Izumi Aibara1 and Kyoko Miwa1,2,*
1
Graduate School of Environmental Science, Hokkaido University Sapporo, 060-0810 Japan
PRESTO, JST Kawaguchi, 332-0012 Japan
2
*Corresponding author: E-mail, [email protected]; Fax, +81-11-706-9272.
(Received September 7, 2014; Accepted October 24, 2014)
How do sessile plants cope with irregularities in soil nutrient
availability? The uptake of essential minerals from the soil
influences plant growth and development. However, most
environments do not provide sufficient nutrients; rather nutrient distribution in the soil can be uneven and change
temporally according to environmental factors. To maintain
mineral nutrient homeostasis in their tissues, plants have
evolved sophisticated systems for coping with spatial and
temporal variability in soil nutrient concentrations.
Among these are mechanisms for modulating root system
architecture in response to nutrient availability. This review
discusses recent advances in knowledge of the two important strategies for optimizing nutrient uptake and translocation in plants: root architecture modification and
transporter expression control in response to nutrient availability. Recent studies have determined (i) nutrient-specific
root patterns; (ii) their physiological consequences; and (iii)
the molecular mechanisms underlying these modulation systems that operate to facilitate efficient nutrient acquisition.
Another mechanism employed by plants in nutrient-heterogeneous soils involves modification of nutrient transport
activities in a nutrient concentration-dependent manner.
In recent years, considerable progress has been made in
characterizing the diverse functions of transporters for
specific nutrients; it is now clear that the expression and
activities of nutrient transporters are finely regulated in
multiple steps at both the transcriptional and post-transcriptional levels for adaptation to a wide range of nutrient
conditions.
Keywords: Arabidopsis thaliana Essential element Gene
expression Nutrient-dependent Root architecture Transporter.
Abbreviations: bHLH, basic helix–loop–helix; bZIP, basic
leucine zipper; B, boron; Ca, calcium; Cl, chloride; Cu,
copper; Fe, iron; K, potassium; LR, lateral root; Mg,
magnesium; Mn, manganese; Mo, molybdenum; N, nitrogen;
Ni, nickel; P, phosphorus; PR, primary root; S, sulfur; UTR,
untranslated region; ZIF2, Zinc-induced Facilitator; Zn, zinc.
Introduction: Spatial and Temporal Changes
in Nutrient Availability
Minerals are major determinants of plant growth and fertility in
nature and agriculture. Plants require 17 essential elements to
complete their life cycle; depletion of these elements causes
various disorders of growth and development. Plants take up
14 of the 17 elements from the soil: nitrogen (N), phosphorus
(P), potassium (K), sulfur (S), calcium (Ca), magnesium (Mg),
iron (Fe), manganese (Mn), copper (Cu), zinc (Zn), molybdenum (Mo), boron (B), chloride (Cl) and nickel (Ni)
(Marschner 2011).
Plants can take up these minerals only as soluble forms, such
as ions in soil solutions. Nutrient solubility depends on the
chemical form of each nutrient, which is affected by environmental factors, including water content, pH, redox potential,
abundance of organic matter, and microorganisms in soils
(Marschner 2011). Since local soil environments are heterogeneous and change readily, soil nutrient availability is highly variable and often limited. In addition, nutrient mobility in soils is
influenced by their chemical form and environmental factors.
The accessibility of nutrients with limited mobility, including P
and Fe, in soil is restricted to roots near the location of the
nutrient. The mobility of those elements which are relatively
mobile in soil depends on the water conditions. These differences, including soil nutrient mobility, result in different spatial
distributions (Jobbagy and Jackson 2001). Therefore, plants
must cope with the uneven spatial distributions and temporal
changes of nutrients to optimize nutrient acquisition throughout their life cycle.
One useful strategy for efficient nutrient uptake is modulation of the root system architecture according to the nutrient
conditions. Nutrient concentrations affect the length, number,
angle and diameters of the primary roots (PRs) and lateral roots
(LRs), and root hair development. These developmental
changes result in nutrient-dependent root system patterns.
