Model behavior: finding out how to increase photosynthesis in C4 crops.

Abstract

How much corn can a single maize plant yield? How much sugar can be harvested from one sugarcane plant? Even when growth conditions are perfect, there is a maximum yield that a single plant can reach, because a plant only converts part of the received sunlight into biomass. C4 plants like maize (Zea mays), sorghum (Sorghum bicolor), sugarcane (Saccharum officinarum), and millet (Panicum miliaceum) have a higher photosynthetic energy conversion efficiency than C3 plants. At least, in theory. In practice, the efficiency for both C3 and C4 plants falls well below the theoretical maximum (Zhu et al., 2008). If the process by which crops fix carbon could be increased, yield could increase. To identify targets for engineering, mathematical modeling has proven valuable. For example, the productivity of tobacco (Nicotiana benthamiana) plants was improved by using the predictions of a model (Kromdijk et al., 2016). However, most models focus on constant, steady-state conditions. In the field, leaves are rarely in a steady state. A cloud, a gust of wind that moves the leaves of the canopy, a sun fleck…the light conditions crops experience in a field are continuously changing. In this issue, Yu Wang and her colleagues present a dynamic photosynthesis model for maize, sugarcane, and sorghum (Wang et al., 2021). All three crops use NADP-malic enzyme (NADP-ME) C4 photosynthesis, a subtype of C4 photosynthesis in which the NADP-dependent malic enzyme is the primary decarboxylation enzyme. To do this, Yu adapted a model that she developed 7 years ago to predict the CO2 assimilation rate under steady-state light conditions. That model consisted of a system of equations that describe the kinetics of the enzyme-catalyzed reactions of the C4 pathway in maize. To adapt the model to fluctuating light conditions, the researchers introduced new parameters (Figure). The enzymes that control carbon fixation are activated by light and deactivated in the absence of light. Under fluctuating light, these enzymes are intermittently activated and de-activated. Moreover, stomata open in response to light and close when subjected to darkness, which alters the amount of CO2 that is taken up by the leaf. The time that it takes for enzymes to get activated and reach a steady state, or for stomata to open after the transition from dark to light, is thought to affect photosynthetic efficiency. To include the reaction times of enzymes and stomatal dynamics in the model, the authors introduced new equations into the steady-state model that parameterize these processes. First, the authors introduced the induction response of the enzyme Pyruvate Phosphate Dikinase (PPDK), which plays an important role in improving the efficiency of carbon fixation in C4 plants. Next, they added the induction response of the key carbon assimilation enzyme Rubisco, and then the induction response of all other light-regulated enzymes. Finally, they added the speed of light-induced stomatal opening. To test how well the model performed, the researchers measured the rate of CO2 uptake and the stomatal conductance in maize, sorghum, and sugarcane plants that were undergoing dark–light transitions, and compared the data to the predictions of the model. The model was able to closely replicate the measurements and thus the authors could predict the factors that affect photosynthetic efficiency. PPDK activation, Rubisco activation, and stomatal dynamics were the major limitations predicted. The activation of other enzymes involved in carbon metabolism was not predicted to have a large effect. Based on their model, the authors think that there are several options to increase photosynthetic efficiency in C4 crops. For example, limitations caused by PPDK activation could be overcome by overexpression of the PPDK regulatory protein (PDRP). This protein regulates both activation and inactivation of PPDK by catalyzing the reversible phosphorylation of a threonine residue. Another option is to increase the activity of both Rubisco and Rubisco activase. Finally, speeding up stomatal opening and closing could increase photosynthetic efficiency, especially in maize, where the stomatal response is slow. Germplasm could be screened, using high-throughput thermal and modulated fluorescence techniques, to identify accessions with a quicker stomatal response. Another possibility is to engineer for smaller stomata, which appear to operate faster than larger stomata. Slow adjustment of photosynthesis to fluctuations in light is estimated to cost 10–40% of potential productivity in field crops (Taylor and Long, 2017; Zhu et al., 2004). There are many opportunities to increase the yield of C4 crops that use the NADP-ME subtype of photosynthesis.