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Journal of Experimental Botany, Vol. 65, No. 3, pp. 809–819, 2014
doi:10.1093/jxb/ert400 Advance Access publication 30 November, 2013
Review paper
Substantial roles of hexokinase and fructokinase in the
effects of sugars on plant physiology and development
David Granot*, Gilor Kelly, Ofer Stein and Rakefet David-Schwartz
Institute of Plant Sciences, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250, Israel
* To whom correspondence should be addressed. E-mail: [email protected]
Received 1 August 2013; Revised 31 October 2013; Accepted 1 November 2013
Abstract
The basic requirements for plant growth are light, CO2, water, and minerals. However, the absorption and utilization of
each of these requires investment on the part of the plant. The primary products of plants are sugars, and the hexose
sugars glucose and fructose are the raw material for most of the metabolic pathways and organic matter in plants.
To be metabolized, hexose sugars must first be phosphorylated. Only two families of enzymes capable of catalysing
the essential irreversible phosphorylation of glucose and fructose have been identified in plants, hexokinases (HXKs)
and fructokinases (FRKs). These hexose-phosphorylating enzymes appear to coordinate sugar production with the
abilities to absorb light, CO2, water, and minerals. This review describes the long- and short-term effects mediated by
HXK and FRK in various tissues, as well as the role of these enzymes in the coordination of sugar production with the
absorption of light, CO2, water, and minerals.
Key words: Fructokinase, guard cells, hexokinase, hexose phosphorylation, minerals, photosynthesis, stomata, sugar,
transpiration, water.
Sugars integrate and affect resource
consumption and govern plant
development and physiology
Plants need light, CO2, water, and minerals (such as ammonium,
nitrate, phosphate, potassium, and several other essential elements) to grow. However, the absorption and utilization of each
of these requires investment on the part of the plant. For example, investment in leaf formation and plastids is necessary for the
absorption of light and the incorporation of CO2, while investment in roots and vascular tissues is necessary for the uptake
and transport of water and minerals. Even under optimal conditions, when all resources are present in sufficient amounts, the
absorption of each input should be well coordinated with that
of the others, to ensure optimal investment in development and
activity of specialized tissues and plant parts. The sessile nature
of plants, which inevitably increases the unpredictability of
resource availability, further necessitates such coordination.
Among the essential resources, only light may be considered relatively predictable. The availability of the other
resources—CO2, water, and minerals—is much less predictable. In fact, the consumption of CO2 and minerals is highly
dependent on the presence of water, which is usually the
major limiting factor for terrestrial plants. For this reason,
terrestrial plants are coated with a water-impermeable cuticle layer that prevents evaporation and water loss (Edwards,
1993). Special pores, known as stomata, allow the uptake
of CO2 for photosynthesis during the day, but under waterlimiting conditions, the stomata are closed. As a result, the
ability of CO2 to enter the plant is dependent on the presence of water, which causes the stomata to open to allow the
uptake and assimilation of CO2 (Raven, 2002). Similarly,
Abbreviations: ABA, abscisic acid; F6P, fructose 6-phosphate; FRK, fructokinase; G6P, glucose 6-phosphate; HXK, hexokinase; INV, invertase; PSI, phosphate
starvation-induced; SUS, sucrose synthase; T6P, trehalose-6-phosphate; UDP-G, UDP-glucose.
© The Author 2013. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.
For permissions, please email: [email protected]
810 | Granot et al.
the acquisition of minerals from the soil and the transport
of minerals within the plant are also dependent on water
(Smith, 1991). In this manner, water governs the unpredictable nature of the resources required for plant survival,
growth, and reproduction. Once water becomes available,
plants respond rapidly, opening stomata to absorb CO2 and
(indirectly) minerals necessary for the production of sugars.
Water is released to the atmosphere through the open stomata, creating a vacuum that draws additional water and
minerals into the plant from the soil solution.
Sugars are the primary products of plants and are the
raw material for all of the metabolic pathways and organic
matter in plants. Accordingly, sugar allocation determines
the plant’s ability to absorb resources and grow. For example, when there is a shortage of water or minerals, more
of the available sugar is diverted towards root development
and the improvement of root absorption functions, at the
expense of aboveground vegetative tissues (Smith, 1982).
On the other hand, when light is in limited supply, more of
the available sugar will be directed towards stem elongation and the development of leaves and plastids (Poorter
and Nagel, 2000). Therefore, it is reasonable to assume
that sugars might coordinate the absorption and uptake of
light, CO2, water, and minerals with plant physiology and
development.
Short- and long-term effects of sugars and
molecular pathways that mediate these
effects
The effects of sugars can be roughly divided into short- and
long-term responses. Short-term responses include rapid,
reversible physiological effects such as changes in stomatal aperture, photosynthesis rate, starch accumulation,
and the absorption of minerals by the roots. Long-term
responses might include slow, long-lasting, possibly irreversible developmental changes such as shoot formation,
leaf development, leaf senescence, and root and vascular
development. Several molecular mechanisms that mediate
sugar responses have been identified in plants (reviewed
by Smeekens et al., 2010). These mechanisms play roles in
two types of situation: when excess sugar is present and
when sugar is in limited supply. The hexokinase (HXK)
sugar-sensing pathway, the trehalose-6-phosphate (T6P)
pathway, and target of the rapamycin (TOR) kinase pathway all play roles in the presence of excess sugar, whereas
SNF-related protein kinases (SNRKs) and the C/S1 bZIP
transcription factor network play important roles when
sugar is in limited supply (Smeekens et al., 2010). The
fructokinases/sucrose synthase (FRK/SUS) pathway may
also control sugar allocation in response to sugar levels
(Granot et al., 2013). This review will focus on the roles of
the hexose-phosphorylating enzymes, HXK and FRK, in
the short- and long-term effects of sugars on plant physiology and development, and will also describe how HXK
and FRK coordinate plant physiology and development
with resource availability.
Origin of the sugars found in source and
sink tissues and their localization
The production of sugars by photosynthesis has been widely
described and has been illustrated in recent reviews (Stitt
et al., 2010; Granot et al., 2013). Nevertheless, it might be
appropriate to review some of the details here, to emphasize
the origin and distribution of glucose and fructose, the substrates of HXK and FRK.
Sucrose is the primary end product of photosynthesis
(Fig. 1). This sucrose can then be metabolized in photosynthetic
tissues, or exported out of the photosynthetic (source) tissues
to non-photosynthetic (sink) tissues, where it serves as an initial substrate for all organic metabolic pathways (Fig. 1). To be
metabolized in sink or photosynthetic source tissues, sucrose
must be cleaved by either invertase (INV) or sucrose synthase
(SUS), the only two families of sucrose-cleaving enzyme that
have been identified in plants (Dennis and Blakeley, 2000).
INV cleaves sucrose into the monomer hexoses glucose and
fructose, whereas SUS cleaves sucrose in the presence of UDP
to yield UDP-glucose (UDP-G) and fructose (Fig. 1). Starch
in photosynthetic tissues (during the dark period) and in sink
tissues is also degraded to yield glucose monomers (Chia et al.,
2004; Smith et al., 2005). Both hexoses, glucose and fructose,
must be phosphorylated before they can be used in any metabolic process. Hence, hexose-phosphorylating enzymes are
essential for all aspects of plant metabolism and development.
