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A scheme for C4 evolution derived from a comparative analysis of the closely related C3, C3–C4 intermediate, C4-like, and C4 species in the genus Flaveria

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A comparative analysis of the genus Flaveria showed a C4 evolutionary process in which the anatomical and metabolic features of C4 photosynthesis were gradually acquired through C3–C4 intermediate stages.

Abstract

C4 photosynthesis has been acquired in multiple lineages of angiosperms during evolution to suppress photorespiration. Crops that perform C4 photosynthesis exhibit high rates of CO2 assimilation and high grain production even under high-temperature in semiarid environments; therefore, engineering C4 photosynthesis in C3 plants is of great importance in the application field. The genus Flaveria contains a large number of C3, C3–C4 intermediate, C4-like, and C4 species, making it a good model genus to study the evolution of C4 photosynthesis, and these studies indicate the direction for C4 engineering. C4 photosynthesis was acquired gradually through the C3–C4 intermediate stage. First, a two-celled C2 cycle called C2 photosynthesis was acquired by localizing glycine decarboxylase activity in the mitochondria of bundle sheath cells. With the development of two-cell metabolism, anatomical features also changed. Next, the replacement of the two-celled C2 cycle by the two-celled C4 cycle was induced by the acquisition of cell-selective expression in addition to the upregulation of enzymes in the C4 cycle during the C3–C4 intermediate stage. This was supported by an increase in cyclic electron transport activity in response to an increase in the ATP/NADPH demand for metabolism. Suppression of the C3 cycle in mesophyll cells was induced after the functional establishment of the C4 cycle, and optimization of electron transport by suppressing the activity of photosystem II also occurred during the final phase of C4 evolution.

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Funding

This work was supported by JSPS KAKENHI (Grant Nos. 17K07456, 16H06557 and 21K05520) from the Japan Society for the Promotion of Science.

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  1. School of Science and Technology, Kwansei Gakuin University, 2-1 Gakuen, Sanda, Hyogo, 669-1337, Japan

    Yuri N. Munekage & Yukimi Y. Taniguchi

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  1. Yuri N. Munekage
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  2. Yukimi Y. Taniguchi
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YNM wrote the manuscript. YYT performed the anatomical analysis and measurements of CO2 compensation points and O2 inhibition of photosynthetic activity.

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Correspondence to Yuri N. Munekage.

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Munekage, Y.N., Taniguchi, Y.Y. A scheme for C4 evolution derived from a comparative analysis of the closely related C3, C3–C4 intermediate, C4-like, and C4 species in the genus Flaveria. Plant Mol Biol 110, 445–454 (2022). https://doi.org/10.1007/s11103-022-01246-z

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