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The N-end rule pathway controls multiple functions during Arabidopsis shoot and leaf development

Graciet, Emmanuelle and Walter, Franziska and Ó Maoiléidigh, Diarmuid and Pollmann, Stephan and Meyerowitz, Elliot M. and Varshavsky, Alexander and Wellmer, Frank (2009) The N-end rule pathway controls multiple functions during Arabidopsis shoot and leaf development. Proceedings of the National Academy of Sciences of the United States of America, 106 (32). pp. 13618-13623. ISSN 0027-8424. PMCID PMC2726413. doi:10.1073/pnas.0906404106.

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The ubiquitin-dependent N-end rule pathway relates the in vivo half-life of a protein to the identity of its N-terminal residue. This proteolytic system is present in all organisms examined and has been shown to have a multitude of functions in animals and fungi. In plants, however, the functional understanding of the N-end rule pathway is only beginning. The N-end rule has a hierarchic structure. Destabilizing activity of N-terminal Asp, Glu, and (oxidized) Cys requires their conjugation to Arg by an arginyl–tRNA–protein transferase (R-transferase). The resulting N-terminal Arg is recognized by the pathway's E3 ubiquitin ligases, called “N-recognins.” Here, we show that the Arabidopsis R-transferases AtATE1 and AtATE2 regulate various aspects of leaf and shoot development. We also show that the previously identified N-recognin PROTEOLYSIS6 (PRT6) mediates these R-transferase-dependent activities. We further demonstrate that the arginylation branch of the N-end rule pathway plays a role in repressing the meristem-promoting BREVIPEDICELLUS (BP) gene in developing leaves. BP expression is known to be excluded from Arabidopsis leaves by the activities of the ASYMMETRIC LEAVES1 (AS1) transcription factor complex and the phytohormone auxin. Our results suggest that AtATE1 and AtATE2 act redundantly with AS1, but independently of auxin, in the control of leaf development.

Item Type:Article
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URLURL TypeDescription CentralArticle
Meyerowitz, Elliot M.0000-0003-4798-5153
Varshavsky, Alexander0000-0002-4011-258X
Additional Information:© 2009 National Academy of Sciences. Contributed by Elliot M. Meyerowitz, June 11, 2009 (sent for review May 25, 2009). Published online before print July 20, 2009, doi: 10.1073/pnas.0906404106 We thank members of our laboratories for helpful discussions, Dr. T. Kavanagh for sharing equipment, and Drs. J. Long and P. Das for comments on the manuscript. This study was supported by Science Foundation Ireland Grant 07/RFP/GEN/F438 (to F. Wellmer), National Institutes of Health Grants GM31530 and DK39520 (to A.V.), and U.S. Department of Energy Grant DE-FG02-88ER13873 (to E.M.M.). E.G. was supported by fellowships from the Human Frontier Science Program and the European Molecular Biology Organization. Author contributions: E.G., E.M.M., A.V., and F. Wellmer designed research; E.G., F. Walter, D.O.M., and S.P. performed research; E.G., F. Walter, D.O.M., S.P., and F. Wellmer analyzed data; and E.G., E.M.M., A.V., and F. Wellmer wrote the paper. The authors declare no conflict of interest. This article contains supporting information online at
Funding AgencyGrant Number
Science Foundation, Ireland07/RFP/GEN/F438
Department of Energy (DOE)DE-FG02-88ER13873
Human Frontier Science ProgramUNSPECIFIED
European Molecular Biology Organization (EMBO)UNSPECIFIED
Subject Keywords:arginine transferase; plant; protein degradation
Issue or Number:32
PubMed Central ID:PMC2726413
Record Number:CaltechAUTHORS:20090828-231031940
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Official Citation:Emmanuelle Graciet, Franziska Walter, Diarmuid Ó Maoiléidigh, Stephan Pollmann, Elliot M. Meyerowitz, Alexander Varshavsky, and Frank Wellmer The N-end rule pathway controls multiple functions during Arabidopsis shoot and leaf development PNAS 2009 106 (32) 13618-13623; published ahead of print July 20, 2009, doi:10.1073/pnas.0906404106
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:15440
Deposited By: George Porter
Deposited On:08 Sep 2009 19:29
Last Modified:08 Nov 2021 23:19

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