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. 2022 Jul 21:2022:9758148.
doi: 10.34133/2022/9758148. eCollection 2022.

3dCAP-Wheat: An Open-Source Comprehensive Computational Framework Precisely Quantifies Wheat Foliar, Nonfoliar, and Canopy Photosynthesis

Tian-Gen Chang  1 , Zai Shi  1 , Honglong Zhao  1 , Qingfeng Song  1 , Zhonghu He  2   3 , Jeroen Van Rie  4 , Bart Den Boer  4 , Alexander Galle  4 , Xin-Guang Zhu  1
Affiliations

3dCAP-Wheat: An Open-Source Comprehensive Computational Framework Precisely Quantifies Wheat Foliar, Nonfoliar, and Canopy Photosynthesis

Tian-Gen Chang et al. Plant Phenomics. .

Abstract

Canopy photosynthesis is the sum of photosynthesis of all above-ground photosynthetic tissues. Quantitative roles of nonfoliar tissues in canopy photosynthesis remain elusive due to methodology limitations. Here, we develop the first complete canopy photosynthesis model incorporating all above-ground photosynthetic tissues and validate this model on wheat with state-of-the-art gas exchange measurement facilities. The new model precisely predicts wheat canopy gas exchange rates at different growth stages, weather conditions, and canopy architectural perturbations. Using the model, we systematically study (1) the contribution of both foliar and nonfoliar tissues to wheat canopy photosynthesis and (2) the responses of wheat canopy photosynthesis to plant physiological and architectural changes. We found that (1) at tillering, heading, and milking stages, nonfoliar tissues can contribute ~4, ~32, and ~50% of daily gross canopy photosynthesis (A cgross; ~2, ~15, and ~-13% of daily net canopy photosynthesis, A cnet) and absorb ~6, ~42, and ~60% of total light, respectively; (2) under favorable condition, increasing spike photosynthetic activity, rather than enlarging spike size or awn size, can enhance canopy photosynthesis; (3) covariation in tissue respiratory rate and photosynthetic rate may be a major factor responsible for less than expected increase in daily A cnet; and (4) in general, erect leaves, lower spike position, shorter plant height, and proper plant densities can benefit daily A cnet. Overall, the model, together with the facilities for quantifying plant architecture and tissue gas exchange, provides an integrated platform to study canopy photosynthesis and support rational design of photosynthetically efficient wheat crops.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1
Figure 1
Modeling wheat canopy architecture and light distribution. (a–e) Photographs of a tiller, the natural status of the leaves on the tiller, the flat shapes of the leaves (by covering a glass), the spikelets, and the front-view and side-view of the spike. (f–i) Reconstructed tiller skeleton, flat leaf shape, 3D spikelet, and 3D spike. (j) 3D reconstruction of a tiller. (k) Nitrogen contents of leaves on different positions of a tiller. (l) Relationship between leaf nitrogen content and leaf chlorophyll content (SPAD values). (m) Modeling leaf reflectance and transmittance based on the SPAD value. (n–p) An illustration of light reflectance and transmittance profiles, the 3D reconstructed canopy, and the light distribution within the canopy. Data measured from cultivar N22 were used.
Figure 2
Figure 2
Characterization of wheat spike photosynthesis. (a) A custom-built P-Chamber to measure gas exchange rates of nonfoliar tissues. (b) Temperature response pattern of relative photosynthetic and respiratory rates of a spike. (c) Simulated light distribution within a spike enclosed in a P-Chamber. (d) The measured and simulated photosynthetic light response curves of the intact and deawned spikes.
Figure 3
Figure 3
A ray-tracing-based model characterizing gas exchange of foliar and nonfoliar tissues in a canopy. (a) The measured and simulated daily dynamic gas exchange rates of the intact and deawned spikes. (b and c), temperature response patterns of leaf/stem photosynthetic and respiratory rates (normalized to 1 at 25°C). Photosynthetic rates were measured under a light level of 1500 μmol m−2 s−1. (d–g), relationship between tissue nitrogen content and the photosynthetic parameters. The four photosynthetic parameters are the net saturated photosynthetic rate (Amax_net), the maximal apparent quantum efficiency of CO2 fixation (ΦCO2), the convexity of the nonrectangular hyperbola (θ), and the dark respiration rate (Rd). Data measured from cultivar N22 were used. Arrows in panel (a) illustrate time when spike respiratory rates were measured.
