Induction of C4genes evolved through changes incisallowing integration into ancestral C3gene regulatory networks

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Abstract

C4photosynthesis has evolved independently in over sixty lineages and in so doing repurposed existing enzymes to drive a carbon pump that limits the RuBisCO oxygenation reaction. In all cases, gene expression is modified such that C4proteins accumulate to levels matching those of the photosynthetic apparatus. To better understand this rewiring of gene expression we undertook RNA- and DNaseI-SEQ on de-etiolating seedlings of C4Gynandropsis gynandra, which is sister to C3Arabidopsis. Changes in chloroplast ultrastructure and C4gene expression were coordinated and rapid. C3photosynthesis and C4genes showed similar induction patterns, but C4genes fromG. gynandrawere more strongly induced than orthologs from Arabidopsis. A gene regulatory network predicted transcription factors operating at the top of the de-etiolation network, including those responding to light, act upstream of C4genes. Light responsive elements, especially G-, E- and GT-boxes were over-represented in accessible chromatin around C4genes. Moreover,in vivobinding of many G-, E- and GT-boxes was detected. Overall, the data support a model in which rapid and robust C4gene expression following light exposure is generated through modifications incisto allow integration into high-level transcriptional networks including those underpinned by conserved light responsive elements.

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