Second International Symposium on Plant Growth Modeling, Simulation, Visualization and Applications

Concepts to model growth and development of plants

J. Vos Crop and Weed Ecology, Wageningen University, Haarweg 333, 6709 RZ, Wageningen, The Netherlands jan.vos@wur.nl Abstract
Models on plant function and plant structure need to describe two different aspects of plant performance: growth and development, including organogenesis. Growth results from light interception and photosynthesis, taking respiratory losses into account. Carbon partitioning and source-sink relations determine the growth rate of simultaneously growing organs. Development can be described as a temperature dependent rate of progression through the life cycle, but needs to include organogenesis and the fate of buds if the model addresses plant structure. The most important concepts used in modelling are highlighted, making a distinction between procesbased (crop) models and functional-structural models. It is stated that truly functional-structural models, that integrate aspects of plant structure and plant function, need extended knowledge of the factors responsible for dormancy or outgrowth of each bud.

E. Heuvelink Horticultural Production Chains, Wageningen University, Marijkeweg 22, 6709 PG Wageningen, The Netherlands ep.heuvelink@wur.nl
processes and give a detailed account of metabolism and plant growth in terms of mass variables [2]. Growth is derived from light interception; rules are defined to partition incremental growth over components (e.g. leaves, stems, roots), taking into account the factors and processes which affect productivity (e.g. temperature, nutrients, water and ambient CO2 concentration). FSPM also simulate (part of) the processes underlying growth, but simulate additionally the 3D structure of plants [3], often treating plants as a conjugation of elementary units such as phytomers or, alternatively named, metamers [2,4]. Examples of such dynamic models, combining divergent aspects of function and structure include LIGNUM [5, 6], ADEL-maize [7], Greenlab [8], LPeach [9], ADEL-wheat [10], GRAAL [11] and VICA [12]. Process-based and functional-structural models both need to deal with two distinct aspects of plant behaviour, i.e. growth and development. Growth concerns the increment in weight and volume; development is the (irreversible) progression through the successive stages of the growth cycle. Temperature is the main common determinant of growth and development. Growth starts with absorption of light and photosynthesis, followed by partitioning of substrates to growth centres and metabolism, involving respiration. In this paper development includes the rates and durations of initiation and expansion of organs and their active life spans. We shall highlight concepts for modelling growth and development that are used either in PBM, FSPM or in both.

1. Introduction
Since the first attempts some 40 years ago, modelling acquired an established position in plant sciences, agronomy and horticulture. Thornley [1] summarized the main purposes of modelling, i.e. (i) to describe and summarize data; (ii) to integrate subsystem knowledge yielding an understanding of the total system, and (iii) to make predictions of the behaviour of real systems and support practical management decisions. All models are simplified representations of a real system. The degree of simplification often depends on the purpose of the modelling exercise. In this context terms are used such as descriptive versus mechanistic models. For the current paper the distinction is relevant between process-based models (PBM) on the one hand and functional-structural plant models (FSPM) on the other hand. PBM simulate physiological

2. Light interception
In process-based crop models, individual leaves are not simulated. A state-variable commonly present in such models is the leaf area index, LAI (m2 leaf area per m2 soil surface). Often, modelling light

978-0-7695-2851-9/07 $20.00 IEEE 0-7695-2851-1/07 $20.00 20072007 IEEE DOI 10.1109/PMA.2006.17

interception is based on Monsi and Saeki [13], who observed: I = Io e kL, where I is the relative light intensity at a point in the plant canopy as a fraction of the light intensity above the plant canopy, I0, and L the leaf area, expressed in LAI units above the point of observation, while k is the light extinction coefficient. Light interception is obtained as (1- e kL)*I0. k is derived from a time series of paired measurements of I0, LAI and I near soil surface. In FSPM the spatial coordinates of each of the basic units are known, though at different degree of detail among modelling approaches. In a detailed approach the plant or plant canopy is represented by a collection of triangular planes or polygons with known coordinates of each of the corners of the polygon. In another (coarser) approach, the canopy space is divided into volume elements or voxels in each of which the amount of leaf present is characterized by mean properties such as leaf density and orientation distribution [14, 15]. Light interception can be calculated using various methods [16, 17]. Monte Carlo ray tracing is a stochastic method consisting of firing light rays from different directions and following their paths through the canopy. At each hit of green tissue the subsequent path of a ray depends on the optical properties of the plant material, i.e. on the probabilities of absorption, transmission and reflection (which, in turn, depend on wave length considered). Also the bi-directional reflection density function (BRDF) has to be taken into account. The BRDF relates the distribution of angles of reflected beams to those of incident beams. The ray tracing method involves few assumptions only and allows multiple scattering in different wavelengths to be calculated. Therefore the method is considered as a reference to other methods, but the demands on computing time may discourage routine use in plant and crop modelling. Radiosity methods allow multiple scattering to be quantified. The classical radiosity method [17, 18] is not suitable for a canopy composed of a number of virtual plants. However, the radiosity method was adapted for crop canopies [16, 17, 19]. This model, called nested radiosity (NR), calculates both the irradiance on and the energy absorbed by each virtual plant organ. To avoid border effects, NR infinitely repeats the simulated canopy. NR has been coupled to L-systems (using CPFG), using a dedicated interface, called Caribu [20]. VegeSTAR [21, 22] is another example of software allowing the visualization of 3-D digitized plants and the computation of light interception from image

processing of the virtual plant pictures. The software computes the values of the 'silhouette to total area ratio' (STAR values) by counting the coloured pixels corresponding to an organ class on the picture. The computation thus disregards multiple scattering and assumes leaves are black bodies. False colours are attributed to plant organs in order to distinguish them on the virtual plant pictures.

