Journal of Experimental Botany, Vol. 62, No. 4, pp. 1399–1409, 2011
doi:10.1093/jxb/erq410 Advance Access publication 31 December, 2010
REVIEW PAPER
Hormonal control of nitrogen acquisition: roles of auxin,
abscisic acid, and cytokinin
Takatoshi Kiba, Toru Kudo, Mikiko Kojima and Hitoshi Sakakibara*
RIKEN Plant Science Center, 1-7-22 Suehiro, Tsurumi, Yokohama 230-0045, Japan
* To whom correspondence should be addressed. E-mail: [email protected]
Received 8 September 2010; Revised 4 November 2010; Accepted 19 November 2010
Abstract
Nitrogen is the mineral nutrient that often limits plant growth and development. In response to changes in nitrogen
supply, plants display elaborate responses at both physiological and morphological levels to adjust their growth and
development. Because higher plants consist of multiple organs with different functions and nutritional requirements,
they rely on local and long-distance signalling pathways to coordinate the responses at the whole-plant level.
Phytohormones have been considered as signalling substances of such pathways. Amongst phytohormones,
abscisic acid, auxin, and cytokinins have been closely linked to nitrogen signalling. Recent evidence has provided
some insights into how nitrogen and the phytohormone signals are integrated to bring about changes in physiology
and morphology. In this review, the evidence is summarized, mostly focusing on examples related to nitrogen
acquisition.
Key words: Abscisic acid, auxin, cytokinin, nitrate, nitrogen, NRT, phytohormone.
Introduction
Nitrogen, an essential macronutrient for plants, is absorbed
from the soil either in inorganic forms such as nitrate or
ammonium, or in organic forms, mostly as free amino
acids. In aerobic soils, nitrate is the major form, but its
availability can fluctuate dramatically both spatially and
temporally, depending on leaching and microbial activity
(Vance, 2001; Miller and Cramer, 2004). Therefore, plants
mount elaborate physiological and morphological responses
to balance the amount of nitrogen acquired from soil with
what is needed for growth and development. These
responses include regulation of uptake capacity (Gazzarrini
et al., 1999; Lejay et al., 1999; Gojon et al., 2009),
adjustment of shoot/root growth balance (Walch-Liu et al.,
2005), and changes in root architecture (Walch-Liu et al.,
2006; Zhang et al., 2007; Forde and Walch-Liu, 2009).
Because a higher plant body is made up of multiple organs
with different functions and nutritional requirements, these
responses must be coordinated at the whole-plant level, and
therefore both local and long-distance signalling are required for the communication of nutrient status between
organs. Nitrate, amino acids, sugars, and phytohormones
have been implicated in this signalling (Forde, 2002;
Oka-Kira and Kawaguchi, 2006; Sakakibara et al., 2006).
Phytohormones were originally defined as a group of
naturally occurring organic substances which influence
growth and development at low concentrations (Davies,
2004). In addition to their basic roles in growth and
development, phytohormones have been linked to various
aspects of environmental responses, such as light, temperature, salt, drought, pathogen, and nutrient responses. Recently, much progress has been made in our understanding
of how plants use phytohormones to integrate these
environmental signals with endogenous growth and developmental programmes (Zhu, 2002; Halliday et al., 2009;
Kazan and Manners, 2009; Patel and Franklin, 2009). It has
been proposed that abscisic acid (ABA), auxin, and
cytokinins (CKs) act to coordinate demand and acquisition
of nitrogen (Signora et al., 2001; Wilkinson and Davies,
2002; Walch-Liu et al., 2006; Argueso et al., 2009).
Regulation of nitrogen acquisition involves modulation
of nitrate uptake systems, and proliferation of lateral roots
(Zhang and Forde, 2000; Forde and Walch-Liu, 2009). In
ª The Author [2010]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
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1400 | Kiba et al.
general, nitrate uptake systems consist of low- and highaffinity nitrate transporters encoded by NRT1 and NRT2
family genes, respectively (Miller et al., 2007; Tsay et al.,
2007; Gojon et al., 2009). The expression of NRT genes is
regulated by numerous signals. For instance, AtNRT2.1,
which constitutes a major component of the high-affinity
nitrate transport system, is induced by nitrate and sugars,
and repressed by nitrogen assimilation products and CKs
(Filleur and Daniel-Vedele, 1999; Lejay et al., 1999; Zhuo
et al., 1999; Brenner et al., 2005). Lateral root outgrowth is
a complex developmental process regulated by various
signals, including nitrate, nitrogen assimilation products,
ABA, auxin, and CKs (reviewed in Forde, 2002; Walch-Liu
et al., 2006; Zhang et al., 2007; Fukaki and Tasaka, 2009).
