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. 2017 Jan 9;12(1):e1273303. doi: 10.1080/15592324.2016.1273303

Environmental nitrate signals through abscisic acid in the root tip

Jeanne M Harris a,✉, Christine A Ondzighi-Assoume b
PMCID: PMC5289525  PMID: 28067583

ABSTRACT

Roots respond to changes in environmental nitrate with a localized stimulation of ABA levels in the root tip. This rise in ABA levels is due to the action of ER-localized β-GLUCOSIDASE 1, which releases bioactive ABA from the inactive ABA-glucose ester. The slow rise in root tip ABA levels stimulates expression of nitrate metabolic enzymes and simultaneously activates a negative feedback loop involving the protein phosphatase, ABI2, which reduces nitrate influx via the AtNPF6.3 transceptor. The rise in root-tip localized ABA also negatively regulates expression of the SCARECROW transcription factor, thus providing a sensitive mechanism for modulating root growth in response to environmental changes.

KEYWORDS: Abscisic Acid, ABA, ABA-GE, ABI2, Arabidopsis thaliana, AtNPF6.3, β-GLUCOSIDASE 1, endodermis, environmental signals, deconjugation, nitrate, root growth, root, root tip, SCARECROW

Nitrogen is one of the most important nutrients for plants, controlling all major aspects of plant growth and development, such as seed germination, root branching, shoot branching, and flowering time.1-5 For plants that do not form a nitrogen-fixing symbiosis, nitrate is a major source of nitrogen nutrition, and thus nitrate sensing and response is a core signaling module that intersects with many hormone signaling pathways, especially that of auxin, cytokinin and gibberellin.6,7 More recently, the intersection of nitrate signaling with abscisic acid signaling has begun to be resolved.

Abscisic acid (ABA) is often characterized as a stress hormone, but is more accurately described as the interpreter of the environment, responding to both abiotic and biotic signals.8,9 ABA mediates responses to a diverse set of environmental signals: drought, salt, cold, osmotic, nitrate, phosphate and light, as well as pathogens.8-12 Having one hormone mediating responses to multiple environmental signals makes it possible to coordinate and optimize responses at a whole plant level. Based on the role of ABA in multiple environmentally-regulated plant developmental processes, it is interesting to speculate that ABA may play a key role in signal integration, optimizing plant responses to conflicting environmental inputs – a fruitful area for future research.

Nitrate and ABA in root development

Plants continuously sense nitrate in the environment, modulating plant growth in response. Root growth is exquisitely sensitive to changes in environmental nitrate, either inhibiting or stimulating growth depending on concentration, location and physiologic context.6 In particular, nitrate has powerful effects on lateral root elongation, either by controlling meristem activation after emergence from the primary root, or by controlling lateral root elongation. Because the presence of nitrate is usually patchy within the soil, changing concentrations of nitrate can have potent effects on root architecture, locally promoting root growth within a nitrate patch, and systemically inhibiting lateral root elongation when overall levels of nitrate are high.8

Although ABA is best known for controlling stomatal closure and seed dormancy,13 it plays a major role in root development, regulating root elongation by modulating the major control points of root growth: cell division and cell elongation.14,15 Additionally, ABA controls lateral root development by regulating initiation, emergence and meristem activation, as well as elongation (reviewed in8). Because ABA mediates responses to many environmental signals, its ability to regulate lateral root formation provides the plant with the flexibility to modulate root architecture in response to a constantly varying environment.8

Root branching in response to local nitrate signals had been previously shown to require abscisic acid (ABA) signaling, but the mechanism was unknown.16,17 Both ABA and nitrate have multiple effects on the elaboration of root architecture, so crosstalk was likely, but it could either be direct or indirect. Recent work analyzing nitrate signaling in Arabidopsis reveals a sensitive mechanism linking nitrate with ABA signaling and activation of a negative feedback loop to reduce nitrate acquisition when environmental nitrate remains high.

