The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid‐mediated floral promotion pathway and through affects on FLC chromatin structure

Jing Bo Jin,Yin Hua Jin,David E Somers,Chan Yul Yoo,Youbong Hyun,Michael Van Oosten,Jiyoung Lee,Ilha Lee,Woe‐Yeon Kim,Paul M Hasegawa,Ray A Bressan,Kenji Miura,Dae‐Jin Yun

doi:10.1111/j.1365-313x.2007.03359.x

Abstract

Loss-of-function siz1 mutations caused early flowering under short days. siz1 plants have elevated salicylic acid (SA) levels, which are restored to wild-type levels by expressing nahG, bacterial salicylate hydroxylase. The early flowering of siz1 was suppressed by expressing nahG, indicating that SIZ1 represses the transition to flowering mainly through suppressing SA-dependent floral promotion signaling under short days. Previous results have shown that exogenous SA treatment does not suppress late flowering of autonomous pathway mutants. However, the siz1 mutation accelerated flowering time of an autonomous pathway mutant, luminidependens, by reducing the expression of FLOWERING LOCUS C (FLC), a floral repressor. This result suggests that SIZ1 promotes FLC expression, possibly through an SA-independent pathway. Evidence indicates that SIZ1 is required for the full activation of FLC expression in the late-flowering FRIGIDA background. Interestingly, increased FLC expression and late flowering of an autonomous pathway mutant, flowering locus d (fld), was not suppressed by siz1, suggesting that SIZ1 promotes FLC expression by repressing FLD. Consistent with this, SIZ1 facilitates sumoylation of FLD that can be suppressed by mutations in three predicted sumoylation motifs in FLD (i.e. FLDK3R). Furthermore, expression of FLDK3R in fld protoplasts strongly reduced FLC transcription compared with expression of FLD, and this affect was linked to reduced acetylation of histone 4 in FLC chromatin. Taken together, the results suggest that SIZ1 is a floral repressor that not only represses the SA-dependent pathway, but also promotes FLC expression by repressing FLD activity through sumoylation, which is required for full FLC expression in a FRIGIDA background.

Highlights

Sumoylation is a post-translational regulatory process that conjugates small ubiquitin modifier peptides (SUMO) to protein substrates (Matunis et al, 1996; Mahajan et al, 1997)
The role of SIZ1 in flowering-time regulation was confirmed by genetic complementation of the siz1 mutation with the wild-type SIZ1 allele
Note that exogenous salicylic acid (SA) treatment does not accelerate the flowering time of autonomous pathway mutants (Martinez et al, 2004). These results suggest that SIZ1 activates FLOWERING LOCUS C (FLC) expression, possibly through an SA-independent pathway, which is required for full FLC activation by ld-1 and FRI

Summary

Introduction

Sumoylation is a post-translational regulatory process that conjugates small ubiquitin modifier peptides (SUMO) to protein substrates (Matunis et al, 1996; Mahajan et al, 1997). SUMO modification of target a 2007 The Authors Journal compilation a 2007 Blackwell Publishing Ltd proteins in yeast and metazoans has been implicated in the regulation of innate immunity, cell-cycle progression and mitosis, DNA repair, chromatin stability, nucleocytoplasmic trafficking, subnuclear targeting, ubiquitination antagonism and transcriptional regulation (Johnson, 2004; Gill, 2005). The Arabidopsis PIAS-type SUMO E3 ligase, AtSIZ1, facilitates SUMO modification of transcription factors, PHR1 and ICE1, which regulate phosphate-starvation signaling and low-temperature response, respectively (Miura et al, 2005, 2007). A SUMO protease, AtESD4 (EARLY SHORT DAY FLOWERING4), and its interacting protein NUA (NUCLEAR PORE ANCHOR) negatively regulate transition to flowering, suggesting that SUMO homeostasis is important for flowering time regulation (Murtas et al, 2003; Reeves et al, 2002; Xu et al, 2007)

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Discussion

Conclusion