Shikimate Kinase-Like 1 Participates in an Ancient and Conserved Role Contributing to Chloroplast Biogenesis in Land Plants.

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Shikimate kinase-like 1 (SKL1) plays an essential role in chloroplast biogenesis in Arabidopsis thaliana whereby mutants present a pigment-defective phenotype. The inability to identify SKL1 in organisms predating land plants suggests an important role for this gene coinciding with the emergence of terrestrial plants. A role for SKL1 in chloroplast biogenesis has previously been determined in Arabidopsis; however, the biological function for SKL1 has not been established in early land plants. In the present study, we provided functional and evolutionary insights into the diversification of SKL1 in the early land plant Marchantia polymorpha. We identified the SK gene homologs common to all land plants, two of which were shown to have high sequence similarity to SK. We confirmed that one member possessed shikimate kinase activity, whereas the second member is inactive. These findings led us to identify MpSK (Mp3g21830) and infer the identity of MpSKL1 (Mp6g03600). Consistent with previous studies in Arabidopsis, disruption of MpSKL1 in Marchantia resulted in a pigment-defective phenotype with abnormal chloroplast morphology and thylakoid network organization. Given an early origin of SKL1 in land plant evolution, we investigated requisite structural modifications to an ancestral SK that led to the functional diversification of SKL1. We provided evidence that SKL1 displays an open and accessible substrate binding pocket, conferring its biological function for chloroplast biogenesis. Together, our results demonstrate that the acquisition of SKL1 corresponds with the emergence of terrestrial land plants and that this biological function is conserved across distant plant lineages.