While the metabolic function of hexose kinases in sink tissues
is essential, their function in photosynthetic tissues during the
day may seem dispensable, as the hexoses obtained from triose
phosphates are already phosphorylated (Fig. 1). Nevertheless,
hexose kinases are present in source tissues (Claeyssen and
Rivoal, 2007; Granot, 2008; Granot et al., 2013) and play a
crucial role in sugar sensing, as described below.
Plant hexokinases and fructokinases
Only two types of glucose- and fructose-phosphorylating
enzymes have been discovered in plants, HXKs and FRKs.
As such, HXKs and FRKs are the gateway for most of the
organic metabolism in plants. Moreover, these enzymes catalyse irreversible reactions (no hexose-phosphate phosphatases
have been found in plants) and therefore may play central roles
in the regulation of plant sugar metabolism. While FRK activity is specific to fructose, HXKs are capable of phosphorylating glucose, fructose, mannose, and glucosamine (reviewed by
Granot, 2007, 2008). Accordingly, in plants, glucose can be
phosphorylated only by HXK, whereas fructose can be phosphorylated by either HXK or FRK. Yet, the affinity of HXKs
for glucose is in the 0.02–0.1 mM range, whereas their affinity
for fructose is about one to three orders of magnitude lower, in
the 2–120 mM range (Granot, 2007). The affinity of FRKs for
fructose is usually high, within the same range as the affinity of
HXKs for glucose (Pego and Smeekens, 2000; Granot, 2007).
As the affinity of HXKs for glucose is much higher than their
affinity for fructose, it has been suggested that in vivo HXKs
probably phosphorylate mainly glucose, whereas fructose is
phosphorylated primarily by FRKs (Granot, 2007). Several
HXK and FRK and plant physiology | 811
Fig. 1. Schematic presentation of sugar metabolism in source and sink tissues. Triose phosphate (triose-P), the product of
photosynthetic CO2 fixation in the Calvin cycle, is exported from the chloroplast to the cytoplasm. Consecutive cytoplasmic enzymatic
steps lead to the formation of glucose 6-phosphate (G6P) independent of HXK and FRK. Further metabolism of G6P yields sucrose,
which is exported to sink tissues. G6P metabolism may also yield trehalose 6-phsophate (T6P) and trehalose. Within the chloroplast,
triose-P is used for the formation of starch during the day. During the dark period, starch degradation may yield glucose. Glucose and
fructose in photosynthetic tissues may also be obtained following the cleavage of sucrose and trehalose. In sink tissues, sucrose can be
cleaved by invertase or sucrose synthase, and the hexose monomers, glucose and fructose, must be phosphorylated by HXK or FRK
before they can be further metabolized. F1,6BP, fructose 1,6-biphosphate; F6P, fructose 6-phosphate; G1P, glucose 1-phosphate;
Suc-P, sucrose-phosphate; UDP, uridine diphosphate; UDP-G, UDP-glucose. (This figure is available in colour at JXB online.)
FRK isozymes are inhibited by their own substrate, fructose,
when it exceeds a certain concentration. This phenomenon
is known as substrate inhibition and its putative biological
significance is described below (Pego and Smeekens, 2000;
German et al., 2003; Damari-Weissler et al., 2009).
So far, three to ten HXK genes and three to seven FRK
genes have been found in different plant species (Cho et al.,
2006a; Granot, 2007; Karve et al., 2010). Two major types of
HXK have been identified in plants based on their intracellular
localization, which is determined by their N-terminal amino
acid sequences (Olsson et al., 2003; Giese et al., 2005; Cho
et al., 2006a; Damari-Weissler et al., 2006; Kandel-Kfir et al.,
2006; Karve et al., 2008). Type A HXKs are located within
plastids and type B HXKs are associated with the mitochondria. A third type, type C HXK, is located in the cytoplasm of
monocots (da-Silva et al., 2001; Cho et al., 2006a; Karve et al.,
2010; Cheng et al., 2011). Similar to HXKs, FRKs are found
in two locations in plants, in plastids and in the cytoplasm.
Most plant species have a single plastidic HXK and a single
plastidic FRK, with multiple HXK and FRK isozymes in the
cytoplasm. Yet, while the cytoplasmic FRKs are located within
the cytosol, all of the cytoplasmic HXKs in eudicots and most
of the cytoplasmic HXKs in monocots are associated with the
mitochondria (Granot, 2008; Granot et al., 2013).
The HXK sugar-sensing pathway
As HXKs are the only enzymes that can phosphorylate glucose in plants, they are probably present in most, if not all
types of plant cells (Granot et al., 2013). Over the last two
812 | Granot et al.
and a half decades, the role of HXK in plants has been studied by exposing plant cells and seedlings to HXK substrates
and substrate analogues and by overexpressing and downregulating type B HXK in planta. The Arabidopsis type B HXK
(AtHXK1) was identified as a genuine glucose sensor that
mediates glucose effects independently of its glucose phosphorylation enzymatic activity [i.e. independently of its products, glucose 6-phosphate (G6P) and fructose 6-phosphate
(F6P), and their downstream metabolism) (Jang and Sheen,
1994; Jang et al., 1997; Moore et al., 2003). Overexpression
of AtHXK1, either the native or the mutated isoform that
lacks the hexose phosphorylation catalytic activity, inhibits
the expression of photosynthetic genes, decreases chlorophyll
levels and reduces the rate of photosynthesis (Jang et al.,
1997; Dai et al., 1999; Xiao et al., 2000; Moore et al., 2003;
Kelly et al., 2012). These effects suggest that AtHXK1 monitors glucose levels, most likely in mesophyll cells of photosynthetic tissues, and inhibits photosynthesis when glucose levels
are sufficiently high (Jang et al., 1997; Dai et al., 1999; Moore
et al., 2003; Kelly et al., 2012). This role of HXK in shoots
(photosynthetic plant parts) as compared with roots was confirmed by reciprocal grafting experiments in which the effects
of overexpression of AtHXK1 were observed only when this
overexpression occurred in the shoots (Dai et al., 1999).
The regulation of photosynthesis by HXK may represent
a short-term, reversible sugar-sensing effect aimed at balancing the investment in sugar production (such as expression of photosynthetic genes and chlorophyll production)
with sugar levels and the capability of utilizing the sugars.
Although constitutive expression of AtHXK1 in Arabidopsis
and tomato plants (under the 35S promoter) has a long-term
growth-inhibiting effect (Jang et al., 1997; Dai et al., 1999;
Kelly et al., 2012), that growth inhibition might be in part an
artificial effect caused by the continuous unnatural reduction
of photosynthesis by HXK.
The origin of glucose sensed by HXK in photosynthetic
mesophyll cells during the day is not clear, as there is seemingly
no need for production of free glucose in these tissues in the
presence of light (Fig. 1) (Granot et al., 2013). Furthermore,
unlike fungal and mammalian cells, there is no evidence for
the production of glucose monomers via gluconeogenesis in
plants, as no hexose-phosphate phosphatases have been found
in plants. Rather, glucose monomers might be generated from
starch degradation during the day, from the cleavage of intracellular sucrose by cytoplasmic invertase (cINV) and/or from
the cleavage of some of the exported extracellular sucrose
by cell wall invertase (cwINV) and subsequent importation
via glucose transporters. Although the cleavage of trehalose
(a glucose–glucose disaccharide) by trehalase yields glucose
monomers that could potentially be sensed by HXK (Fig. 1),
trehalose is usually found in very small quantities that may
not be sufficient to stimulate a HXK sugar-sensing effect
(Paul, 2007). Furthermore, the effects of exogenously added
trehalose on plant growth and sugar metabolism occur independently of the expression level of AtHXK1 (Ramon et al.,
2007), perhaps eliminating trehalose as a potential source
of the glucose sensed by HXK in photosynthetic tissues.
