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

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  • Ming-Ju Amy Lyu

    (Chinese Academy of Sciences)

  • Huilong Du

    (Chinese Academy of Sciences
    School of Life Sciences, Institute of Life Sciences and Green Development, Hebei University)

  • Hongyan Yao

    (Fudan University)

  • Zhiguo Zhang

    (Chinese Academy of Agricultural Sciences)

  • Genyun Chen

    (Chinese Academy of Sciences)

  • Yuhui Huang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xiaoxiang Ni

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Faming Chen

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yong-Yao Zhao

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Qiming Tang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Fenfen Miao

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yanjie Wang

    (Chinese Academy of Sciences
    University of 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)

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.

Suggested Citation

  • 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 &, 2025. "A dominant role of transcriptional regulation during the evolution of C4 photosynthesis in Flaveria species," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-56901-y
    DOI: 10.1038/s41467-025-56901-y
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