For example, under P starvation, PR elongation is inhibited,
while LR formation is enhanced concomitantly (Williamson
et al. 2001, Lopez-Bucio et al. 2002), resulting in the formation
of a shallow root morphology and increased root
Plant Cell Physiol. 55(12): 2027–2036 (2014) doi:10.1093/pcp/pcu156, Advance Access publication on 6 November 2014,
available online at www.pcp.oxfordjournals.org
! The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
All rights reserved. For permissions, please email: [email protected]
Mini Review
Strategies for Optimization of Mineral Nutrient Transport
in Plants: Multilevel Regulation of Nutrient-Dependent
Dynamics of Root Architecture and Transporter Activity
I. Aibara and K. Miwa | Regulation of mineral nutrient transport
surface area. Phosphate tends to accumulate in the topsoil layer
(as it readily binds to soil organic matter) where it is
immobilized (Jobbagy and Jackson 2001). Thus, below-ground
morphological responses of plants to P starvation probably
contribute to efficient acquisition of phosphate by exposing a
large root surface area to P. In contrast, for water-soluble nutrients such as nitrate and sulfate, which are readily leached to
deeper soil layers, root development towards lower layers is
preferred.
Another major strategy is modulation of transport activity
within and among plant organs. Nutrient transporters regulate
nutrient uptake into root cells and subsequent translocation
within the plant body. Transport molecules for each essential
nutrient have been identified in Arabidopsis thaliana.
Increasing evidence indicates that plants have evolved diverse
transporters with distinct substrate specificities, transport affinities, cell type expression and subcellular localization to ensure
appropriate flux and compartmentalization of each transport
process within the plant body/cell. Many examples of the nutrient-dependent regulation of transporter expression are available. Nutrient conditions strictly regulate transporter gene
expression at both the transcriptional and post-transcriptional
levels. Transporters also undergo post-translational modification to control transport activities. This regulation at multiple
steps benefits nutrient homeostasis under a wide range of nutrient conditions.
This article reviews recent advances in two important
aspects of plant adaptation to nutrient conditions: the
nutrient-dependent dynamics of root system architecture
and transporter expression for efficient nutrient uptake and
homeostasis (Fig. 1). In our examination of root system architecture, we provide (i) a comprehensive analysis of root
morphology; (ii) its physiological significance; and (iii) the
molecular mechanisms involved in root system structural
responses to shifting environmental conditions. Regarding
transporters, we emphasize the diverse physiological functions
and the control of transporter expression at multiple steps.
Nutrient-Dependent Root Architecture
Dynamics of root morphology
Soil nutrient conditions affect overall root architecture and
local root architecture. Since nutrient availability is highly variable at a coarse scale, even in the same habitat, modulation of
whole root systems is among the strategies used by individual
plants responding to their immediate nutrient environments
during post-embryonic development. Furthermore, each root
encounters patchy distributions of nutrients; plants are able to
alter root morphology at millimeter scales in response to finescale variability in nutrient availability, thereby improving the
efficiency of acquisition. We focus here on two recent reports
describing changes in whole root architecture when nutrients
are in short supply.
Changes in whole root architecture in response to P and N
conditions have been well characterized. However, the effects of
other nutrients on root architecture have not been reported or
2028
described. Gruber et al. (2013) recently reported the profiles of
root system architecture in A. thaliana grown under nine
macro- and micronutrient deficiencies (P, N, Ca, K, Mg, S, Fe,
Mn and B). They determined the optimal gelling agent to
induce deficiency in each nutrient, due to contamination of
essential elements in gelling agents. Then, plants were grown
in solid medium containing stepwise nutrient concentration
gradients. Seven root traits were measured: PR length, firstorder LR number, first-order LR length, second-order LR
number, second-order LR length, length of the PR branching
zone and length of the first-order LR branching zone. Based on
principal component analysis of these parameters, a root plasticity chart was constructed. There were some similarities in the
patterns of root architecture among several elements; however,
each of the elements had unique effects, indicating that root
architecture changes in a nutrient-specific manner. It is not yet
clear how these architectural changes benefit the plants in
terms of soil nutrient acquisition; however, this study provided
a global and comparative view of the architectural modification
of roots induced by deficiencies of single nutrients.
In natural soil environments, deficiencies in multiple nutrients can occur simultaneously and in various combinations.
Although the effects of multiple nutrient disorders on root
architecture have hardly been addressed due to the complexity
of the problem, Kellermeier et al. (2014) recently characterized
the root system architecture induced in A. thaliana by deficiencies of combinations of macronutrients. They grew plants
under 16 nutrient conditions, comprising combinations of N
(in the form of nitrate), P, K and S sufficiency/deficiency. In
addition, plants were grown under two photoperiods (9 and
16 h per day) to determine the influence of carbon status on
root architectural responses to nutrients. Thirteen root system
architecture parameters were measured, including the path
lengths of the basal and branched zones, angle of PRs and the
sum of path lengths of LRs. The statistical analysis indicated
that combinations of nutrient deficiencies could prioritize or
enhance the effects of single deficiencies and induce a new root
system architecture that could not be explained by the effects
of deficiencies in a single nutrient. This work demonstrated that
plants are able to integrate multiple sources of information on
environmental conditions and adjust their root plasticity responses appropriately.
