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In grasses the phyllochron is defined as the time interval between the emergence of successive leaves above the pseudostem cylinder (whorl) made by sheaths of previously emerged leaves (Klepper et al., 1982). As reviewed by Skinner & Nelson (1995), the phyllochron depends on the simultaneous processes of leaf initiation, leaf elongation and construction of the dimension of the whorl. Despite this, for most grasses the phyllochron, expressed in thermal time, is conservative for long periods of plant development (Rickman & Klepper, 1995). It has not yet been elucidated how this regularity emerges from a complex dynamic system. According to Lafarge & Tardieu (2002), the regularity of the phyllochron arises from a genetically defined regularity in the timing of leaf elongation, when expressed in thermal time. Erickson & Michelini (1957); Maksymowych (1973); Hay & Kemp (1990) proposed that regularities in the leaf elongation scheme occurred because the development of all leaves is controlled by the same physiological clock: the rate of initiation of the primordia at the apex. Other authors (Sharman, 1942; Etter, 1951; Gallagher, 1979; Malvoisin, 1984; Wilson & Laidlaw, 1985; Durand et al., 1999; Fournier & Andrieu, 2000a) defend the idea of a self-regulating dynamic system in which the emergence of a leaf controls the elongation and thus the timing of emergence of the younger ones. In the context of architectural modelling, the later hypothesis is particularly appealing as it points to a constructor, rather than a descriptor, of plant form. Here we provide more details on the relationships between leaf emergence and leaf elongation, and elaborate a dynamic model.
The phases of grass leaf elongation have been related to the ontogeny of the growing zone by several authors (Williams, 1975; Martin, 1988; Skinner & Nelson, 1995; Durand et al., 1999; Fournier & Andrieu, 2000a; Muller et al., 2001) as follows (Fig. 1). In a first stage, cell division and elongation are coordinated so that mean cell length remains constant. During this stage the entire primordium is a homogeneous division zone, and might be associated with the first, exponential phase of elongation. In a second stage, cells stop dividing at the top of the division zone, giving rise to the ‘elongation only’ zone. In the later zone, cells elongate more rapidly than in the division zone. This produces the first phase change, which is an abrupt acceleration of the relative elongation rate (RER). Third, cells stop elongating at the end of the elongation zone, and enter the mature zone, marking the second phase change: the beginning of the quasi-linear phase of elongation. During this phase a quasi-steady influx of cells into the mature zone is established, which explains the relative stability of the leaf elongation rate. Ultimately, the growth zone regresses and gives rise to the fade-out phase of elongation.
Figure 1. Schematic representation of the time course of leaf length from primordial stage to maturity (a), and of the parallel ontogeny of the growth zone (b), as described by the model. Numbers indicate the different phases of leaf elongation. Vertical lines indicate times of major phase changes of leaf elongation and their corresponding ontogenic change in the growth zone. Inset, time course of leaf length in a semilogarithmic scale. During the first phase of leaf elongation (1) the leaf is considered as a unique compartment consisting of the division zone (DZ). At a given time the elongation-only zone (EOZ) is created by a flux of tissue from the division zone, resulting in an acceleration of leaf elongation (phase 2). Following a short delay, mature tissue leaves the EOZ and begins to accumulate in the mature zone (MZ). This progressively balances the influx of tissues from DZ, and gives rise to the quasi-linear phase of leaf elongation (3). Ultimately, the outflow from EOZ to MZ overcomes the influx from DZ and the leaf elongation rate decays (phase 4).
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This scheme applies to the ontogeny of the growth zone of the whole leaf (blade + sheath), as the position of the blade–sheath boundary inside the growth zone does not disturb its functioning (Schnyder et al., 1990; Ben Haj Salah, 1996). That is, this boundary is displaced passively within the growth zone as if it was stuck to a transverse cell wall. The characterization of blade and sheath elongation therefore consists only of being able to position the blade–sheath boundary at any arbitrary time of leaf ontogeny.
There is no definitive evidence that the emergence of leaf tips and leaf collars influences the ontogeny of the growth zone and the timing of phases of leaf elongation of that leaf or younger leaves, but two lines of circumstantial strongly support this hypothesis.
First, the length of the whorl has a strong influence on the elongation of the leaves that grow within. In pasture grasses, it is well known that cutting the whorl (by grazing) results in plants producing shorter leaves. More recent experimental studies (Davies et al., 1983; Wilson & Laidlaw, 1985; Casey et al., 1999), in which the length of the whorl has been manipulated (by means of sheath cutting, sheath incision and artificial sheath elongation with foil), demonstrated a direct effect of whorl length on both the blade and sheath length of leaves that grow within. More indirectly, Yu et al. (1975); Fournier (2000) and Ljutovac (2002) found that the relationships between leaf length and the length of the whorl they grew in were more stable in contrasted environmental conditions than classical relationships between leaf length and leaf position. Besides mature leaf length, the leaf elongation rate, the length of the growth zone, and cell flux toward the mature zone are also generally correlated with the length of the whorl the leaf grew in. Such a set of correlations was observed for leaves of different ranks by numerous authors (Robson, 1974; Kemp, 1980; Volenec & Nelson, 1983; Durand et al., 1995; Beemster et al., 1996), and for leaves of contrasting lengths from different genotypes (Fiorani et al., 2000; Arredondo & Schnyder, 2003). To summarize, it appears that longer whorls are generally associated with longer leaves, which grow more quickly primarily because they have a longer elongation zone that produces a higher cell flux.
