The heterogeneity and spatial patterning of structure and physiology across the leaf surface in giant leaves of Alocasia macrorrhiza

Abstract

Leaf physiology determines the carbon acquisition of the whole plant, but there can be considerable variation in physiology and carbon acquisition within individual leaves. Alocasia macrorrhiza (L.) Schott is an herbaceous species that can develop very large leaves of up to 1 m in length. However, little is known about the hydraulic and photosynthetic design of such giant leaves. Based on previous studies of smaller leaves, and on the greater surface area for trait variation in large leaves, we hypothesized that A. macrorrhiza leaves would exhibit significant heterogeneity in structure and function. We found evidence of reduced hydraulic supply and demand in the outer leaf regions; leaf mass per area, chlorophyll concentration, and guard cell length decreased, as did stomatal conductance, net photosynthetic rate and quantum efficiency of photosystem II. This heterogeneity in physiology was opposite to that expected from a thinner boundary layer at the leaf edge, which would have led to greater rates of gas exchange. Leaf temperature was 8.8°C higher in the outer than in the central region in the afternoon, consistent with reduced stomatal conductance and transpiration caused by a hydraulic limitation to the outer lamina. The reduced stomatal conductance in the outer regions would explain the observed homogeneous distribution of leaf water potential across the leaf surface. These findings indicate substantial heterogeneity in gas exchange across the leaf surface in large leaves, greater than that reported for smaller-leafed species, though the observed structural differences across the lamina were within the range reported for smaller-leafed species. Future work will determine whether the challenge of transporting water to the outer regions can limit leaf size for plants experiencing drought, and whether the heterogeneity of function across the leaf surface represents a particular disadvantage for large simple leaves that might explain their global rarity, even in resource-rich environments.

Figure 1. A typical leaf of Alocasia macrorrhiza (L.) Schott, showing the two transect directions for anatomical and physiological measurements.

Figure 2. Leaf anatomical and structural characteristics from the leaf base towards the apex adjacent to the midrib.

(a) leaf thickness, (b) the ratio of palisade to sponge tissue thickness (P/S ratio), (c) leaf mass per area (LMA), (d) chlorophyll concentrations per area, (e) guard cell length, (f) stomatal density, (g) minor vein length per unit leaf area (minor VLA). The X-axis represents the distance from the leaf base towards the apex within leaves (see Figure 1). Bars denote 1 SE. Each mean value at each point was the average of six leaf discs.

Figure 3. Leaf anatomical and structural characteristics from the leaf center to the outer regions adjacent to the secondary vein.

(a) leaf thickness, (b) the ratio of palisade to sponge tissue thickness (P/S ratio), (c) leaf mass per area (LMA), (d) chlorophyll concentration per area, (e) guard cell length, (f) stomatal density and (g) minor vein length per unit leaf area (minor VLA). The X-axis represents the distance from the center to the outer regions within leaves (see Figure 1). Bars denote 1 SE. Each mean value at each point was the average of six leaf discs.

Figure 4. Correlations of stomatal density with leaf vein length per area (VLA) within leaves of Alocasia macrorrhiza.

Data were fitted by linear regression. Error bars indicate ±1 SE.

Figure 5. Leaf physiological characteristics at midday on sunny days from the basal area towards the leaf apical area adjacent to the midrib and from the center to the outer region and adjacent to the secondary vein.

(a, b) stomatal conductance to water vapor (g _s), (c, d) CO₂ assimilation per leaf area (A), (e, f) the quantum yield of PSII (Φ_PSII), (g, h) leaf water potential. The X-axis indicates the distance from the leaf base towards the tip (left panels) or from the middle vein towards leaf lateral margin (right panels) as illustrated in Figure 1. Bars denote 1 SE. Each mean value at each point was the average of six leaf discs.

Figure 6. Thermal colour images and the diurnal time courses of leaf temperature in an Alocasia macrorrhiza leaf on a clear day during the rainy season.

In panel a, the different colors represent the differences of temperature within a whole leaf. In panels b (along the midrib) and c (along the secondary vein), the numbers with different colors indicate the distance from the leaf base towards the tip (left panels) or from the middle vein towards leaf lateral margin (right panels) within leaves. Numbers are the distance at the two directions.

Figure 7. Illustrations of leaf dieback in the marginal areas of Alocasia macrorrhiza.

Photos by S. Li and W.-L. Zhao.