Physiological significance of root system changes
Nutrient-dependent shifts in root architecture are considered
important for optimizing nutrient uptake. These shifts correspond to specific patterns in the distribution and mobility of
each soil nutrient. This premise has been explored through
experimental and theoretical investigations of the physiological
consequences of changes in root morphology.
The effects of root architecture on nutrient uptake and subsequent plant growth have been examined experimentally by
comparing genotypes with different root architecture phenotypes. Two genotypes of the common bean (Phaseolus vulgaris
L.) with shallow vs. deep root phenotypes were grown together
in a field where competition for phosphate acquisition was
likely. The shoot biomass developed by the shallow root
Plant Cell Physiol. 55(12): 2027–2036 (2014) doi:10.1093/pcp/pcu156
(1) Primary root
- Length
- Angle
(2) Lateral root
- Length
- Number
- Density
- Angle
- Diameter
(3) Root hair
- Length
- Density
(2) mRNA stability
(5) Protein
(6) Protein
P
Fig. 1 Schematic model of two major strategies for optimizing essential nutrient transport when nutrient conditions shift spatially and
temporally: regulation of (i) root system architecture and (ii) activities of nutrient transporters in response to nutrient availability. Strategy
(i) involves modulation of root system architecture (comprising primary roots, lateral roots and root hairs) in response to nutrient conditions.
Typical root traits are indicated in the schematic. Changes in these root traits create nutrient-specific root morphology patterns that correspond
to different distributions and mobilities of the diverse nutrients in soil. Strategy (ii) involves regulation of the expression and activity of
transporters at multiple steps at both the transcriptional and post-transcriptional levels. The regulation steps involved in responses to nutrient
availabilities are indicated in the schematic. Transporters are responsible for selective transport of the nutrients; quantitative and qualitative
regulation of transporters is important for maintaining nutrient homeostasis under a wide range of nutrient conditions. Different brown tones
indicate different nutrient conditions in the soil.
genotype was about double that of the deep root genotype
(Rubio et al. 2003), an outcome consistent with a view that
shallow roots are beneficial for efficient acquisition of phosphate accumulated in the topsoil layer. In contrast, when
both genotypes were grown in hydroponic culture, the biomass
of the two genotypes did not differ significantly, suggesting that
root architecture was important in soil but not in artificial
hydroponic culture. In addition to heterogeneous nutrient distribution in soil, the effects of physical stimuli on roots should
also be considered.
In combination with empirical data, mathematical modeling
has contributed to better understanding of the physiological
significance of root system changes in adaptive responses to
different nutrition conditions. The formation of a shallow root
system under P deficiency has been analyzed extensively. The
simulation by Ge et al. (2000) supports the view that forming a
shallow root system is advantageous for P acquisition. The
simulation was performed with SimRoot, a mathematical
model of root systems based on empirical growth parameters
of common beans (Lynch et al. 1997). This model predicted
that a shallow root system would obtain 34% more P than a
deep root system (Ge et al. 2000). More recently, a field-scale
mathematical model of wheat (based on the root system model
described by Roose et al. 2001) showed that P uptake is elevated
by 142% when root branching in the topsoil is increased
(Heppell et al. 2014). We believe that such modeling studies
when combined with empirical data will enhance understanding of the regulatory network responses to spatial and temporal
2029
I. Aibara and K. Miwa | Regulation of mineral nutrient transport
changes in nutrient availability. Further evaluations of physiological consequences will require determinations of the dynamics and distribution patterns of mineral nutrients in soil.
Molecular mechanisms underlying root
morphology
Molecular genetic studies of A. thaliana have identified and
characterized several genes involved in nutrient-dependent
root architecture changes, particularly the root architecture
responses to nitrate deficiency. The nitrate transporter
NRT1.1, also characterized as a nitrate sensor (Ho et al. 2009),
mediates signal transduction for root development in response
to nitrate conditions. In an NRT1.1 knock-out mutant, the
elongation of LRs in the nitrate-rich area was reduced compared with that in wild-type plants (Remans et al. 2006a).
