Disentangling the Complexity of Mitogen-Activated Protein Kinases and Reactive Oxygen Species Signaling

Pitzschke, Andrea; Hirt, Heribert

doi:10.1104/pp.108.131557

Cited by 121 publications

(77 citation statements)

References 82 publications

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“…A number of stress-related putative target genes, including WIPK, have been identified by microarray analysis. MPK3 is also subject to transcriptional control (13). However, a self-amplifying circuit of MPK3 signaling via VIP1-similar to NtWIF-induced WIPK gene expression (31)-appears unlikely, since no VRE sequences are found in the MPK3 promoter.…”

Section: Chromatin Immunoprecipitation Reveals Stress-dependent In Vivomentioning

confidence: 99%

VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression

Pitzschke

Djamei

Teige

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

127

159

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The plant pathogen Agrobacterium tumefaciens transforms plant cells by delivering its T-DNA into the plant cell nucleus where it integrates into the plant genome and causes tumor formation. A key role of VirE2-interacting protein 1 (VIP1) in the nuclear import of T-DNA during Agrobacterium-mediated plant transformation has been unravelled and VIP1 was shown to undergo nuclear localization upon phosphorylation by the mitogen-activated protein kinase MPK3. Here, we provide evidence that VIP1 encodes a functional bZIP transcription factor that stimulates stress-dependent gene expression by binding to VIP1 response elements (VREs), a DNA hexamer motif. VREs are overrepresented in promoters responding to activation of the MPK3 pathway such as Trxh8 and MYB44. Accordingly, plants overexpressing VIP1 accumulate high levels of Trxh8 and MYB44 transcripts, whereas stress-induced expression of these genes is impaired in mpk3 mutants. Trxh8 and MYB44 promoters are activated by VIP1 in a VRE-dependent manner. VIP1 strongly enhances expression from a synthetic promoter harboring multiple VRE copies and directly interacts with VREs in vitro and in vivo. Chromatin immunoprecipitation assays of the MYB44 promoter confirm that VIP1 binding to VREs is enhanced under conditions of MPK3 pathway stimulation. These results provide molecular insight into the cellular mechanism of target gene regulation by the MPK3 pathway.signal propagation ͉ transcription factor ͉ promoter motif ͉ bZIP ͉ Arabidopsis T he plant pathogen Agrobacterium tumefaciens transforms plant cells by delivering its transfer-DNA (T-DNA) into the plant cell nucleus, where it integrates into the plant genome. The subsequent growth of crown galls at the infection sites substantially interferes with plant development. There is ample experimental evidence demonstrating a key role of VIP1 (VirE2-interacting protein 1) in the nuclear import of T-DNA during Agrobacterium-mediated plant transformation (1, 2). VIP1 exhibits a stress-dependent subcellular localization; and phosphorylation of VIP1 at serine 79 by the stress-activated MAPK MPK3 (3) triggers its translocation from cytoplasm to the nucleus (2). Analysis of the vip1-1 mutant line, which produces only a truncated VIP1 protein, has shown that the N-terminal portion of VIP1 is sufficient to bind to and target VirE2 to the nucleus to facilitate transient genetic transformation by Agrobacterium (4). However, this is insufficient for stable genetic transformation and Agrobacterium-induced tumorigenesis (4). Apart from agrobacterial transformation, no in planta function has yet been ascribed to VIP1 in Arabidopsis. Considering that the only purpose of a plant protein would not merely lie in assisting pathogen invasion, we aimed to investigate the in planta function of VIP1 and the functional relevance of its stress-dependent nuclear translocation.In this work, we focus on the molecular events immediately downstream of stress-activated VIP1. We report on the role of VIP1 as a transcriptional regulator of genes that are ta...

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Section: Chromatin Immunoprecipitation Reveals Stress-dependent In Vivomentioning

confidence: 99%

VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression

Pitzschke

Djamei

Teige

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

127

159

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“…In the sequential treatment (OP), B. nigra activated defense responses that resembled a response to herbivore stress alone (P; Fig. 2, H and I): lipoxygenases LOX2 and LOX3 (Felton et al, 1994;Halitschke and Baldwin, 2003), the trypsin inhibitor WSCP (Zavala and Baldwin, 2004;Boex-Fontvieille et al, 2015), and the mitogen-activated protein kinase MPK3 (Pitzschke and Hirt, 2009). Notably, genes involved in stress responses and phytohormone signaling were differentially regulated between O 3 stress alone and the herbivore treatments (e.g.…”

Section: Transcriptome Responsesmentioning

confidence: 99%

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

et al. 2016

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Plants have evolved adaptive mechanisms that allow them to tolerate a continuous range of abiotic and biotic stressors. Tropospheric ozone (O 3 ), a global anthropogenic pollutant, directly affects living organisms and ecosystems, including plant-herbivore interactions. In this study, we investigate the stress responses of Brassica nigra (wild black mustard) exposed consecutively to O 3 and the specialist herbivore Pieris brassicae. Transcriptomics and metabolomics data were evaluated using multivariate, correlation, and network analyses for the O 3 and herbivory responses. O 3 stress symptoms resembled those of senescence and phosphate starvation, while a sequential shift from O 3 to herbivory induced characteristic plant defense responses, including a decrease in central metabolism, induction of the jasmonic acid/ethylene pathways, and emission of volatiles. Omics network and pathway analyses predicted a link between glycerol and central energy metabolism that influences the osmotic stress response and stomatal closure. Further physiological measurements confirmed that while O 3 stress inhibited photosynthesis and carbon assimilation, sequential herbivory counteracted the initial responses induced by O 3 , resulting in a phenotype similar to that observed after herbivory alone. This study clarifies the consequences of multiple stress interactions on a plant metabolic system and also illustrates how omics data can be integrated to generate new hypotheses in ecology and plant physiology.

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“…ABA boosts pre-invasive penetration resistance (Phase I) by stimulating PAMP-induced stomatal closure [6]. A pathway that involves the mitogen-activated protein kinase kinase 1 (MKK1)-mitogen-activated protein kinase 6 (MPK6) signaling cascade [55] and the protein kinase OST1 (OPEN STOMATA 1) [56] regulates ABA-induced ROS production, which consecutively regulates stomatal closure and other downstream signaling events. After tissue penetration by pathogens, ABA can either promote or suppress early post-invasive defenses (Phase II).…”

Section: Priming Of Early Post-invasive Penetration Resistancementioning

confidence: 99%

The multifaceted role of ABA in disease resistance

Ton

Flors

Mauch‐Mani

2009

Trends in Plant Science

750

583

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Disentangling the Complexity of Mitogen-Activated Protein Kinases and Reactive Oxygen Species Signaling

Cited by 121 publications

References 82 publications

VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression

VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

The multifaceted role of ABA in disease resistance

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