Quantification of the pluriannual dynamics of grapevine growth responses to nitrogen supply using a Bayesian approach.

The effect of nitrogen (N) nutrition on grapevine carbon (C) dynamics has been well studied at the annual scale, but poorly addressed at a pluriannual timescale. The aim of this study was to quantify, in an integrated conceptual framework, the effect of N nutrition on potted grapevine growth and storage over 2 consecutive years. The consequences of using destructive measurements were investigated using a hierarchical Bayesian model. The rate and duration of leaf growth were both positively impacted by the chlorophyll content of the leaves, but they were negatively impacted by the initial carbohydrate measurements, raising a distortion in the estimation of initial reserves. The C production per unit of global radiation depended on the leaf area dynamics. The allocation of dry matter mainly relied on the phenological stage. The present study highlights the importance of using appropriate statistical methods to overcome uncertainties due to destructive measurements. The genericity of the statistical approach presented may encourage its implementation in other agronomy studies. Based on our results, a simple conceptual framework of grapevine pluriannual growth under various N supplies was built. This provides a relevant basis for a future model of C and N balance and responses to N fertilization in grapevine.

Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots.

As multicellular organisms grow, positional information is continually needed to regulate the pattern in which cells are arranged. In the Arabidopsis root, most cell types are organized in a radially symmetric pattern; however, a symmetry-breaking event generates bisymmetric auxin and cytokinin signaling domains in the stele. Bidirectional cross-talk between the stele and the surrounding tissues involving a mobile transcription factor, SHORT ROOT (SHR), and mobile microRNA species also determines vascular pattern, but it is currently unclear how these signals integrate. We use a multicellular model to determine a minimal set of components necessary for maintaining a stable vascular pattern. Simulations perturbing the signaling network show that, in addition to the mutually inhibitory interaction between auxin and cytokinin, signaling through SHR, microRNA165/6, and PHABULOSA is required to maintain a stable bisymmetric pattern. We have verified this prediction by observing loss of bisymmetry in shr mutants. The model reveals the importance of several features of the network, namely the mutual degradation of microRNA165/6 and PHABULOSA and the existence of an additional negative regulator of cytokinin signaling. These components form a plausible mechanism capable of patterning vascular tissues in the absence of positional inputs provided by the transport of hormones from the shoot.

A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution.

The link between genetic regulation and the definition of form and size during morphogenesis remains largely an open question in both plant and animal biology. This is partially due to the complexity of the process, involving extensive molecular networks, multiple feedbacks between different scales of organization and physical forces operating at multiple levels. Here we present a conceptual and modeling framework aimed at generating an integrated understanding of morphogenesis in plants. This framework is based on the biophysical properties of plant cells, which are under high internal turgor pressure, and are prevented from bursting because of the presence of a rigid cell wall. To control cell growth, the underlying molecular networks must interfere locally with the elastic and/or plastic extensibility of this cell wall. We present a model in the form of a three dimensional (3D) virtual tissue, where growth depends on the local modulation of wall mechanical properties and turgor pressure. The model shows how forces generated by turgor-pressure can act both cell autonomously and non-cell autonomously to drive growth in different directions. We use simulations to explore lateral organ formation at the shoot apical meristem. Although different scenarios lead to similar shape changes, they are not equivalent and lead to different, testable predictions regarding the mechanical and geometrical properties of the growing lateral organs. Using flower development as an example, we further show how a limited number of gene activities can explain the complex shape changes that accompany organ outgrowth.

A data-driven integrative model of sepal primordium polarity in Arabidopsis.

Flower patterning is determined by a complex molecular network but how this network functions remains to be elucidated. Here, we develop an integrative modeling approach that assembles heterogeneous data into a biologically coherent model to allow predictions to be made and inconsistencies among the data to be found. We use this approach to study the network underlying sepal development in the young flower of Arabidopsis thaliana. We constructed a digital atlas of gene expression and used it to build a dynamical molecular regulatory network model of sepal primordium development. This led to the construction of a coherent molecular network model for lateral organ polarity that fully recapitulates expression and interaction data. Our model predicts the existence of three novel pathways involving the HD-ZIP III genes and both cytokinin and ARGONAUTE family members. In addition, our model provides predictions on molecular interactions. In a broader context, this approach allows the extraction of biological knowledge from diverse types of data and can be used to study developmental processes in any multicellular organism.

Spatio-temporal water dynamics in mature Banksia menziesii trees during drought.

