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1.  Generalist insects behave in a jasmonate-dependent manner on their host plants, leaving induced areas quickly and staying longer on distant parts 
Plants are sessile, so have evolved sensitive ways to detect attacking herbivores and sophisticated strategies to effectively defend themselves. Insect herbivory induces synthesis of the phytohormone jasmonic acid which activates downstream metabolic pathways for various chemical defences such as toxins and digestion inhibitors. Insects are also sophisticated animals, and many have coevolved physiological adaptations that negate this induced plant defence. Insect behaviour has rarely been studied in the context of induced plant defence, although behavioural adaptation to induced plant chemistry may allow insects to bypass the host's defence system. By visualizing jasmonate-responsive gene expression within whole plants, we uncovered spatial and temporal limits to the systemic spread of plant chemical defence following herbivory. By carefully tracking insect movement, we found induced changes in plant chemistry were detected by generalist Helicoverpa armigera insects which then modified their behaviour in response, moving away from induced parts and staying longer on uninduced parts of the same plant. This study reveals that there are plant-wide signals rapidly generated following herbivory that allow insects to detect the heterogeneity of plant chemical defences. Some insects use these signals to move around the plant, avoiding localized sites of induction and staying ahead of induced toxic metabolites.
PMCID: PMC3574365  PMID: 23390101
Arabidopsis thaliana; behavioural resistance; Helicoverpa armigera; luciferase imaging; induced plant defence; Plutella xylostella
2.  Towards aspect-oriented functional–structural plant modelling 
Annals of Botany  2011;108(6):1025-1041.
Background and Aims
Functional–structural plant models (FSPMs) are used to integrate knowledge and test hypotheses of plant behaviour, and to aid in the development of decision support systems. A significant amount of effort is being put into providing a sound methodology for building them. Standard techniques, such as procedural or object-oriented programming, are not suited for clearly separating aspects of plant function that criss-cross between different components of plant structure, which makes it difficult to reuse and share their implementations. The aim of this paper is to present an aspect-oriented programming approach that helps to overcome this difficulty.
The L-system-based plant modelling language L+C was used to develop an aspect-oriented approach to plant modelling based on multi-modules. Each element of the plant structure was represented by a sequence of L-system modules (rather than a single module), with each module representing an aspect of the element's function. Separate sets of productions were used for modelling each aspect, with context-sensitive rules facilitated by local lists of modules to consider/ignore. Aspect weaving or communication between aspects was made possible through the use of pseudo-L-systems, where the strict-predecessor of a production rule was specified as a multi-module.
Key Results
The new approach was used to integrate previously modelled aspects of carbon dynamics, apical dominance and biomechanics with a model of a developing kiwifruit shoot. These aspects were specified independently and their implementation was based on source code provided by the original authors without major changes.
This new aspect-oriented approach to plant modelling is well suited for studying complex phenomena in plant science, because it can be used to integrate separate models of individual aspects of plant development and function, both previously constructed and new, into clearly organized, comprehensive FSPMs. In a future work, this approach could be further extended into an aspect-oriented programming language for FSPMs.
PMCID: PMC3189837  PMID: 21724653
L-system; aspect-oriented programming; Actinidia deliciosa (kiwifruit); functional–structural plant model; plant architecture; carbon dynamics; biomechanics; hormone transport
3.  A functional–structural kiwifruit vine model integrating architecture, carbon dynamics and effects of the environment 
Annals of Botany  2010;107(5):747-764.
Background and Aims
Functional–structural modelling can be used to increase our understanding of how different aspects of plant structure and function interact, identify knowledge gaps and guide priorities for future experimentation. By integrating existing knowledge of the different aspects of the kiwifruit (Actinidia deliciosa) vine's architecture and physiology, our aim is to develop conceptual and mathematical hypotheses on several of the vine's features: (a) plasticity of the vine's architecture; (b) effects of organ position within the canopy on its size; (c) effects of environment and horticultural management on shoot growth, light distribution and organ size; and (d) role of carbon reserves in early shoot growth.
