecological or biological studies. In this work, closed-form scaling laws for modal characteristics were derived from the dimensional analysis of idealized fractal trees that sketched the major architectural and allometrical regularities of real trees. These scaling laws were compared to three-dimensional FEM modal analyses of two completely digitized trees with maximal architectural contrast. Despite their simplifying hypotheses, the models explained most of the spatiotemporal characteristics of modes that involved the trunk and branches, especially for sympodial trees. These scaling laws reduce the tree to (1) a fundamental frequency and (2) one architectural and three biometrical parameters. They also give quantitative insights into the possible biological control of wind excitability of trees through architecture and allometries.

A frequency lock-in mechanism in the interaction between wind and crop canopies.

The interaction between wind dynamics and the waving of crop canopies is explored. On-site experiments with wheat and alfalfa fields have allowed us to quantify the motion of a large set of plants subject to wind, using an image-correlation technique. The coherent part of the waving motion is extracted by a bi-orthogonal decomposition of the spatio-temporal velocity field of the crop surface. It is shown that the corresponding space and time features cannot be explained using predictions from the mixing-layer analogy of wind above canopies, which is the most common model for perturbations in this environment. We show that the plant bending stiffness plays an important role in the frequency and wavelength selection for the coherent motion of the canopy. A fully coupled model, where the wind fluctuations and the plant dynamics interact through a drag term, is then proposed. This model allows us to demonstrate a lock-in mechanism, similar in principle to what is found in vortex-induced vibration, whereby the frequency of the instability deviates from its expected value when approaching the natural frequency of the oscillating medium. This finding is then compared with data from on-site experiments, and good agreement, in both the frequency and wavelength of the propagating patterns observed on the canopy surface, is found.

Estimating the three-dimensional geometry of a maize crop as an input of radiation models: comparison between three-dimensional digitizing and plant profiles

Abstract The radiation regime of the plant canopies is largely influenced by the geometrical structure, i.e. the angular and spatial distributions of the leaf area. In this paper, two methods for investigating the structure of a maize row crop are compared. The first is a new method which consists of a three-dimensional (3D) digitizing of the foliage using a sonic 3D digitizer. The second one is the plant profile method in which a picture of the plant is taken and then digitized in two dimensions. The latter assumes that the leaves of a plant are in a single vertical plane called the ‘azimuthal plane’. The 3D digitizer has the ability to locate a given point with an accuracy of within ±1 cm: the representation and the repeatability of a leaf description are satisfactory and not largely influenced by the digitizing density. The azimuthal plane assumption of the plant profile method was then tested using the results of 3D digitizing as the reference. Regarding the individual plant description, the leaf azimuth function is bimodal as expected for the maize phyllotaxy. The theoretical azimuthal plane was computed by a principal component analysis. The plant leaf area projection onto this plane represents about 96% of the 3D spatial distribution. Moreover, this plane is close to the azimuthal plane estimated by eye. That is why the spatial distributions of the leaf area in the azimuthal plane are quite similar for the two methods. However, the leaf area with an azimuth within ±15° around the plant azimuth is less than 40% of the total area and the foliage spreads out in a slice 40 cm thick, around the azimuthal plane. Regarding the canopy structure description, the two methods gave similar results for both the leaf inclination and the vertical leaf area density function. In contrast, the distributions in the horizontal plane were different: the plant profile method overestimates the row effect, increasing the foliage clumping around the stem because of the plant azimuth plane assumption. Such discrepancies have repercussions on the modelled radiative balance of a row crop, so the plant profile method should not be used in estimating the spatial distribution of the leaf area in the horizontal plane.

The gravitropic response of poplar trunks: key roles of prestressed wood regulation and the relative kinetics of cambial growth versus wood maturation.

In tree trunks, the motor of gravitropism involves radial growth and differentiation of reaction wood (Archer, 1986). The first aim of this study was to quantify the kinematics of gravitropic response in young poplar (Populus nigra x Populus deltoides, ‘I4551’) by measuring the kinematics of curvature fields along trunks. Three phases were identified, including latency, upward curving, and an anticipative autotropic decurving, which has been overlooked in research on trees. The biological and mechanical bases of these processes were investigated by assessing the biomechanical model of Fournier et al. (1994). Its application at two different time spans of integration made it possible to test hypotheses on maturation, separating the effects of radial growth and cross section size from those of wood prestressing. A significant correlation between trunk curvature and Fourniers model integrated over the growing season was found, but only explained 32% of the total variance. Moreover, over a weeks time period, the model failed due to a clear out phasing of the kinetics of radial growth and curvature that the model does not take into account. This demonstrates a key role of the relative kinetics of radial growth and the maturation process during gravitropism. Moreover, the degree of maturation strains appears to differ in the tension woods produced during the upward curving and decurving phases. Cell wall maturation seems to be regulated to achieve control over the degree of prestressing of tension wood, providing effective control of trunk shape.