Krouk et al. (2010) found that NRT1.1 promoted auxin influx
in a heterologous expression system, and this transport activity
was inhibited by high nitrate concentrations. They speculated
that nitrate/auxin dual transport activity is the molecular basis
of the involvement of NRT1.1 in the nitrate-dependent root
architecture response: the elevated auxin transport by NRT1.1
under nitrate-limited conditions reduces accumulation of auxin
in LR tips, and thereby inhibits LR elongation (in comparison
with nitrate-rich conditions) (Krouk et al. 2010, Mounier et al.
2014).
The transcription factors responsible for the response of
root morphology to nitrate have been identified, of which
ANR1 was the first. ANR1 encodes a MADS-box transcription
factor that positively regulates LR elongation under high-nitrate
conditions, via the same pathway as NRT1.1 (Zhang and Forde
1998, Remans et al. 2006a). A loss of ANR1 function alters the
root response to low nitrate (Zhang and Forde 1998), and its
overexpression confirmed the positive effect of ANR1 on LR
elongation, but not on PR development (Gan et al. 2012). The
architectural changes of roots under low-nitrate conditions are
also induced by the high-affinity nitrate transporter NRT2.1 and
its transcriptional factors TGA1 and TGA4 (Remans et al.
2006b, Alvarez et al. 2014). NRT2.1 represses LR initiation
under severe nitrate deprivation independently of nitrate transport, while its nitrate transport activity affects the root system
architecture (Little et al. 2005, Remans et al. 2006b). The basic
leucine zipper (bZIP) transcription factors TGA1 and TGA4
regulate the expression of NRT2.1 and NRT2.2 (Alvarez et al.
2014). Increased LR emergence with nitrate application was
reduced relative to the wild type in both tga1/tga4 and
nrt2.1/nrt2.2 plants, but the reduction was considerably greater
in tga1/tga4. Further, PR growth in response to nitrate application was decreased in tga1/tga4, but was unaffected in nrt2.1/
nrt2.2. This suggests that TGA1 and TGA4 regulate the nitrateresponsive root architecture partly via the same pathway as
NRT2.1 and NRT2.2, but also an independent pathway. These
studies revealed the complex nature of the regulatory network
that involves transcription factors, transporters and root
architecture.
Plant hormones are involved in root development and architecture determination. The significance of phytohormones,
2030
particularly auxin, in the nutrient-dependent regulation of
the root system is now clear. Auxin transport by NRT1.1
(described above) is important in this context. The distribution
of auxin, which is controlled by both its transport and biosynthesis, is probably a major signal that modulates root development in a nutrient-dependent manner. LR elongation in
response to localized iron is induced by the AUX1-mediated
redistribution of auxin (Giehl et al. 2012). Auxin can also control
PR elongation, and PR growth is inhibited by the redistribution
of auxin by PIN1 in the presence of excess copper (H.M. Yuan
et al. 2013). Ma et al. (2014) reported that auxin biosynthesis by
TAR2 contributes to LR emergence under mild nitrate deprivation. Phytohormones affect root architecture, and emerging
molecular evidence suggests that nutrients and hormones
interact in a complex manner. A broader picture of the regulatory network will be revealed by further work on this issue
together with studies of transcription factors and transporters.
Diverse Functions of Transporters
Distinct functions of transporters for specific
processes
To acquire and distribute essential nutrients efficiently under
nutrient starvation, nutrient transport must be co-ordinated by
transport molecules in plant organs. The major transport processes within an individual plant include: (i) uptake from the
soil to root cells; (ii) xylem loading; and (iii) distribution/remobilization into sink organs in shoots.
Recent studies have revealed the involvement of novel
players belonging to previously categorized families in the
transport of specific elements at different steps, such as
uptake into root cells and subsequent xylem loading in roots.
For example, A. thaliana NRT2.4 and NRT2.5, high-affinity nitrate transporters, participate in nitrate uptake into the roots,
as well as regulating nitrate levels in the phloem together with
NRT2.1 under N limitation (Kiba et al. 2012, Lezhneva et al.
2014). Arabidopsis thaliana requires MGT6, an Mg transporter
localized to the plasma membrane, for Mg uptake into roots
and normal growth under low-Mg conditions (Mao et al. 2014).
