Blocking then stinging as a case of two-step evolution of defensive cage architectures in herbivore-driven ecosystems.

Dense branching and spines are common features of plant species in ecosystems with high mammalian herbivory pressure. While dense branching and spines can inhibit herbivory independently, when combined, they form a powerful defensive cage architecture. However, how cage architecture evolved under mammalian pressure has remained unexplored. Here we show how dense branching and spines emerged during the age of mammalian radiation in the Combretaceae family and diversified in herbivore-driven ecosystems in the tropics. Phylogenetic comparative methods revealed that modern plant architectural strategies defending against large mammals evolved via a stepwise process. First, dense branching emerged under intermediate herbivory pressure, followed by the acquisition of spines that supported higher speciation rates under high herbivory pressure. Our study highlights the adaptive value of dense branching as part of a herbivore defence strategy and identifies large mammal herbivory as a major selective force shaping the whole plant architecture of woody plants.

Why incorporate plant architecture into trait-based ecology?

Trait-based ecology has improved our understanding of the functioning of organisms, communities, ecosystems, and beyond. However, its predictive ability remains limited as long as phenotypic integration and temporal dynamics are not considered. We highlight how the morphogenetic processes that shape the 3D development of a plant during its lifetime affect its performance. We show that the diversity of architectural traits allows us to go beyond organ-level traits in capturing the temporal and spatial dimensions of ecological niches and informing community assembly processes. Overall, we argue that consideration of multilevel topological, geometrical, and ontogenetic features provides a dynamic view of the whole-plant phenotype and a relevant framework for investigating phenotypic integration, plant adaptation and performance, and community structure and dynamics.

Spatio-temporal analysis of strawberry architecture: insights into the control of branching and inflorescence complexity.

Plant architecture plays a major role in flowering and therefore in crop yield. Attempts to visualize and analyse strawberry plant architecture have been few to date. Here, we developed open-source software combining two- and three-dimensional representations of plant development over time along with statistical methods to explore the variability in spatio-temporal development of plant architecture in cultivated strawberry. We applied this software to six seasonal strawberry varieties whose plants were exhaustively described monthly at the node scale. Results showed that the architectural pattern of the strawberry plant is characterized by a decrease of the module complexity between the zeroth-order module (primary crown) and higher-order modules (lateral branch crowns and extension crowns). Furthermore, for each variety, we could identify traits with a central role in determining yield, such as date of appearance and number of branches. By modeling the spatial organization of axillary meristem fate on the zeroth-order module using a hidden hybrid Markov/semi-Markov mathematical model, we further identified three zones with different probabilities of production of branch crowns, dormant buds, or stolons. This open-source software will be of value to the scientific community and breeders in studying the influence of environmental and genetic cues on strawberry architecture and yield.

If self-shading is so bad, why is there so much? Short shoots reconcile costs and benefits.

If trees minimize self-shading, new foliage in shaded parts of the crown should remain minimal. However, many species have abundant foliage on short shoots inside their crown. In this paper, we test the hypothesis that short shoots allow trees to densify their foliage in self-shaded parts of the crown thanks to reduced costs. Using 30 woody species in Mediterranean and tropical biomes, we estimated the contribution of short shoots to total plant foliage, calculated their costs relative to long shoots including wood cost and used 3D plant simulations calibrated with field measurements to quantify their light interception, self-shading and yield. In species with short shoots, leaves on short shoots account for the majority of leaf area. The reduced cost of short stems enables the production of leaf area with 36% less biomass. Simulations show that although short shoots are more self-shaded, they benefit the plant because they cost less. Lastly, the morphological properties of short shoots have major implications for whole plant architecture. Taken together, our results question the validity of only assessing leaf costs to understand leaf economics and call for more integrated observations at the crown scale to understand light capture strategies in woody plants.

Identifying Developmental Patterns in Structured Plant Phenotyping Data.

Technological breakthroughs concerning both sensors and robotized plant phenotyping platforms have totally renewed the plant phenotyping paradigm in the last two decades. This has impacted both the nature and the throughput of data with the availability of data at high-throughput from the tissular to the whole plant scale. Sensor outputs often take the form of 2D or 3D images or time series of such images from which traits are extracted while organ shapes, shoot or root system architectures can be deduced. Despite this change of paradigm, many phenotyping studies often ignore the structure of the plant and therefore loose the information conveyed by the temporal and spatial patterns emerging from this structure. The developmental patterns of plants often take the form of succession of well-differentiated phases, stages or zones depending on the temporal, spatial or topological indexing of data. This entails the use of hierarchical statistical models for their identification.The objective here is to show potential approaches for analyzing structured plant phenotyping data using state-of-the-art methods combining probabilistic modeling, statistical inference and pattern recognition. This approach is illustrated using five different examples at various scales that combine temporal and topological index parameters, and development and growth variables obtained using prospective or retrospective measurements.

The relative weight of ontogeny, topology and climate in the architectural development of three North American conifers.