3. Photosynthesis
Possible approaches to compute growth from light absorption are not fundamentally different for PBM and FSPM. In the simplest approach, often used in crop growth models, incremental growth is obtained from multiplying the amount of absorbed light with the light use efficiency coefficient. This is based on the strong linear association between cumulative light absorption over time and dry matter accumulation of crops [23]. In this approach the calculation of gross photosynthesis and respiration are by-passed [24]. Photosynthesis (Pg) light response curves of leaves can be described with different saturation-type equations, e.g. a negative exponential relationship. These equations can be generalised to: Pg = Pg,max f(x) where Pg,max stands for the maximum rate of leaf photosynthesis, and x for the dimensionless group H/Pg,max, for the initial light use efficiency and H for absorbed radiation per unit leaf area. One of the most general functions for this relation f(x) is the nonrectangular hyperbola [25]. These models have 3 or 4 parameters that describe the response. Common parameters include the rate of dark respiration at zero light, the initial slope of the light response, and the (asymptote of) the maximum rate of photosynthesis at light saturation (Pg,max). Light-response curves are descriptive in nature, but the dominant parameter Pg,max shows a strong association with nitrogen mass per unit leaf area [26]. The photosynthetic capacity of leaves is related to the nitrogen content primarily because the proteins of the Calvin cycle and thylakoids represent the majority of leaf nitrogen [27]. In the widely-used biochemical photosynthesis model of Farquhar et al. [28], [29] the photosynthetic properties of the leaf are expressed in the basic characteristics of Rubisco enzyme kinetics and electron transport capacity. This approach enables an explanatory description of the temperature and CO2 dependence of photosynthesis. In the model, calculation of the Rubisco-regeneration limited CO2assimilation rate depends on whether it is insufficient ATP or NADPH that causes electron transport

limitation. A new, generalized equation that allows colimitation of NADPH and ATP on electron transport was presented by Yin et al.[29]. In comparison with the original model, the new model enables analysis of photosynthetic regulation via the electron transport pathways in response to environmental stresses. Especially at high light levels or when plants experience water stress, stomatal resistance may limit photosynthesis. Models for stomatal resistance do exist (reviewed in [30]), however, control of stomatal opening is complex and influenced by many factors [31].

serving as energy dissipating safety system [37] that is commonly not explicitly treated in plant modelling.

5. Source-sink partitioning

relations

and

carbon

4. Respiration
Paradigms on modelling respiration [32] often distinguish growth respiration from maintenance respiration and wastage or idle respiration. Growth respiration concerns the energy requirement of the biosynthesis of structural plant components. Maintenance respiration regards the energy required to maintain a living organism in steady state and includes protein turnover and the maintenance of ion gradients. These concepts were initially based on a statistical approach [33], splitting up total respiration into a component proportional to photosynthetic activity (i.e. growth respiration) and a component proportional to the standing biomass (i.e. maintenance respiration). Penning de Vries and co-workers [34, 35] calculated growth respiration coefficients from biochemical pathways and concluded that lumping plant products into carbohydrates, nitrogenous compounds (proteins), organic acids, lipids, lignins and minerals yields an appropriate estimation of the respiratory losses involved. Per unit weight of each of these categories of products coefficients were calculated for the requirements of glucose, oxygen and ATP and the production of CO2. This approach and these coefficients have not been fundamentally challenged since. In addition to growth respiration, respiratory cost of nitrate reduction, uptake of N and other ions, phloem loading and symbiotic N2 fixation can be modelled sufficiently accurately [36]. Conceptually and quantitatively maintenance respiration has remained a difficult phenomenon to model. In [36] it is stated that maintenance or residual maintenance (i.e. after accounting for all processes with known respiratory demands) is related to tissue N content and can be modelled phenomenologically, i.e. using empirical coefficients. Wastage or idle respiration is a nonphosphorylating or uncoupled (alternative) pathway,