Velocimetric third-harmonic generation microscopy: micrometer-scale quantification of morphogenetic movements in unstained embryos

We demonstrate the association of third-harmonic generation (THG) microscopy and particle image velocimetry (PIV) analysis as a novel functional imaging technique for automated micrometer-scale characterization of morphogenetic movements in developing embryos. Using a combined two-photon-excited fluorescence and THG microscope, we characterize the optical properties of Drosophila embryos and show that sustained THG imaging does not perturb sensitive developmental dynamics. Velocimetric THG imaging provides a quantitative description of the dynamics of internal structures in unstained wild-type and mutant embryos.

Leaves as Shell Structures: Double Curvature, Auto-Stresses, and Minimal Mechanical Energy Constraints on Leaf Rolling in Grasses

A bstractGrass leaves are natural examples of shell structures because they are thin and display a double curvature. An important mechanical property of shells is that changes in longitudinal and transverse curvatures are not independent. The basis of this mechanical coupling is presented using simple diagrams. The relevance of the structural constraints for the processes of hydronastic rolling and developmental unrolling in grass leaves is then reviewed. I show that mechanical constraints can explain a large part of the genetic and developmental variability of hydronastic rolling in grasses, without reference to specific anatomic features such as bulliform cells. Mechanical analysis of a rolled maize mutant also revealed that developmental unrolling is not limited to a pure transverse expansion of hinge cells and involves both longitudinal and transverse dimensional changes in the upper epidermis. Interest in using mechanical models as a tool to reveal structural interactions at the tissue and organ level is discussed, and the importance of Paul Greens biophysical approach to the study of plant morphogenesis is emphasized.

Effect of Plant Interaction on Wind-Induced Crop Motion

Plant motion due to wind affects plant growth, a phenomenon called thigmomorphogenesis. Despite intensive studies of the turbulence over plant canopies, the study of plant motion induced by wind has often been limited to individual trees or cereal plants. Few models of global canopy motions are available. Moreover the numerical analysis of models that are based on individual stems becomes time consuming when dealing with crops. A model of motion within the canopies is proposed here using a wave propagation equation within a homogenized continuous medium, and a forcing function representing turbulent gusts advected over the canopy. This model is derived from a discrete model of a set of plant shoots represented as individual oscillators, including elastic contacts between shoots. Such contacts induce nonlinearities into the wave equation. A new experimental method to measure stem dynamical properties and elastic collision properties is presented with an illustration on alfalfa stems. Results obtained modeling plant motions in an alfalfa crop are presented.

Phylogenetic Study of Plant Q-type C2H2 Zinc Finger Proteins and Expression Analysis of Poplar Genes in Response to Osmotic, Cold and Mechanical Stresses

Plant Q-type C2H2 zinc finger transcription factors play an important role in plant tolerance to various environmental stresses such as drought, cold, osmotic stress, wounding and mechanical loading. To carry out an improved analysis of the specific role of each member of this subfamily in response to mechanical loading in poplar, we identified 16 two-fingered Q-type C2H2-predicted proteins from the poplar Phytozome database and compared their phylogenetic relationships with 152 two-fingered Q-type C2H2 protein sequences belonging to more than 50 species isolated from the NR protein database of NCBI. Phylogenetic analyses of these Q-type C2H2 proteins sequences classified them into two groups G1 and G2, and conserved motif distributions of interest were established. These two groups differed essentially in their signatures at the C-terminus of their two QALGGH DNA-binding domains. Two additional conserved motifs, MALEAL and LVDCHY, were found only in sequences from Group G1 or from Group G2, respectively. Functional significance of these phylogenetic divergences was assessed by studying transcript accumulation of six poplar C2H2 Q-type genes in responses to abiotic stresses; but no group specificity was found in any organ. Further expression analyses focused on PtaZFP1 and PtaZFP2, the two genes strongly induced by mechanical loading in poplars. The results revealed that these two genes were regulated by several signalling molecules including hydrogen peroxide and the phytohormone jasmonate.

Acclimation kinetics of physiological and molecular responses of plants to multiple mechanical loadings

During their development, plants are subjected to repeated and fluctuating wind loads, an environmental factor predicted to increase in importance by scenarios of global climatic change. Notwithstanding the importance of wind stress on plant growth and development, little is known about plant acclimation to the bending stresses imposed by repeated winds. The time-course of acclimation of young poplars (Populus tremula L.xP. alba L.) to multiple stem bendings is studied here by following diameter growth and the expression of four genes PtaZFP2, PtaTCH2, PtaTCH4, and PtaACS6, previously described to be involved in the mechanical signalling transduction pathway. Young trees were submitted either to one transient bending per day for several days or to two bendings, 1-14 days apart. A diminution of molecular responses to subsequent bending was observed as soon as a second bending was applied. The minimum rest periods between two successive loadings necessary to recover a response similar to that observed after a single bending, were 7 days and 5 days for growth and molecular responses, respectively. Taken together, our results show a desensitization period of a few days after a single transitory bending, indicating a day-scale acclimation of sensitivity to the type of wind conditions plants experience in their specific environment. This work establishes the basic kinetics of acclimation to low bending frequency and these kinetic analyses will serve as the basis of ongoing work to investigate the molecular mechanisms involved. Future research will also concern plant acclimation to higher wind frequencies.