Knowledge of plant architecture allows retrospective study of plant development, hence provides powerful tools, through modelling and simulation, to link this development with environmental constraints, and then predict its response to global change. The present study aims to determine some of the main endogenous and exogenous variables driving the architectural development of three North American conifers. We measured architectural traits retrospectively on the trunk, branches and twigs of whole tree crowns for each species: annual shoot length (ASL), needle length, branching patterns and reproduction organs (male and female). We fitted a partial least square (PLS) regression to explain each architectural trait with respect to topological, ontogenic and climatic variables. Results showed a significant weight of these three groups of variables for previous and current year, corresponding, respectively, to organogenesis and elongation. Topological and ontogenic variables had the greatest weight in models. Particularly, all architectural traits were strongly correlated with ASL. We highlighted a negative architectural response of two species to higher than average temperatures, whereas the third one took advantage of these higher temperatures to some degree. Tree architectural development weekly but significantly improved with higher precipitation. Our study underlines the strong weight of topology and ontogeny in tree growth patterns at twig and branch scales. The correlation between ASL and other tree architectural traits should be integrated into architectural development models. Climate variables are secondary in importance at the twig scale. However, interannual climate variations influence all axis categories and branching orders and therefore significantly impact crown development as a whole. This latter impact may increase with climate change, especially as climate affects architectural traits over at least 2 years, through organogenesis and elongation.

Integrated dataset of anatomical, morphological, and architectural traits for plant species in Madagascar.

In this work, we present a dataset, which provides information on the structural diversity of some endemic tropical species in Madagascar. The data were from CIRAD xylotheque (since 1937), and were also collected during various fieldworks (since 1964). The field notes and photographs were provided by French botanists; particularly by Francis Hallé. The dataset covers 250 plant species with anatomical, morphological, and architectural traits indexed from digitized wood slides and fieldwork documents. The digitized wood slides were constituted by the transverse, tangential, and radial sections with three optical magnifications. The main specific anatomical traits can be found within the digitized area. Information on morphological and architectural traits were indexed from digitized field drawings including notes and photographs. The data are hosted in the website ArchiWood (http://archiwood.cirad.fr).

Integrative models for joint analysis of shoot growth and branching patterns.

Plants exhibit dependences between shoot growth and branching that generate highly structured patterns. The characterization of the patterning mechanism is still an open issue because of the developmental processes involved with both succession of events (e.g. internode elongation, axillary shoot initiation and elongation) and complex dependences among neighbouring positions along the parent shoot. Statistical models called semi-Markov switching partitioned conditional generalized linear models were built on the basis of apple and pear tree datasets. In these models, the semi-Markov chain represents both the succession and lengths of branching zones, whereas the partitioned conditional generalized linear models represent the influence of parent shoot growth variables on axillary productions within each branching zone. Parent shoot growth variables were shown to influence specific developmental events. On this basis, the growth and branching patterns of two apple tree (Malus domestica) cultivars, as well as of pear trees (Pyrus spinosa) between two successive growing cycles, were compared. The proposed integrative statistical models were able to decipher the roles of successive developmental events in the growth and branching patterning mechanisms. These models could incorporate other parent shoot explanatory variables, such as the local curvature or the maximum growth rate of the leaf.

Automatic identification and characterization of radial files in light microscopy images of wood.

BACKGROUND AND AIMS: Analysis of anatomical sections of wood provides important information for understanding the secondary growth and development of plants. This study reports on a new method for the automatic detection and characterization of cell files in wood images obtained by light microscopy. To facilitate interpretation of the results, reliability coefficients have been determined, which characterize the files, their cells and their respective measurements. METHODS: Histological sections and blocks of the gymnosperms Pinus canariensis, P. nigra and Abies alba were used, together with histological sections of the angiosperm mahogany (Swietenia spp.). Samples were scanned microscopically and mosaic images were built up. After initial processing to reduce noise and enhance contrast, cells were identified using a 'watershed' algorithm and then cell files were built up by the successive aggregation of cells taken from progressively enlarged neighbouring regions. Cell characteristics such as thickness and size were calculated, and a method was developed to determine the reliability of the measurements relative to manual methods. KEY RESULTS: Image analysis using this method can be performed in less than 20 s, which compares with a time of approx. 40 min to produce the same results manually. The results are accompanied by a reliability indicator that can highlight specific configurations of cells and also potentially erroneous data. CONCLUSIONS: The method provides a fast, economical and reliable tool for the identification of cell files. The reliability indicator characterizing the files permits quick filtering of data for statistical analysis while also highlighting particular biological configurations present in the wood sections.

Identifying ontogenetic, environmental and individual components of forest tree growth.

BACKGROUND AND AIMS: This study aimed to identify and characterize the ontogenetic, environmental and individual components of forest tree growth. In the proposed approach, the tree growth data typically correspond to the retrospective measurement of annual shoot characteristics (e.g. length) along the trunk. METHODS: Dedicated statistical models (semi-Markov switching linear mixed models) were applied to data sets of Corsican pine and sessile oak. In the semi-Markov switching linear mixed models estimated from these data sets, the underlying semi-Markov chain represents both the succession of growth phases and their lengths, while the linear mixed models represent both the influence of climatic factors and the inter-individual heterogeneity within each growth phase. KEY RESULTS: On the basis of these integrative statistical models, it is shown that growth phases are not only defined by average growth level but also by growth fluctuation amplitudes in response to climatic factors and inter-individual heterogeneity and that the individual tree status within the population may change between phases. Species plasticity affected the response to climatic factors while tree origin, sampling strategy and silvicultural interventions impacted inter-individual heterogeneity. CONCLUSIONS: The transposition of the proposed integrative statistical modelling approach to cambial growth in relation to climatic factors and the study of the relationship between apical growth and cambial growth constitute the next steps in this research.

