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Integration of shoot-derived polypeptide signals by root TGA transcription factors is essential for survival under fluctuating nitrogen environments [ChIP-seq]

ABSTRACT: Unlike plants in the field, which experience significant temporal fluctuations in environmental conditions, plants in the laboratory are typically grown in controlled, stable environments. Therefore, signaling pathways evolved for survival in continuously fluctuating environments often remain functionally latent in laboratory settings. Here, we show that TGA1 and TGA4 act as hub transcription factors through which the expression of genes involved in high-affinity nitrate uptake are regulated in response to shoot-derived phloem mobile polypeptides, CEP DOWNSTREAM 1 (CEPD1), CEPD2 and CEPD-like 2 (CEPDL2) as nitrogen (N) deficiency signals, and Glutaredoxin S1 (GrxS1) to GrxS8 as N sufficiency signals. CEPD1/2/CEPDL2 and GrxS1-S8 competitively bind to TGA1/4 in roots, with the former acting as transcription coactivators that enhance the uptake of nitrate, while the latter function as corepressor complexes together with TOPLESS (TPL), TPL-related 1 (TPR1) and TPR4 to limit nitrate uptake. Arabidopsis plants deficient in TGA1/4 maintain basal nitrate uptake and exhibit growth similar to wild-type plants in a stable N environment, but were impaired in regulation of nitrate acquisition in response to shoot N demand, leading to defective growth under continuously fluctuating N environments where rhizosphere nitrate ions switch periodically between deficient and sufficient states. TGA1/4 are crucial transcription factors that enable plants to survive under fluctuating and challenging N environmental conditions.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE240737 | GEO | 2024/07/11

REPOSITORIES: GEO

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Integration of shoot-derived polypeptide signals by root TGA transcription factors is essential for survival under fluctuating nitrogen environments [RNA-seq]

Project description:Unlike plants in the field, which experience significant temporal fluctuations in environmental conditions, plants in the laboratory are typically grown in controlled, stable environments. Therefore, signaling pathways evolved for survival in continuously fluctuating environments often remain functionally latent in laboratory settings. Here, we show that TGA1 and TGA4 act as hub transcription factors through which the expression of genes involved in high-affinity nitrate uptake are regulated in response to shoot-derived phloem mobile polypeptides, CEP DOWNSTREAM 1 (CEPD1), CEPD2 and CEPD-like 2 (CEPDL2) as nitrogen (N) deficiency signals, and Glutaredoxin S1 (GrxS1) to GrxS8 as N sufficiency signals. CEPD1/2/CEPDL2 and GrxS1-S8 competitively bind to TGA1/4 in roots, with the former acting as transcription coactivators that enhance the uptake of nitrate, while the latter function as corepressor complexes together with TOPLESS (TPL), TPL-related 1 (TPR1) and TPR4 to limit nitrate uptake. Arabidopsis plants deficient in TGA1/4 maintain basal nitrate uptake and exhibit growth similar to wild-type plants in a stable N environment, but were impaired in regulation of nitrate acquisition in response to shoot N demand, leading to defective growth under continuously fluctuating N environments where rhizosphere nitrate ions switch periodically between deficient and sufficient states. TGA1/4 are crucial transcription factors that enable plants to survive under fluctuating and challenging N environmental conditions.

2024-07-11 | GSE240736 | GEO

Integration of shoot-derived polypeptide signals by root TGA transcription factors is essential for survival under fluctuating nitrogen environments

2024-07-11 | PXD044498 | JPOST Repository

Shoot-to-root mobile CEPD-like 2 integrates shoot nitrogen status to systemically regulate nitrate uptake in Arabidopsis

Project description:Plants modulate the efficiency of root nitrogen (N) acquisition in response to shoot N demand. However, molecular components directly involved in this shoot-to-root communication remain to be identified. Here, we show that phloem-mobile CEPD-like 2 (CEPDL2) polypeptide is upregulated in the leaf vasculature in response to decreased shoot N status and, after translocation to the roots, promotes high-affinity uptake and root-to-shoot transport of nitrate by activating nitrate transporter genes such as NRT2.1, NRT3.1 and NRT1.5. Loss of CEPDL2 decreases nitrate uptake and root-to-shoot transport activity in roots, leading to a reduction in shoot nitrate content and plant biomass. CEPDL2 contributes to N acquisition cooperatively with CEPD1 and CEPD2 that mediate root N status, and their complete loss severely impairs N homeostasis in plants. Reciprocal grafting analysis provided conclusive evidence that the shoot CEPDL2/CEPD genotype defines the root high-affinity uptake activity of nitrate. Our results indicate that plants integrate shoot N status and root N status in leaves and systemically regulate the efficiency of root N acquisition.