Using the L-system modelling platform, a functional–structural plant model of a kiwifruit vine was created that integrates architectural development, mechanistic modelling of carbon transport and allocation, and environmental and management effects on vine and fruit growth. The branching pattern was captured at the individual shoot level by modelling axillary shoot development using a discrete-time Markov chain. An existing carbon transport resistance model was extended to account for several source/sink components of individual plant elements. A quasi-Monte Carlo path-tracing algorithm was used to estimate the absorbed irradiance of each leaf.
Key Results
Several simulations were performed to illustrate the model's potential to reproduce the major features of the vine's behaviour. The model simulated vine growth responses that were qualitatively similar to those observed in experiments, including the plastic response of shoot growth to local carbon supply, the branching patterns of two Actinidia species, the effect of carbon limitation and topological distance on fruit size and the complex behaviour of sink competition for carbon.
The model is able to reproduce differences in vine and fruit growth arising from various experimental treatments. This implies it will be a valuable tool for refining our understanding of kiwifruit growth and for identifying strategies to improve production.
PMCID: PMC3077975  PMID: 20855486
Actinidia deliciosa; kiwifruit; L-systems; plant architecture; carbon allocation; functional–structural plant model
4.  A functional–structural modelling approach to autoregulation of nodulation 
Annals of Botany  2010;107(5):855-863.
Background and Aims
Autoregulation of nodulation is a long-distance shoot–root signalling regulatory system that regulates nodule meristem proliferation in legume plants. However, due to the intricacy and subtleness of the signalling nature in plants, molecular and biochemical details underlying mechanisms of autoregulation of nodulation remain largely unknown. The purpose of this study is to use functional–structural plant modelling to investigate the complexity of this signalling system. There are two major challenges to be met: modelling the 3D architecture of legume roots with nodulation and co-ordinating signalling-developmental processes with various rates.
Soybean (Glycine max) was chosen as the target legume. Its root system was observed to capture lateral root branching and nodule distribution patterns. L-studio, a software tool supporting context-sensitive L-system modelling, was used for the construction of the architectural model and integration with the internal signalling.
Key Results
A branching pattern with regular radial angles was found between soybean lateral roots, from which a root mapping method was developed to characterize the laterals. Nodules were mapped based on ‘nodulation section’ to reveal nodule distribution. A root elongation algorithm was then developed for simulation of root development. Based on the use of standard sub-modules, a synchronization algorithm was developed to co-ordinate multi-rate signalling and developmental processes.
The modelling methods developed here not only allow recreation of legume root architecture with lateral branching and nodulation details, but also enable parameterization of internal signalling to produce different regulation results. This provides the basis for using virtual experiments to help in investigating the signalling mechanisms at work.
PMCID: PMC3077977  PMID: 20826439
Legume; soybean; soya bean; virtual plant; L-system; root reconstruction; synchronization; nodulation
5.  Computational Complementation: A Modelling Approach to Study Signalling Mechanisms during Legume Autoregulation of Nodulation 
PLoS Computational Biology  2010;6(2):e1000685.
Autoregulation of nodulation (AON) is a long-distance signalling regulatory system maintaining the balance of symbiotic nodulation in legume plants. However, the intricacy of internal signalling and absence of flux and biochemical data, are a bottleneck for investigation of AON. To address this, a new computational modelling approach called “Computational Complementation” has been developed. The main idea is to use functional-structural modelling to complement the deficiency of an empirical model of a loss-of-function (non-AON) mutant with hypothetical AON mechanisms. If computational complementation demonstrates a phenotype similar to the wild-type plant, the signalling hypothesis would be suggested as “reasonable”. Our initial case for application of this approach was to test whether or not wild-type soybean cotyledons provide the shoot-derived inhibitor (SDI) to regulate nodule progression. We predicted by computational complementation that the cotyledon is part of the shoot in terms of AON and that it produces the SDI signal, a result that was confirmed by reciprocal epicotyl-and-hypocotyl grafting in a real-plant experiment. This application demonstrates the feasibility of computational complementation and shows its usefulness for applications where real-plant experimentation is either difficult or impossible.
