Ancestral light and chloroplast regulation form the foundations for C4 gene expression

Abstract

C4 photosynthesis acts as a carbon concentrating mechanism that leads to large increases in photosynthetic efficiency. The C4 pathway is found in more than 60 plant lineages1 but the molecular enablers of this evolution are poorly understood. In particular, it is unclear how non-photosynthetic proteins in the ancestral C3 system have repeatedly become strongly expressed and integrated into photosynthesis gene regulatory networks in C4 leaves. Here, we provide clear evidence that in C3 leaves, genes encoding key enzymes of the C4 pathway are already co-regulated with photosynthesis genes and are controlled by both light and chloroplast-to-nucleus signalling. In C4 leaves this regulation becomes increasingly dependent on the chloroplast. We propose that regulation of C4 cycle genes by light and the chloroplast in the ancestral C3 state has facilitated the repeated evolution of the complex and convergent C4 trait.

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Figure 1: Light induction of C4 genes in G. gynandra.
Figure 2: Chloroplast regulation of C4 genes in G. gynandra.
Figure 3: Proposed model of changes in light regulation during evolution of the C4 pathway in G. gynandra.

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Acknowledgements

The work was funded by the European Union 3to4 project and Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/J011754/1. I.G.-M. was supported by the Amgen Foundation. Research on chloroplast signalling by M.J.T. was supported by BBSRC grant (BB/J018139/1).

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Contributions

S.J.B., M.J.T. and J.M.H. designed the study. S.J.B., I.G.-M. and M.J.G.-G. carried out the experimental work. S.J.B. and C.B. conducted the bioinformatics. S.J.B., M.J.T. and J.M.H. interpreted results and wrote the paper.

Corresponding author

Correspondence to Julian M. Hibberd.

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Burgess, S., Granero-Moya, I., Grangé-Guermente, M. et al. Ancestral light and chloroplast regulation form the foundations for C4 gene expression. Nature Plants 2, 16161 (2016). https://doi.org/10.1038/nplants.2016.161

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