Signaling mechanism

Entry

Nitrate uptake into plant cells is mediated by a host of transporters from the large NPF (NRT1.1 and Peptide Transporter Family) gene family, many of which transport nitrate, as well as from the smaller Nitrate Transporter 2 (NRT2) family.6,18 The NPF family is much smaller in Arabidopsis, which has only 53 members, than in other angiosperm taxa, such as Medicago truncatula and rice, which each have around 80. Although NRT2 transporters appear to be specific for nitrate, many NPF proteins transport substrates other than, or in addition to, nitrate.18,19 Nonetheless, there are many different ways nitrate can enter an Arabidopsis cell. Expression of characterized transporters in Arabidopsis is restricted to specific cells and tissues, allowing the plant fine control over nitrate movement both into and within the plant.6

In the Arabidopsis root, 6 different transporters have been shown to transport nitrate from the environment into root cells.6,20 Under conditions of low external nitrate, uptake is mediated primarily by the high-affinity transporter, AtNRT2.1, and to a lesser degree by AtNRT2.2 and AtNRT2.421-23; under nitrate starvation conditions uptake is mediated mainly by AtNRT2.5, with some contribution by AtNRT2.1.24,25 At high concentrations of environmental nitrate, the dual-affinity transporter AtNPF6.3 (AtNRT1.1) and the low-affinity transporter AtNPF4.6 (AtNRT1.2; AtAIT1) come into play.26,27

Two of these transporters, AtNPF6.3 and AtNRT2.1, have also been proposed to function as receptors, thus earning the name of “transceptor”.28-31 The coupling of transport to sensing allows the cell to have an accurate perception of the amount of nitrate it is acquiring; once nitrate enters the cytoplasm, it can either be moved to the vacuole, exported from the cell or rapidly converted to other forms of inorganic nitrogen and subsequently assimilated, making accurate assessment of nitrate pools in the cytoplasm problematic.20,32 The strongest case can be made for AtNPF6.3 being a transceptor, with a nitrate sensing role that can be uncoupled from transport.30

Nitrate activation of ABA signaling by release of bioactive ABA from inactive stores

Once nitrate is increased in the environment of the root, it triggers the gradual accumulation of ABA in the root tip, stimulating ABA signaling, and ultimately regulating first nitrate metabolism, then uptake (Fig. 1).33 This ABA signaling module is activated by stimulation of β-GLUCOSIDASE 1 (AtBG1) expression within 2 hours.33 AtBG1 encodes an ER-localized β-glucosidase that cleaves the inactive ABA conjugate, ABA glucose ester (ABA-GE), releasing ABA, which is transported to the cytoplasm, where it accumulates.33,34 Subsequently, expression of both ABA-responsive and nitrate-responsive genes is induced.

Figure 1.

Figure 1.

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Overview of nitrate signaling via release of bioactive ABA in the Arabidopsis root tip. As levels of nitrate (NO3¯) rise in the environment, nitrate is actively transported into the root cell via the dual-affinity AtNPF6.3 (AtNRT1.1) transporter, which also functions as a nitrate sensor.30 Transport of nitrate through AtNPF6.3 competitively inhibits transport of its other ligand, auxin (IAA), into the cell.62 Once inside the cell, nitrate is converted into ammonium (NH4+), by the sequential action of the nitrate reductase and nitrite reductase enzymes, encoded by NIA1 and NIA2, and NIR1, respectively. Nitrate also stimulates expression of the AtBG1 gene, encoding an ER-localized β-glucosidase, that cleaves the inactive ABA conjugate, ABA-glucose ester (ABA-GE), releasing bioactive ABA.33 Although AtBG1 gene expression is strongly induced within 2 hours of adding nitrate, the ABA levels gradually rise over the course of 2 d, 33 binding the intracellular PYR/PYL/RCAR receptor, stimulating expression of NIA1, NIA2 and NIR1, and inactivating the ABA co-receptor, ABI2.13,63 Once ABI2 is inactivated, the CIPK23/CBL1 complex is free to act, phosphorylating AtNPF6.3 and inhibiting its ability to transport.37 Thus, nitrate transport into the cell activates a slow-acting negative feedback loop, mediated by BG1 and ABA, that reduces further nitrate import and stimulates nitrate assimilation.