AmapSim: a structural whole-plant simulator based on botanical knowledge and designed to host external functional models.

BACKGROUND AND AIMS: AmapSim is a tool that implements a structural plant growth model based on a botanical theory and simulates plant morphogenesis to produce accurate, complex and detailed plant architectures. This software is the result of more than a decade of research and development devoted to plant architecture. New advances in the software development have yielded plug-in external functions that open up the simulator to functional processes. METHODS: The simulation of plant topology is based on the growth of a set of virtual buds whose activity is modelled using stochastic processes. The geometry of the resulting axes is modelled by simple descriptive functions. The potential growth of each bud is represented by means of a numerical value called physiological age, which controls the value for each parameter in the model. The set of possible values for physiological ages is called the reference axis. In order to mimic morphological and architectural metamorphosis, the value allocated for the physiological age of buds evolves along this reference axis according to an oriented finite state automaton whose occupation and transition law follows a semi-Markovian function. KEY RESULTS: Simulations were performed on tomato plants to demonstrate how the AmapSim simulator can interface external modules, e.g. a GREENLAB growth model and a radiosity model. CONCLUSIONS: The algorithmic ability provided by AmapSim, e.g. the reference axis, enables unified control to be exercised over plant development parameter values, depending on the biological process target: how to affect the local pertinent process, i.e. the pertinent parameter(s), while keeping the rest unchanged. This opening up to external functions also offers a broadened field of applications and thus allows feedback between plant growth and the physical environment.

Analyzing growth components in trees.

Observed growth, as given, for instance, by the length of successive annual shoots along the main axis of a plant, is mainly the result of two components: an ontogenetic component and an environmental component. An open question is whether the ontogenetic component along an axis at the growth unit or annual shoot scale takes the form of a trend or of a succession of phases. Various methods of analysis ranging from exploratory analysis (symmetric smoothing filters, sample autocorrelation functions) to statistical modeling (multiple change-point models, hidden semi-Markov chains and hidden hybrid model combining Markovian and semi-Markovian states) are applied to extract and characterize both the ontogenetic and environmental components using contrasted examples. This led us in particular to favor the hypothesis of an ontogenetic component structured as a succession of stationary phases and to highlight phase changes of high magnitude in unexpected situations (for instance, when growth globally decreases). These results shed light in a new way on botanical concepts such as "phase change" and "morphogenetic gradient".

Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny.

BACKGROUND AND AIMS: The architecture of a plant depends on the nature and relative arrangement of each of its parts; it is, at any given time, the expression of an equilibrium between endogenous growth processes and exogenous constraints exerted by the environment. The aim of architectural analysis is, by means of observation and sometimes experimentation, to identify and understand these endogenous processes and to separate them from the plasticity of their expression resulting from external influences. SCOPE: Using the identification of several morphological criteria and considering the plant as a whole, from germination to death, architectural analysis is essentially a detailed, multilevel, comprehensive and dynamic approach to plant development. Despite their recent origin, architectural concepts and analysis methods provide a powerful tool for studying plant form and ontogeny. Completed by precise morphological observations and appropriated quantitative methods of analysis, recent researches in this field have greatly increased our understanding of plant structure and development and have led to the establishment of a real conceptual and methodological framework for plant form and structure analysis and representation. This paper is a summarized update of current knowledge on plant architecture and morphology; its implication and possible role in various aspects of modern plant biology is also discussed.

Epicormic branches: a growth indicator for the tropical forest tree, Dicorynia guianensis Amshoff (Caesalpiniaceae).

Architectural analyses of temperate tree species using a chronological approach suggest that the expression of epicormic branches is closely related to low growth rates in the axes that make up the branching system. Therefore, sole consideration of epicormic criteria may be sufficient to identify trees with low secondary growth levels or with both low primary and secondary growth levels. In a tropical tree such as Dicorynia guianensis (basralocus), where chronological studies are difficult, this relationship could be very useful as an easily accessible indicator of growth potentials. A simple method of architectural tree description was used to characterize the global structure of more than 1650 basralocus trees and to evaluate their growth level. Measurements of simple growth characters [height, basal diameter, internode length of submittal part (top of the main axis of the tree)] and the observation of four structural binary descriptors on the main stem (presence of sequential branches and young epicormic branches, state of the submittal part, global orientation), indicated that epicormic branch formation is clearly related to a decrease in length of the successive growth units of the main stem. Analysis of height vs. diameter ratios among different tree subgroups, with and without epicormic branching, suggested that trees with epicormic branches generally have a low level of secondary growth compared with primary growth.