Here, the roles of phytohormones in the regulation of
nitrate uptake systems and lateral root proliferation in
response to changes in nitrogen availability are discussed,
together with new data and recent progress.
Cytokinins
CKs are a class of phytohormones implicated in many
aspects of plant growth and development (Mok and Mok,
2001; Sakakibara, 2006), including nitrogen signalling.
A CK–nitrogen link has been indicated by findings that
nitrogen supply and CK content are closely correlated in
barley (Samuelson and Larsson, 1993), tobacco (Singh
et al., 1992), and Urtica dioica (Wagner and Beck, 1993),
and that exogenous treatment with CKs can partially
overcome growth-limiting effects caused by low nitrogen
supply in Plantago major (Kuiper, 1988). Nitrogen supplementation causes an increase in CK content in xylem sap
(also in roots and shoots) of maize (Takei et al., 2001),
indicating that CKs function as a root-to-shoot longdistance signal of nitrogen supplement (Sakakibara et al.,
2006). A similar association has been reported in Arabidopsis (Takei et al., 2004). Furthermore, it was detected that
Arabidopsis seedlings grown on high concentrations of
nitrate (HN, 10 mM) contain higher levels of CKs than
those grown on low nitrate (LN, 0.1 mM; Table 1, and
Supplementary Table S1 available at JXB online), implying
that CKs are not just a nitrogen supplement signal but
are also a nitrogen status signal. Recent evidence consistently indicates that CKs also act as a local signal or as
a shoot-to-root long-distance signal (Miyawaki et al., 2004;
Matsumoto-Kitano et al., 2008). Because the role of CKs as
a root-to-shoot long-distance signal has been well reviewed
(Sakakibara et al., 2006; Hirose et al., 2008; Kudo et al.,
2010), this section focuses mainly on CK function as a local
signal or as a shoot-to-root long-distance signal.
Regulation of CK biosynthesis by nitrogen
Until the identification of genes encoding adenosine phosphate-isopentenyltransferase (IPT), which catalyses the
initial step of CK biosynthesis, it was believed that CKs are
synthesized in roots (Letham, 1994). In Arabidopsis, IPT is
encoded by seven genes that are differentially expressed in
various tissues, indicating that CK production is not
confined to roots (Miyawaki et al., 2004; Takei et al.,
2004). Among these seven genes, AtIPT3 is nitrate inducible. Accumulation of CKs was greatly attenuated in an
atipt3 mutant, indicating that AtIPT3 is a key determinant
of nitrate-dependent CK biosynthesis (Miyawaki et al.,
2004; Takei et al., 2004). Interestingly, nitrate-inducible
expression of AtIPT3 was also observed in detached shoots
(Miyawaki et al., 2004). Similarly, nitrogen supplementation
induces CK accumulation in detached sunflower and
tobacco leaves (Salama and Wareing, 1979; Singh et al.,
1992). Microarray analyses have shown that the nitrateinducible expression of AtIPT3 is partly mediated by
NRT1.1/CHL1 (NRT1.1), a protein which functions as
a dual-affinity nitrate transporter and nitrate sensor (Liu
et al., 1999; Ho et al., 2009; Wang et al., 2009). AtIPT3 is
expressed in phloem throughout the plant (Miyawaki et al.,
Table 1. Auxin, ABA, and CK contentsa in shoots and roots of seedlings grown in HN and LNb
Phytohormones (pmol gFW 1)
Shoot
HN
c
tZ-type CK
iP-type CKd
IAAe
ABAf
a
17.1363.46
15.5960.51
23596149
8.1461.67
Root
LN
2.7860.56
5.5761.68
23276240
7.8362.21
dec***
dec***
g
HN
LN
45.7963.33
10.2760.8
34666936
16.2667.28
10.3861.59
6.6760.7
49116585
12.0462.37
dec***
dec***
inc*
Mean value from four replicate samples with SD.
