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, Fa‐Ming Chen, Yong-Yao Zhao, Qiming Tang, Fenfen Miao, Yanjie Wang, Yuhui Zhao, Hongwei Lu, Fang Lü, Qiang Gao, Yiying Qi, Qing Zhang, Jisen Zhang, Tao Yang, Xuean Cui, Chengzhi Liang, Tiegang Lu, Xin‐Guang Zhu
Abstract
Abstract C 4 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 C 3 to C 4 photosynthesis. Chromosome-scale genome sequence analyses reveal a gradual increase in genome size during the evolution of C 4 photosynthesis attributed to the expansion of transposable elements. Systematic annotation of genes encoding C 4 enzymes and transporters identify additional copies of three C 4 enzyme genes through retrotranspositions in C 4 species. C 4 genes exhibit elevated mRNA and protein abundances, reduced protein-to-RNA ratios, and comparable translation efficiencies in C 4 species, highlighting a critical role of transcriptional regulation in C 4 evolution. Furthermore, we observe an increased abundance of ethylene response factor (ERF) transcription factors and cognate cis -regulatory elements associated with C 4 genes regulation. Altogether, our study provides valuable genomic resources for the Flaveria genus and sheds lights on evolutionary and regulatory mechanisms underlying C 4 photosynthesis.