Author Summary
Endogenous signals, such as phytohormones, play a vital role in plant development and function, controlling processes such as flowering, branching, disease response, and nodulation. However, the signalling mechanisms are so subtle and so complex that details about them remain largely unknown. In this study, we develop a “Computational Complementation” approach for the investigation of long-distance signalling networks during legume autoregulation of nodulation (AON). The key idea is to use computational modelling to complement the deficiency of an empirical model of an AON deficient mutant with hypothesised AON components. If the complementation restores a wild-type nodulation phenotype, the modelled hypotheses would be supported as reasonable. To evaluate the feasibility of this approach, we tested whether wild-type soybean cotyledons participate in AON, commonly controlled by “real” leaves. The test gave an affirmative result (i.e., cotyledons do have AON activity), which was subsequently confirmed by a graft experiment on real plants. Future applications of this approach may be to test candidate AON signals such as auxins, flavones, and CLE peptides, and other plant signalling networks.
PMCID: PMC2829028  PMID: 20195551
6.  A Canopy Architectural Model to Study the Competitive Ability of Chickpea with Sowthistle 
Annals of Botany  2008;101(9):1311-1318.
Background and Aims
Improving the competitive ability of crops is a sustainable method of weed management. This paper shows how a virtual plant model of competition between chickpea (Cicer arietinum) and sowthistle (Sonchus oleraceus) can be used as a framework for discovering and/or developing more competitive chickpea cultivars.
The virtual plant models were developed using the L-systems formalism, parameterized according to measurements taken on plants at intervals during their development. A quasi-Monte Carlo light-environment model was used to model the effect of chickpea canopy on the development of sowthistle. The chickpea–light environment–sowthistle model (CLES model) captured the hypothesis that the architecture of chickpea plants modifies the light environment inside the canopy and determines sowthistle growth and development pattern. The resulting CLES model was parameterized for different chickpea cultivars (viz. ‘Macarena’, ‘Bumper’, ‘Jimbour’ and ‘99071-1001’) to compare their competitive ability with sowthistle. To validate the CLES model, an experiment was conducted using the same four chickpea cultivars as different treatments with a sowthistle growing under their canopy.
Results and Conclusions
The growth of sowthistle, both in silico and in glasshouse experiments, was reduced most by ‘99071-1001’, a cultivar with a short phyllochron. The second rank of competitive ability belonged to ‘Macarena’ and ‘Bumper’, while ‘Jimbour’ was the least competitive cultivar. The architecture of virtual chickpea plants modified the light inside the canopy, which influenced the growth and development of the sowthistle plants in response to different cultivars. This is the first time that a virtual plant model of a crop–weed interaction has been developed. This virtual plant model can serve as a platform for a broad range of applications in the study of chickpea–weed interactions and their environment.
PMCID: PMC2710251  PMID: 18375962
Plant architecture; virtual plant modelling; L-systems formalism; crop/weed competition; integrated weed management; chickpea; Cicer arietinum; sowthistle; Sonchus oleraceus
7.  Rice Morphogenesis and Plant Architecture: Measurement, Specification and the Reconstruction of Structural Development by 3D Architectural Modelling 
Annals of Botany  2005;95(7):1131-1143.
• Background and Aims The morphogenesis and architecture of a rice plant, Oryza sativa, are critical factors in the yield equation, but they are not well studied because of the lack of appropriate tools for 3D measurement. The architecture of rice plants is characterized by a large number of tillers and leaves. The aims of this study were to specify rice plant architecture and to find appropriate functions to represent the 3D growth across all growth stages.
• Methods A japonica type rice, ‘Namaga’, was grown in pots under outdoor conditions. A 3D digitizer was used to measure the rice plant structure at intervals from the young seedling stage to maturity. The L-system formalism was applied to create ‘3D virtual rice’ plants, incorporating models of phenological development and leaf emergence period as a function of temperature and photoperiod, which were used to determine the timing of tiller emergence.
• Key Results The relationships between the nodal positions and leaf lengths, leaf angles and tiller angles were analysed and used to determine growth functions for the models. The ‘3D virtual rice’ reproduces the structural development of isolated plants and provides a good estimation of the tillering process, and of the accumulation of leaves.
• Conclusions The results indicated that the ‘3D virtual rice’ has a possibility to demonstrate the differences in the structure and development between cultivars and under different environmental conditions. Future work, necessary to reflect both cultivar and environmental effects on the model performance, and to link with physiological models, is proposed in the discussion.
PMCID: PMC4246908  PMID: 15820987
Rice; Oryza sativa; morphogenesis; plant architecture; L-system; 3D modelling

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