These results may also eliminate the possibility that G6P
produced by HXK is important for the synthesis of T6P by
trehalose phosphate synthase (TPS), the enzyme that generates T6P from UDP-G and G6P. Nevertheless, expression of
Arabidopsis TPS1 might be dependent on AtHXK1 (Avonce
et al., 2004), perhaps representing a common role in the
short-term effects of HXK and T6P. Such induction of TPS1
expression by AtHXK1 (via an as-yet-unknown mechanism)
may indicate the presence of excess sugar, which may further
inhibit photosynthesis and divert resources from sugar production to starch accumulation.
It has been demonstrated that a small fraction of the mitochondria-associated AtHXK1 is transported to the nucleus,
where it forms a complex that includes the vacuolar H+ATPase B1 (VHA-B1) and the 19S regulatory particle of the
proteasome subunit (RPT5B) (Cho et al., 2006b). This complex can bind the promoters of specific genes, such as CAB2,
and may inhibit their expression independently of glucose
metabolism, further supporting the role of HXK as a glucose
sensor in photosynthetic tissues that mediates the short-term
effects of sugar on photosynthesis.
Constitutive overexpression of AtHXK1 in tomato and
Arabidopsis plants under the 35S promoter accelerates leaf
senescence (Dai et al., 1999; Xiao et al., 2000; Swartzberg
et al., 2011; Kelly et al., 2012). Leaf senescence is occasionally
associated with high sugar levels and with the remobilization
of nitrogen and minerals from senescing (old) leaves to other
plant parts (Wingler et al., 2006; Wingler and Roitsch, 2008).
It is very likely that, under normal conditions, high levels of
sugar in old leaves are sensed by HXK and stimulate senescence. Such an effect would represent a long-term effect of
HXK (Dai et al., 1999; Xiao et al., 2000; Moore et al., 2003).
In addition to its role as a glucose sensor in photosynthetic tissues that probably inhibits unnecessary investment
in photosynthesis, HXK is also required for proper growth.
For example, the Arabidopsis hxk1 (gin2-1) mutant displays
reduced shoot and root growth under increasing light intensities (Moore et al., 2003). While HXK inhibition of photosynthesis is a genuine signalling effect that is independent of
HXK catalytic activity (Moore et al., 2003), the importance
of the signalling function of HXK in growth promotion as
compared with that of its metabolic function is not yet clear.
Suppression of the mitochondria-associated NtHXK1 in
tobacco plants resulted in growth inhibition and in the accumulation of starch and glucose, suggesting that the NtHXK1
has a metabolic function and is essential for maintaining
starch turnover, glycolytic activity, and normal growth (Kim
et al., 2013).
A role for HXK in the juvenile-to-adult
transition
After germination, plants undergo transitions between juvenile, adult, and reproductive developmental stages. The transitions between these stages are governed by various external
and endogenous factors, such as day length, temperature, and
nutritional status (Poethig, 1990; Amasino, 2010). It has been
established that, after germination, microRNA156 (miR156)
HXK and FRK and plant physiology | 813
function is necessary and sufficient for the transition to the
juvenile stage, while its repression allows the transition from
the juvenile stage to the adult stage (Wu et al., 2009). Recently,
the repression of miR156 has been shown to be mediated
by a leaf-derived signal (Yang et al., 2011). Furthermore,
newly published studies investigating the connection between
nutritional status and the juvenile-to-adult transition in
Arabidopsis have demonstrated that the leaf-derived signal is
sugar (Yang et al., 2013; Yu et al., 2013). It has been shown
that chlorophyll-deficient mutants and plants from which
leaves have been removed have elevated miR156 levels and
demonstrate delayed juvenile-to-adult transition. In addition,
external sugar application, which resulted in the downregulation of miR156, further demonstrated the role of photosynthesis products in phase transition. Analyses of the gin2-1
mutant at different developmental stages have revealed that
the miR156 transcript level at the early juvenile developmental stage is partially dependent on HXK signalling, whereas
the expression of miR156 at the later stage is independent
of HXK (Yang et al., 2013; Yu et al., 2013). These results
suggest that HXK prevents the accumulation of miR156 and
promotes early juvenile phase transition in response to sugar.
Additional studies are required to determine how sugar prevents the accumulation of miR156 at later developmental
stages independently of HXK. Interestingly, suppression of
miR156 is also required for the transition to the reproductive
(floral) stage and the accumulation of miR156 is affected by
TPS1 and T6P (Van Dijken et al., 2004; Wahl et al., 2013).
However, the possible link between HXK and the floral phase
has not yet been tested.
HXK in the regulation of stomatal closure
A surprising role for HXK in guard cells and stomatal behavior has recently been discovered (Kelly et al., 2013). About a
century ago, it was proposed that sugars generated from the
degradation of starch in guard cells at dawn are the primary
guard-cell osmolytes stimulating the movement of water into
the guard cells and stomatal opening (Lloyd, 1908). This
hypothesis was later modified by the discovery that K+ ions,
together with Cl– and malate ions, are the primary osmolytes
that accumulate in guard cells and open stomata (Schroeder
et al., 2001; Roelfsema and Hedrich, 2005; Pandey et al.,
2007). However, in addition to these ions, it has been suggested that the accumulation of sucrose in guard cells over
the course of the day as a result of starch degradation, photosynthetic carbon fixation, or the import of apoplastic
(intercellular) sucrose also contributes to the osmotic state
of the guard cells and the opening of the stomata (Gotow
et al., 1988; Tallman and Zeiger, 1988; Poffenroth et al., 1992;
Talbott and Zeiger, 1993, 1996).
The data from the studies that do support the role of
sucrose as a stomata-opening osmolyte are mostly correlative.
Sucrose levels in guard cells have been measured in correlation with stomatal aperture (Amodeo et al., 1996; Talbott and
Zeiger, 1998). Otherwise, almost no functional studies of the
role of sucrose in guard cells have been carried out (Talbott
and Zeiger, 1988, 1998; Lawson, 2009). In contrast to the
prevailing hypothesis, a recent study has shown that sucrose
closes stomata (Kelly et al., 2013). Furthermore, the closure
of stomata by sucrose is mediated by HXK and abscisic acid
(ABA) within guard cells (Kelly et al., 2013). These findings
support the existence of a feedback-inhibition mechanism
that is mediated by sugars (the product of photosynthesis)
and HXK (Outlaw, 2003; Kang et al., 2007). According to
this hypothesis, when the rate of sucrose production exceeds
the rate at which sucrose is loaded into the phloem, the surplus sucrose is carried towards the stomata by the transpiration stream and stimulates stomatal closure via HXK,
thereby preventing the loss of precious water. This feedback
system may represent a short-term, rapid mechanism that
coordinates CO2 uptake, sugar production, and sugar utilization with water loss. This mechanism inevitably also controls
the uptake of water and minerals by the plant.
The effect of HXK on stomatal closure and its indirect
effect on the uptake of water and minerals are in line with the
effects of HXK on the mesophyll photosynthesis rate. The
effect of HXK on photosynthesis in guard cells has not yet
been studied. Yet, in both mesophyll and guard cells, excess
sugar is sensed by HXK, leading to reduced expression of
photosynthetic genes in mesophyll cells and closure of the
stomata. The closure of the stomata reduces CO2 uptake, further minimizing the rate of mesophyll photosynthesis. These
HXK-mediated effects are probably part of a constant, ongoing physiological response that coordinates sugar production
with the investment in photosynthesis and water uptake and
water loss (Fig. 2). When the sugars are used and sugar levels
carried towards the stomata drop, the expression of photosynthetic genes and the uptake of CO2, water, and minerals
may resume, once again allowing the production of sugars.