Wild-type seedlings were grown on high nitrate plates (HN, 10 mM) or low nitrate plates (LN, 0.1 mM) for 3 d as described in the legend of
Fig. 2. Shoots and roots were harvested separately, and phytohormone analyses were conducted as described by Kojima et al. (2009). The full
list of phytohormonal compounds and the quantification results are provided in Supplementary Table S1 at JXB online.
c
Sum of trans-zeatin (tZ), tZ riboside (tZR), and tZR 5’-phosphates. See Supplementary Table S1 at JXB online for the quantification result of
each compound.
d
Sum of N6-(D2-isopentenyl)adenine (iP), iP riboside (iPR), and iPR 5’-phosphates. See Supplementary Table S1 at JXB online for the
quantification result of each compound.
e
Indole-3-acetic acid.
f
Abscisic acid.
g
Asterisks indicate that the contents of the compound were significantly increased (inc) or decreased (dec) in LN compared with HN
(*P <0.05, ***P <0.001, Student’s t-test).
b
Phytohormones and nitrogen acquisition | 1401
2004; Takei et al., 2004), and this expression pattern
overlaps with that of NRT1.1 in roots (Guo et al., 2001).
However, in shoots, NRT1.1 expression is detected only in
young leaves (Guo et al., 2001). Therefore, whether or not
NRT1.1 mediates nitrate-inducible AtIPT3 expression in
shoots is an open question. Given that AtIPT3 is expressed
in phloem, it is likely that CKs synthesized by AtIPT3 in
shoots function as a shoot-to-root long-distance signal of
shoot nitrate availability. In this context, it has been
shown that xylem sap predominantly contains trans-zeatin
(tZ)-type CKs, and phloem sap mostly contains N6-(D2isopentenyl)adenine (iP)-type and cis-zeatin (cZ)-type CKs
(Hirose et al., 2008). Thus, either the iP- or cZ-type CKs, or
possibly both, could be the shoot-to-root long-distance
signal in Arabidopsis. Grafting experiments using a higher
order atipt mutant (atipt1;3;5;7) have provided unequivocal
evidence that iP-type CKs are translocated from the shoot
to the root (Matsumoto-Kitano et al., 2008). The
atipt1;3;5;7 mutant is characterized by extremely low iPand tZ-type cytokinin levels, retarded shoot growth, and
enhanced lateral root outgrowth. When a wild-type shoot
was grafted onto the atipt1;3;5;7 mutant root, the normal
growth phenotype and levels of iP-type CKs were restored
in the mutant root, indicating that iP-type CKs translocated
from the shoot are biologically functional (MatsumotoKitano et al., 2008). Notably, the expression of AtIPT3 is
also regulated by iron, phosphate, and sulphate availability,
both in shoots and in roots (Hirose et al., 2008; Seguela
et al., 2008). It could be that AtIPT3 functions as an
integrator of nutrient availability signals.
Regulation of nitrogen uptake by CKs
CKs produced locally within the root, or translocated from
the shoot may signal that there is sufficient nitrogen present.
In this regard, one of the proposed roles of CKs is negative
regulation of nitrogen uptake-related genes. Microarray
analyses have shown that exogenous application of CK
represses two AtNRT2 genes (AtNRT2.1 and AtNRT2.3),
three ammonium transporter genes, three amino acid transporter genes, and a urea transporter gene in Arabidopsis
(Fig. 1; Brenner et al., 2005; Kiba et al., 2005; Sakakibara
et al., 2006; Yokoyama et al., 2007). Because the expression
levels of AtNRT1 and AtNRT2 correlate well with low- and
high-affinity nitrate transport activity, respectively (Forde,
2000; Okamoto et al., 2003), it is conceivable that CK
repression of the AtNRT genes results in a reduction in
nitrate uptake activity. To form a more complete picture of
CK regulation, the effect of CKs, along with other
phytohormones, on each of the AtNRT genes (AtNRT2.1–
AtNRT2.7, AtNRT1.1–AtNRT1.7, and AtNAR2.1) was
analysed by quantitative PCR (qPCR). Under the experimental conditions used, it was found that CKs repress all
the root-type AtNRT genes (R/L ratio in log2 >1; Fig. 2).
