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SIZ1-Mediated Sumoylation of ICE1 Controls CBF3/DREB1A Expression and Freezing Tolerance in Arabidopsis^[W],[OA]

^a Center for Plant Environmental Stress Physiology, Purdue University, West Lafayette, Indiana 47907-2010
^b College of Natural Sciences, Forestry and Agriculture, University of Maine, Orono, Maine 04469-5782
^c Division of Applied Life Science (BK21 Program), Plant Molecular Biology and Biotechnology Research Center, Environmental Biotechnology National Core Research Center, Gyeongsang National University, Jinju 660-701, Korea

¹ To whom correspondence should be addressed. E-mail djyun{at}gsnu.ac.kr or paul.m.hasegawa.1{at}purdue.edu; fax 82-55-759-9363 or 765-494-0391.

SIZ1 is a SUMO E3 ligase that facilitates conjugation of SUMO to protein substrates. siz1-2 and siz1-3 T-DNA insertion alleles that caused freezing and chilling sensitivities were complemented genetically by expressing SIZ1, indicating that the SIZ1 is a controller of low temperature adaptation in plants. Cold-induced expression of CBF/DREB1, particularly of CBF3/DREB1A, and of the regulon genes was repressed by siz1. siz1 did not affect expression of ICE1, which encodes a MYC transcription factor that is a controller of CBF3/DREB1A. A K393R substitution in ICE1 [ICE1(K393R)] blocked SIZ1-mediated sumoylation in vitro and in protoplasts identifying the K393 residue as the principal site of SUMO conjugation. SIZ1-dependent sumoylation of ICE1 in protoplasts was moderately induced by cold. Sumoylation of recombinant ICE1 reduced polyubiquitination of the protein in vitro. ICE1(K393R) expression in wild-type plants repressed cold-induced CBF3/DREB1A expression and increased freezing sensitivity. Furthermore, expression of ICE1(K393R) induced transcript accumulation of MYB15, which encodes a MYB transcription factor that is a negative regulator of CBF/DREB1. SIZ1-dependent sumoylation of ICE1 may activate and/or stabilize the protein, facilitating expression of CBF3/DREB1A and repression of MYB15, leading to low temperature tolerance.

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