Systems approach identifies <scp>TGA</scp>1 and <scp>TGA</scp>4 transcription factors as important regulatory components of the nitrate response of <i><scp>A</scp>rabidopsis thaliana</i> roots

Álvarez, José M.; Riveras, Eleodoro; Vidal, Elena A.; Gras, Diana E.; Contreras‐López, Orlando; Tamayo, Karem P.; Aceituno, Felipe F.; Gómez, Isabel; Ruffel, Sandrine; Lejay, Laurence; Jordana, Xavier; Gutiérrez, Rodrigo A.

doi:10.1111/tpj.12618

Cited by 260 publications

(309 citation statements)

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“…These eight TFs interacted with PYL6, a member of the recently identified PYR/PYL/ RCAR ABA receptor family (37)(38)(39)(40). Consistent with previous observations (41,42), the TF-NAPPA network also revealed molecular links between the ABA and nitrate signaling pathways via ARR14 and TGA1, which have been found to regulate nitrate response (43), although the molecular mechanism of this connection remains unclear. Our TF-NAPPA network provides a hypothesis that ABA and nitrate signaling cross-regulation occurs through protein-protein interactions between PYL6 and TGA1, and also suggests an interaction of the ABA signaling pathway with other plant hormones such as brassinosteroid (BZR1) or jasmonic acid (MYC2).…”

Section: Halotag-nappa Reveals a Potential Role Of Tfs In Plant Hormonesupporting

confidence: 71%

Mapping transcription factor interactome networks using HaloTag protein arrays

Yazaki

Galli

Kim

et al. 2016

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

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Protein microarrays enable investigation of diverse biochemical properties for thousands of proteins in a single experiment, an unparalleled capacity. Using a high-density system called HaloTag nucleic acid programmable protein array (HaloTag-NAPPA), we created high-density protein arrays comprising 12,000 Arabidopsis ORFs. We used these arrays to query protein-protein interactions for a set of 38 transcription factors and transcriptional regulators (TFs) that function in diverse plant hormone regulatory pathways. The resulting transcription factor interactome network, TF-NAPPA, contains thousands of novel interactions. Validation in a benchmarked in vitro pull-down assay revealed that a random subset of TF-NAPPA validated at the same rate of 64% as a positive reference set of literaturecurated interactions. Moreover, using a bimolecular fluorescence complementation (BiFC) assay, we confirmed in planta several interactions of biological interest and determined the interaction localizations for seven pairs. The application of HaloTag-NAPPA technology to plant hormone signaling pathways allowed the identification of many novel transcription factor-protein interactions and led to the development of a proteome-wide plant hormone TF interactome network.protein arrays | interactome | hormone | systems biology | Arabidopsis thalianaA major objective in the postgenomic era is to assign detailed molecular function(s) to the many protein-coding genes that remain uncharacterized even in model organisms such as the reference plant Arabidopsis thaliana (1). It is estimated that Arabidopsis contains more than 2,000 transcription factors and transcriptional regulators (hereafter "TFs"), most of which are uncharacterized (2). TFs function as key players in plant hormone signal transduction pathways and are responsible for directing the widespread changes in gene expression that are essential for the regulation of growth and development in plants (3, 4). The TFs within these transcriptional regulatory networks do not work independently but rather undergo complex interactions with other proteins (2). Understanding how these TFs interact with other proteins will ultimately lead to a greater comprehension of biological systems.For determination of physical protein-protein interactions (PPIs), protein microarrays (5-10) are complementary to other PPI technologies such as the yeast two-hybrid system (Y2H) (11) and protein complex purification coupled with mass spectrometry (AP-MS) (12, 13). With conventional protein microarrays it is necessary to purify thousands of in vivo expressed proteins and to spot these purified proteins on a solid surface (5-8). In contrast, in situ synthesis protein microarray technologies simplify protein microarray fabrication by circumventing the steps of in vivo protein expression and purification (9,10,14,15). This streamlining facilitates an increase in the number of target genes that can be assayed, allowing for thousands of protein-encoding plasmids to be spotted at lower cost and in less time. Such ...

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Section: Halotag-nappa Reveals a Potential Role Of Tfs In Plant Hormonesupporting

confidence: 71%

Mapping transcription factor interactome networks using HaloTag protein arrays

Yazaki

Galli

Kim

et al. 2016

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

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“…Nevertheless, it has not been tested if this phenotype can be recovered after nitrogen depletion for these mutants. On the contrary, nlp7, tga1/tga4, and lbd37/38/39 mutants have been analyzed after nitrogen starvation and the results showed inhibited induction of nitrate-responsive genes in nlp7 and tga1/tga4 mutants but higher induction in lbd37/38/39 mutants after nitrate treatments (Castaings et al, 2009;Rubin et al, 2009;Alvarez et al, 2014). However, the expression of nitrate-induced genes in these mutants has not been investigated without nitrogen starvation to date.…”