Fig. 1. The effect of phytohormones on the expression of nitrogen uptake-related genes in Arabidopsis. Microarray data were obtained
from the Gene Expression Omnibus (GEO; http://www.ncbi.nlm.nih.gov/), and fold change values were calculated between
phytohormone-treated and control data. Microarray data for abscisic acid (GSE7112), auxin (GSE1110), brassinosteroid (GSE862),
cytokinins (GSE5698, GSE1766, and GSE20232), ethylene (GSE5174), gibberellin (GSE20223), and jasmonic acid (GSE21762)
treatment were analysed. Among nitrogen uptake-related genes listed in Supplementary Table S3 at JXB online, genes with a >2-fold
difference with statistical significance (P <0.05) are presented. Up-regulated (fold change >2) genes and down-regulated (fold change
<0.5) genes are indicated with ‘U’ in orange cells and ‘D’ in blue cells, respectively. The Arabidopsis ATH1 Genome Array is unable to
distinguish AtAMT1;3 from AtAMT1;5 (indicated by an asterisk). Numbers in parentheses indicate GEO data sets: 1, GSE5698 (Kiba
et al., 2005); 2, GSE1766 (Brenner et al., 2005); 3, GSE20232 (Yokoyama et al., 2007); 4, GSE1110 (Redman et al., 2004); 5, GSE3350
(Vanneste et al., 2005); 6, GSE863 (Nemhauser et al., 2004); 7, GSE5174 (Olmedo et al., 2006).
1402 | Kiba et al.
Fig. 2. The effect of phytohormones on the expression profiles of AtNRT genes in roots. (A) Transcript level of each AtNRT in
phytohormone-treated seedling roots grown on high nitrate plates (HN, 10 mM) relative to that in non-treated seedlings. (B) Transcript
level of each AtNRT in phytohormone-treated seedling roots grown on low nitrate plates (LN, 0.1 mM) relative to that in non-treated
seedlings. Wild-type seedlings were grown vertically on HN plates (modified from Fujiwara et al., 1992) for 8 d under the following
conditions: 12 h light/12 h dark cycles (80 m 2 s 1) at 22 C. Then, the seedlings were treated with 10 6 M phytohormones for 3 d on
HN or LN plates. Roots were harvested and the expression pattern of each AtNRT gene was analysed by qPCR using specific primer
sets (Supplementary Table S2 at JXB online). A root/shoot expression ratio (R/L ratio) was calculated using the expression level of each
gene in shoots and roots of non-treated seedlings grown under HN or LN conditions. Based on the R/L ratio, all AtNRT genes were
grouped into four categories: root-type genes (R/L ratio in log2 >1), shoot-type genes (R/L ratio in log2 < –1), whole plant-type genes (R/L
ratio in log2 between –1 and 1), and genes that were not detected in roots. Plant hormones tested were trans-zeatin (tZ), indole-3-acetic
acid (IAA), abscisic acid (ABA), gibberellin 3 (GA), 1-amino-1-cyclopropane-carboxylic acid (ACC), brassinolide (BL), salicylic acid (SA),
and jasmonic acid (JA). Each experiment was performed twice and mean values are shown on a log2 scale. Asterisks indicate that the
values are of no statistical significance because the expression level in one of the samples was below the detection limit. A colour code is
used to visualize data, and samples that were expressed below the detection limit are shown in grey (ND).
The repression was observed under both HN (Fig. 2A) and
LN conditions (Fig. 2B), indicating that the CK effect is
independent of the nitrogen status of plants. On the other
hand, no such consistent repression was observed with other
phytohormones, implying that the effect is CK specific (Fig. 2).