ABA appears to be essential for HXK-mediated effects.
ABA mutants with mutations involving ABA biosynthesis
genes such as ABA1 (zeaxanthin epoxidase), ABA2 (shortchain dehydrogenase reductase 1), and ABA3 (molybdenum cofactor sulfurase), or in the ABA signalling pathway,
such as the ABIs (ABA-insensitive) 3–5 (B3, AP2, and bZIP
transcription factors, respectively) are insensitive to HXKmediated photosynthetic and growth-inhibiting effects (Zhou
et al., 1998; Laby et al., 2000; Cheng et al., 2002; Leon and
Sheen, 2003; Rolland et al., 2006; Rognoni et al., 2007; Ramon
et al., 2008). ABA produced in guard cells is also necessary
for the HXK-mediated stomatal closure (Kelly et al., 2013).
Unlike the situation in guard cells, in which the molecular
role of ABA in stomatal closure is well known, the molecular
mechanism by which ABA participates in the inhibition of
photosynthesis is not known. In all studies to date, inhibition
of photosynthesis and growth has been observed upon the
expression of HXK under the global 35S promoter, which is
also expressed in guard cells. It is tempting to speculate that
some portion of the observed photosynthetic and growthinhibiting effects might be due to the stomatal closure effect
of HXK in guard cells, which may provide an explanation for
the involvement of ABA. Yet Arabidopsis and tomato plants
that express HXK specifically in guard cells do not exhibit any
inhibition of photosynthesis or growth (Kelly et al., 2013),
perhaps indicating that ABA plays a guard-cell-independent
814 | Granot et al.
Fig. 2. Roles of HXK and FRK in plant physiology. During the
day, HXK plays a continuous role in the coordination of sugar
production with the uptake of CO2, water, and minerals. This
figure illustrates the direct inhibitory effects (solid lines) of HXK
on photosynthesis and transpiration, and how stomatal closure
by HXK reduces the uptake of CO2, water, and minerals (dashed
blue line). HXK also enhances mineral uptake by roots (dashed
black line). Unlike HXK, FRK controls the allocation of sugar for
vascular development, which may also affect sugar water and
mineral transport and whole-plant development and physiology.
N, nitrogen; P, phosphate; K, potassium; Zn, zinc; S, sulfur. (This
figure is available in colour at JXB online.)
role in the HXK-mediated inhibition of photosynthesis. Still,
the fact that guard-cell-specific expression of HXK does not
appear to have any growth-inhibiting effects might be due to
the low levels of HXK expression in the examined lines (Kelly
et al., 2012, 2013). It remains to be determined whether high
levels of HXK expression in guard cells will have a growth
inhibition effect.
Similarly to HXK, overexpression of trehalase, which
cleaves trehalose into its glucose monomers, was recently
shown to induce stomatal closure via the ABA signalling
pathway (Van Houtte et al., 2013). However, the trehalase
response seems to act downstream of ABA, whereas HXK
acts upstream of ABA (Kelly et al., 2013; Van Houtte et al.,
2013). Therefore, it is not clear whether there is a connection
between trehalase and HXK in the regulation of stomatal
closure.
A role for HXK in the uptake of minerals
Photosynthesis and sugars have been shown to play a dominant role in regulating root mineral uptake (Forde, 2002a,b;
Lillo, 2008). Several studies have shown that, upon high
sugar production by photosynthesis or external application
of sugar, the expression of different ion transporters that
facilitate the transport of nitrate, ammonium, oligopeptides,
sulfur, zinc, and potassium is induced in roots (Lejay et al.,
2003, 2008). Nineteen ion transporter-encoding genes were
found to be upregulated by sugars and/or upon light exposure (Lejay et al., 2008). Using the HXK inhibitor glucosamine, the authors of that study found that the expression
of 16 of the 19 genes was HXK dependent. Yet, mannose, a
HXK substrate that is believed to stimulate the HXK sugarsensing pathway but is poorly further metabolized (Klein and
Stitt, 1998; Pego et al., 1999), did not stimulate the expression
of the above genes (except for the oligopeptide transporter
At5g41000), suggesting that the HXK-dependent expression
of the ion transporters is unrelated to sugar sensing but may
be related to sugar metabolism downstream of HXK (Lejay
et al., 2003, 2008). Yet, the nitrate transporters of maize
(Zea mays), ZmNrt2.1 and ZmNrt2.2, have been shown to
be upregulated by sugars and by sugar analogues known to
stimulate the HXK sensing mechanism (Trevisan et al., 2008).
A role for HXK in mediating the crosstalk of sugars and
phosphate uptake has also been proposed. The phosphate
starvation response in Arabidopsis, which requires sugars,
induces lateral root formation and expression of phosphate
starvation-induced (PSI) genes. AtHXK1 (gin2-1) mutants
display a significant reduction in lateral root formation and
suppression of PSI genes (Karthikeyan et al., 2007). These
results suggest that the interaction between sugars and phosphate is mediated by HXK but could be related to sugar
metabolism downstream of HXK involving glycolysis rather
than sugar sensing. A HXK-independent pathway for the
interaction between sugars and the phosphate starvation
response has also been proposed (Muller et al., 2005).
FRKs and fructose sensing
Fructose accounts for at least half of the hexose obtained
from sucrose cleavage. As the affinities of FRKs for fructose
are usually two orders of magnitude greater than those of
HXKs for fructose (Granot, 2007), it was hypothesized that
FRK, like HXK, might act as a fructose sensor. However, no
role for FRK (or HXK) in fructose sensing has been established. Rather, growth inhibition of Arabidopsis seedlings
in 6% fructose is mediated by fructose 1,6-bisphosphatase
(FINS1/FBP) and the transcription factor FSQ6/ANAC089
(Cho and Yoo, 2011; Li et al., 2011). A truncated form of
FSQ6/ANAC089 lacking the membrane-associated domain
(thus rendering the FSQ6/ANAC089 transcription factor
constitutively active) abolishes the growth-inhibition effect of
fructose (Li et al., 2011). These results indicate the existence
of a fructose-specific signalling pathway in Arabidopsis that
does not involve FRK and HXK.
A role for FRKs in vascular development
It has been proposed previously that FRKs are important
for starch accumulation in tomato (Schaffer and Petreikov,
1997b). However, studies of tomato and potato plants with
HXK and FRK and plant physiology | 815
antisense suppression of FRK did not reveal any effects
on starch accumulation (Dai et al., 2002; Odanaka et al.,
2002; Davies et al., 2005). Instead, FRK2, the major FRK in
tomato plants, was found to be important for vascular development (German et al., 2003; Damari-Weissler et al., 2009).
Antisense suppression of FRK2 in tomato plants resulted
in thinner secondary cell walls of xylem vessels and fibres,
smaller and deformed xylem vessels, reduced cambium activity, and smaller sieve (phloem) elements with low levels of
callose deposition at the sieve plate (Damari-Weissler et al.,
2009). These effects resulted in reduced hydraulic conductivity and reduced sugar transport (Damari-Weissler et al.,
2009). Reduced FRK activity in FRK2-RNAi hybrid aspen
(Populus tremula×tremuloides) wood also resulted in thinner xylem fibres and cell walls with lower cellulose content
(Roach et al., 2012). These findings point to the importance
of FRKs for vascular development.