Analysis of gene expression reveals a curious pause. Although nitrate-induced stimulation of AtBG1 expression is quite rapid, and exogenous ABA induces the expression of both nitrate-responsive and ABA-responsive genes within 2 hours, nonetheless, nitrate induction of these same genes is much slower, and takes approximately 2 d to show a significant difference.33 This could be simply the result of nitrate-induced changes in gene expression that are restricted to a small zone of the root, say, the root tip, and are thus swamped out when the entire root is used to analyze gene expression, as compared with ABA, which may induce the expression of these genes throughout the root. However, ABA accumulation itself appears to be delayed.33 In addition, analysis of a ProRAB18:GFP reporter gene fusion indicates that the response is largely constrained to the root tip both after ABA and after nitrate treatment and yet the nitrate-induced ProRAB18:GFP expression features a similar 2-day lag.33 These observations suggest that the interval between induction of AtBG1 gene expression and ABA responses may be due to some post-transcriptional regulation of BG1 function. Lee and colleagues have shown that polymerization of the BG1 enzyme results in a 4-fold increase in enzymatic activity.34 Thus, the time lag between induction of the AtBG1 gene and accumulation of ABA, may imply the existence of a second event, or signal, that induces BG1 polymerization or perhaps an additional activation step. Alternatively, the process of polymerization itself may be slow, although Lee and colleagues report that over 80% of BG1 molecules are in higher order complexes within 10 hours of exposure to dehydration stress.34

ABA-induced inhibition of nitrate influx

With our findings of nitrate-induced ABA release from inactive stores, paired with recent studies from Benoit Lacombe's laboratory, the outline of a slow-acting negative feedback loop, by which nitrate inhibits its own uptake, using ABA as a key mediator, begins to take shape. In this model, as nitrate-induced ABA accumulates in the cytoplasm, it activates a negative feedback loop, inhibiting nitrate influx (Fig. 1). This negative feedback loop is dependent on 2 key enzymes, the ER-localized AtBG1 β-glucosidase, and the cytoplasmic AtABI2 type 2C protein phosphatase (PP2C). AtBG1 expression is stimulated by nitrate and catalyzes the release of ABA from inactive stores.33 ABA is transported to the cytoplasm, where it binds the PYR/PYL/RCAR receptors and a protein phosphatase 2C (PP2C) coreceptor.35,36 AtABI2 is a PP2C that functions both as a coreceptor for ABA,35,36 and additionally serves to inactivate the CIPK23 kinase complex that phosphorylates the nitrate/auxin transporter AtNPF6.3, inhibiting its ability to transport nitrate.30,37 Interestingly, when a PP2C binds the ABA/receptor complex, its phosphatase ability is inhibited.35,36 As ABA levels rise within the cell, more ABI2 molecules become bound to, and inactivated by, the ABA/receptor complex, thereby relieving repression of the CIPK23/CBL1 kinase complex, which is now free to phosphorylate AtNPF6.3, inhibiting nitrate transport into the cell (Fig. 1).37 This gradual accumulation of intracellular ABA in response to increased environmental nitrate thus activates a slow-acting negative feedback loop, mediated by AtBG1 and ABA, that reduces further nitrate import and stimulates nitrate assimilation.

Some puzzles

Although nitrate clearly signals via ABA, adding nitrate to the root is not the same as adding ABA. Let's examine 2 puzzles:

  • Puzzle 1: ABA treatment stimulates significantly more expression of ABA-responsive and nitrate-responsive genes than nitrate treatment does. However, nitrate-treated roots accumulate even more ABA in the root tip than ABA–treated roots.33 How can this be?

  • Puzzle 2: Addition of ABA exogenously generally results in inhibition of root growth. If 10 mM NO3¯ increases ABA to high levels then we should expect inhibition of root growth, which was not observed in this system.33

Some insights

The answer likely lies in the more controlled spatial and temporal regulation of ABA levels in response to an increase in environmental nitrate rather than the uniform, high levels of apoplastic ABA the plant experiences when the root is suddenly flooded with ABA during exogenous ABA treatment.

