High-Resolution Three-Dimensional Structural Data Quantify the Impact of Photoinhibition on Long-Term Carbon Gain in Wheat Canopies in the Field

Abstract

Photoinhibition reduces photosynthetic productivity; however, it is difficult to quantify accurately in complex canopies partly because of a lack of high-resolution structural data on plant canopy architecture, which determines complex fluctuations of light in space and time. Here, we evaluate the effects of photoinhibition on long-term carbon gain (over 1 d) in three different wheat (Triticum aestivum) lines, which are architecturally diverse. We use a unique method for accurate digital three-dimensional reconstruction of canopies growing in the field. The reconstruction method captures unique architectural differences between lines, such as leaf angle, curvature, and leaf density, thus providing a sensitive method of evaluating the productivity of actual canopy structures that previously were difficult or impossible to obtain. We show that complex data on light distribution can be automatically obtained without conventional manual measurements. We use a mathematical model of photosynthesis parameterized by field data consisting of chlorophyll fluorescence, light response curves of carbon dioxide assimilation, and manual confirmation of canopy architecture and light attenuation. Model simulations show that photoinhibition alone can result in substantial reduction in carbon gain, but this is highly dependent on exact canopy architecture and the diurnal dynamics of photoinhibition. The use of such highly realistic canopy reconstructions also allows us to conclude that even a moderate change in leaf angle in upper layers of the wheat canopy led to a large increase in the number of leaves in a severely light-limited state.

Figure 1.

Stages of the reconstruction of a single plant from multiple color images. A and D, An example photograph of a wheat plant including the calibration target, from one viewpoint, of the parent line (upright leaves) and line 2 (more curled leaves), respectively. B and E, Point cloud reconstruction: the output when each set of images is run through VisualSFM (Wu, 2011). C and F, The final output mesh after using the reconstructor software (Pound et al., 2014) with the ears removed.

Figure 2.

Wheat canopy reconstructions. All plots were made from single-plant reconstructions (as in Fig. 1), duplicated, randomly rotated, and spaced on a 3- × 3-plant grid. A, Parent line. B, Line 1. C, Line 2.

Figure 3.

Properties of each canopy. A, cLAI (Eq. 1): the area of leaf material per unity ground as a function of depth through the canopy at 12 pm. B, Fractional interception (Eq. 3) as a function of depth in the canopy at 12 pm. Curves were calculated with step Δd = 1 mm.

Figure 4.

Diagrams depicting the heterogeneity of light environment of the three contrasting wheat canopies. A, Density histogram showing the predicted light levels at 12 pm within each canopy described as the logarithm of the ratio of light received on a horizontal surface to light intercepted by a point on a leaf as a function of depth: parent line (left), line 1 (center), and line 2 (right). B, Frequency of PPFD values according to the fraction of surface area received at the top layer within each canopy: at 9 am (left), 12 pm, and 3 pm (right).

Figure 5.

Experimental validation of the predicted light levels. The logarithm of the ratio of light received on a horizontal surface to light intercepted by a point of a leaf (L_n[L/L₀]) predicted by ray tracing (box and whiskers) is compared with measurements made manually using a ceptometer (asterisks). Leaves were not all horizontal. Predicted and measured data are for line 2 in top, middle, and bottom layers in the canopy at 12 pm.

Figure 6.

Simplified overview of the modeling method.

Figure 7.

Data used for the parameterization of the photoinhibition model. A, Example light response curves from the top (flag leaf; black), middle (FL-1; dark gray), and bottom (FL-2; light gray) layers of line 2 (light response curves for the parent line and line 1 can be found in Supplemental Fig. S3). Values of the maximum photosynthetic capacity for each layer were obtained from fitting the nonrectangular hyperbola (Eq. 5) to each of the curves. The graph shows the experimental data (mean ± se of three measurements) and fitted curves. B, Dark-adapted F_v/F_m data per plot and layer measured at 12 pm. The means of five replicates are presented with sem. C, Distortion of Equation 5 based on parameters from top layer of line 2 and scenario 1 at 12 pm: reduction in ϕ (left), reduction in θ (center), and reduction in ϕ and θ (right).

Figure 8.

Results of the model: the predicted effect of photoinhibition on carbon gain (Eq. 10). A, Percentage reduction in carbon gain relative to a noninhibited canopy based on photoinhibition scenario 1, with depression in F_v/F_m occurring for 6 h around midday according to a hyperbolic relationship. B, Percentage reduction in carbon gain relative to a nonphotoinhibited canopy based on photoinhibition scenario 2, with depression in F_v/F_m beginning at dawn and ending at dusk according to a hyperbolic relationship. C, Percentage reduction in carbon gain relative to a nonphotoinhibited canopy based photoinhibition on scenario 1 as a function of the triangle angle relative to vertical. Results are for a distortion in both ϕ and θ. D, Graph indicating the importance of canopy architecture on the model output. The P_max and SF according to photoinhibition scenario 1 of line 2 were applied to the canopy and ray-tracing output of the parent line and vice versa. The difference in the percentage reduction in carbon gain was then calculated relative to the results obtained from the donor line. Positive values indicate a greater reduction in carbon gain for the parent line, whereas negative values indicate a greater reduction for line 2.

Figure 9.

Graph indicating the frequency of light levels as a function of the fraction of the total surface area of the canopy received at 12 pm by the top (A), middle (B), and bottom (C) layers in each canopy and the average irradiance, indicated by arrows, overlaid on the light response curve and distorted light response curve of line 2.