A transcription factor hierarchy defines an environmental stress response network

Song, Liang; Huang, Shao‐shan Carol; Wise, Aaron; Castanon, Rosa; Nery, Joseph R.; Chen, Huaming; Watanabe, Marina; Thomas, Jerushah; Bar‐Joseph, Ziv; Ecker, Joseph R.

doi:10.1126/science.aag1550

Cited by 407 publications

(475 citation statements)

References 99 publications

(96 reference statements)

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“…The promoter and 59 UTR region of the P5CS1 gene contains most conserved cis elements, which were predicted as potential TF binding sites (Supplemental Figs. S1 and S2;Fichman et al, 2015;Song et al, 2016). Besides the 59 regulatory region, introns have been reported to carry regulatory elements with capacity to enhance transcription in a number of genes (Lohmann et al, 2001;Casas-Mollano et al, 2006;Gallegos and Rose, 2015), including the high-affinity phosphate transporter AtPht1;4 (Karthikeyan et al, 2009).…”

Section: Phosphate Starvation Response Factors Identified By a Yeastmentioning

confidence: 99%

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Proline Accumulation Is Regulated by Transcription Factors Associated with Phosphate Starvation

et al. 2017

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ORCID ID: 0000-0002-9163-9875 (L.S.).Pro accumulation in plants is a well-documented physiological response to osmotic stress caused by drought or salinity. In Arabidopsis (Arabidopsis thaliana), the stress and ABA-induced D1-PYRROLINE-5-CARBOXYLATE SYNTHETASE1 (P5CS1) gene was previously shown to control Pro biosynthesis in such adverse conditions. To identify regulatory factors that control the transcription of P5CS1, Y1H screens were performed with a genomic fragment of P5CS1, containing 1.2-kB promoter and 0.8-kb transcribed regions. The myeloblastosis (MYB)-type transcription factors PHOSPHATE STARVATION RESPONSE1 (PHR1) and PHR1-LIKE1 (PHL1) were identified to bind to P5CS1 regulatory sequences in the first intron, which carries a conserved PHR1-binding site (P1BS) motif. Binding of PHR1 and PHL1 factors to P1BS was confirmed by Y1H, electrophoretic mobility assay and chromatin immunoprecipitation. Phosphate starvation led to gradual increase in Pro content in wild-type Arabidopsis plants as well as transcriptional activation of P5CS1 and PRO DEHYDROGENASE2 genes. Induction of P5CS1 transcription and Pro accumulation during phosphate deficiency was considerably reduced by phr1 and phl1 mutations and was impaired in the ABA-deficient aba2-3 and ABA-insensitive abi4-1 mutants. Growth and viability of phr1phl1 double mutant was significantly reduced in phosphate-depleted medium, while growth was only marginally affected in the aba2-3 mutants, suggesting that ABA is implicated in growth retardation in such nutritional stress. Our results reveal a previously unknown link between Pro metabolism and phosphate nutrition and show that Pro biosynthesis is target of cross talk between ABA signaling and regulation of phosphate homeostasis through PHR1-and PHL1-mediated transcriptional activation of the P5CS1 gene.

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Section: Phosphate Starvation Response Factors Identified By a Yeastmentioning

confidence: 99%

“…A recent chromatin immunoprecipitation (ChIP)-seq study suggests that several ABA-regulated transcription factors (TFs) can bind to the promoter region of the P5CS1 gene (Supplemental Fig. S2; Song et al, 2016).…”

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Proline Accumulation Is Regulated by Transcription Factors Associated with Phosphate Starvation

et al. 2017

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“…Among these, AKS1 exhibited a unique behavior that seemed to show dissociation from DNA in response to ABA Song et al, 2016). A positive relationship between the binding of transcription factors to DNA and gene expression appeared to exist (Song et al, 2016). However, how ABA regulates this binding of transcription factors to DNA remained unknown.…”

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confidence: 99%

“…Systematic study on transcription factors highlighted the dynamic changes in the ABA-dependent binding of transcription factors to DNA. Among these, AKS1 exhibited a unique behavior that seemed to show dissociation from DNA in response to ABA Song et al, 2016). A positive relationship between the binding of transcription factors to DNA and gene expression appeared to exist (Song et al, 2016).…”