Amongst the root-type genes, AtNRT2.1, AtNRT2.2,
AtNRT1.1, and AtNRT1.5 have been characterized and
shown to act as major components of the nitrate uptake
and xylem loading system (Liu et al., 1999; Orsel et al.,
2004; Li et al., 2007; Lin et al., 2008). These results support
Phytohormones and nitrogen acquisition | 1403
Relative amount of RNA
(A)
1.2
AtNRT2.4
1.5
1
1
0.9
0.6
0.6
0.4
0.4
0.6
0.2
0.2
0.3
(B)
4
Relative amount of RNA
3.5
DMSO 10
-9
10
-8
10
-7
10
-6
10
-5
AtNRT2.7
0
8
DMSO 10
-9
10
-8
10
-7
10
-6
10
0
-5
DMSO 10
12
AtNRT1.3
10
3
2
2
2
10
-7
10
-6
10
-5
AtNRT1.7
2
0.5
(C)
-8
4
1
0
10
6
4
1.5
-9
8
6
2.5
AtNRT1.5
1.2
0.8
0.8
0
Relative amount of RNA
1.2
AtNRT2.1
DMSO 10
-9
10
-8
10
-7
10
-6
10
-5
0
10
AtNRT1.2
DMSO 10
-9
10
-8
10
-7
10
-6
10
-5
DMSO 10
-9
10
-8
10
-7
10
-6
10
-5
trans-zeatin conc. (M)
ARR7
Col.
8
1.5
0
ahk3-3 cre1-12
arr3,4,5,6,8,9
6
1
4
0.5
2
0
DMSO 10
-9
10
-8
10
-7
10
-6
10
trans-zeatin conc. (M)
-5
0
DMSO 10
-9
10
-8
10
-7
10
-6
10
-5
trans-zeatin conc. (M)
Fig. 3. CKs mediate both induction and repression of AtNRT genes via AHK4/CRE1/WOL- and/or AHK3-dependent His–Asp
phosphorelay. Dose-dependent effect of CK on (A) CK-repressive AtNRT genes, (B) CK-inducible AtNRT genes, and (C) control genes in
wild-type, cre1-12 ahk3-3, and arr3,4,5,6,8,9 roots. Seedlings were grown for 8 d on HN plates, and then treated on LN plates
supplemented with trans-zeatin for 3 d, as indicated. Roots were harvested and transcript levels were determined by qPCR using
specific primer sets (Supplemetary Table S1 at JXB online). All quantifications were standardized with AtACT8 transcript levels as an
internal standard. Relative values indicate comparison with the transcript level of dimethylsulphoxide (DMSO)-treated roots. Error bars
represent standard deviations of three technical replicates. The experiment was performed twice with similar results.
the hypothesis that CKs act as a satiety signal of nitrogen to
inhibit nitrate uptake in the root. Similarly, it has been
reported that CKs negatively regulate other nutrient
acquisition-related genes in Arabidopsis, such as highaffinity phosphate transporter genes (Pht1;2 and Pht1;4;
Martin et al., 2000; Sakakibara et al., 2006), high-affinity
sulphate transporter genes (SULTR1;2 and SULTR1;4;
Maruyama-Nakashita et al., 2004), and iron deprivation-
inducible genes (IRT1, FRO2, and FIT; Seguela et al.,
2008). Similar regulation was also reported in rice (Hirose
et al., 2007), indicating that CK regulation of nutrient
acquisition-related genes is a common mechanism in both
dicots and monocots. In Arabidopsis, these repression
effects have been shown to depend on the CK receptors
AHK4/CRE1/WOL (CRE1) and/or AHK3, suggesting the
involvement of CK signal transduction mediated by
1404 | Kiba et al.
the His–Asp phosphorelay (Franco-Zorrilla et al., 2002;
Maruyama-Nakashita et al., 2004; Seguela et al., 2008). As
expected, any CK effect on the AtNRT genes is also
dependent on the canonical CK signal transduction system
(Fig. 3). The cre1 ahk3 double mutant (Higuchi et al., 2004)
showed reduced sensitivity in the CK repression (Fig. 3A)
and CK induction (Fig. 3B) of AtNRT genes. In contrast,
the hextuple mutant (arr3,4,5,6,8,9; To et al., 2004) of
negative regulators of the CK signalling system displayed
hypersensitivity (Fig. 3A, B). It has been reported that CKrepressive nutrient acquisition-related genes are largely
expressed in root epidermal or cortical cells. Thus, it is
possible that CKs specifically target those cell types. In the
case of iron starvation-inducible genes, CKs repress IRT1,
FRO2, and FIT, all of which are expressed in epidermal
cells. In contrast, vascular tissue-expressed AtNRAMP3 and
AtNRAMP4 are not affected by CKs (Seguela et al., 2008),
supporting the idea that the site of CK action is epidermal
or cortical. However, this assumption may be an oversimplification, because it was found that AtNRT1.5, which
is expressed in pericycle cells, is repressed by CKs (Fig. 3A;
Lin et al., 2008), whereas epidermal cell-expressed
AtNRT1.2 is not (Fig. 3C; Huang et al., 1999).