A second line of evidence is that several synchronies exist between emergence events at the top of the whorl and the major phase changes in the kinetics of elongation of leaves (Fig. 1). The first phase of leaf elongation (exponential phase) was found to end nearly synchronously with the emergence of the collar of the leaf two ranks below (Ljutovac, 2002). The end of the transition from the exponential phase to the rapid elongation phase (quasi-linear phase) was found to coincide with the time of tip emergence of the previous leaf (Williams, 1975; Gallagher, 1979; Malvoisin, 1984; Tesarováet al., 1992; Skinner & Nelson, 1995; Lafarge & Tardieu, 2002; Ljutovac, 2002). The differentiation of the ligule at the base of the growth zone was reported to occur synchronously with emergence of the tip of the same leaf (Sharman, 1942; Tesarováet al., 1992; Skinner & Nelson, 1995). Finally, the end of rapid elongation phase, after which the elongation rate rapidly decays, was found to occur around the time of collar emergence (Williams, 1975; Girardin et al., 1986; Skinner & Nelson, 1995).
The existence of such synchronies suggests that the mode of action of emergence events on leaf elongation is via a triggering of their phase changes. The hypothesis of a triggering of the end of leaf elongation by collar emergence has long been proposed to explain why cutting the whorl results in shorter leaves (Sharman, 1942; Etter, 1951; Dobrynin, 1960). More recently, Durand et al. (1998) implemented triggering of the transition from blade to sheath elongation by the emergence of leaf tips in a model of leaf elongation, and were able to predict changes in mature length and of the blade–sheath ratio. Fournier & Andrieu (2000a, 2000b) suggested that triggering of early phase changes could control the length of the growing zone of maize internodes and explain subsequent effects on the elongation rate.
The objectives of this study are to model the relationships between the ontogeny of the growth zone and the phase changes of kinetics of elongation, and to analyse how this can help in interpreting the role of emergence events on leaf elongation in two published data sets.
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The hypothesis of direct control by emergence events of leaf growth zone ontogeny and elongation kinetics allows us to explain several important aspects of leaf elongation patterns in two contrasting cases. In the case of wheat, the hypothesis offers a synthetic explanation for the observed variation of elongation curves with leaf rank, together with the emergence of a regular phyllochron. In the tall fescue example, the hypothesis allowed us to understand better the effect of a temperature treatment, which could not be explained by a thermal time analysis.
The simple improvements we introduced into the model of Durand et al. (1999) allow for a realistic simulation of the first phases of elongation, and significantly ease the interpretation of its parameters. Particularly, the less intuitive ones, relating to the regulation of tissue fluxes between compartments, were associated with characteristic times of the elongation curve. This allows the model to infer the functioning of the growth zone, using only data on leaf and sheath elongation. The fitting exercise confirms almost all of the hypothesis used to build the model, and demonstrates its ability to predict realistic dependencies between phases, such as the differences in RER between leaves and sheaths during the transition period. However, the model lacks an automatic fitting procedure, and has some structural drawbacks for direct use in a predictive dynamic model. For example, conservation of parameter values in phyllochronic units is of no help for simulation, as the phyllochron is precisely dependent on the dynamic that is being modelled. A way to address this problem in future versions of the model might be to express more mechanistically the dependencies of adz and beoz on cell dynamics within the growth zone.
The physiological mechanism that underlies the triggering of leaf kinetics by emergence events remains unclear. The hypothesis of a role of light quality (Begg & Wright, 1962) is supported by experimental evidence of the direct effect of red/far-red ratio on leaf elongation (Skinner & Simmons, 1993), possibly acting at long distance via systemic signalling (Thomas et al., 2003). Alternatively, enrichment in ethylene within the whorl is realistic, and might affect leaf extension (Fiorani et al., 2002). Finally, a signal could be induced by direct contact of tips and collars with the ligule at the top of the whorl, as the ligule is known to deposit a lot of chemical compounds on growing leaves (Chaffey, 2000).
To conclude, the analysis presented here questions the classical approach of analysing and modelling leaf length as the product of elongation rate and duration of elongation, as both terms were found here to be dynamically determined during leaf growth. Understanding of how a plant regulates leaf length and leaf elongation therefore cannot be separated from the analysis and modelling of their relationships with leaf emergence. The model presented here offers a framework for such an analysis, but still needs to be adapted for use in predictive models. Architectural models of grasses, which consider both the elongation process at the level of individual leaves, and the modelling of whorl geometry (Fournier & Andrieu, 1998; Kaitaniemi et al., 1999; Werneke et al., 2000; Fournier et al., 2003), appear particularly well suited for the development of such applications.