Data obtained under controlled conditions and in the field at different plant densities show that the allometric coefficient between shoot N accumulation and shoot mass decreases with plant density.
Moreover, the quantity of N accumulated in the shoot per unit of LA appears remarkably constant (1.7 g N m–2 on average), regardless of the conditions: high versus low plant density, field versus controlled conditions, solution culture versus soil conditions. All of these factors could affect the developmental changes in the individual plant in terms of leaf:stem ratio. Consequently, these changes affect the dynamics of shoot N accumulation. It appears from these data that the developmental decrease in shoot N concentration as the plant gets bigger is the consequence of the developmental decline in leaf area ratio (LAR) or leaf weight ratio (LWR). This decline in LAR (or in LWR) is increased by plant density as a result of competition for light. These factors have a potential influence on biomass allocation, height growth, plant shape, and leaf morphology and physiology (Pons et al., 1989
). However, regardless of the cause of this change in plant development, it appears that the changes of shoot N accumulation by an individual plant seem to be determined by its LA or its leaf mass expansion. This type of empirical relationship between shoot N accumulation and LAI has been previously proposed for dense plant stands (Grindlay et al., 1993, for wheat; Plénet and Lemaire, 1999, for maize), whereas, in this study, a generalization of such a relationship at the level of the individual plant is proposed, regardless of its density within a wide range of conditions and its hierarchical position within the canopy in relation to light interception (shaded versus unshaded plants).
From a mechanistic point of view, LA expansion should be considered as the consequence of shoot N accumulation and not the reverse if we consider that shoot N represents N availability for leaf expansion (Hirose et al., 1996, 1997; Gastal and Nelson, 1994). This approach is correct when shoot N accumulation varies according to the level of N supply. Leaf expansion can then be analysed as a response to N supply. In this experiment, N supply is constant and what was observed through the relationships Nsh–Wsh or/and Nsh–LA (or Nsh–WL) is actually the feedback regulation of N uptake by plant growth or leaf expansion. Plant N uptake, regardless of the source of N supply (nitrate or ammonium uptake, or N2 fixation), is regulated by shoot N and C signalling: a positive signal from photosynthesis C supply and a negative one from organic N recirculating from shoot to root through the phloem (Cooper and Clarkson, 1989; Ismande and Touraine, 1994; Lejay et al., 1999; Touraine et al., 2001; Forde 2002), which act as a N satiety signal. Therefore, the proportionality between LA expansion and shoot N accumulation can be explained by the fact that LA expansion (i) increases the photosynthetic activity of the plant that provides larger quantities of C compounds to roots for supporting their N uptake activity and (ii) increases the capacity of plants to store organic N in leaves as in Rubisco (Millard, 1988). This last action is crucial to avoid the depletion of root N uptake capacity by recirculating N compounds such as amino acids. Therefore, the relationship between Nsh and LA could be interpreted as the consequence of the overall regulation of N uptake by plant growth itself. The slope of this relationship (1.7 g N m–2) represents the quantity of N that the plant is able to accumulate in the shoots for each additional unit of LA expansion. According to equation 2, as the plant gets bigger, each additional LA unit is accompanied by a greater proportion of biomass not directly involved in area expansion (leaf thickness or stem fraction), which is mainly composed of supporting and structural tissue. Therefore, as a result, a greater proportion of the 1.7 g N is allocated to this structural component with a low N concentration. Thus, as the plant gets bigger, an increasing proportion of its N content is allocated to non-photosynthetic tissues and is ‘diluted’ within structural tissues, as reflected in equation 1, that supports clearly the first hypothesis presented in the Introduction. These data show that this ‘dilution’ effect is accelerated by plant density because the plants adapt to competition for light through an increasing allocation of dry matter to structural tissues, i.e. stems. The shoot N accumulation capacity of plants is determined by the coefficient a/k1 of equation 2. The coefficient a is very sensitive to the level of N supply (Lemaire and Gastal, 1997), while Plénet and Lemaire (1999) showed that k1 was not affected by the level of N supply in maize. The coefficient a/k1 therefore reflects the level of plant N nutrition.
The results obtained on individual plants within a dense canopy also support the hypothesis that leaf growth determines the dynamics of N shoot accumulation (Fig. 5). Regardless of their hierarchical position within the canopy and, subsequently, independently of their access to light, plants with the same leaf mass accumulate similar quantities of N in shoots (leaf+stem). Suppressed plants have less leaf per unit shoot mass than dominant plants and, consequently, a lower N content for a similar shoot mass. This result supports the hypothesis that N is partitioned among individual plants within a dense stand in proportion to their contribution to the leaf area of the whole canopy. This result appears to be in contradiction with most of the recorded data that show that leaf N is not distributed uniformly within the canopy and that shaded leaves at the bottom of the canopy have a much lower N per unit area than unshaded leaves at the top (Hirose et al., 1988). However, this contradiction is only apparent. In Fig. 6, it can be observed that at the same leaf mass, suppressed plants have both a lower leaf and stem N concentration than dominant plants because they are shaded (Fig. 6A, B), in keeping with the second hypothesis presented in Introduction section. However, the suppressed plants develop a lower leaf:stem ratio because of a stronger competition for light. Therefore, for a similar leaf area (or leaf mass) they accumulate a greater quantity of N in their stems, leading to a shoot N per unit of leaf mass similar to that of dominant plants. Thus, within a dense stand, the competition for light between plants produces two different effects: (i) a decrease in leaf and stem N concentration of the more shaded plants that should lead to a decrease in shoot N per unit of leaf area or leaf mass, and (ii) a decrease in the leaf:stem ratio that leads to an increase in shoot N per unit leaf area or leaf mass. These two opposite effects result in a more or less constant shoot N per unit of leaf mass or leaf area. Therefore, the two hypotheses presented in the Introduction to explain N dilution in a dense canopy are not mutually exclusive and their combination leads to a remarkably constant plant N accumulation per unit of leaf area or leaf mass.