Dosage sensitivity: Many ABA responses are highly dosage sensitive, with different levels of ABA resulting in a graded series of physiologic responses. Classic examples include ABA regulation of stomatal closing, calcium spiking during initiation of legume nodulation and elongation of both primary and lateral roots.38-41 Thus, the careful control of ABA levels can result in a more nuanced response to environmental signals.

Internal vs. external location: Perhaps the nitrate-induced ABA accumulation produces a more fine-tuned regulation of ABA accumulation, allowing us to observe ABA's positive effect on root growth, rather than the inhibitory effect seen with exogenous ABA treatment.15,38,42,43 The internal location of ABA within the root may matter: nitrate-induced ABA accumulation occurs in the root tip, and intracellularly, rather than via the apoplast, as it is during exogenous ABA treatment. Although even exogenously added ABA ultimately accumulates in the endodermis, just as native ABA does,33 it must pass through the epidermal and cortical cell layers to reach it. Perhaps even a transient ABA flux through these outer cell layers influences the response of the root to endodermal ABA. The major difference, however, is that exogenously added ABA is present first in the root apoplast, and must be transported into the cells at some point on its journey to the endodermis. While there is evidence supporting the existence of both extracellular and intracellular sites of ABA perception, it is clear that the intracellular PYR/PYL/RCAR receptors comprise the predominant perception module.44-46 However, even if ABA is not perceived extracellularly, or via a transceptor, the process of transporting all of the ABA from the apoplast to the inside of the cell may have an effect. Recently, several ABA transporters have been identified, many of which also transport other substrates.19,47-50 Increasing the concentration of one substrate is likely to have effects on the transport of the others. For AtNPF4.1, transport of the gibberellin, GA3, competes with ABA transport.51 The closely related transporter, AtNPF4.6 (AtAIT1; AtNRT1.2), transports both nitrate and ABA, making it an intriguing candidate to coordinate signaling of these 2 pathways.27,47 Kanno and colleagues have shown that nitrate does not competitively inhibit ABA transport and that ABA is the preferred substrate.51 Is it possible that ABA competitively inhibits nitrate transport through AtNPF4.6? Alternatively, the act of entering may trigger a change. Both the AtNPF4.6 and AtNPF4.1 ABA transporters are in the same family as the AtNPF6.3 (AtNRT1.1) transceptor, which both transports nitrate into the cell and transduces a signal. Although there is yet no genetic evidence for an ABA transceptor, this is another possible mechanism. These possibilities are just a few ways in which flooding the apoplast with high levels of ABA may have the effect of altering the influx of other molecules in a way in which a strictly intracellular increase of ABA would not. Thus, the different effects of exogenous ABA and nitrate-induced ABA accumulation on root growth may be due to the different ways in which ABA reaches the cells that are its site of action.

Timing: The role of timing may also be important. Nitrate stimulates ABA accumulation in the root tip, but this is a slow response, and takes place over the course of 2 d.33 Perhaps a slow rise in ABA levels has a different effect on root growth than a sudden, global ABA treatment that is the hallmark of exogenous ABA studies. Perhaps cells passing sequentially through a series of graded ABA concentrations, rather than jumping in one step to the final concentration, sets up a different physiologic state in the root. This is an appealing model, but one that will need to be tested in a system in which responses of individual cells can be measured over time.

A mechanism for ABA and nitrate control of root growth: Regulation of SCARECROW expression

Both ABA and nitrate modulate root growth, increasing or decreasing root elongation as well as controlling various stages of lateral root formation.4,8 How are nitrate and ABA able to dial root length up or down? What is the mechanism by which they control root growth? Both ABA and nitrate control both cell division and cell elongation within the root tip.14,15,52-54 How do they intersect with these cellular controls? The GRAS transcription factor, SCARECROW (SCR), controls the stem cell niche in the root, thereby controlling the root's ability to produce new cells and drive further growth. Accumulation of ABA and expression of SCR in the root tip are coincident,33 suggesting a possible regulatory connection between the 2. In fact, Cui and colleagues demonstrated that SCR represses expression of ABA INSENSITIVE 4 (ABI4) and ABI5 in the root apical meristem and that ABI4 expression levels control root growth, by controlling the number of cells in the root meristem.55 They found that both ABI4 levels that are higher or lower than normal decrease root elongation, indicating that ABI4 acts as a sensitive, root-control dial in Arabidopsis, allowing the plant to dial up or down root growth as conditions indicate.55