2020-02-10 | GSE140834 | GEO

Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition

Project description:Plants uptake nitrogen (N) from the soil mainly in the form of nitrate. However, nitrate is often distributed heterogeneously in natural soil. Plants, therefore, have a systemic long-distance signaling mechanism by which N-starvation on one side of the root leads to a compensatory N uptake on the other N-rich side. This systemic N acquisition response is triggered by a root-to-shoot mobile peptide hormone, C-terminally Encoded Peptide (CEP), originating from the N-starved roots, but the molecular nature of the descending shoot-to-root signal remains elusive. Here, we show that phloem-specific polypeptides that are induced in leaves upon perception of root-derived CEP act as descending long-distance mobile signals translocated to each root. These shoot-derived polypeptides, which we named CEP Downstream 1 (CEPD1) and CEPD2, upregulate the expression of the nitrate transporter gene NRT2.1 in roots specifically when nitrate is present in the rhizosphere. Arabidopsis plants deficient in this pathway show impaired systemic N-acquisition response accompanied with N-deficiency symptoms. These fundamental mechanistic insights should provide a conceptual framework for understanding systemic nutrient acquisition responses in plants. We prepared total RNA from vascular tissues of wild type, CEP1-treated wild type, and cepr1-1 mutant, and used a microarray analysis to identify genes specifically induced by CEP1.

2017-04-06 | GSE94161 | GEO

Root nitrate response of Col-0 plants and tga1/tga4 mutant plants

2013-03-31 | GSE43011 | GEO

Root nitrate response of Col-0 plants and tga1/tga4 mutant plants

Project description:Nitrate regulates plant growth and development and acts as a potent signal to control gene expression in Arabidopsis. Using an integrative bioinformatics approach we identified TGA1 and TGA4 as putative regulatory factors that mediate nitrate responses in Arabidopsis thaliana roots. We showed that both TGA1 and TGA4 mRNAs accumulate strongly and quickly after nitrate treatments in root organs in a tissue-specific manner. Phenotypic analysis of tga1/tga4 double mutant plants indicated that TGA1 and TGA4 are necessary for nitrate modulation of both primary and lateral root growth. Global gene expression analysis revealed that 97% of the genes with altered expression in tga1/tga4 double mutant plants are regulated by nitrate treatments indicating these transcription factors have a specific role in nitrate responses in Arabidopsis root organs. Among the nitrate-responsive genes that depend on TGA1/TGA4 for normal regulation of gene expression, we found nitrate transporters NRT2.1, NRT2.2 and nitrite reductase (NIR) genes. Specific binding of TGA1 to its cognate DNA sequence on the target gene promoters was confirmed by chromatin immunoprecipitation assays. These results identify TGA1 and TGA4 as important regulatory factors of the nitrate response in Arabidopsis roots. Arabidopsis seedlings of the Col-0 and tga1/tga4 genotypes were grown on hydroponic medium containing 1X MS salts without Nitrogen, supplemented with 0.5 mM ammonium succinate as Nitrogen source and 3 mM sucrose on a Percival chamber under a photoperiod of 16 hours of light (100 ?E/m2/sec) and 8 hours of dark at 22°C for 14 days. The plants were treated at the onset of the light cycle with 5 mM KNO3 or 5 mM KCl as control for 2 hours. Whole roots were cut from seedlings and frozen on liquid Nitrogen. Total RNA was extracted using the TriZol reagent. 3 independent biological replicates were performed.