Figure 4
Figure 4
A comprehensive validation of the 3dCAP-wheat canopy photosynthesis model by precise predicting canopy gas exchange at different growth stages, under different weather, and under different perturbations. (a–c) Canopy architecture, weather, and canopy photosynthesis at the tillering stage. (d–f) Canopy architecture, weather, and canopy photosynthesis at the heading stage. (g–i) Canopy architecture, weather, and canopy photosynthesis at the grain milk stage. (j) Increase of the diurnal net canopy photosynthesis by removing the spikes. (k) Changes of the diurnal net canopy photosynthesis by top-covering a PVC film with 90% transmittance and top-covering a scattering film with 90% transmittance and 50% scattering. (l and m) Temperature responses of canopy night respiratory rate (Rcd) and canopy photosynthetic rate under high light (Acnet_HL; PPFD >1500 μmol m−2 s−1) at the heading stage. Note that canopy night respiratory rate was normalized to 1 at 10°C (Rcd_10oC), while canopy photosynthetic rate under high light was normalized to 1 at 20°C (Acnet_HL_20oC). Data measured and simulated for cultivar N22 were used.
Figure 5
Figure 5
A landscape of photosynthetic characteristics of different foliar and nonfoliar tissues in the canopy. The 24-hour dynamic net gas exchange rate of different tissues in the canopy at the tillering (a), heading (c), and grain milk (e) stages on typical sunny days. The daily net photosynthesis, daily gross photosynthesis, daily light absorption, and daily light use efficiency (LUE) of different tissues at the tillering (b), heading (d), and grain milk (f) stages on typical sunny days. An (%): the ratio between tissue daily net photosynthesis and canopy daily net photosynthesis; Ag (%): the ratio between tissue daily gross photosynthesis and canopy daily gross photosynthesis; Ia (%): the ratio between tissue daily light absorption and canopy daily light absorption; LUE: the ratio between the daily gross photosynthesis and the daily light absorption. The cultivar N22 was used.
Figure 6
Figure 6
The change pattern of daily Acnet and daily spike gross photosynthesis with change in different spike traits. The spike traits are spike number (a), spike length (b), spikelet size (c), awn length (d), maximal photosynthetic capacity of the spikelets (e), and maximal photosynthetic capacity of the awns (f). The arrows show the real values of traits in wheat cultivar N22.
Figure 7
Figure 7
The conversion from tissue level photosynthetic capacity enhancement to canopy level daily net photosynthetic gain is dependent on covariation in tissue respiratory rate. (a–c) Change in daily net canopy photosynthesis with different leaf tissue nitrogen content at the tillering stage (a), the heading stage (b), and the grain milk stage (c) for wheat cultivar N22. (d–f) Change in daily net canopy photosynthesis with different leaf tissue nitrogen content at the tillering stage (d), the heading stage (e), and the grain milk stage (f) for wheat cultivar Y20. (g–h) The relationship between daily net canopy photosynthesis and maximal photosynthetic capacity of the uppermost leaves at the tillering stage (g), the heading stage (h), and the grain milk stage (i) for both cultivars. (j) The increase in daily net canopy photosynthesis by 10% increase of leaf/stem/spike maximal photosynthetic capacity (Amax), apparent quantum efficiency (ΦCO2), or both at the heading stage. The arrows show the real values of traits in wheat cultivar N22 or Y20.
Figure 8
Figure 8
Erect leaves, lower spike, shorter plant height, and proper plant density benefit canopy photosynthesis at the heading stage. (a–b) Responses of daily net tissue and canopy photosynthesis and light absorption to a 50% decreased stem height (a) or a 50% increased stem height (b). (c) The responses of daily net canopy photosynthesis to different manipulations of plant architecture: (1) leaving out the twisting feature of leaves; (2) straightening leaves along their initial direction at leaf base; (3) coinciding the base points of the spike and the uppermost leaf; and (4) a combination of (1), (2), and (3). (d) Plant density, diurnal Acnet, and daily Acnet under different combinations of row distance and plant density in a row.
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