posted on 2018-08-21, 09:04authored byMark D. White, Maria Klecker, Richard J. Hopkinson, Daan A. Weits, Carolin Mueller, Christin Naumann, Rebecca O'Neill, James Wickens, Jiayu Yang, Jonathan C. Brooks-Bartlett, Elspeth F. Garman, Tom N. Grossmann, Nico Dissmeyer, Emily Flashman
Crop yield loss due to flooding is a threat to food security. Submergence-induced hypoxia in plants results in stabilization of group VII ETHYLENE RESPONSE FACTORs (ERF-VIIs), which aid survival under these adverse conditions. ERF-VII stability is controlled by the N-end rule pathway, which proposes that ERF-VII N-terminal cysteine oxidation in normoxia enables arginylation followed by proteasomal degradation. The PLANT CYSTEINE OXIDASEs (PCOs) have been identified as catalysts of this oxidation. ERF-VII stabilization in hypoxia presumably arises from reduced PCO activity. We directly demonstrate that PCO dioxygenase activity produces Cys-sulfinic acid at the N terminus of an ERF-VII peptide, which then undergoes efficient arginylation by an arginyl transferase (ATE1). This provides molecular evidence of N-terminal Cys-sulfinic acid formation and arginylation by N-end rule pathway components, and a substrate of ATE1 in plants. The PCOs and ATE1 may be viable intervention targets to stabilize N-end rule substrates, including ERF-VIIs, to enhance submergence tolerance in agriculture.
Funding
Petra Majovsky, Domenika Thieme and Wolfgang Hoehenwarter from the Proteomics Unit of the Leibniz Institute of Plant Biochemistry (IPB), Halle, are acknowledged for MS of recombinant ATE1. David Staunton from the Biophysical Facility, Department of Biochemistry, University of Oxford, is acknowledged for multi-angle light scatter analysis of PCO1/4. Geoff Grime from the University of Surrey Ion Beam Centre is acknowledged for assistance with the microPIXE data collection. This work was supported by a Biotechnology and Biological Sciences Research Council (U.K.) New Investigator grant (BB/M024458/1) to E.F., a grant for setting up the junior research group of the ScienceCampus Halle–Plant-based Bioeconomy to N.D., by a PhD fellowship of the Landesgraduiertenförderung Sachsen-Anhalt awarded to C.N., by an Engineering and Physical Sciences Research Council (U.K.) studentship (EP/G03706X/1) to J.C.B.-B., a Royal Society Dorothy Hodgkin Fellowship to E.F., a William R. Miller Junior Research Fellowship (St Edmund Hall, Oxford) to R.J.H. and grant DI 1794/3-1 by the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG) to N.D. Financial support came from the Leibniz Association, the state of Saxony Anhalt, the Deutsche Forschungsgemeinschaft (DFG) Graduate Training Center GRK1026 ‘Conformational Transitions in Macromolecular Interactions’ at Halle, and the Leibniz Institute of Plant Biochemistry (IPB) at Halle, Germany. We thank Professor J. van Dongen (RWTH Aachen University, Germany) and Professor F. Licausi (Scuolo Superiore Sant’Anna, Pisa, Italy) for sharing pDEST-PCO plasmids and helpful discussions. The manuscript was deposited as pre-print before publication (https://doi.org/10.1101/069336) at bioRxiv—the preprint server for biology, operated by Cold Spring Harbor Laboratory (biorxiv.org). Publication of this article was funded by the Open Access fund of the Leibniz Institute of Plant Biochemistry (IPB). This work was supported by the network
History
Citation
Nature Communications, 2017, 8:14690
Author affiliation
/Organisation/COLLEGE OF SCIENCE AND ENGINEERING/Department of Chemistry