Unfortunately, these data do not allow it to be determined if it is leaf area or leaf mass that is the most relevant variable. A previous study by Lemaire
et al. (1991)
showed that in a dense lucerne crop, leaf mass per unit leaf area (
LMA) decreases from 4 to 2 mg cm
–2 from the top to the bottom of the canopy, respectively. A similar result was also reported by Anten
et al. (1998)
for another dicotyledonous herb (
Xanthium canadense). It can therefore be assumed that the leaves of the suppressed plants that grow within the lower layers of the canopy have lower
LMA than those of the dominant plants. Therefore,
equation 4 can be rewritten as:
| Nsh = a / k2L M A L A |
(5) |
that is the equivalent of
equation 2. If it is assumed that the
LMA of dominant plants is significantly higher than that of suppressed plants, then the quantity of N accumulated in shoot per unit of
LA (coefficient
a/
k1 of
equation 2) in dominant plants should be higher than in suppressed plants, explaining the small differences observed in terms of quantity of shoot N per unit leaf mass in
Fig. 5.
These data support the idea that competition for light among individual plants within a dense canopy induces developmental changes in plant morphology (leaf versus stem) and explains the differences observed in shoot N concentration. Different allometries among individual plants within different size categories were discussed earlier by Anten and Hirose (1998) in relation to light partitioning. Plants detect neighbour density and respond by an increase in stem or petiole elongation through a phytochrome-mediated shade avoidance response (Weiner, 1990; Varlet-Grancher and Gautier, 1995). This type of response leads to a lower leaf:stem ratio. Nevertheless, Anten and Hirose (1998) found that suppressed plants allocated a higher fraction of mass to leaves than dominant ones, which is apparently contradictory with this study's results. However, in Fig. 4B, comparisons between plant categories are made at similar shoot mass. When compared at similar dates, it is possible that the suppressed plants have higher leaf:stem ratios than the dominant plants only because they are smaller in size. This point demonstrates that comparisons of morphological plant traits such as leaf:stem ratio, LAR or LWR are only relevant if plants of a similar size are compared, and that the coefficients k1 and k2 of equations 2 and 4 provide intrinsic morphological plant traits for interspecific comparisons. In the same way, when the comparison between plant classes is made at the same date, the suppressed plants should have higher shoot N concentrations because they are smaller than the dominant plants, according to the ‘dilution effect’ described by equation 1. In fact, they have a slightly lower N% because they have a much lower leaf:stem ratio. Therefore, the partition of N among the population of plants within a dense canopy follows the partition of light. LA per plant should be a more relevant variable than leaf mass because it more closely reflects the contribution of each plant category in terms of light interception. If it is taken into account that suppressed plants intercept less light per unit of LA than dominant plants because they are more shaded, it can then be explained why they accumulate less N in their shoots than dominant plants at similar LA.
These results could be widely used in plant and crop modelling. It has been demonstrated that shoot N accumulation increases linearly with leaf area, both at the individual plant level as well as at the canopy level. In most crop models such as STICS (Brisson et al., 2003), APSIM (McCown et al., 1996), and CERES (Jones and Kiniry, 1986), LAI is calculated through a morphological sub-model related to temperature and water availability. LAI is then used to calculate the intercepted radiation. The relationship between shoot N and LAI that is proposed here could then be used in crop models for estimating the dynamics of crop N demand, i.e. the crop N uptake necessary to produce optimum LAI expansion and to provide the maximum interception of light.
It can be postulated that these observations within a population of plants of the same species could be extrapolated to multispecific plant populations, when plants of a given species are dominated by plants of other species (Hirose and Werger, 1994; Anten and Hirose, 1999). Some models are now able to simulate the proportion of incident light intercepted by the species components of a crop mixture (Sinoquet et al., 2000). In these types of situations, it could, therefore, be hypothesized that the sharing of N among the species within a crop mixture should be proportional to their respective contribution to the light interception, as suggested by the data on lucerne. It would be interesting to test this hypothesis with non N2-fixing species with different levels of N supply in the soil in order to analyse to what extent competition for light within plant communities can interfere with competition for soil N resources when soil N supply is limited.
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