Improving photosynthesis

Abstract

Photosynthesis is the basis of plant growth, and improving photosynthesis can contribute toward greater food security in the coming decades as world population increases. Multiple targets have been identified that could be manipulated to increase crop photosynthesis. The most important target is Rubisco because it catalyses both carboxylation and oxygenation reactions and the majority of responses of photosynthesis to light, CO₂, and temperature are reflected in its kinetic properties. Oxygenase activity can be reduced either by concentrating CO₂ around Rubisco or by modifying the kinetic properties of Rubisco. The C₄ photosynthetic pathway is a CO₂-concentrating mechanism that generally enables C₄ plants to achieve greater efficiency in their use of light, nitrogen, and water than C₃ plants. To capitalize on these advantages, attempts have been made to engineer the C₄ pathway into C₃ rice (Oryza sativa). A simpler approach is to transfer bicarbonate transporters from cyanobacteria into chloroplasts and prevent CO₂ leakage. Recent technological breakthroughs now allow higher plant Rubisco to be engineered and assembled successfully in planta. Novel amino acid sequences can be introduced that have been impossible to reach via normal evolution, potentially enlarging the range of kinetic properties and breaking free from the constraints associated with covariation that have been observed between certain kinetic parameters. Capturing the promise of improved photosynthesis in greater yield potential will require continued efforts to improve carbon allocation within the plant as well as to maintain grain quality and resistance to disease and lodging.

Figure 1.

Targets for improving photosynthesis. Processes associated with light capture from the canopy to the thylakoid membranes are shown on the left side, while conductances for CO₂ diffusion are shown along the top. Chloroplast processes, dominated by Rubisco, other limiting enzymes, and CO₂-concentrating mechanism components are shown on the right side. Complex traits where metabolic pathways are modified are shown along the bottom. SBPase, Sedoheptulose bisphosphatase.

Figure 2.

Canopy gross CO₂ assimilation rate as a function of irradiance. Data measured with a wheat crop (Evans and Farquhar, 1991) are as follows: leaf area index, 7.1; leaf temperature, 22°C; ambient CO₂ partial pressure, 340 µbar. Lines are as follows: 1, maximum photon yield for C₃ plants in the absence of photorespiration (0.088 mol of CO₂ per mol of PAR photons); 2, maximum photon yield for C₄ plants (0.069); 3, photon yield for C₃ plants in normal atmosphere (0.058); 4, response curve for gross canopy CO₂ assimilation; 5, response curve for a single wheat leaf. Curve parameters are as follows: light-saturated gross CO₂ assimilation rate, 135 or 30 µmol CO₂ m⁻² s⁻¹ for the canopy and leaf, respectively; Θ (the convexity term), 0.7 using Equation 1a from Ögren and Evans (1993). On the right side, four regions for improvement are indicated: A, reducing photorespiration; B, increasing photosynthetic capacity; C, reducing losses due to non-steady-state conditions and sink limitations; D, increasing the PAR waveband.

Figure 3.

Comparison of Rubisco kinetic parameters from different species and transgenic constructs to examine whether parameters can vary independently. A, K_c versus k_cat (25°C except for data from Ishikawa et al. [2009, shown in blue measured at 28°C). Due to the variability in assay results between studies, separate regressions are shown for subsets of species measured in blue (K_c = −97 + 303 k_cat [r² = 0.87]; Ishikawa et al., 2009, 2011) and in red (K_c = −156 + 160 k_cat [r² = 0.97]; Whitney et al., 2011b). B, Γ_* (which is inversely related to the specificity factor; Eq. 2) versus k_cat. The regression equations are Γ_* = 33 + 3.8 k_cat (r² = 0.22; black line, all data) and Γ_* = 47 + 0.53 k_cat (r² = 0.23; red line, Flaveria spp. data). Hollow and solid black squares represent C₃ and C₄ species, respectively, combined from Parry et al. (2011) and Whitney et al. (2011a); red solid triangles are from Whitney et al. (2011b); blue hollow and solid hexagons are C₃ and C₄ species, respectively, from Ishikawa et al. (2009); and blue circles are from Ishikawa et al. (2011) as follows: hollow circle, rice; solid circle, sorghum; half-solid circle, chimeric Rubisco with rice large subunits and sorghum small subunits.

Figure 4.

Relationships between CO₂ assimilation rate per Rubisco site and Rubisco k_cat for C₃ and C₄ species. A, Performance in a C₃ leaf calculated using Rubisco kinetic parameters from Parry et al. (2011) at 25°C and assuming a partial pressure of CO₂ in the chloroplast of 200 µbar (Eq. 3). B, Performance of C₄ species recalculated from Ghannoum et al. (2005) at 30°C, differentiating between two decarboxylation subtypes. ME, Malic enzyme.

Figure 5.

Dependence of carboxylation yield on CO₂ partial pressure and temperature. Carboxylation yield, ϕ (mol CO₂ assimilated per mol electron in linear electron transport) is described by the function (Farquhar and von Caemmerer, 1982), where Γ_* is the CO₂ compensation point in the absence of day respiration (Eqs. 1 and 2). This equation assumes that NADPH regeneration limits photosynthesis. The temperature dependence of Γ_* is taken from Brooks and Farquhar (1985).

Figure 6.

Relative photon yield for a C₃ leaf as a function of Γ_*. Relative and a constant value for C are assumed (235 µbar). The temperature response function of Γ_* was measured with spinach (Brooks and Farquhar, 1985), and the squares indicate 5°C increments. The striped area illustrates the range in Γ_* that has been found for diverse terrestrial plants, including both C₃ and C₄ species (Kent and Tomany, 1995; Evans and Loreto, 2000; Galmes et al., 2005; Parry et al., 2011). To interconvert between Γ_* and S_c/o, divide 3,961 by Γ_* or S_c/o (valid for 25°C; von Caemmerer et al., 1994); that is, a value of 40 µbar for Γ_* is equivalent to 99 for S_c/o.

Figure 7.

Radiation use efficiency as a function of year of release for wheat cultivars in the United Kingdom (UK; Shearman et al., 2005) and Australia (Sadras et al., 2012). The slope of the regression in both cases was 0.011 g MJ⁻¹ year⁻¹. Radiation use efficiency, calculated using PAR, was determined for growth between the stages of stem elongation and flowering.