2013-03-31 | E-GEOD-43011 | biostudies-arrayexpress

A type 2C protein phosphatase activates high-affinity nitrate uptake by directly dephosphorylating NRT2.1 in Arabidopsis

Project description:Nitrate transporter NRT2.1, which plays a central role in high-affinity nitrate uptake in roots, is activated at the post-translational level in response to nitrogen (N) starvation. However, critical enzymes required for post-translational activation of NRT2.1 remain to be identified. Here, we show that a type 2C protein phosphatase, designated CEPD-induced phosphatase (CEPH), activates high-affinity nitrate uptake by directly dephosphorylating S501 of NRT2.1, a residue that functions as a negative phospho-switch. CEPH is predominantly expressed in epidermal and cortex cells in roots and up-regulated by N starvation via a CEPDL2/CEPD1/2-mediated long-distance signaling from shoots. Loss of CEPH leads to a marked decrease in high-affinity nitrate uptake, tissue nitrate content, and plant biomass. Collectively, our results identify CEPH as a crucial enzyme in N starvation-dependent activation of NRT2.1, providing molecular and mechanistic insights into how plants regulate high-affinity nitrate uptake at the post-translational level in response to the N environment. We prepared total RNA from roots of wild type, CEPD1ox, CEPD2ox and CEPDL2ox plants grown on N-replete vertical plates for 14 d, and used a microarray analysis to identify genes specifically induced by CEPD family peptides.

2020-11-06 | GSE160649 | GEO

A type 2C protein phosphatase activates high-affinity nitrate uptake by directly dephosphorylating NRT2.1 in Arabidopsis

2021-03-02 | PXD022343 | Pride

Shoot responses to different nitrate supply to roots in wild-type and genotypes affected for cytokinin biosynthesis and transport

Project description:Plants face temporal and spatial variation in nitrogen (N) availability. This includes heterogeneity in soil nitrate (NO3-) content. To face these constraints, plants modify their gene expression and physiological processes to optimize N acquisition. This plasticity relies on a complex long-distance root-shoot-root signaling network that remains poorly understood. We previously showed that cytokinin (CK) biosynthesis is required to trigger systemic N signaling. Here, we performed split-root experiments and used a combination of CK-related mutant analyses, hormone profiling, transcriptomic analysis, NO3- uptake assays, and root growth measurements to gain insight into systemic N signaling in Arabidopsis thaliana. By comparing wild-type plants and mutants affected in CK biosynthesis and ABCG14-dependent root-to-shoot translocation of CK, we revealed an important role for active trans-Zeatin (tZ) in systemic N signaling. Both rapid sentinel gene regulation and long-term functional acclimation to heterogeneous NO3- supply, including NO3- transport and root growth regulation, are likely mediated by the integration of tZ content in shoots. Furthermore, shoot transcriptome profiling revealed that glutamate/glutamine metabolism is likely a target of tZ root-to-shoot translocation, prompting an interesting hypothesis regarding shoot-to-root communication. Finally, this study highlights tZ-independent pathways regulating gene expression in shoots as well as NO3- uptake activity in response to total N-deprivation. We used microarrays to detail transcriptional reprogramming occurring in shoots in response to heterogeneous nitrate supply compared to homogeneous nitrate supply in wild-type Arabidopsis thaliana plants and in two mutants affected in cytokinin biosynthesis and transport.

2018-05-09 | GSE114162 | GEO

Transcriptome analysis of Arabidopsis shoots and roots whose nitrate levels and IPT3 expression are manipulated in a shoot-specific manner

Project description:In plants, nitrate is suggested to act as an indicator of nitrogen (N) status that modulates N responses under steady-state conditions. Our preceding study suggested that shoot nitrate accumulation alone represses expression of N starvation-inducible genes in shoots and roots. Notably, we observed that shoot nitrate accumulation was accompanied by increases in shoot expression of ISOPENTENYL TRANSFERASE 3 (IPT3) and shoot levels of N6-(Δ2-isopentenyl) adenine (iP)-type CK. IPT3 expression is localized primarily in phloem companion cells, and iP-type CKs, which are synthesized by IPT3, are phloem-mobile. Hence, both local and systemic responses to shoot nitrate status may be regulated by IPT3-synthesized iP-type CKs. Thus, the present study aims to dissect the local/systemic responses to shoot nitrate status and their dependence on shoot IPT3. To achieve this, we developed a novel experimental system to manipulate nitrate levels and IPT3 expression in a shoot-specific manner using grafted plants derived from the plants lacking nitrate reductase and/or IPT3. Using shoots and roots from the grafted plants, RNA-seq analysis was performed.

2024-08-31 | E-MTAB-14302 | biostudies-arrayexpress

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