A few additional observations support the specific role of
FRK in vascular tissues. In the stems of wild-type tomato,
there is much more FRK activity in the secondary xylem
than in the pith or cortex (German et al., 2003). Two additional tomato FRKs, FRK1 and the plastidic FRK3, are also
expressed in vascular tissues (OS and DG, unpublished data).
In situ staining of FRK activity in potato tubers showed
localization of FRK in vascular bundles (Sergeeva and
Vreugdenhil, 2002). A cluster of FRK expressed sequence
tags is over-represented in the developing xylem of poplar (Populus tremula×Populus alba; Dejardin et al., 2004)
and in maritime pine (Pinus pinaster Ait.) in response to a
non-vertical orientation of the stem (Plomion et al., 2000).
FRK protein was also found in the stems of 6-month-old
Eucalyptus grandis (Celedon et al., 2007), and specific expression of an FRK gene (At3g59480) was observed in the xylem
of Arabidopsis hypocotyls (Zhao et al., 2005). These observations further support the suggestion that FRK plays a role in
long-term developmental processes in vascular development.
The vascular tissues are sink tissues whose development
is dependent on sugar metabolism and, accordingly, some
of the sucrose transported in the phloem must be metabolized to allow vascular development and maintenance. SUS
is probably the major sucrose-cleaving enzyme in vascular
tissues (Tomlinson et al., 1991; Sung et al., 1993; Nolte et al.,
1995; Schafer et al., 2004; Le Hir et al., 2005; Nairn et al.,
2008; Goren et al., 2011; Péron et al., 2011), yielding fructose
and UDP-G. UDP-G may be used for the synthesis of cellulose and cell walls, whereas phosphorylated fructose can
be utilized for energy production or fed into other metabolic
pathways. SUS activity is feedback inhibited by its product, fructose, when the concentration of fructose exceeds
0.5–1 mM (Schaffer and Petreikov, 1997a). As SUS activity
is not inhibited by F6P, the product of FRK (Morell and
Copeland, 1985; Matic et al., 2004), the phosphorylation
of fructose by FRK, which decreases the concentration of
fructose, might be necessary to drive the cleavage of sucrose
by SUS to promote vascular metabolism and development
(German et al., 2003; Damari-Weissler et al., 2009). Indeed,
antisense suppression of FRK2 in tomato stem resulted in
fructose and sucrose accumulation and inhibited vascular
development (Damari-Weissler et al., 2009). On the other
hand, there is a need to control the amount of sucrose used
for vascular development, to prevent excess consumption
in the vascular tissues at the expense of other sink tissues,
such as roots and fruits. To that end, several FRK isozymes,
such as the potato FRK and the tomato FRK2 and FRK3
isozymes (the major FRKs in tomato plants), are inhibited
by their own substrate, fructose, when its concentration
exceeds 0.5–1 mM, a phenomenon known as substrate inhibition (Dai et al., 1997; Petreikov et al., 2001; German et al.,
2004). It is very likely that the substrate inhibition of FRK
(such as the tomato FRK2 and FRK3) and the inhibition of
SUS by fructose together form a ‘double brake’ that restricts
the amount of sucrose used for vascular development (Pego
and Smeekens, 2000; German et al., 2003).
Involvement of FRK in other developmental
and physiological processes
The tomato FRK4 is specifically expressed in anthers during
the late stages of pollen development and during pollen germination (David-Schwartz et al., 2013), suggesting that this
enzyme might be required for the procurement of the carbohydrates necessary for cell-wall synthesis during pollentube development. Tomato FRK1 was found to be related to
flowering, as FRK1-antisense plants showed delayed transition to flowering (Odanaka et al., 2002). Other FRKs might
be involved in responses of plants to abiotic stress. In maize,
FRK2 is upregulated in response to short-term salt stress
(Zorb et al., 2011). In sunflower (Helianthus annuus), a plastidic FRK is upregulated along with other proteins related
to carbon metabolism, in response to drought stress (Fulda
et al., 2011). In sugar beet (Beta vulgaris) roots, an increase
in FRK activity was observed in response to wound stress
(Klotz et al., 2006). In rice (Oryza sativa), two FRKs are differentially regulated under anoxic conditions: OsFK2 expression increases, while OsFK1 expression decreases under
low-oxygen conditions (Guglielminetti et al., 2006). The differential expression patterns and different kinetic properties
(primarily the substrate inhibition) of different FRKs suggest
that different FRKs may play important roles in regulating
the amount of carbohydrate metabolized in different tissues
under changing conditions.
Summary
HXK and FRK are important for physiological and developmental processes at the whole-plant level, coordinating
carbohydrate availability with growth. Ever-changing environmental conditions and nutrient availability necessitate rapid,
short-term responses to coordinate sugar production with the
availability of water and minerals. The mitochondria-associated HXK appears to act as a sugar sensor in the mesophyll
and guard cells of photosynthetic tissues, for the rapid, shortterm coordination of the rate of photosynthesis (sugar production) with the rate of transpiration. When the sugar level
is high, HXK inhibits the expression of photosynthetic genes
816 | Granot et al.
and reduces the rate of photosynthesis and, at the same time,
closes the stomata, thereby reducing the uptake of CO2 (further reducing photosynthesis) and reducing transpiration and
water loss (Fig. 2). In turn, reduced transpiration limits the
uptake of water and minerals from the soil solution (Fig. 2).
In addition, HXK in roots mediates sugar stimulation of root
mineral uptake required for the utilization of sugars and the
production of other organic molecules, such as amino acids
and nuclear acids. In this way, HXK coordinates sugar production with the absorption and uptake of light, CO2, water,
and minerals. The effects of HXK on photosynthesis, stomata, and mineral uptake suggest that HXK plays a continuous diurnal role in the coordination of sugar production with
the absorption of light, CO2, water, and minerals.
Unlike HXK, there is no evidence to date for the involvement of FRK in sugar sensing. Rather, specific FRKs may
control the amount of sugars allocated for the development
of vascular tissues. As such, FRKs affect long-term developmental processes important for the transport of sugar, water
and minerals. Together, it appears that (specific) HXK and
FRK enzymes, the only two groups of enzymes catalysing the
essential irreversible first step of glucose and fructose phosphorylation, are involved in short- and long-term effects that
coordinate sugar production with the absorption of light,
CO2, water, and minerals and determine whole-plant physiology and development.
Cheng WH, Endo A, Zhou L, et al. 2002. A unique short-chain
dehydrogenase/reductase in Arabidopsis glucose signaling and
abscisic acid biosynthesis and functions. Plant Cell 14, 2723–2743.
Acknowledgements
Dai N, Schaffer A, Petreikov M, Shahak Y, Giller Y, Ratner K,
Levine A, Granot D. 1999. Overexpression of Arabidopsis
hexokinase in tomato plants inhibits growth, reduces photosynthesis,
and induces rapid senescence. Plant Cell 11, 1253–1266.
We wish to thank Aya Kelly for her excellent artistic contribution to the figures. This research was supported by the Israel
Ministry of Agriculture, Chief Scientist Research Grants
261–0865 and 261–0845, and by grant no. IS-4541-12 from
BARD, the United States–Israel Binational Agricultural and
Development Fund.
References
Amasino R. 2010. Seasonal and developmental timing of flowering.
