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

Abstract

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.

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Acknowledgments

The authors thank anonymous reviewers for constructive comments. The National Basic Research and Development Program of the Ministry of Science and Technology of China (#2015CB150104), the Bill and Melinda Gates Foundation (#OPP1014417) and the international collaboration program of the National Science Foundation of China, Ministry of Science and Technology of China (# 2011DFA31070) supported this study. We thank Dr. Gane Wong, who organized the 1KP project on which this study was based.

Authors’ contribution

XGZ conceived the study, wrote and revised the manuscript. ML and YT conducted all analyses, wrote the manuscript, and generated the figures. All authors read and approved the final manuscript.

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Correspondence to Xin-Guang Zhu.

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Tao, Y., Lyu, MJ.A. & Zhu, XG. Transcriptome comparisons shed light on the pre-condition and potential barrier for C4 photosynthesis evolution in eudicots. Plant Mol Biol 91, 193–209 (2016). https://doi.org/10.1007/s11103-016-0455-x

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Keywords

  • C4 photosynthesis
  • C4 evolution
  • Transcriptome
  • Flaveria
  • PPT
  • Stress