Journal Article

The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria

Mallmann, Julia, Lercher, Martin J, Bräutigam, Andrea, Weber, Andreas PM, Gowik, Udo, Heckmann, David, Westhoff, Peter

2014

Overview

C4 photosynthesis represents a most remarkable case of convergent evolution of a complex trait, which includes the reprogramming of the expression patterns of thousands of genes. Anatomical, physiological, and phylogenetic and analyses as well as computational modeling indicate that the establishment of a photorespiratory carbon pump (termed C2 photosynthesis) is a prerequisite for the evolution of C4. However, a mechanistic model explaining the tight connection between the evolution of C4 and C2 photosynthesis is currently lacking. Here we address this question through comparative transcriptomic and biochemical analyses of closely related C3, C3–C4, and C4 species, combined with Flux Balance Analysis constrained through a mechanistic model of carbon fixation. We show that C2 photosynthesis creates a misbalance in nitrogen metabolism between bundle sheath and mesophyll cells. Rebalancing nitrogen metabolism requires anaplerotic reactions that resemble at least parts of a basic C4 cycle. Our findings thus show how C2 photosynthesis represents a pre-adaptation for the C4 system, where the evolution of the C2 system establishes important C4 components as a side effect. Environmental pressures sometimes cause different organisms to independently evolve the same traits. A dramatic example of this phenomenon, which is called convergent evolution, can be seen in the modes used by plants to convert carbon dioxide from the air into starch during photosynthesis. Early plants existed in an environment with high levels of carbon dioxide in the air. Over time, carbon dioxide levels decreased, so plants evolved more efficient types of photosynthesis to cope. A very efficient type of photosynthesis, called C4 photosynthesis essentially represents a carbon dioxide concentration mechanism. It has evolved at least 62 times independently in 19 different families of flowering plants. Scientists have shown that a less advanced, low-efficiency version of photosynthetic carbon dioxide concentration, called C2 photosynthesis, is a stepping-stone to C4 photosynthesis. It is also known that the evolution of C4 photosynthesis required changes to the expression patterns of thousands of genes, but the exact mechanism that leads from C2 photosynthesis to C4 photosynthesis is not clear. To explore this in greater detail, Mallmann, Heckmann et al. studied plants from the genus Flaveria, which belongs to the same family as sunflowers and asters. Under identical greenhouse conditions, plants that use three different photosynthetic pathways—C3 photosynthesis, C4 photosynthesis, or an intermediate between the two—were grown and their gene expression patterns were compared. Computer simulations were used to model the metabolism of plants that relied on C2 photosynthesis. Based on the modeling, it appears that C2 photosynthesis shifts the balance of nitrogen metabolism between two types of cell that are critical to photosynthesis. To rebalance the nitrogen, several genes are expressed to trigger an ammonia recycling mechanism. The same genes are turned on during C4 photosynthesis, and this recycling mechanism include parts of the C4 process. The findings of Mallmann, Heckmann et al. suggest that the initial steps in C4 photosynthesis evolved to prevent nitrogen imbalance. Over time, this mechanism was co-opted to become part of a more efficient form of photosynthesis, which may explain why so many different plants evolved from C2 to C4 photosynthesis.

• Publisher: eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Biological Evolution / C4 photosynthesis / Carbon / Carbon - metabolism / Carbon fixation / Cell Respiration - radiation effects / Computer applications / Developmental biology / Enzymes / Evolution / Flaveria / Flaveria - genetics / Flaveria - physiology / Flaveria - radiation effects / Flaveria brownii / Gene Expression Profiling / Gene Expression Regulation, Plant - radiation effects / Genomics and Evolutionary Biology / Light / Mesophyll / Models, Biological / Photorespiration / Photosynthesis / Photosynthesis - radiation effects / Phylogenetics / Phylogeny / Plant Biology / Plant Leaves - genetics / Plant Leaves - radiation effects / Proteins / RNA, Messenger - genetics / RNA, Messenger - metabolism