The Plant Journal 61, 1001–1013.
Amodeo G, Talbott LD, Zeiger E. 1996. Use of potassium and
sucrose by onion guard cells during a daily cycle of osmoregulation.
Plant and Cell Physiology 37, 575–579.
Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P,
Thevelein JM, Iturriaga G. 2004. The Arabidopsis trehalose-6-P
synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and
stress signaling. Plant Physiology 136, 3649–3659.
Celedon PAF, de Andrade A, Xavier Meireles KG, de Carvalho
MCDCG, Gomes Caldas DG, Moon DH, Carneiro RT,
Franceschini LM, Oda S, Labate CA. 2007. Proteomic analysis
of the cambial region in juvenile Eucalyptus grandis at three ages.
Proteomics 7, 2258–2274.
Cheng W, Zhang H, Zhou X, Liu H, Liu Y, Li J, Han S, Wang Y.
2011. Subcellular localization of rice hexokinase in the mesophyll
protoplasts of tobacco. Biologia Plantarum 55, 173–177.
Chia T, Thorneycroft D, Chapple A, Messerli G, Chen J,
Zeeman SC, Smith SM, Smith AM. 2004. A cytosolic
glucosyltransferase is required for conversion of starch to sucrose in
Arabidopsis leaves at night. Plant Journal 37, 853–863.
Cho JI, Ryoo N, Ko S, Lee SK, Lee J, Jung KH, Lee YH,
Bhoo SH, Winderickx J, An G, Hahn TR, Jeon JS. 2006a.
Structure, expression, and functional analysis of the hexokinase gene
family in rice (Oryza sativa L.). Planta 224, 598–611.
Cho YH, Yoo SD, Sheen J. 2006b. Regulatory functions of nuclear
hexokinase1 complex in glucose signaling. Cell 127, 579–589.
Cho YH, Yoo SD. 2011. Signaling role of fructose mediated by
FINS1/FBP in Arabidopsis thaliana. PLoS Genet 7, e1001263.
Claeyssen E, Rivoal J. 2007. Isozymes of plant hexokinase:
occurrence, properties and functions. Phytochemistry 68, 709–731.
Dai N, German MA, Matsevitz T, Hanael R, Swartzberg D,
Yeselson Y, Petreikov M, Schaffer AA, Granot D. 2002. LeFRK2,
the gene encoding the major fructokinase in tomato fruits, is not
required for starch biosynthesis in developing fruits. Plant Science
162, 423–430.
Dai N, Schaffer A, Petreikov M, Granot D. 1997. Potato (Solanum
tuberosum L.) fructokinase expressed in yeast exhibits inhibition by
fructose of both in vitro enzyme activity and rate of cell proliferation.
Plant Science 128, 191–197.
Damari-Weissler H, Kandel-Kfir M, Gidoni D, Mett A, Belausov E,
Granot D. 2006. Evidence for intracellular spatial separation of
hexokinases and fructokinases in tomato plants. Planta 224, 1495–1502.
Damari-Weissler H, Rachamilevitch S, Aloni R, German MA,
Cohen S, Zwieniecki MA, Michele Holbrook N, Granot D. 2009.
LeFRK2 is required for phloem and xylem differentiation and the
transport of both sugar and water. Planta 230, 795–805.
da-Silva WS, Rezende GL, Galina A. 2001. Subcellular distribution
and kinetic properties of cytosolic and non-cytosolic hexokinases in
maize seedling roots: implications for hexose phosphorylation. Journal
of Experimental Botany 52, 1191–1201.
David-Schwartz R, Weintraub L, Vidavski R, Zemach H,
Murakhovsky L, Swartzberg D, Granot D. 2013. The SlFRK4
promoter is active only during late stages of pollen and anther
development. Plant Science 199–200, 61–70.
Davies HV, Shepherd LV, Burrell MM, et al. 2005. Modulation
of fructokinase activity of potato (Solanum tuberosum) results in
substantial shifts in tuber metabolism. Plant Cell Physiology 46,
1103–1115.
Dejardin A, Leple JC, Lesage-Descauses MC, Costa G, Pilate G.
2004. Expressed sequence tags from poplar wood tissues—a
comparative analysis from multiple libraries. Plant Biology 6, 55–64.
Dennis DT, Blakeley SD. 2000. Carbohydrate metabolism. In:
Buchanan BB, Gruissem W, Jones RL, eds. Biochemistry and
HXK and FRK and plant physiology | 817
molecular biology of plants . Rockville, MD: American Society of Plant
Physiologists, 676–728.
and stomatal aperture size in the apoplastic phloem loader Vicia faba
L. Plant, Cell & Environment 30, 551–558.
Edwards D. 1993. Cells and tissues in the vegetative sporophytes of
early land plants. New Phytologist 125, 225–247.
Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC,
Raghothama KG. 2007. Phosphate starvation responses are
mediated by sugar signaling in Arabidopsis. Planta 225, 907–918.
Forde BG. 2002a. Local and long-range signalling pathways regulating
plant responses to nitrate. Annual Review of Plant Biology 53, 203–224.
Forde BG. 2002b. The role of long-distance signalling in plant
responses to nitrate and other nutrients. Journal of Experimental
Botany 53, 39–43.
Fulda S, Mikkat S, Stegmann H, Horn R. 2011. Physiology and
proteomics of drought stress acclimation in sunflower (Helianthus
annuus L.). Plant Biology (Stuttgart) 13, 632–642.
German MA, Asher I, Petreikov M, Dai N, Schaffer AA,
Granot D. 2004. Cloning, expression and characterization of LeFRK3,
the fourth tomato (Lycopersicon esculentum Mill.) gene encoding
fructokinase. Plant Science 166, 285–291.
German MA, Dai N, Matsevitz T, Hanael R, Petreikov M,
Bernstein N, Ioffe M, Shahak Y, Schaffer AA, Granot D. 2003.
Suppression of fructokinase encoded by LeFRK2 in tomato stem
inhibits growth and causes wilting of young leaves. The Plant Journal
34, 837–846.
Giese JO, Herbers K, Hoffmann M, Klosgen RB, Sonnewald U.
2005. Isolation and functional characterization of a novel plastidic
hexokinase from Nicotiana tabacum. FEBS Letters 579, 827–831.
Goren S, Huber SC, Granot D. 2011. Comparison of a novel
tomato sucrose synthase, SlSUS4, with previously described
SlSUS isoforms reveals distinct sequence features and differential
expression patterns in association with stem maturation. Planta 233,
1011–1023.
Gotow K, Taylor S, Zeiger E. 1988. Photosynthetic carbon fixation
in guard cell protoplasts of Vicia faba L.: evidence from radiolabel
experiments. Plant Physiology 86, 700–705.
Granot D. 2007. Role of tomato hexose kinases. Functional Plant
Biology 34, 564–570.
Granot D. 2008. Putting plant hexokinases in their proper place.
Phytochemistry 69, 2649–2654.
Karve A, Rauh BL, Xia X, Kandasamy M, Meagher RB, Sheen J,
Moore BD. 2008. Expression and evolutionary features of the
hexokinase gene family in Arabidopsis. Planta 228, 411–425.
Karve R, Lauria M, Virnig A, Xia X, Rauh BL, Moore BD.
2010. Evolutionary lineages and functional diversification of plant
hexokinases. Molecular Plant 3, 334–346.
