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Environment-coupled metabolic models for engineering high-temperature and drought REsistant LEAF metabolism.

Periodic Reporting for period 1 - Re-Leaf (Environment-coupled metabolic models for engineering high-temperature and drought REsistantLEAF metabolism.)

Reporting period: 2018-08-02 to 2020-08-01

Nearly all plants use energy from sunlight and carbon dioxide from the air to generate sugars and oxygen in a process called photosynthesis. Throughout evolutions different types of photosynthesis have evolved to allow plants to grow in various habitats. Most plants perform C3 photosynthesis. These, so called, C3 plants open their stomata - pores on the leaf’s surface that allow for gas exchange - during the day and carbon dioxide uptake and conversion to sugars proceeds at the same time. While this process is energetically efficient it can lead to high water loss in hot and dry climates. Therefore, some plant species have evolved Crassulacean Acid Metabolism (CAM), a type of photosynthesis where carbon dioxide is taken up at night and initially fixed to form an acid that is stored in specialized storage compartments termed vacuoles. During the day, when sufficient energy from the sun is available this acid is used to build energy-rich sugars. Some plants can switch from one type of photosynthesis to the other or operate in an intermediate state - depending on the environment.
There is great interest in engineering more drought-resistant crop species by introducing CAM into C3 plants. However, one of the open questions is whether full CAM or alternative water saving modes would be more productive in the environments typically experienced by C3 crops.
To answer this question we utilized a mathematical model that describes the leaf’s metabolism in dependence of environmental parameters such as temperature and relative humidity. This model allowed us to quantify the productivity and water loss of a plant leaf operating in C3, CAM or alternative modes across a wide range of environments.
The model predicted that vacuolar storage capacity in the leaf is a major determinant of the extent of the CAM. We identified a novel metabolic route for fixation of carbon dioxide at night that differs from the canonical CAM cycle. This alternative water saving pathway involves an additional carbon dioxide fixing enzyme termed ICDH. We furthermore demonstrate that introducing this metabolic cycle does not significantly increase the total cost of producing the metabolic machinery of the cell. Simulations across a wide range of environmental parameters show that the water saving potential of CAM strongly depends on the environment and that the additional water saving effect of carbon fixation by ICDH can reach up to 4% for the conditions tested. Insights generated from these modelling studies address the urgent need to develop water-use efficient crop species that maintain high productivity in large range of current and future environments.
We have devised a novel computational framework that allows us to study the impact of environmental parameters such as light intensity, temperature and relative humidity on plant leaf metabolism. This was achieved by extending a previously established framework for integrated diel (day-night) flux balance analysis of leaf metabolic networks (Cheung et al (2014) Plant Physiol 165: 917–929). In our model of leaf metabolism we account for water-loss through the stomata in dependence of the diel cycle of temperature and relative humidity as well as the leaf’s demand for carbon dioxide. As a result of imposing a water saving optimisation objective to our model we observe the emergence of CAM-like and full CAM behaviors. Thus, this study presents the first quantitative analysis of leaf metabolic fluxes in response to environmental parameters such as light, temperature and relative humidity.
The generated insight into plant leaf metabolism in different environments might lead to patentable and commercially exploitable results if research results were to be implemented by academic or industry partners who are attempting to engineer CAM photosynthesis in C3 plants.