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Transcriptome comparisons shed light on the pre-condition and potential barrier for C4 photosynthesis evolution in eudicots

Tao, Yimin, Lyu, Ming-Ju Amy, Zhu, Xin-Guang
Plant molecular biology 2016 v.91 no.1-2 pp. 193-209
C3 photosynthesis, C3 plants, C4 photosynthesis, C4 plants, Caryophyllales, Poales, brassinosteroids, ethylene, evolution, gene expression, gene expression regulation, genes, genetic variation, hormone metabolism, signal transduction, stress response, transcriptome, transcriptomics
C₄ photosynthesis evolved independently from C₃ photosynthesis in more than 60 lineages. Most of the C₄ lineages are clustered together in the order Poales and the order Caryophyllales while many other angiosperm orders do not have C₄ species, suggesting the existence of biological pre-conditions in the ancestral C₃ species that facilitate the evolution of C₄ photosynthesis in these lineages. To explore pre-adaptations for C₄ photosynthesis evolution, we classified C₄ lineages into the C₄-poor and the C₄-rich groups based on the percentage of C₄ species in different genera and conducted a comprehensive comparison on the transcriptomic changes between the non-C₄ species from the C₄-poor and the C₄-rich groups. Results show that species in the C₄-rich group showed higher expression of genes related to oxidoreductase activity, light reaction components, terpene synthesis, secondary cell synthesis, C₄ cycle related genes and genes related to nucleotide metabolism and senescence. In contrast, C₄-poor group showed up-regulation of a PEP/Pi translocator, genes related to signaling pathway, stress response, defense response and plant hormone metabolism (ethylene and brassinosteroid). The implications of these transcriptomic differences between the C₄-rich and C₄-poor groups to C₄ evolution are discussed.