MAP Kinase Cascades Regulate the Cold Response by Modulating ICE1 Protein Stability

Zhao, Chunzhao; Wang, Pengcheng; Si, Tong; Hsu, Chuan‐Chih; Wang, Lu; Zayed, Omar; Yu, Zheping; Zhu, Yingfang; Dong, Juan; Tao, W. Andy; Zhu, Jian‐Kang

doi:10.1016/j.devcel.2017.09.024

Cited by 389 publications

(353 citation statements)

References 46 publications

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“…Another piece of evidence in support of ICE1 as a regulator of CBF3 is the result recently obtained in transient expression assays in Arabidopsis protoplasts (Zhao et al 2017). The Arabidopsis protoplasts co‐transfected with ICE1 and CBF3‐LUC showed a much higher luciferase activity than the protoplasts transfected with CBF3‐LUC alone, showing that ICE1 is a positive regulator of CBF3 gene expression (Zhao et al 2017).…”

Section: Accession Numbermentioning

confidence: 92%

The transcription factor ICE1 functions in cold stress response by binding to the promoters of CBF and COR genes

Tang

Zhao

Ren

et al. 2020

JIPB

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110

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A recent paper by Kidokoro et al. (2020) in The Plant Cell reported a transgene‐dependent transcriptional silencing phenomenon in the dominant ice1‐1 Arabidopsis mutant containing the CBF3‐LUC reporter, and questioned whether ICE1 may regulate CBF genes and may be involved in plant cold response. Here, we evaluate available evidence supporting the involvement of ICE1 in plant cold response, and provide ChIP‐seq data showing ICE1 binding to the promoters of CBF genes and other regulatory genes known to be critical for cold response as well as to the promoters of some COR genes.

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Section: Accession Numbermentioning

confidence: 92%

The transcription factor ICE1 functions in cold stress response by binding to the promoters of CBF and COR genes

Tang

Zhao

Ren

et al. 2020

JIPB

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110

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“…In turn, OsDREB1s can promote expression of OsPLDα1 , thus creating positive feedback regulation (Huo et al ). MPK3/6 (MAPK3/6) negatively regulates cold responses in Arabidopsis by phosphorylating ICE1 following the initiation of cold signaling, resulting in ICE1 polyubiquitination and degradation (Li et al ; Zhao et al ). In contrast, OsMAPK3 enhances chilling tolerance in rice by phosphorylating OsbHLH002/OsICE1 under cold stress, which prevents its degradation (Zhang et al ).…”

Section: Cold Signal Transduction From the Plasma Membrane To The Numentioning

confidence: 99%

“…The protein kinases MPK3 and MPK6 phosphorylate ICE1, reducing its stability and transcriptional activity, which therefore negatively regulates CBF expression and freezing tolerance in plants. Conversely, the MEKK1‐MKK1/2‐MPK4 cascade promotes freezing tolerance by antagonizing the MPK3/6 pathway (Li et al ; Liu and Zhou ; Zhao et al ). During the early stages of cold stress, ICE1 is activated through OST1‐mediated phosphorylation, which inhibits its degradation.…”

Section: Cold Signal Transduction From the Plasma Membrane To The Numentioning

confidence: 99%

Cold signaling in plants: Insights into mechanisms and regulation

Guo

Liu

Chong

2018

JIPB

441

272

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To survive under cold temperatures plants must be able to perceive a cold signal and transduce it into downstream components that induce appropriate defense mechanisms. In addition to inducing adaptive defenses, such as the production of osmotic factors to prevent freezing and the reprogramming of transcriptional pathways, cold temperatures induce changes in plant growth and development which can affect the plant life cycle. In this review, we summarize recent progress in characterizing cold-related genes and the pathways that allow transduction of the cold signal in plants, focusing primarily on studies in Arabidopsis thaliana and rice (Oryza sativa). We summarize cold perception and signal transduction from the plasma membrane to the nucleus, which involves cold sensors, calcium signals, calcium-binding proteins, mitogen-activated protein kinase cascades, and the C-repeat binding factor/dehydration-responsive element binding pathways, as well as trehalose metabolism. Finally, we describe the balance between plant organogenesis and cold tolerance mechanisms in rice. This review encapsulates the known cold signaling factors in plants and provides perspectives for ongoing cold signaling research.

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“…Cold-induced CBF expression is positively regulated by several transcription factors, including ICE1 (inducer of CBF expression 1), CAMTA3 (calmodulin-binding transcription activator 3), and BZR1 (brassinazole-resistant 1; Chinnusamy et al, 2003;Doherty et al, 2009;Li et al, 2017b). Recent studies showed that ICE1 protein is phosphorylated by protein kinases, including OST1 (open stomata 1) and MPK3/6 in Arabidopsis, and OsMAPK3 in rice (Ding et al, 2015;Li et al, 2017a;Zhang et al, 2017;Zhao et al, 2017;Shi et al, 2018). ICE1 is targeted for degradation after ubiquitination by HOS1 (high expression of osmotically responsive gene 1; Dong et al, 2006), whereas it is stabilized after sumoylation by SIZ1 (SAP and Miz;Miura et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…ICE1 functions as a master regulator of CBF expression (Chinnusamy et al, 2003). Under cold conditions, MPK3/6 phosphorylate ICE1 and promote ICE1 degradation in Arabidopsis, while OsMAPK3 phosphorylates and stabilizes OsICE1 in rice (Li et al, 2017a;Zhang et al, 2017;Zhao et al, 2017;Guo et al, 2018). Recent studies showed that ICE1 protein is phosphorylated by protein kinases, including OST1 (open stomata 1) and MPK3/6 in Arabidopsis, and OsMAPK3 in rice (Ding et al, 2015;Li et al, 2017a;Zhang et al, 2017;Zhao et al, 2017;Shi et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

EGR 2 phosphatase regulates OST 1 kinase activity and freezing tolerance in Arabidopsis

et al. 2018

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OST1 (open stomata 1) protein kinase plays a central role in regulating freezing tolerance in Arabidopsis; however, the mechanism underlying cold activation of OST1 remains unknown. Here, we report that a plasma membrane-localized clade-E growth-regulating 2 (EGR2) phosphatase interacts with OST1 and inhibits OST1 activity under normal conditions. EGR2 is N-myristoylated by Nmyristoyltransferase NMT1 at 22°C, which is important for its interaction with OST1. Moreover, myristoylation of EGR2 is required for its function in plant freezing tolerance. Under cold stress, the interaction of EGR2 and NMT1 is attenuated, leading to the suppression of EGR2 myristoylation in plants. Plant newly synthesized unmyristoylated EGR2 has decreased binding ability to OST1 and also interferes with the EGR2-OST1 interaction under cold stress. Consequently, the EGR2-mediated inhibition of OST1 activity is released. Consistently, mutations of EGRs cause plant tolerance to freezing, whereas overexpression of EGR2 exhibits decreased freezing tolerance. This study thus unravels a molecular mechanism underlying cold activation of OST1 by membranelocalized EGR2 and suggests that a myristoyl switch on EGR2 helps plants to adapt to cold stress.

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MAP Kinase Cascades Regulate the Cold Response by Modulating ICE1 Protein Stability

Cited by 389 publications

References 46 publications

The transcription factor ICE1 functions in cold stress response by binding to the promoters of CBF and COR genes

The transcription factor ICE1 functions in cold stress response by binding to the promoters of CBF and COR genes

Cold signaling in plants: Insights into mechanisms and regulation

EGR 2 phosphatase regulates OST 1 kinase activity and freezing tolerance in Arabidopsis

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