Besides this negative effect, CKs also have a positive
regulatory effect on some AtNRT genes. It was found that
most shoot-expressed AtNRTs (R/L ratio in log2 less than –1;
Fig. 2) are up-regulated by CKs under both HN and LN
conditions (Fig. 2). Recent studies have assigned physiological functions to the shoot-type genes AtNRT2.7,
AtNRT1.4, and AtNRT1.7 in aerial organs (Chiu et al.,
2004; Chopin et al., 2007; Fan et al., 2009). Considering the
evidence that transcript abundance of these shoot-type
genes in roots is much lower than that of root-type genes
(data not shown), it is unlikely that shoot-type AtNRT
genes play a major role in nitrate uptake. Although
clarification of the function of shoot-type AtNRT genes in
roots awaits further analysis, a plausible explanation is that
shoot-type AtNRT genes are similarly induced in shoots by
CKs and enhance nitrate distribution and translocation.
A possible role for CKs in the regulation of root
architecture in response to nitrogen
CKs also have a regulatory role in root architecture
development. Many reports describe the inhibitory effects
of exogenous CKs on lateral root formation (Wightman
et al., 1980; Laplaze et al., 2007). In contrast, mutants and
transgenic plants with reduced CK levels, such as higher
order atipt mutants (Miyawaki et al., 2006) and transgenic
plants overexpressing the gene encoding the CK-degrading
enzyme CKX (Werner et al., 2003), or decreased CK
sensitivity, such as the higher order signalling mutants ahk
(Higuchi et al., 2004), exhibit enhanced root growth and
branching. CKs act at both initiation and organization of
the lateral root primordium (LRP), most probably through
perturbation of the auxin gradient, to inhibit LRP formation (Laplaze et al., 2007). In general, a uniformly high
nitrogen supply suppresses root branching, while nitrogen
limitation accelerates root growth and root branching
(Linkohr et al., 2002; Tranbarger et al., 2003). Given that
nitrogen status and CK content are closely correlated
(Table 1, and Supplementary Table S1 at JXB online), it is
very likely that CKs have a role in regulating root
architecture in response to nitrogen availability. However,
there is as yet no solid evidence to support this. Now that
a number of CK signalling and biosynthesis mutants are
available, questions about the CK regulation of root
architecture development can be answered.
Abscisic acid
ABA is generally known as a stress hormone involved in
abiotic and biotic stress responses. Although there is
considerable evidence linking ABA levels and nitrogen
status in several plant species (Radin et al., 1982; Peuke
et al., 1994; Brewitz et al., 1995; Wilkinson and Davies,
2002), there is not necessarily a consistent correlation
between the two. For example, in Arabidopsis, there is no
statistically significant difference in ABA contents between
seedlings grown under the HN and LN conditions used here
(Table 1, and Supplementary Table S1 at JXB online).
Thus, whether changes in ABA content are relevant to
nitrogen signalling is still unclear, but involvement of ABA
in nitrogen signalling is becoming increasingly evident.
Several reports provide genetic evidence for the involvement of ABA in lateral root development in response to
high nitrate supply in Arabidopsis. Signora et al. (2001)
clearly showed that ABA-insensitive mutants (abi4-1, abi42, and abi5-1) and ABA-deficient mutants (aba1-1, aba2-3,
aba2-4, and aba3-2) are less sensitive to the inhibitory
effects of high nitrate. A set of mutants identified based on
their ability to produce lateral roots in the presence of ABA
(labi mutants) shows reduced sensitivity to the inhibitory
effects of high nitrate (Zhang et al., 2007). Identification of
the labi genes would provide a breakthrough toward
understanding the mechanisms underlying this inhibition
effect. A recent study in a Medicago truncatula latd mutant
provides another line of evidence for a link between ABA
and nitrogen signalling (Yendrek et al., 2010). The latd
mutant is characterized by severe defects in root meristem
maintenance and root growth, which is rescued by exogenous ABA application (Bright et al., 2005; Liang et al.,
2007). Interestingly, the primary root growth of the latd
mutant is insensitive to nitrate, and the LATD gene encodes
a transporter belonging to the NRT1 (PTR) family
(Yendrek et al., 2010). However, whether LATD acts as
a nitrate transporter/sensor remains to be shown.