Southwest Australian Banksia woodlands are highly diverse plant communities that are threatened by drought- or temperature-induced mortality due to the region's changing climate. We examined water relations in dominant Banksia menziesii R. Br. trees using magnetic leaf patch clamp pressure (ZIM-) probes that allow continuous, real-time monitoring of leaf water status. Multiple ZIM-probes across the crown were complemented by traditional ecophysiological measurements. During summer, early stomatal downregulation of transpiration prevented midday balancing pressures from exceeding 2.5 MPa. Diurnal patterns of ZIM-probe and pressure chamber readings agreed reasonably well, however, ZIM-probes recorded short-term dynamics, which are impossible to capture using a pressure chamber. Simultaneous recordings of three ZIM-probes evenly spaced along leaf laminas revealed intrafoliar turgor gradients, which, however, did not develop in a strictly basi- or acropetal fashion and varied with cardinal direction. Drought stress manifested as increasing daily signal amplitude (low leaf water status) and occasionally as rising baseline at night (delayed rehydration). These symptoms occurred more often locally than across the entire crown. Microclimate effects on leaf water status were strongest in crown regions experiencing peak morning radiation (East and North). Extreme spring temperatures preceded the sudden death of B. menziesii trees, suggesting a temperature- or humidity-related tipping point causing rapid hydraulic failure as evidenced by collapsing ZIM-probe readings from an affected tree. In a warmer and drier future, increased frequency of B. menziesii mortality will result in significantly altered community structure and ecosystem function.

Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules.

Actinorhizal symbioses are mutualistic interactions between plants and the soil bacteria Frankia that lead to the formation of nitrogen-fixing root nodules. Little is known about the signaling mechanisms controlling the different steps of the establishment of the symbiosis. The plant hormone auxin has been suggested to play a role. Here we report that auxin accumulates within Frankia-infected cells in actinorhizal nodules of Casuarina glauca. Using a combination of computational modeling and experimental approaches, we establish that this localized auxin accumulation is driven by the cell-specific expression of auxin transporters and by Frankia auxin biosynthesis in planta. Our results indicate that the plant actively restricts auxin accumulation to Frankia-infected cells during the symbiotic interaction.

Modelling transport of inhibiting and activating signals and their combined effects on floral induction: application to apple tree.

Floral induction (FI) in shoot apical meristems (SAM) is assumed to be triggered by antagonistic endogenous signals. In fruit trees, FI occurs in some SAM only and is determined by activating and inhibiting signals originating from leaves and fruit, respectively. We developed a model (SigFlow) to quantify on 3D structures the combined impact of such signals and distances at which they act on SAM. Signal transport was simulated considering a signal 'attenuation' parameter, whereas SAM fate was determined by probability functions depending on signal quantities. Model behaviour was assessed on simple structures before being calibrated and validated on a unique experimental dataset of 3D digitized apple trees with contrasted crop loads and subjected to leaf and fruit removal at different scales of tree organization. Model parameter estimations and comparisons of two signal combination functions led us to formulate new assumptions on the mechanisms involved: (i) the activating signal could be transported at shorter distances than the inhibiting one (roughly 50 cm vs 1 m) (ii) both signals jointly act to determine FI with SAM being more sensitive to inhibiting signal than activating one. Finally, the genericity of the model is promising to further understand the physiological and architectural determinisms of FI in plants.

Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development.

Plants continuously generate new organs through the activity of populations of stem cells called meristems. The shoot apical meristem initiates leaves, flowers, and lateral meristems in highly ordered, spiralled, or whorled patterns via a process called phyllotaxis. It is commonly accepted that the active transport of the plant hormone auxin plays a major role in this process. Current hypotheses propose that cellular hormone transporters of the PIN family would create local auxin maxima at precise positions, which in turn would lead to organ initiation. To explain how auxin transporters could create hormone fluxes to distinct regions within the plant, different concepts have been proposed. A major hypothesis, canalization, proposes that the auxin transporters act by amplifying and stabilizing existing fluxes, which could be initiated, for example, by local diffusion. This convincingly explains the organised auxin fluxes during vein formation, but for the shoot apical meristem a second hypothesis was proposed, where the hormone would be systematically transported towards the areas with the highest concentrations. This implies the coexistence of two radically different mechanisms for PIN allocation in the membrane, one based on flux sensing and the other on local concentration sensing. Because these patterning processes require the interaction of hundreds of cells, it is impossible to estimate on a purely intuitive basis if a particular scenario is plausible or not. Therefore, computational modelling provides a powerful means to test this type of complex hypothesis. Here, using a dedicated computer simulation tool, we show that a flux-based polarization hypothesis is able to explain auxin transport at the shoot meristem as well, thus providing a unifying concept for the control of auxin distribution in the plant. Further experiments are now required to distinguish between flux-based polarization and other hypotheses.