Some members of the MRS/MGT Mg transporter family in
Oryza sativa are localized to chloroplasts (Saito et al. 2013),
suggesting that distinct subcellular localization establishes mineral homeostasis in the organelles in which the nutrients are
required. Further, an additional unknown K uptake pathway
was implied, other than HAK5 and AKT1, major transport molecules for K acquisition in A. thaliana (Caballero et al. 2012). For
micronutrients, OsNramp5 is essential for efficient Mn uptake
into roots and normal growth under Mn-limited conditions in
rice (Ishimaru et al. 2012, Sasaki et al. 2012). OsHMA5, a heavy
metal P-type ATPase, has a fundamental role in the root to
shoot translocation of Cu; it is expressed in the root pericycle
and xylem of the vascular bundles (Deng et al. 2013).
One remarkable recent discovery was the identification of
transporters that modulate the nutrient distribution in the
aerial portion of plants. OsHMA2 was first shown to function
in the root to shoot translocation of Zn in rice (Satoh-Nagasawa
Plant Cell Physiol. 55(12): 2027–2036 (2014) doi:10.1093/pcp/pcu156
et al. 2012), but is also expressed in the phloem of the vascular
bundles and functions in the preferential distribution of Zn into
sink organs during the reproductive stage of rice (Yamaji et al.
2013b). OsNramp3, which is expressed in the nodes, calibrates
Mn transport to young growing leaves in rice (Yamaji et al.
2013a). OsYSL16, a Cu–nicotianamine transporter expressed
in the phloem of nodes, is responsible for distributing Cu
from mature to growing leaves and from the flag leaf to panicles, ensuring fertility (Zheng et al. 2012). COPT6, a CTR/COPT
Cu transport protein expressed in aerial organ vascular bundles,
is also important for Cu distribution from leaves to seeds under
Cu limitation in A. thaliana (Garcia-Molina et al. 2013).
NRT2.10 and NRT2.11, low-affinity nitrate transporters, are expressed in companion cells in mature leaves and mediate nitrate distribution into young leaves to sustain plant growth in
the presence of high nitrate levels (Hsu and Tsay 2013). In
addition, in the reproductive organs, it was reported that the
B exporter OsBOR4 is expressed predominantly in pollen and is
required for pollen germination and pollen tube elongation
(Tanaka et al. 2013).
These studies show that plants allocate specific transporters
to particular cells and processes with distinct transport substrates, affinities and subcellular localizations. These transporters with diverse functions appear to have evolved via
neofunctionalization and subfunctionalization, to maximize
not only the initial uptake in roots but also source to sink
translocation and cellular compartmentalization during both
vegetative and reproductive stages.
Variation of transporters among plant species
Transporters for essential nutrients have been identified
and characterized in the model plants A. thaliana and O.
sativa. With the increased genomic information on nonvascular plants and crops now available, the physiological
functions of transporter homologs have begun to be verified
experimentally. In Physcomitrella patens, a model moss, the
disruption of PpHAK2, a HAK transporter gene homolog, impairs growth under K starvation (Haro et al. 2013). PpHAK13,
another HAK transporter gene, encodes a high-affinity Na
transporter that functions under K limitation (Benito et al.
2012), implying a role in Na transport. For commercially important plants, the high-affinity ammonium importers
ZmAMT1;1a and ZmAMT1;3 have been characterized in Zea
mays (Gu et al. 2013), and CmNRT2, an N-inducible nitrate
transporter, has been isolated from Chrysanthemum morifolium
(Gu et al. 2014). Homologs of BOR1, a B exporter required under
B limitation, have been identified in Triticum aestivum
(Leaungthitikanchana et al. 2013) and Vitis vinifera (PerezCastro et al. 2012). In addition, the genes encoding a B transport
molecule, ZmNIP3;1 and RTE/BOR1, were shown to be responsible for the tassel-less1 (tls1) and rotten ear (rte) maize mutants, which exhibited impaired development of tassels and
ears, respectively (Chatterjee et al. 2014, Durbak et al. 2014,
Leonard et al. 2014). These studies are examples of the clarification of conserved or diverged functions of transporters in a
wide range of plant species. It is of particular interest to discuss
the diversification of transporters along with changes in
nutrient requirements and vascular systems from an evolutionary perspective.
Nutrient-Dependent Regulation of
Transporter Expression
Transcription
Regulation of transporter expression such that each transporter
performs its function at the appropriate time and location to
maintain overall homeostasis is crucial. The transcriptional control of transporter genes has been investigated extensively as an
initial step in gene expression. Several transcriptional factors
regulating the same transporter have been identified using different approaches. The expression of HAK5, the gene encoding
a high-affinity K transporter, is increased upon K starvation in
A. thaliana (Ahn et al. 2004). Using the activation tagging
method, the transcription factor RAP2.11 was shown to
induce HAK5 expression under low K (Kim et al. 2012). Four
other candidate transcription factors have been identified using
the TF FOX library (Hong et al. 2013). Among investigations of
nitrate signaling, two reports have demonstrated that the transcription factor NIN-LIKE PROTEINs (NLPs) controls nitrateinducible transcription of genes, including nitrate transporter
NRT genes (Konishi and Yanagisawa 2013, Marchive et al. 2013).
