A dominant role of transcriptional regulation during the evolution of C4 photosynthesis in Flaveria species

Ming-Ju Amy Lyu (), Huilong Du, Hongyan Yao, Zhiguo Zhang, Genyun Chen, Yuhui Huang, Xiaoxiang Ni, Faming Chen, Yong-Yao Zhao, Qiming Tang, Fenfen Miao, Yanjie Wang, Yuhui Zhao, Hongwei Lu, Lu Fang, Qiang Gao, Yiying Qi, Qing Zhang, Jisen Zhang, Tao Yang, Xuean Cui, Chengzhi Liang (), Tiegang Lu () and Xin-Guang Zhu ()
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Ming-Ju Amy Lyu: Chinese Academy of Sciences
Huilong Du: Chinese Academy of Sciences
Hongyan Yao: Fudan University
Zhiguo Zhang: Chinese Academy of Agricultural Sciences
Genyun Chen: Chinese Academy of Sciences
Yuhui Huang: Chinese Academy of Sciences
Xiaoxiang Ni: Chinese Academy of Sciences
Faming Chen: Chinese Academy of Sciences
Yong-Yao Zhao: Chinese Academy of Sciences
Qiming Tang: Chinese Academy of Sciences
Fenfen Miao: Chinese Academy of Sciences
Yanjie Wang: Chinese Academy of Sciences
Yuhui Zhao: Chinese Academy of Sciences
Hongwei Lu: Chinese Academy of Sciences
Lu Fang: Chinese Academy of Sciences
Qiang Gao: Chinese Academy of Sciences
Yiying Qi: Fujian Agriculture and Forestry University
Qing Zhang: Fujian Agriculture and Forestry University
Jisen Zhang: Fujian Agriculture and Forestry University
Tao Yang: China National GeneBank
Xuean Cui: Chinese Academy of Agricultural Sciences
Chengzhi Liang: Chinese Academy of Sciences
Tiegang Lu: Chinese Academy of Agricultural Sciences
Xin-Guang Zhu: Chinese Academy of Sciences

Nature Communications, 2025, vol. 16, issue 1, 1-17

Abstract: Abstract C4 photosynthesis exemplifies convergent evolution of complex traits. Herein, we construct chromosome-scale genome assemblies and perform multi-omics analysis for five Flaveria species, which represent evolutionary stages from C3 to C4 photosynthesis. Chromosome-scale genome sequence analyses reveal a gradual increase in genome size during the evolution of C4 photosynthesis attributed to the expansion of transposable elements. Systematic annotation of genes encoding C4 enzymes and transporters identify additional copies of three C4 enzyme genes through retrotranspositions in C4 species. C4 genes exhibit elevated mRNA and protein abundances, reduced protein-to-RNA ratios, and comparable translation efficiencies in C4 species, highlighting a critical role of transcriptional regulation in C4 evolution. Furthermore, we observe an increased abundance of ethylene response factor (ERF) transcription factors and cognate cis-regulatory elements associated with C4 genes regulation. Altogether, our study provides valuable genomic resources for the Flaveria genus and sheds lights on evolutionary and regulatory mechanisms underlying C4 photosynthesis.

Date: 2025
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DOI: 10.1038/s41467-025-56901-y

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