Depending on conditions, plants widely differing in strucutural composition can grow from the same seed. Individual plant organs like leaves or internodes can show a large variation in size. Also the degree of branching (dicotyledonous species) or tillering (Gramineae) is strongly modified by conditions. At each stage of development active growth may occur simultaneously in several centers of growth in the plant. These phenomena indicate that plant modelling has to address the question: how to treat the simultaneous and successive growth of plant organs? (Review: [38].) In a simple approach particularly applicable in PBM of determinate plant species, descriptive functions are included describing the fraction of incremental growth being allocated to the groups of organs the model distinguishes, e.g. all leaves, stems or roots. The partitioning coefficients are commonly a function of the developmental stage, DVS, where DVS is the fraction at any time of the total thermal time (e.g. oC d) that is needed to complete a particular developmental phase (e.g. from emergence to flowering). This approach is called descriptive allometry and these models describe dry matter distribution often only under a limited range of growth conditions and cannot deal with dynamic fluctuations in dry matter allocation. Sink regulation models calculate source capacity, i.e. the amount of substrates available from concurrent production and reserves at each point in time, and assign sink strength to growing organs, i.e. a potential growth rate that is realized under conditions of non-limiting assimilate supply [39]. Such models depart from a number of assumptions: (i) all sinks draw on one common source (reserve pool), (ii) there is negligible resistance to transport of assimilates across the plant components, (iii) there is no preferential feeding of a sink by its nearest source. These assumptions have been shown to be realistic in many cases [38]. In each time step a particular organ i attracts a fraction fi of the available substrates equal to its share Si in the total sink strength SS, summed for all sinks; in formula: fi = Si / SSS Variable partitioning of assimilates to fruits and vegetative organs is an emergent property of this approach when applied to indeterminate crops.

FSPM allow local (i.e. organ level) calculation of photosynthesis. Because of the modular organization of such models one can calculate in each time step for each module the balance of production and consumption of assimilates, and the import or export of assimilates to adjacent modules. Such approaches are referred to by transport-resistance models [38, 40]. Ohms law analogies, that are applicable to transport of other substances than carbohydrates too, are used to calculate direction and magnitude of fluxes between modules [41]. An efficient implementation of this approach is given in [9] and [42], but parameterization may appear a demanding task. .

6. Development and organogenesis

In PBM crop development is commonly simply expressed as a DVS (previous section). The rate of progress of development is the fraction of the total heat sum that is accumulated during the time step considered. That heat sum can be made dependent on photoperiod in species where flowering or other developmental phenomena respond to photoperiod. Developmental stage and carbon partitioning are often linked in these models. It is an essential aim of FSPM to simulate the development of the 3D architecture and not just phenology, e.g. the appearance of flowers. Therefore, FSPMs need to deal in some degree of detail with organogenesis1: the initiation and formation of individual organs. Modelling development and organogenesis starts with the recognition of the basic plan of development, i.e. are we dealing with an annual or a perennial plant? Is it a monocarpic or a polycarpic species? Does the species show a determinate or an indeterminate growth habit? What kind of organs does the plant produce and where are the topological positions on the plant (e.g. potato with basal and apical branches, stolons, terminal tubers on stolons or on branches of stolons, terminal inflorescences). Based on the work of Hall and Oldeman (e.g.[44]) the term architectural model has acquired a special meaning in the botanical literature. These authors drew attention to the various typifying patterns of branching and flowering of plants, called architectural models, named after botanists. Examples

of such models include: Corners model, Leeuwenbergs model, and Rauhs model. The French AMAP community developed concepts of analysis of branching structures, recognizing systematic patterns on the one hand and stochasticity of expression of branching on the other hand [45, 46]. Software tools were developed aiding the measurement and analysis of plant structure [47] and tools to visualize or simulate 3D plants [48]. The second step in the quantification of development and organ formation boils down to measuring rates and duration of initiation and expansion of the organs and quantifying the duration of their active life span (e.g. [49]). Such rates and duration can be expressed in thermal time (e.g. [50]). The initiation and growth of fruits is a key determinant of yield in several crop species. Usually, the number of fruits is limited by abortion, rather than initiation. The fraction or number of non-aborting fruits is often simulated as a function of source and sink strength [25]. However, these models are mostly not very accurate and incorporation of stochastic elements or hormonal control might improve them [25, 51]. Commonly, ontogenetic changes are apparent in properties of phytomers along an axis. For instance, often a bell shaped pattern emerges if one plots the areas of successive leaves along the axis of a determinate crop as a function of phytomer number (e.g. [52, 53]). This means that the properties of phytomer n+1 can be related to those of phytomer n. In cereals the concept of phytomer shift and relative phytomer number (RPN) was developed [54] [55]. Phytomers with equal RPN share the same properties. For phytomers of the main axis their rank number is equal to their RPN. RPN of phytomers on tillers is the sum of the phytomer rank on the tiller in question plus a shift value, which is unique for each tiller type. Recognition of such patterns of inheritance of properties is important as it reduces the complexity of the model and fits well with often used object-oriented approaches of modelling. In FSPM the shape and spatial orientation needs to be defined for each organ. Without going into detail it is mentioned that there are also basic, conservative patterns here, e.g. phyllotaxis.

7. Linking structure and function

The previous section painted a rather descriptive approach to modelling development of the 3D structure. Probably it will always be needed to depart from some scheme of potential development of the

Another definition from [43] P. B. Green, "Organogenesis-a biophysical view," Annual Review of Plant Physiology, vol. 31, pp. 51, 1980.is: organogenesis is defined as the appearance of a new organ, initially as a protrusion, at a site where only a parent structure was present before.

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