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Evolution from DNA to RNA recognition by the bI3 LAGLIDADG maturase

Nature Structural & Molecular Biology volume 12, pages 779–787 (2005)Cite this article

Abstract

LAGLIDADG endonucleases bind across adjacent major grooves via a saddle-shaped surface and catalyze DNA cleavage. Some LAGLIDADG proteins, called maturases, facilitate splicing by group I introns, raising the issue of how a DNA-binding protein and an RNA have evolved to function together. In this report, crystallographic analysis shows that the global architecture of the bI3 maturase is unchanged from its DNA-binding homologs; in contrast, the endonuclease active site, dispensable for splicing facilitation, is efficiently compromised by a lysine residue replacing essential catalytic groups. Biochemical experiments show that the maturase binds a peripheral RNA domain 50 Å from the splicing active site, exemplifying long-distance structural communication in a ribonucleoprotein complex. The bI3 maturase nucleic acid recognition saddle interacts at the RNA minor groove; thus, evolution from DNA to RNA function has been mediated by a switch from major to minor groove interaction.

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Figure 1: Translation of the bI3 maturase holoprotein and core maturase domain.
Figure 2: Overview of the bI3 maturase structure.
Figure 3: Conserved shape complementarity between LAGLIDADG proteins and consecutive DNA major grooves.
Figure 4: Superposition of the bI3 maturase (in)active site with catalytic residues and divalent ions from the I-CreI DNA endonuclease–DNA substrate complex.
Figure 5: Solvent-based hydroxyl radical footprinting of the bI3 maturase–P5-P4-P6 domain complex.
Figure 6: Site-directed hydroxyl radical footprinting of the bI3 maturase–P5-P4-P6 domain complex.
Figure 7: Maturase-RNA interactions.
Figure 8: Maturase-facilitated folding of the bI3 intron RNA via action at a distance.

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Acknowledgements

We are indebted to L. Pedersen and Z. Dauter for assistance with synchrotron data collection at beamline X9B at Brookhaven National Laboratory, D. de Oliveira for performing DNA binding assays and our colleagues for critical comments on the manuscript. This work was supported by the US National Institutes of Health (NIH) grant GM56222 to K.M.W. and by the Intramural Research Program of the NIH, National Institute of Environmental Health Sciences (T.M.T.H.).

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  1. Antonella Longo, Christopher W Leonard and Gurminder S Bassi: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Chemistry, University of North Carolina, Chapel Hill, 27599-3290, North Carolina, USA

    Antonella Longo, Christopher W Leonard, Gurminder S Bassi, Daniel Berndt & Kevin M Weeks

  2. Laboratory of Structural Biology, National Institute of Environmental Health Sciences, US National Institutes of Health, Research Triangle Park, 27709, North Carolina, USA

    Antonella Longo, Joseph M Krahn & Traci M Tanaka Hall

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Supplementary information

Supplementary Fig. 1

2′-O-methyl interference analysis of the bI3 maturase-RNA interaction. (PDF 150 kb)

Supplementary Fig. 2

bI3 maturase-facilitated splicing of the AnCOB group I intron RNA in the cytochrome b gene of Aspergillus nidulans. (PDF 172 kb)

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Longo, A., Leonard, C., Bassi, G. et al. Evolution from DNA to RNA recognition by the bI3 LAGLIDADG maturase. Nat Struct Mol Biol 12, 779–787 (2005). https://doi.org/10.1038/nsmb976

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