6.1.3  Leaf area

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(a)  Patterns of cell division and cell enlargement

LAR can be an important driving variable for whole-plant growth so that dynamics of leaf expansion will underpin RGR responses to genetic and environmental effects. Indeed, variation in LAR is frequently perceived as having more direct impact on whole-plant growth than variation in NAR. Accordingly, leaf growth deserves some attention in this present context of plant growth analysis.

Leaves are first discernible as tiny primordia which are initiated by meristems in strict accord with a genetically programmed developmental morphology. As shoot growth proceeds, dicotyledonous primordia undergo extensive cycles of cell division (peak doubling time c. 0.5 d) emerging as recognisable leaves that unfold and expand. Lamina expansion follows a coordinated pattern of cell division and cell enlarge-ment that is under genetic control but modified by the environment. Final leaf size and shape vary accordingly.

Leaf growth in grasses (monocotyledons) such as rice, wheat, coarse grains and pasture grasses is qualitatively different from that in broad-leafed plants (dicotyledons) such as sun-flower, cucurbit, tobacco and pasture legumes. Primordia of dicotyledons bear a superficial resemblance to those of monocotyledons, but as grass leaves emerge cell division is confined to basal meristems which give rise to a zone of cell expansion. Leaf maturation proceeds from tip to base. Cell division and cell enlargement proceed concurrently, but are separated spatially. By contrast, broad-leafed plants show more of a temporal separation where a phase of cell division precedes a subsequent phase of cell enlargement (but with some overlap as discussed later). Notwithstanding such distinctions in cell growth dynamics, the net outcome for area increase is similar. Lamina expansion in both monocotyledons and dicotyledons is approximately sigmoidal in time and asymmetric about a point of inflexion which coincides with maximum rate of area increase.


Figure 6.2 Leaves of cucumber (node 2 on plants in growth cabinets) show an approximately sigmoidal increase in area with time (broken lines) where final size and cell number vary with daily irradiance (0.6, 1.9 or 4.4 MJ m-2 d-1). During an initial exponential phase in area growth, cell number per leaf (solid lines) also increases exponentially. The slope of a semi-log plot (hence relative rate of cell division) is higher under stronger irradiance. Cell number per leaf approaches asymptote (sell division slows) as leaf area becomes linear (Based on Milthorpe and Newton 1963)

Taking cucumber as an archetype for dicotyledonous leaves (Figure 6.2), this inflexion point occurs later under lower irradiance (compare data on leaf area increase under 0.6 with 4.4 MJ m–2 d–1 in Figure 6.2). Early expansion of leaf primordia is driven primarily by cell division, and cell number per leaf increases exponentially prior to unfolding (solid lines in Figure 6.2). Rate of cell division during this early phase is increased by irradiance, so that potential size of these cucumber leaves at maturity is also enhanced. Using the upper curves in Figure 6.2 as an example (highest irradiance), cell number per lamina reaches a plateau around 20 d, but area continues to increase to at least 30 d. Clearly, expansion of existing cells is largely responsible for lamina expansion between 20 and 30 d after sowing.

While the initial (exponential) phase of dicotyledonous leaf growth is driven largely by cell division, and the sub-sequent (asymptotic) phase is largely due to enlargement of the resulting cell population, the distinction between these two phases is somewhat arbitrary. Improved techniques for tissue maceration and cell counting have shown that cell division can continue well into the cell-expansion phase of leaf growth. Formation of such new cells is conservative, but does mean that about 90% of cells in a mature cucumber leaf can originate subsequent to unfolding. Data for tobacco and sunflower are closely comparable to those shown here for cucumber (see Table 2 in Dale 1982).


Figure 6.3  Carbon exchange by a cotton leaf (node 7 main stem under cloudy conditions; photon irradiance 17 mol quanta m-2 d-1) shows a peak in both net photosynthesis and export of photoassimilate as leaf growth (expansion) slows. An initial phase of carbon import helps sustain early expansion (shown here as a negative export). Positive export of photoassimilate is evident after about 9 d, coinciding with rapid expansion and a time of maximum carbon investment in leaf growth. (Note expanded scale for growth and respiration) (Based on Constable and Rawson 1980)

Contrasting time-courses for cell division and subsequent enlargement hold implications for leaf function. For example, epidermal layers usually cease division ahead of mesophyll tissues so that leaf thickness can increase for some time after leaves reach full size (Dale 1976, 1982) and by implication have a greater depth of photosynthetic tissue. Typically, photosynthetic capacity will reach a maximum just before leaves reach full size (Figure 6.3) although export of photosynthetic products does not peak until leaves are at full size (dashed line in Figure 6.3; Figure 5.12). Cell division has normally ceased at that stage (see Table 6 in Dale 1976).

(b)  Resources for cell division and cell enlargement

In leaves of both dicotyledons and monocotyledons, cell number dictates potential size, but expression of that potential is determined by cell enlargement, and these two phases of lamina expansion have distinct needs. Cell division is substrate intensive but cell enlargement is not, and carbon requirement for later phases of leaf growth is demonstrably small. In cotton, for example (Figure 6.3), local photosynthesis plus some imported substrate were necessary for early expansion but a net export of photoassimilate was apparent within only 7–8 d of unfolding. Respiratory losses were at most only 10% of daily fixation with remaining photoassimilate going to export.