Section: Discussionmentioning

confidence: 99%

“…A suppression study of NLP6 demonstrated that this gene plays an important role in nitrate signaling and other NLP members are also speculated to have similar function (Konishi and Yanagisawa, 2013). Using systems biology, SPL9, TGA1, TGA4, AFB3, and NAC4 have been identified as nitrate regulators involved in early nitrate response signaling (Krouk et al, 2010b;Vidal et al, 2010Vidal et al, , 2013Alvarez et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…In addition, CIPK23 can interact with and phosphorylate NRT1.1 at amino acid Thr-101 to maintain the high-affinity response under low-nitrate conditions (Ho et al, 2009). So far, several transcription factors (ANR1, LBD37/38/39, NLP6, NLP7, SPL9, TGA1, TGA4, and NAC4) have been identified to be nitrate regulatory genes (Zhang and Forde, 1998;Remans et al, 2006;Castaings et al, 2009;Rubin et al, 2009;Wang et al, 2009;Krouk et al, 2010b;Vidal et al, 2010Vidal et al, , 2013Gan et al, 2012;Konishi and Yanagisawa, 2013;Marchive et al, 2013;Alvarez et al, 2014). The Arabidopsis thaliana MADS box transcription factor ANR1 was the first to be characterized to regulate lateral root growth in response to nitrate treatment (Zhang and Forde, 1998;Gan et al, 2005Gan et al, , 2012.…”

Section: Introductionmentioning

confidence: 99%

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The Arabidopsis NRG2 Protein Mediates Nitrate Signaling and Interacts with and Regulates Key Nitrate Regulators

et al. 2016

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We show that NITRATE REGULATORY GENE2 (NRG2), which we identified using forward genetics, mediates nitrate signaling in Arabidopsis thaliana. A mutation in NRG2 disrupted the induction of nitrate-responsive genes after nitrate treatment by an ammonium-independent mechanism. The nitrate content in roots was lower in the mutants than in the wild type, which may have resulted from reduced expression of NRT1.1 (also called NPF6.3, encoding a nitrate transporter/receptor) and upregulation of NRT1.8 (also called NPF7.2, encoding a xylem nitrate transporter). Genetic and molecular data suggest that NRG2 functions upstream of NRT1.1 in nitrate signaling. Furthermore, NRG2 directly interacts with the nitrate regulator NLP7 in the nucleus, but nuclear retention of NLP7 in response to nitrate is not dependent on NRG2. Transcriptomic analysis revealed that genes involved in four nitrogen-related clusters including nitrate transport and response to nitrate were differentially expressed in the nrg2 mutants. A nitrogen compound transport cluster containing some members of the NRT/ PTR family was regulated by both NRG2 and NRT1.1, while no nitrogen-related clusters showed regulation by both NRG2 and NLP7. Thus, NRG2 plays a key role in nitrate regulation in part through modulating NRT1.1 expression and may function with NLP7 via their physical interaction.

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“…A number of molecular components involved in nitrate signaling have been identified to date in Arabidopsis. These include the nitrate sensor AtNPF6.3/ NRT1.1 (Ho et al, 2009), the CBL-INTERACTING PROTEIN KINASEs AtCIPK8 and AtCIPK23 (Ho et al, 2009;Hu et al, 2009), the RWP-RK TF NIN LIKE PROTEIN7 (AtNLP7; Castaings et al, 2009;Marchive et al, 2013), the LATERAL ORGAN BOUNDARY DOMAIN (LBD) gene family of TFs (AtLBD37, AtLBD38, and AtLBD39; Rubin et al, 2009), the auxin receptor AtAFB3 and its target AtNAC4 (Vidal et al, 2013), the TF TEOSINTE BRANCHED1/CYCLOIDEA/ PROLIFERATING CELL FACTOR1-20 (Guan et al, 2014), and the TGACG motif-binding factors AtTGA1 and AtTGA4 (Alvarez et al, 2014). However, nitrate signaling is not understood well in cereal crops such as wheat, rice, and maize, which are the most important food crops in the world.…”

Section: Tanac2 Belongs To a Cereal-specific Clade Of Nac Proteinsmentioning

confidence: 99%

The nitrate inducible NAC transcription factor TaNAC2-5A controls nitrate response and increases wheat yield

et al. 2015

Plant Physiol.

123

143

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Nitrate is a major nitrogen resource for cereal crops; thus, understanding nitrate signaling in cereal crops is valuable for engineering crops with improved nitrogen use efficiency. Although several regulators have been identified in nitrate sensing and signaling in Arabidopsis (Arabidopsis thaliana), the equivalent information in cereals is missing. Here, we isolated a nitrateinducible and cereal-specific NAM, ATAF, and CUC (NAC) transcription factor, TaNAC2-5A, from wheat (Triticum aestivum). A chromatin immunoprecipitation assay showed that TaNAC2-5A could directly bind to the promoter regions of the genes encoding nitrate transporter and glutamine synthetase. Overexpression of TaNAC2-5A in wheat enhanced root growth and nitrate influx rate and, hence, increased the root's ability to acquire nitrogen. Furthermore, we found that TaNAC2-5A-overexpressing transgenic wheat lines had higher grain yield and higher nitrogen accumulation in aerial parts and allocated more nitrogen in grains in a field experiment. These results suggest that TaNAC2-5A is involved in nitrate signaling and show that it is an exciting gene resource for breeding crops with more efficient use of fertilizer.

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Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots

Cited by 260 publications

References 60 publications

Mapping transcription factor interactome networks using HaloTag protein arrays

Mapping transcription factor interactome networks using HaloTag protein arrays

The Arabidopsis NRG2 Protein Mediates Nitrate Signaling and Interacts with and Regulates Key Nitrate Regulators

The nitrate inducible NAC transcription factor TaNAC2-5A controls nitrate response and increases wheat yield

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