Kelly G, David-Schwartz R, Sade N, Moshelion M, Levi A,
Alchanatis V, Granot D. 2012. The pitfalls of transgenic selection
and new roles of AtHXK1: a high level of AtHXK1 expression
uncouples hexokinase1-dependent sugar signaling from exogenous
sugar. Plant Physiology 159, 47–51.
Kelly G, Moshelion M, David-Schwartz R, Halperin O, Wallach R,
Attia Z, Belausov E, Granot D. 2013. Hexokinase mediates stomatal
closure. The Plant Journal 75, 977–988.
Kim YM, Heinzel N, Giese JO, Koeber J, Melzer M, Rutten T,
von Wiren N, Sonnewald U, Hajirezaei MR. 2013. A dual role
of tobacco hexokinase 1 in primary metabolism and sugar sensing.
Plant, Cell & Environment doi: 10.1111/pce.12060 [Epub ahead of
print].
Klein D, Stitt M. 1998. Effects of 2-deoxyglucose on the expression
of rbcS and the metabolism of Chenopodium rubrum cell-suspension
cultures. Planta 205, 223–234.
Klotz KL, Finger FL, Anderson MD. 2006. Wounding increases
glycolytic but not soluble sucrolytic activities in stored sugarbeet root.
Postharvest Biology and Technology 41, 48–55.
Laby RJ, Kincaid MS, Kim D, Gibson SI. 2000. The Arabidopsis
sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid
synthesis and response. The Plant Journal 23, 587–596.
Lawson T. 2009. Guard cell photosynthesis and stomatal function.
New Phytologist 181, 13–34.
Granot D, David-Schwartz R, Kelly G. 2013. Hexose kinases and
their role in sugar-sensing and plant development. Frontiers in Plant
Science 4, 44.
Le Hir R, Pelleschi-Travier S, Viemont JD, LeDuc N. 2005.
Sucrose synthase expression pattern in the rhythmically growing
shoot of common oak (Quercus robur L.). Annals of Forest Science
62, 585–591.
Guglielminetti L, Morita A, Yamaguchi J, Loreti E, Perata P,
Alpi A. 2006. Differential expression of two fructokinases in Oryza
sativa seedlings grown under aerobic and anaerobic conditions.
Journal of Plant Research 119, 351–356.
Lejay L, Gansel X, Cerezo M, Tillard P, Muller C, Krapp A, von
Wiren N, Daniel-Vedele F, Gojon A. 2003. Regulation of root ion
transporters by photosynthesis: functional importance and relation
with hexokinase. Plant Cell 15, 2218–2232.
Jang JC, Leon P, Zhou L, Sheen J. 1997. Hexokinase as a sugar
sensor in higher plants. Plant Cell 9, 5–19.
Lejay L, Wirth J, Pervent M, Cross JM, Tillard P, Gojon A. 2008.
Oxidative pentose phosphate pathway-dependent sugar sensing as a
mechanism for regulation of root ion transporters by photosynthesis.
Plant Physiology 146, 2036–2053.
Jang JC, Sheen J. 1994. Sugar sensing in higher plants. Plant Cell
6, 1665–1679.
Kandel-Kfir M, Damari-Weissler H, German MA, Gidoni D,
Mett A, Belausov E, Petreikov M, Adir N, Granot D. 2006. Two
newly identified membrane-associated and plastidic tomato HXKs:
characteristics, predicted structure and intracellular localization. Planta
224, 1341–1352.
Kang Y, Outlaw WH, Jr., Andersen PC, Fiore GB. 2007. Guard-cell
apoplastic sucrose concentration—a link between leaf photosynthesis
Leon P, Sheen J. 2003. Sugar and hormone connections. Trends in
Plant Science 8, 110–116.
Li P, Wind JJ, Shi X, Zhang H, Hanson J, Smeekens SC, Teng S.
2011. Fructose sensitivity is suppressed in Arabidopsis by the
transcription factor ANAC089 lacking the membrane-bound domain.
Proceedings of the National Academy of Sciences, USA 108,
3436–3441.
818 | Granot et al.
Lillo C. 2008. Signalling cascades integrating light-enhanced nitrate
metabolism. Biochemistry Journal 415, 11–19.
Lloyd FE. 1908. The physiology of stomata. Carnegie Institute
Washington Year Book 82, 1–142.
Matic S, Akerlund HE, Everitt E, Widell S. 2004. Sucrose synthase
isoforms in cultured tobacco cells. Plant Physiology and Biochemistry
42, 299–306.
Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I,
Jones T, Sheen J. 2003. Role of the Arabidopsis glucose sensor HXK1
in nutrient, light, and hormonal signaling. Science 300, 332–336.
Morell M, Copeland L. 1985. Sucrose synthase of soybean nodules.
Plant Physiology 78, 149–154.
Muller R, Nilsson L, Nielsen LK, Nielsen TH. 2005. Interaction
between phosphate starvation signalling and hexokinase-independent
sugar sensing in Arabidopsis leaves. Physiologia Plantarum 124,
81–90.
Nairn CJ, Lennon DM, Wood-Jones A, Nairn AV, Dean JF.
2008. Carbohydrate-related genes and cell wall biosynthesis in
vascular tissues of loblolly pine (Pinus taeda). Tree Physiology 28,
1099–1110.
Nolte KD, Hendrix DL, Radin JW, Koch KE. 1995. Sucrose
synthase localization during initiation of seed development and
trichome differentiation in cotton ovules. Plant Physiology 109,
1285–1293.
Odanaka S, Bennett AB, Kanayama Y. 2002. Distinct physiological
roles of fructokinase isozymes revealed by gene-specific suppression
of frk1 and frk2 expression in tomato. Plant Physiology 129,
1119–1126.
Olsson T, Thelander M, Ronne H. 2003. A novel type of chloroplast
stromal hexokinase is the major glucose-phosphorylating enzyme in
the moss Physcomitrella patens. Journal of Biological Chemistry 278,
44439–44447.
Plomion C, Pionneau C, Brach J, Costa P, Bailleres H. 2000.
Compression wood-responsive proteins in developing xylem of
maritime pine (Pinus pinaster Ait.). Plant Physiology 123, 959–969.
Poethig RS. 1990. Phase change and the regulation of shoot
morphogenesis in plants. Science 250, 923–930.
Poffenroth M, Green DB, Tallman G. 1992. Sugar concentrations
in guard cells of Vicia faba illuminated with red or blue light: analysis
by high performance liquid chromatography. Plant Physiology 98,
1460–1471.
Poorter H, Nagel O. 2000. The role of biomass allocation in the
growth response of plants to different levels of light, CO2, nutrients
and water: a quantitative review. Australian Journal of Plant Physiology
27, 595–607.
Ramon M, Rolland F, Sheen J. 2008. Sugar sensing and signaling.
Arabidopsis Book 6, e0117.
Ramon M, Rolland F, Thevelein JM, Van Dijck P, Leyman B.
2007. ABI4 mediates the effects of exogenous trehalose on
Arabidopsis growth and starch breakdown. Plant Molecular Biology
63, 195–206.
Raven JA. 2002. Selection pressures on stomatal evolution. New
Phytologist 153, 371–386.
Roach M, Gerber L, Sandquist D, et al. 2012. Fructokinase is
required for carbon partitioning to cellulose in aspen wood. The Plant
Journal 70, 967–977.
Roelfsema MR, Hedrich R. 2005. In the light of stomatal opening:
new insights into ‘the Watergate’. New Phytologist 167, 665–691.
Rognoni S, Teng S, Arru L, Smeekens SCM, Perata P. 2007.