Suppression of NLP6 function reduces mRNA induction of
NRT1.1 and NRT2.1 upon nitrate supply (Konishi and
Yanagisawa 2013). The Fe-dependent transcript regulation of
IRON-REGULATED TRANSPORTER 1 (IRT1) is controlled by several transcription factors. FIT (AtbHLH29) forms heterodimers
with AtbHLH38, AtbHLH39, AtbHLH100 and AtbHLH101, and
mediates the Fe starvation-induced transcription of IRT1
(Colangelo and Guerinot 2004, Yuan et al. 2008, Wang et al.
2013). As in the root architecture response, transcription factors play important roles in regulation, although those controlling root architecture and transporter expression are not always
shared, suggesting that multiple systems regulate the sensing of
nutrients and the responses thereto.
mRNA stability
The control of mRNA stability is also vital for maintaining
mRNA levels and controlling the rate of change in mRNA accumulation. mRNA stability is controlled by the 30 and 50 untranslated regions (UTRs). Several studies have shown examples
of the control of mRNA stability in response to environmental
stimuli in plants (Bhat et al. 2004, Chiba et al. 2013). In an
exploration of nutrient-dependent mRNA stability, Tanaka
et al. (2011) demonstrated that the mRNA of A. thaliana
NIP5;1, a gene encoding the NIP5;1 boric acid channel, was
destabilized in the presence of sufficient boric acid. NIP5;1, a
member of the major intrinsic family, is required for B uptake
under B limitation, and NIP5;1 mRNA is elevated 15-fold when
transferred to B-deficient conditions (Takano et al. 2006).
Tanaka et al. (2011) demonstrated that an 18 bp sequence in
the 50 UTR is required to decrease the half-life of mRNA upon
exposure to high B conditions. Further, transgenic plants carrying NIP5;1 without the 50 UTR accumulated more B in shoots
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I. Aibara and K. Miwa | Regulation of mineral nutrient transport
and exhibited a growth defect under a high level of B supply,
probably due to excess B uptake by constitutive accumulation
of NIP5;1. This study provides clear evidence that nutrient availability controls mRNA turnover, and this control is critical for
normal growth. A study by Yuan et al. (2007) indicates that
mRNA accumulation of the ammonium transporter AtAMT1;1
is post-transcriptionally controlled by N availability. In
Nicotiana tabacum, transcript levels of AtAMT1;1 (driven by
the Cauliflower mosaic virus 35S promoter) are reduced when
ammonium is supplied. The regulation of mRNA turnover is
more efficient than transcriptional down-regulation in terms of
reducing transcript levels rapidly. Depending on the transporters and properties of the nutrient, mRNA turnover regulation might facilitate adaptation to changes in nutrient
conditions.
Alternative splicing and translation
Few reports on translational regulation in response to nutrient
availability in plants have been published. The translation of the
transporter ZIF2 (Zinc-induced Facilitator 2) is enhanced under
high Zn conditions in A. thaliana by producing a splice variant
that increases translation under high Zn conditions (Remy et al.
2014). ZIF2 is localized to the tonoplast and promotes Zn tolerance via Zn compartmentalization. At least nine splice variants are produced from the ZIF2 gene, all of which encode the
same full size ZIF2 transporter. Two splice variants are produced predominantly in roots: ZIF2.1 and ZIF2.2. ZIF2.2 contains
an intron sequence in its 50 UTR; this is removed in ZIF2.1, and
the ZIF2.2 mRNA level was increased preferentially under a high
level of Zn. The longer 50 UTR in ZIF2.2 caused higher translational efficiency under standard conditions and induced a
greater Zn-dependent translation response than the ZIF2.1
50 UTR. Moreover, the prediction of RNA secondary structures
indicated that the ZIF2.2 splice variant has the potential to form
a stable stem–loop structure upstream from the start codon;
this is absent in ZIF2.1. A mutation that destabilized the predicted stem–loop markedly weakened the translation induced
by a high Zn concentration. These results demonstrate that a
specific sequence/structure in the ZIF2.2 50 UTR induced Zndependent translation. The increased ZIF2.2 mRNA abundance
under high Zn conditions probably has synergistic effects on
increasing the translation efficiency of the ZIF2 gene. Based on
the differences in splicing variant abundances among organs
and conditions, this study suggests that control of translation,
which is associated with alternative splicing, enables synthesis
of the appropriate quantity of transporters to meet the variable
demand.