Auxin
Auxin has long been a candidate for mediating nitrogen
signals from shoot to root because auxin is transported
basipetally, and enhances lateral root initiation and development (Forde, 2002; Fukaki and Tasaka, 2009). Auxin
contents in phloem sap and roots are lower in maize
Phytohormones and nitrogen acquisition | 1405
supplied with high doses of nitrate, and this reduction is
correlated with reduced root growth (Tian et al., 2008).
Similarly, transfer from high nitrate media to low nitrate
media has been shown to increase auxin contents in roots,
which is followed by lateral root outgrowth in Arabidopsis
(Walch-Liu et al., 2006). Furthermore, it has been confirmed that Arabidopsis seedlings grown in LN conditions
contain higher levels of root auxin than seedlings grown in
HN conditions (Table 1, and Supplementary Table S1 at
JXB online), indicating that dicots and monocots share
a common system to regulate auxin levels in the root
depending on the nitrogen status of the plant. However, it
was also reported that the inhibitory effect of high nitrate
on lateral root growth is not alleviated by exogenous
application of auxin, indicating that the auxin content is
not the only factor regulating lateral root development
(Zhang et al., 2007).
Recent progress in understanding auxin action indicates
that, in addition to auxin levels in the tissue, a concentration
gradient and the differential sensitivity of various cell types
are the driving force of auxin-regulated growth and development (Overvoorde et al., 2010; Zazimalova et al.,
2010). The auxin gradient is established by cell-to-cell polar
transport, and differential sensitivity is accomplished by
modulation of signalling components (Overvoorde et al.,
2010; Zazimalova et al., 2010). Several lines of recent
evidence suggest that nitrogen signalling is mediated by
these same, or similar mechanisms (Gifford et al., 2008;
Krouk et al., 2010; Vidal et al., 2010). Using a cell sorting
technique, Gifford et al. (2008) identified a nitrogen-in
ducible Auxin Response Factor (ARF8) which is expressed
in pericycle cells, and whose transcript level is repressed
by microRNA167a (miR167a). Although transcription of
ARF8 is not regulated by nitrogen, miR167a levels are
under the control of glutamine or some downstream
metabolite (Gifford et al., 2008). Hence, in the presence of
glutamine or a downstream metabolite, miR167a levels in
pericycle cells are down-regulated, thus permitting ARF8
transcript to accumulate in the cell. The arf8 mutant and
MIR167a-overexpressing seedlings fail to respond to nitrogen treatment by increasing the ratio of initiating/emerging
lateral roots, providing genetic evidence that the nitrogen
signal regulates auxin signalling through the action of
miR167a to control lateral root initiation (Gifford et al.,
2008). Recently, the auxin receptor gene AFB3 was found to
be nitrate inducible (Vidal et al., 2010). The induction was
also observed in a nitrate reductase (NR)-null mutant,
suggesting that it is triggered by nitrate itself. Analysis of
the afb3 mutant revealed that the mutant is insensitive to
nitrate in the regulation of primary root growth and lateral
root density, indicating that nitrate signal regulates root
architecture through AFB3, possibly by modulating auxin
signalling (Vidal et al., 2010). Surprisingly, Krouk et al.
(2010) provided another link between nitrate and auxin by
showing that NRT1.1/CHL1, which is known as a dualaffinity nitrate transporter and nitrate sensor (Liu et al.,
1999; Ho et al., 2009), also facilitates cell-to-cell auxin
transport. Detailed analyses of an nrt1.1 (chl1) mutant
revealed that chl1 accumulates auxin in lateral root
primordia, which led the authors to hypothesize that
NRT1.1 transports auxin. Data obtained from transport
assays in heterologous systems and in planta were consistent
with this hypothesis. Furthermore, nitrate was shown to be
an inhibitor of the auxin transport activity (Krouk et al.,
2010). Localization studies demonstrated that NRT1.1 is
present within the anticlinal membranes of the outermost
cell layer of lateral roots, indicating that NRT1.1 facilitates
auxin movement out of the root tip. Thus, apparently under
low nitrate conditions, NRT1.1 prevents auxin accumulation in the root tip, resulting in inhibition of lateral root
growth. In contrast, under high nitrate conditions the auxin
transport activity of NRT1.1 is inhibited by nitrate,
resulting in an accumulation of auxin within the root tip,
leading to lateral root outgrowth (Krouk et al., 2010).
