Journal Article

Evolution of C4 photosynthesis predicted by constraint-based modelling

Bräutigam, Andrea, Blätke, Mary-Ann

2019

Overview

Constraint-based modelling (CBM) is a powerful tool for the analysis of evolutionary trajectories. Evolution, especially evolution in the distant past, is not easily accessible to laboratory experimentation. Modelling can provide a window into evolutionary processes by allowing the examination of selective pressures which lead to particular optimal solutions in the model. To study the evolution of C4 photosynthesis from a ground state of C3 photosynthesis, we initially construct a C3 model. After duplication into two cells to reflect typical C4 leaf architecture, we allow the model to predict the optimal metabolic solution under various conditions. The model thus identifies resource limitation in conjunction with high photorespiratory flux as a selective pressure relevant to the evolution of C4. It also predicts that light availability and distribution play a role in guiding the evolutionary choice of possible decarboxylation enzymes. The data shows evolutionary CBM in eukaryotes predicts molecular evolution with precision. Virtually all plants use energy from sunlight to convert carbon dioxide and water into oxygen and sugars via a process called photosynthesis. This process has many steps that each rely on different enzymes to drive specific chemical reactions. Most plants use a pathway of enzymes that is referred to as C3 photosynthesis. Plants absorb carbon dioxide gas from the atmosphere. However, the levels of carbon dioxide in the atmosphere are very low, so this limits the amount of photosynthesis plants can perform. To overcome this problem, some plants have evolved a different type of photosynthesis – called C4 photosynthesis – with a mechanism that increases the levels of carbon dioxide in the cells. Today, plants that use C4 photosynthesis (so-called ‘C4 plants’) typically grow faster than other plants, especially in warmer climates. This gives C4 plants, such as corn, an advantage over their competitors and also helps them to colonize harsh environments that other plants struggle to thrive in. However, it remains unclear how C4 photosynthesis evolved in some plants living in wet habitats, or why other plants use forms of photosynthesis that are intermediate between C4 and C3 photosynthesis. C4 photosynthesis uses pathways containing enzymes that are found in all plants; therefore, C4 plants evolved by changing how they used enzymes they already had. To understand how these different enzyme pathways may have evolved, Blätke and Bräutigam used an approach known as constraint-based modelling. The researchers built a mathematical model of C3 photosynthesis and used it to predict the optimal enzyme pathways (for example, pathways involving the fewest enzymes or requiring the least energy) for photosynthesis under particular conditions. The model predicted that, in addition to shortages in carbon dioxide, shortages in an important plant nutrient known as nitrogen may have driven the evolution of C4 photosynthesis. Furthermore, enzyme pathways that were intermediate between C3 and C4 photosynthesis were predicted to be optimal solutions under particular conditions. Together, the findings of Blätke and Bräutigam may explain why different variations of C4 photosynthesis exist in plants. These findings could be used to breed crops that use the most efficient type of photosynthesis for the conditions they are grown in, leading to better yields.

• Publisher: eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Acids / Arabidopsis - metabolism / Biological Evolution / C4 photosynthesis / Carbon / Carbon - metabolism / Carbon Dioxide - metabolism / Chloroplasts / Computational and Systems Biology / constraint-based model / Decarboxylation / Dehydrogenases / Enzymes / Evolution / Evolution, Molecular / flux balance analysis / Genes, Plant / Genomes / Light / metabolic networks / Metabolism / Metabolites / model evolution / Models, Biological / Molecular evolution / Photosynthesis / Photosynthesis - physiology / Plant Biology / Plant Leaves - metabolism / Systems Biology