Polar localization
The polar localization of transporters is thought to be important for the directional transport of substrates. Increasing numbers of mineral transporters in plants are reported to have polar
localization. These include Lsi and Lsi2 (transporters of silicon,
which is a beneficial element) (Ma et al. 2006, Ma et al. 2007),
OsNramp5 (Sasaki et al. 2012) in rice, the Fe transporter IRT1
(Barberon et al. 2014), the B transporters BOR1 and NIP5;1
(Takano et al. 2010) and the nitrate transporter NRT2.4 (Kiba
2032
et al. 2012) in A. thaliana. However, few reports on the underlying molecular mechanisms and physiological impact of polar
localization exist. The Fe transporter IRT1 is localized to the
plasma membrane facing the rhizosphere in the root epidermis
under metal depletion (Barberon et al. 2014). IRT1 is a key
player in Fe acquisition, but also transports other metals,
such as Zn, Mn and Co (Vert et al. 2002). While IRT1 is localized
to early endosomes/trans-Golgi network compartments under
standard conditions via ubiquitin-dependent endocytosis
(Barberon et al. 2011), it is localized to the outer domain of
the plasma membrane in root epidermal cells under the depletion of secondary metal substrates (Zn, Mn and Co) (Barberon
et al. 2014). FYVE1, a phosphatidylinositol-3-phosphate (PI3P)binding protein, was found to be responsible for the recycling
and polar localization of IRT1, thereby controlling metal
homeostasis (Barberon et al. 2014). The boric acid/borate channel NIP5;1 and the B exporter BOR1 are localized to root cells
with polarity toward the outer and inner domains of the plasma
membrane, respectively (Takano et al. 2010). Characterization
of a mutant with defective localization of green fluorescent
protein (GFP)–NIP5;1 showed that D-galactose synthesis by
UDP-glucose 4-epimerase 4 (UGE4) is required for general
endomembrane organization (Uehara et al. 2014). The polar
localization of BOR1 requires three tyrosine residues (Tyr373,
Tyr398 and Tyr405) in a putative cytoplasmic loop; these are
potential tyrosine-based motifs for membrane trafficking, while
Tyr414, which is also located in the loop, is not involved
(Takano et al. 2010, Yoshinari et al. 2012). The three tyrosine
residues are also required for the degradation of BOR1 under
high-B conditions, as described below (Takano et al. 2010).
These results suggest that membrane trafficking is the molecular basis for establishment of polarity, including recycling between the plasma membrane and endosomes. Further
identification of the molecules and amino acid residues in
transporters that are essential for polar localization will clarify
the effect of polarity on the directional flow of substrates and
subsequent nutrient accumulation.
Protein degradation
Most essential elements are toxic at high concentrations.
Control of protein degradation is critical for the regulation of
transporter levels and the down-regulation of transporters
required to avoid overloading when nutrient concentrations
are elevated. Recent studies have demonstrated that the ubiquitination of transporters triggers their selective degradation.
The E2 ubiquitin-conjugating enzyme and E3 ubiquitin ligase
involved in this process have been identified. Within the PHT1
phosphate transporter family, RING-type E3 ligase NLA
(NITROGEN LIMITATION ADAPTATION), which was initially
assigned a role in the N response (Peng et al. 2007), was
found to mediate the ubiquitination and subsequent degradation of PHT1 under P-replete conditions (Lin et al. 2013).
Furthermore, expression of PHO2, which encodes the E2 conjugase UBC24, is required for the ubiquitination and degradation of the phosphate transporter Pht1;4 (also a member of
the PHT1 family) under inorganic phosphorus (Pi)-sufficient
conditions (Park et al. 2014). Under Pi starvation, the transcript
Plant Cell Physiol. 55(12): 2027–2036 (2014) doi:10.1093/pcp/pcu156
levels of NLA and PHO2 are down-regulated by low-P-inducible
miR827 and miR399, respectively (Hsieh et al. 2009), indicating
that protein degradation is regulated by the post-transcriptional regulation of ubiquitination-related genes. High-B-inducible degradation of BOR1, a B transporter, is mediated by the
ubiquitination of a lysine residue (Takano et al. 2005, Kasai et al.
