Plant Cell Advance Online Publication
Published on April 6, 2007; 10.1105/tpc.106.048397
OPEN ACCESS ARTICLE
Received October 21, 2006
Returned for revision February 15, 2007
Accepted March 19, 2007
SIZ1-Mediated Sumoylation of ICE1 Controls CBF3/DREB1A Expression and Freezing Tolerance in Arabidopsis
Kenji Miura 1, Jing Bo Jin 1, Jiyoung Lee 1, Chan Yul Yoo 1, Vicki Stirm 1, Tomoko Miura 1, Edward N. Ashworth 2, Ray A. Bressan 1, Dae-Jin Yun 3*, and Paul M. Hasegawa 1
1 Center for Plant Environmental Stress Physiology, Purdue University, West Lafayette, Indiana 47907-2010
2 College of Natural Sciences, Forestry and Agriculture, University of Maine, Orono, Maine 04469-5782
3 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
* To whom correspondence should be addressed. E-mail: paul.m.hasegawa.1{at}purdue.edu.
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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