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Reconstitution of Abscisic Acid Signaling from the Receptor to DNA via bHLH Transcription Factors

2017

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ORCID IDs: 0000-0002-9406-4093 (Y.T.); 0000-0001-6450-8506 (K.S.).The plant hormone abscisic acid (ABA) confers drought tolerance in plants through stomatal closure and regulation of gene expression. The complex consisting of the ABA receptor PYRABACTIN RESISTANCE/REGULATORY COMPONENTS OF ABA RECEPTOR (PYR/RCAR), type 2C protein phosphatase (PP2C), and SNF1-related protein kinase 2 (SnRK2) has a key role in ABA signaling. Basic helix-loop-helix (bHLH) transcriptional activator ABA-RESPONSIVE KINASE SUBSTRATE1 (AKS1, also known as FBH3) is released from DNA by phosphorylation-induced monomerization in response to ABA in guard cells. Here we reconstituted the release of AKS1 from DNA via the ABA signaling core complex in vitro. We first obtained evidence to confirm that AKS1 is an endogenous substrate for SnRK2s. Phosphorylation of AKS1 and activation of SnRK2 showed the same time course in response to ABA in guard cells. AKS1 was bound to SnRK2.6 in vivo. Three ABA-responsive SnRK2s (SnRK2.2/ SRK2D, SnRK2.3/SRK2I, and SnRK2.6/SRK2E/OST1) phosphorylated AKS1 in vitro, and the phosphorylation was eliminated by the triple mutation of SnRK2s in plants. We reconstituted the AKS1 phosphorylation in vitro via the signaling complex containing the ABA receptor PYR1, a PP2C, HYPERSENSITIVE TO ABA1 (HAB1), and a protein kinase, SnRK2.6 in response to ABA. We further reconstituted the release of AKS1 from the target gene of POTASSIUM CHANNEL IN ARABIDOPSIS THALIANA 1 (KAT1) via the complex in response to ABA. These results demonstrate that AKS1 provides a link between the signaling complex and ABA-responsive genes and furnish evidence for a minimal signaling mechanism from ABA perception to DNA.

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“…8–13 ABRE-dependent gene expression plays a major role in ABA-responsive gene expression as ABA signal output under dehydration stress. 14,15 A growing body of evidence suggests that protein kinase CK2, formerly known as casein kinase II, is involved in ABA signaling in response to abiotic stress in plants. 16,17 …”

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Protein kinase CK2α subunits constitutively activate ABA signaling in Arabidopsis

Nagatoshi

Fujita

2018

Plant Signaling & Behavior

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Protein kinase CK2 (formerly known as casein kinase II), a Ser/Thr protein kinase highly conserved in eukaryotes, is essential for cell survival by regulating a wide range of plant growth, development, and stress responses. A growing body of evidence has shown a link between CK2 and abscisic acid (ABA) signaling in response to abiotic stress. However, the roles of CK2 subunits in ABA signaling remain unclear in plants. Our recent work in Arabidopsis thaliana has revealed that CK2α and CK2β subunits inversely modulate ABA signal output. Here, we examine the roles of CK2αs, by assessing how CK2αs affect ABA signaling. Together with the previous findings, our mutant and transient expression analyses demonstrate that CK2αs positively modulate ABA signaling through the core ABA signaling pathway in the presence of ABA, though the positive effect of CK2αs are much smaller than that of core ABA signaling components in ABA response. In addtion, our current and previous findings also suggest that CK2αs play a role in maintaining constitutively active ABA signaling even in the absence of ABA independently of the core ABA signaling pathway. Thus, we found that CK2αs constitutively activate ABA signaling in the presence or absence of ABA in a different manner in Arabidopsis plants.

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A transcription factor hierarchy defines an environmental stress response network

Cited by 407 publications

References 99 publications

Proline Accumulation Is Regulated by Transcription Factors Associated with Phosphate Starvation

Proline Accumulation Is Regulated by Transcription Factors Associated with Phosphate Starvation

Reconstitution of Abscisic Acid Signaling from the Receptor to DNA via bHLH Transcription Factors

Protein kinase CK2α subunits constitutively activate ABA signaling in Arabidopsis

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