During leaf expansion, volumes of constituent cells can increase 10–100-fold depending upon location and function, cells such as spongy mesophyll showing the greatest increase and guard cells the least. Photoassimilate is readily available and generally sufficient (discussed above) but a positive turgor must be sustained for cell enlargement and leaf expansion which in turn depends on water plus inorganic resources that must all be imported. A reliable supply of nitrogen, phosphorus, potassium and magnesium is crucial (Dale 1982) and especially significant for synthetic events within enlarging cells. Chloroplast replication in spinach is a case in point where plastid numbers per cell increase from 10 or 20 at leaf unfolding up to 200 per cell in full-sized leaves (Possingham 1980).

Nutrient requirements to sustain such prodigious syntheses are substantial, and again taking cucumber as indicative of broad-leafed plants Milthorpe (1959) demonstrated that rate of leaf production (and by impliction cell division in terminal meristems) was comparatively insensitive to depletion of external nutrients whereas expanding leaves had a high demand. Similarly leaf growth in subterranean clover (Trifolium subterraneum) proved more sensitive to potassium and magnesium deficiency than did photosynthesis, so that photoassimilate actually accumulated in nutrient-deficient plants (Bouma et al. 1979).

(c)  Mathematical analysis of leaf expansion

The collective activities of cells in an expanding lamina are amenable to mathematical analysis. Despite differences between monocotyledons and dicotyledons in spatial and temporal patterns of leaf growth, as well as differences between dividing cells and enlarging cells in their requirements for carbon and nutrients, growth curves for single leaves can prove instructive.


Figure 6.4 Leaf expansion in sunflower shows a sigmoidal increase in lamina area with time where relative rate of area increase (r) and final size (Ax) both vary with nodal position, reaching a maximum around node 20 (based on Rawson and Turner 1982)

Differences in canopy development (genetic or environmental causes) can be attributed to three sources, namely (1) frequency of new leaf initiation, (2) size of primordia and (3) time-course of lamina expansion. All three sources can be inferred to some extent from comprehensive measurement of lamina expansion by successive leaves, and a determinate plant such as sunflower (Figure 6.4) provides a convenient example. The curves in Figure 6.4 were drawn by hand through all data points (two measurements of leaf length (L) and leaf breadth (B) per week with area (A) estimated from the relationship A = 0.73 (L × B)). Leaf area (A) is shown as a function of time for eight nodes selected between node 6 and node 40.

Curves change shape in a characteristic fashion according to node position, and carry important implications for underlying growth processes. Node 20 produced the largest leaf on this plant, while slowest growth and smallest final size was recorded for node 40 (adjacent to the terminal inflorescence).

Frequency of leaf initiation can be inferred from a more comprehensive family of such curves where early exponential growth in area for each successive leaf is recorded and plotted as log10 area versus time. This results in a near-parallel set of lines which intersect an arbitrary abscissa (Figure 6.5). Each time interval between successive points of intersection on this abscissa is a ‘phyllochron’ and denotes the time interval between comparable stages in the development of successive leaves. This index is easily inferred from the time elapsed between successive lines on a semi-log plot (Figure 6.5). Cumulative phyllochrons serve as an indicator of a plant’s physiological age in the same way as days after germination represent chronological age.


Figure 6.5   Leaves of subterranean clover achieve a 10-million-fold increase in size from primordium to final area (volume of primordia shown as dotted lines; leaf fresh mass shown as solid lines). Successive leaves are initiated and enlarge in a beautifully coordinated fashion revealed here as a family of straight lines on a semi-log plot. Intervals along an arbitrary abscissa (arrow at 100 × 10-3 mm3) that intersects theses lines represent time elapsed (about 1.8 d) between attainment of a given development status by successive leaves (phyllochron). Full-sized leaves exceed about 100 mm3 in volume (Based on Williams 1975)

The dynamics of lamina expansion following leaf unfolding in dicotyledons, or of leaf extension in monocotyledons, is a third and most definable source of variation in canopy development. Each leaf follows a qualitatively similar time-course (e.g. Figure 6.5) and is commonly described by a Richards (1959, 1969) function reparameterised by Cromer et al. (1993) to yield:



The four parameters Ax, t0, r and d have a clear geometric meaning. Ax (cm2) stands for the final area attained by a leaf, and is the asymptotic value for A at large t, t0 (d) is the time when A(t) undergoes inflexion from initially exponential to subsequently asymptotic increase, r (d–1) is relative rate of area increase by a leaf (RGRAREA) with an area of A(t) at t0, and d determines the shape of the curve of A versus t (larger d results in an inflexion point higher up the curve).

Mathematical analysis of leaf expansion now becomes a vehicle for defining environmental effects on canopy devel-opment, or for making genetic comparisons. Some examples of environmental effects on A(t) and r are given later (Section 6.2).