Sugar effects on early seedling development in Arabidopsis. Plant
Growth Regulation 52, 217–228.
Rolland F, Baena-Gonzalez E, Sheen J. 2006. Sugar sensing and
signaling in plants: conserved and novel mechanisms. Annual Review
of Plant Biology 57, 675–709.
Outlaw WH. 2003. Integration of cellular and physiological
functions of guard cells. Critical Reviews in Plant Sciences 22,
503–529.
Schafer WE, Rohwer JM, Botha FC. 2004. Protein-level expression
and localization of sucrose synthase in the sugarcane culm.
Physiologia Plantarum 121, 187–195.
Pandey S, Zhang W, Assmann SM. 2007. Roles of ion channels
and transporters in guard cell signal transduction. FEBS Letters 581,
2325–2336.
Schaffer AA, Petreikov M. 1997a. Inhibition of fructokinase and
sucrose synthase by cytosolic levels of fructose in young tomato fruit
undergoing transient starch synthesis. Physiologia Plantarum 101,
800–806.
Paul M. 2007. Trehalose 6-phosphate. Current Opinion in Plant
Biology 10, 303–309.
Pego JV, Smeekens SC. 2000. Plant fructokinases: a sweet family
get-together. Trends in Plant Sciency 5, 531–536.
Schaffer AA, Petreikov M. 1997b. Sucrose-to-starch metabolism
in tomato fruit undergoing transient starch accumulation. Plant
Physiology 113, 739–746.
Pego JV, Weisbeek PJ, Smeekens SC. 1999. Mannose inhibits
Arabidopsis germination via a hexokinase-mediated step. Plant
Physiology 119, 1017–1023.
Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D. 2001.
Guard cell signal transduction. Annual Review of Plant Physiology and
Plant Molecular Biology 52, 627–658.
Péron T, Véronési C, Mortreau E, Pouvreau J-B, Thoiron S,
Leduc N, Delavault P, Simier P. 2011. Role of the sucrose
synthase-encoding PrSus1 gene in the development of the parasitic
plant Phelipanche ramosa L. (Pomel). Molecular Plant-Microbe
Interactions 25, 402–411.
Sergeeva LI, Vreugdenhil D. 2002. In situ staining of activities of
enzymes involved in carbohydrate metabolism in plant tissues. Journal
of Experimental Botany 53, 361–370.
Petreikov M, Dai N, Granot D, Schaffer AA. 2001. Characterization
of native and yeast-expressed tomato fruit fructokinase enzymes.
Phytochemistry 58, 841–847.
Smeekens S, Ma J, Hanson J, Rolland F. 2010. Sugar signals and
molecular networks controlling plant growth. Current Opinion in Plant
Biology 13, 274–279.
Smith AM, Zeeman SC, Smith SM. 2005. Starch degradation.
Annual Review of Plant Biology 56, 73–98.
HXK and FRK and plant physiology | 819
Smith H. 1982. Light quality, photoperception, and plant strategy.
Annual Review of Plant Physiology 33, 481–518.
drought stress tolerance in Arabidopsis and is involved in abscisic
acid-induced stomatal closure. Plant Physiology 161, 1158–1171.
Smith JAC. 1991. Ion-transport and the transpiration stream.
Botanica Acta 104, 416–421.
Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T,
Franke A, Feil R, Lunn JE, Stitt M, Schmid M. 2013. Regulation of
flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana.
Science 339, 704–707.
Stitt M, Lunn J, Usadel B. 2010. Arabidopsis and primary
photosynthetic metabolism—more than the icing on the cake. The
Plant Journal 61, 1067–1091.
Sung SJ, Kormanik PP, Black CC. 1993. Vascular cambial sucrose
metabolism and growth in loblolly pine (Pinus taeda L.) in relation to
transplanting stress. Tree Physiology 12, 243–258.
Swartzberg D, Hanael R, Granot D. 2011. Relationship between
hexokinase and cytokinin in the regulation of leaf senescence and
seed germination. Plant Biology 13, 439–444.
Talbott LD, Zeiger E. 1993. Sugar and organic acid accumulation
in guard cells of Vicia faba in response to red and blue light. Plant
Physiology 102, 1163–1169.
Talbott LD, Zeiger E. 1996. Central roles for potassium and sucrose
in guard-cell osmoregulation. Plant Physiology 111, 1051–1057.
Wingler A, Purdy S, MacLean JA, Pourtau N. 2006. The role of
sugars in integrating environmental signals during the regulation of leaf
senescence. Journal of Experimental Botany 57, 391–399.
Wingler A, Roitsch T. 2008. Metabolic regulation of leaf senescence:
interactions of sugar signalling with biotic and abiotic stress
responses. Plant Biology (Stuttgart) 10 (Suppl. 1), 50–62.
Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig
RS. 2009. The sequential action of miR156 and miR172 regulates
developmental timing in Arabidopsis. Cell 138, 750–759.
Xiao W, Sheen J, Jang JC. 2000. The role of hexokinase in plant
sugar signal transduction and growth and development. Plant
Molecular Biology 44, 451–461.
Talbott LD, Zeiger E. 1998. The role of sucrose in guard cell
osmoregulation. Journal of Experimental Botany 49, 329–337.
Yang L, Conway SR, Poethig RS. 2011. Vegetative phase change
is mediated by a leaf-derived signal that represses the transcription of
miR156. Development 138, 245–249.
Tallman G, Zeiger E. 1988. Light quality and osmoregulation in Vicia
guard cells: evidence for involvement of three metabolic pathways.
Plant Physiology 88, 887–895.
Yang L, Xu M, Koo Y, He J, Poethig RS. 2013. Sugar promotes
vegetative phase change in Arabidopsis thaliana by repressing the
expression of MIR156A and MIR156C. eLife 2.
Tomlinson PT, Duke ER, Nolte KD, Koch KE. 1991. Sucrose
synthase and invertase in isolated vascular bundles. Plant Physiology
97, 1249–1252.
Yu S, Cao L, Zhou C-M, Zhang T-Q, Lian H, Sun Y, Wu J,
Huang J, Wang G, Wang J-W. 2013. Sugar is an endogenous cue
for juvenile-to-adult phase transition in plants. eLife 2.
Trevisan S, Borsa P, Botton A, Varotto S, Malagoli M, Ruperti B,
Quaggiotti S. 2008. Expression of two maize putative nitrate
transporters in response to nitrate and sugar availability. Plant Biology
(Stuttgart) 10, 462–475.
Zhao C, Craig JC, Petzold HE, Dickerman AW, Beers EP. 2005.
The xylem and phloem transcriptomes from secondary tissues of the
Arabidopsis root-hypocotyl. Plant Physiology 138, 803–818.
Van Dijken AJ, Schluepmann H, Smeekens SC. 2004.
Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal
vegetative growth and transition to flowering. Plant Physiology 135,
969–977.
Van Houtte H, Vandesteene L, Lopez-Galvis L, et al. 2013.
Overexpression of the trehalase gene AtTRE1 leads to increased
Zhou L, Jang JC, Jones TL, Sheen J. 1998. Glucose and ethylene
signal transduction crosstalk revealed by an Arabidopsis glucoseinsensitive mutant. Proceedings of the National Academy of Sciences,
USA 95, 10294–10299.
Zorb C, Schmitt S, Muhling KH. 2011. Proteomic changes in
maize roots after short-term adjustment to saline growth conditions.
Proteomics 10, 4441–4449.