2011). As indicated above, the tyrosine residues important for
polar localization are also required for degradation (Takano
et al. 2010). Mono-ubiquitination of the Lys146 (or Lys171)
residue in the intracellular loop of the Fe transporter IRT1 is
responsible for the turnover of IRT1 protein in a mechanism
that regulates plant Fe accumulation (Kerkeb et al. 2008,
Barberon et al. 2011). A corresponding E3 ubiquitin ligase
that mediates IRT1 degradation has been identified and
named IDF1 (IRT1 DEGRADATION FACTOR 1) (Shin et al.
2013). Thus, membrane trafficking is also an important process
for selective protein degradation.
Because enhanced protein stability may reduce the effects
on protein quantity of down-regulation of transcript levels or
translation, control of protein turnover is important for regulation of protein levels. Importantly, a single transporter can be
regulated at multiple steps. Identification of mechanisms that
co-ordinate multistep regulation is clearly crucial for improved
understanding of transporter quantity optimization.
Protein modification
Transporter activity is controlled by protein quantity and is
regulated in part by post-translational modifications that can
directly affect transport properties. The A. thaliana nitrate
transporter NRT1.1/CHL1 functions as a dual-affinity nitrate
transporter, depending on its phosphorylation state (Wang
et al. 1998, Liu et al. 1999, Liu and Tsay 2003), and contributes
to both high- and low-affinity nitrate uptake systems (Wang
et al. 1998, Liu et al. 1999). The phosphorylation of Thr101
converts the affinity from low to high (Liu and Tsay 2003).
The replacement of Thr101 with alanine and aspartic acid (to
prevent and mimic phosphorylation, respectively) converts
NRT1.1 activity to constitutive low-affinity transport and
high-affinity transport, respectively. The protein kinase
CIPK23 is responsible for the phosphorylation of Thr101 in response to low nitrate (Ho et al. 2009). A recent study showed
that the shift in the affinity mode of NRT1.1 is associated with
dimer assembly and disassembly, which is caused by dephosphorylation and phosphorylation, respectively, of Thr101
(Parker and Newstead 2014, Sun et al. 2014). Another example
of a change in transporter activity is seen in the A. thaliana
ammonium transporters AMT1;1 and AMT1;3, which govern
ammonium uptake and form homo- and heterotrimers
(L. Yuan et al. 2013). High ammonium supply inactivates
both AMT1;1 and AMT1;3 via the phosphorylation of threonine residues in its cytosolic C-terminus (Loque et al. 2007,
Lanquar et al. 2009, L. Yuan et al. 2013), demonstrating that a
phosphorylated isomer disrupts the transport activity of the
entire complex. In the regulation of transporter expression, affinity switching and inactivation via phosphorylation may
enable the most rapid change in nutrient transport in response
to nutrient conditions. The regulation of transport by direct
modification of the transporter protein would be beneficial,
especially during dramatic fluctuations in environmental nutrient concentrations in a short period of time.
Concluding Remarks
This review focused on how plants have evolved sophisticated
systems to modulate root system architecture and transporter
expression dynamically in response to nutrient availability. One
remaining challenge is determining how plants sense the external/internal nutrient condition as the initial step in the response to a specific nutrient. How (local sensor/systemic
signal), where (external environment/cells/organelles) and
using what (mineral itself/metabolites) plants recognize nutrient status should be determined. Another challenge remaining
for the future will be evaluation of the physiological advantages
and trade-offs, if any, of these nutrient-dependent controls in
the presence of the spatial and temporal changes in nutrient
conditions. Mathematical modeling together with experimental data will facilitate elucidation of the optimization of plant
systems in terms of the responses to particular environments.
Furthermore, an understanding of these nutrient-dependent responses will enable fundamental questions in plant science to be addressed. Nutrient-dependent root plasticity is one
example of the unique flexible body plan of plants. The establishment of polarity within a cell is also a basis for the development of multicellular organisms. Further research on the
mechanisms of nutrient transport will shed light on the strategies of adaptation to changing environments.
Funding
This work was supported by the Ministry of Education, Culture,
Sports, Science, and Technology (MEXT), Japan [a Grant-in-Aid
for Scientific Research on Innovative Areas grant No.
25114502)]; the Japan Science and Technology Agency (JST)
[PRESTO].
Disclosures
The authors have no conflicts of interest to declare.
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