Interestingly, SHORTROOT (SHR), another GRAS-type transcription factor, thought to be the primary regulator of SCR expression, is not involved in the SCR-controlled root meristem expression of ABI4 and ABI5 and does not mediate the glucose signaling that these 3 genes function in, leaving the process that controls SCR expression in ABI4 regulation a mystery.55 We found that SCR expression is controlled by both ABA and nitrate (Fig. 2),33 raising the intriguing possibility that the transcription factor(s) that act upstream of SCR in ABI4 and ABI5 root meristem signaling are, in fact, components of the ABA/ NO3¯ signaling pathway. ABI4 and ABI5 expression have long been known to be induced by ABA,56-58 and nitrate modulation of root architecture requires the function of both ABI4 and ABI5, but not other ABI genes.16 Together, these observations suggest that SCR is an integral component of the ABA signaling network regulating root growth, and that ABI4 and ABI5 function downstream of nitrate in the control of root growth. Finally, the position of SCR squarely within the ABA signaling pathway indicates that ABA must stimulate expression of responsive genes ABI4 and ABI5 by inhibiting an inhibitor, SCR (Fig. 2).

Figure 2.

Figure 2.

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ABA and nitrate regulate SCARECROW (SCR) gene expression in the Arabidopsis root tip. (A) Exogenous ABA (10 μM) or KNO3 (10 mM) treatments reduce expression of the proSCR-erGFP reporter gene (indicated by green arrowheads), as compared with a control treatment of 10 mM KCl. Treatment with ABA and nitrate simultaneously result in a strong reduction of proSCR-erGFP expression and an increase in root hair growth close to the root tip.33 Roots are counterstained with propidium iodide (red). Confocal images from www.plantcell.org.33 Copyright American Society of Plant Biologists. (B) Diagram of the regulatory network involving ABA, NO3¯, SCR and root growth. Nitrate stimulates expression of the BG1 β-glucosidase, thus resulting in the release of bioactive ABA from the inactive ABA-glucose ester (ABA-GE) conjugate, and the repression of proSCR-erGFP. Because the effects of ABA and nitrate on proSCR-erGFP expression are additive, it may be that they function in parallel to regulate SCR expression, with NO3¯, regulating SCR expression separate from its action on BG1 and ABA accumulation. This second pathway is indicated with a dashed line, to indicate the lack of direct evidence to support it.

Conclusions and future prospects

The relationship between nitrate and ABA is starting to become clearer. Transporters and receptors have been identified, we now have the broad outline of an ABA-mediated negative feedback loop that restricts nitrate import and stimulates expression of nitrate metabolic enzymes, as well as a molecular mechanism integrating nitrate and ABA signaling with cell division via the SCR transcription factor. And yet, many questions remain unanswered. Response of nitrogen-starved roots to nitrate treatment differs from that of roots grown in the presence of fixed nitrogen. What happens to ABA during nitrate starvation and subsequent release? The response to excess nitrate is the other side of the coin. Excess nitrate signals through both the CHOTTO1 transcription factor as well as ABI4, indicating a central role for ABA.59,60 Does this response also involve repression of SCR? What happens to ABA accumulation following a stressful treatment of excess nitrate?

Finally, what happens to ABA accumulation and signaling during a localized nitrate treatment? Does ABA accumulate in the root tips exposed to nitrate? What happens on other parts of the root system not exposed to nitrate? Is ABA part of the signal that moves through the root system? Or does it respond in all root tips, as they receive a systemic signal reporting a localized nitrate patch?

The connections between nitrate and ABA are beginning to be untangled, but systems biology approaches reveal multiple layers of connections linking these 2 important regulators of the root system.61 Determining the location and timing of ABA accumulation during development of the root system is a key piece in this story.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.

Funding

Research in the Harris laboratory is funded by USDA Hatch grant VT-H02104

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