Conclusions and perspectives
It has long been proposed that there is an interaction
between nitrogen signalling and phytohormone activity.
Recent genetic studies have provided compelling evidence
Fig. 4. Schematic representation of the interaction between
nitrogen and phytohormones (abscisic acid, auxin, and cytokinin)
in the regulation of nitrogen acquisition. Abscisic acid (ABA), auxin
(AUX), and cytokinin (CK) produced locally, or translocated from
shoots, regulate nitrogen (N) acquisition events. N availability
and/or nitrate (NO–3) signal interacts with CK biosynthesis (AtIPT3),
cell-to-cell auxin transport (NRT1.1), auxin perception (AFB3), and
auxin signal transduction (ARF8/miR167a) to regulate N acquisition. NRT1.1/CHL1 has dual activity, namely as an AUX transporter
and NO–3 sensor. Arrows and blunted lines designate positive and
inhibitory interactions, respectively. Solid lines represent defined
interactions; dashed lines indicate presumed interactions.
1406 | Kiba et al.
that ABA, auxin, and CKs are involved in nitrogen signalling (Fig. 4). In addition, it was found that brassinosteroid
(BR) up-regulates a large number of AtNRT genes (Fig. 2).
Although it has been reported that there is a shared
signalling pathway for BR and auxin (Goda et al., 2004;
Nemhauser et al., 2004), auxin or other phytohormones did
not induce AtNRT genes in any way similar to BR,
implying that the effect is BR specific. Because BR
promotes lateral root growth and development (Mori
et al., 2002; Bao et al., 2004), it is tempting to speculate
that BR enhances nitrogen acquisition, in opposition to
CK action. However, both the mechanism and physiological relevance of this regulation remain to be elucidated.
Given the apparent involvement of multiple phytohormones
in nitrogen signalling, one future challenge will be to
understand how phytohormones interact to convey the
nitrogen signal.
A growing body of evidence shows that phytohormones
interact not only with nitrogen but also with other nutrients.
For instance, CKs interact with iron (Seguela et al., 2008),
sulphur (Maruyama-Nakashita et al., 2004), and phosphorus
signalling (Wagner and Beck, 1993; Franco-Zorrilla et al.,
2002), and auxin interacts with phosphorus signalling (Nacry
et al., 2005), indicating that phytohormones are not the
specific (direct) signal of a certain nutrient itself. Rather, they
might be the translated (indirect) signals to coordinate
growth and development with nutritional status within an
organ and/or between organs, and act concurrently with the
other nutrient-specific signals to trigger a response characteristic to each nutrient. Although this is an intriguing
hypothesis, many questions remain to be answered. How is
the nutritional status sensed and translated into phytohormone signals? In which cell, tissue, or organ does the sensing
and translation occur? What is the nature of the nutrientspecific signal? How are the phytohormone and nutrientspecific signals transported to target sites? Where and how
are the phytohormone signal and nutrient-specific signal
perceived, and integrated to bring about a characteristic
response to each nutrient? Now that classic biochemical,
physiological, and genetic approaches can be combined with
state-of-the-art ‘omics’ (e.g. highly sensitive and highthroughput phytohormonome analysis; Kojima et al., 2009)
and systems approaches, it will not take long until the
answers to these questions are known.
Supplementary data
Supplementary data are available at JXB online.
Table S1. Auxin, ABA, and CK contents in shoots and
roots of seedlings grown in HN and LN.
Table S2. Primers used for quantitative PCR.
Table S3. A list of nitrogen uptake-related genes in
Arabidopsis.
Acknowledgements
We would like to thank Dr T. Kakimoto for cre1-12 ahk3-3,
and Dr J. J. Kieber for arr3,4,5,6,8,9 mutant seeds.
Research in our laboratory is supported by the Ministry of
Education, Culture, Sports, Science, and Technology and
the Ministry of Agriculture, Forestry and Fisheries, Japan.
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