Download Transport of primary metabolites across the plant vacuolar membrane

FEBS Letters 581 (2007) 2223–2226
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Transport of primary metabolites across the plant vacuolar membrane
H. Ekkehard Neuhaus*
Pflanzenphysiologie, Technische Universitat Kaiserslautern, Postfach 3049, D-67653 Kaiserslautern, Germany
Received 16 January 2007; revised 2 February 2007; accepted 3 February 2007
Available online 12 February 2007
Edited by Ulf-Ingo Flügge and Julian Schroeder
Abstract Mesophyll cells and most types of storage cells harbor
large central vacuoles representing the main cellular store for
sugars and other primary metabolites like carboxylic- or and
amino acids. The general biochemical characteristics of sugar
transport across the vacuolar membrane are already known since
a couple of years but only recently the first tonoplast sugar
carriers have been identified on the molecular level. A candidate
sucrose carrier has been identified in a proteomic approach. In
Arabidopsis, the tonoplast monosaccharide transporters (TMT)
represent a small protein family comprising only three members,
which reside in the vacuolar membrane. Two of three tmt genes
are induced upon cold, drought or salt stress and tmt knock out
mutants exhibit altered monosaccharide levels upon cold induction. These observations indicate that TMT proteins represent
the first examples of tonoplast sugar carriers involved in the cellular response upon osmotic stress stimuli.
Ó 2007 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved.
Keywords: Vacuole; Carboxylic-acid; Sugar transporters
1. General features of central vacuoles
Central vacuoles are surprisingly large, can occupy (e.g. in
CAM plants or fruit tissues) more than 80% of the total cell
volume [1] and are separated from the surrounding cytosol
by a single, semi-permeable membrane, the so called tonoplast.
Already these facts make the central vacuole uniquely suited to
fulfill essential storage functions. Therefore, it is not surprising
that the number of different inorganic and organic solutes
found in the vacuole is extremely large. In fact, the substantial
structural and functional diversity of compounds stored in the
vacuole identifies this organelle as a core structure in plant cells
important for processes like the cellular energy management,
accumulation of reserves and nutrients, regulation of cellular
pressure, detoxification and ecological interactions.
Several of the compounds given below accumulate via secondary active transporters in the vacuole against an existing
concentration gradient. The driving forces for these carriers
are either a proton- or an electrochemical gradient generated
*
Fax: +49 631 2052600.
E-mail address: [email protected]
Abbreviations: AtTMT, Arabidopsis thaliana tonoplast monosaccharide transporter; AtTDT, Arabidopsis thaliana tonoplast dicarboxylate
transporter
by the activity of two types of proton pumps; a vacuolar-type
(V-type) H+-ATPase and a H+-PPiase [2–5]. As far as we
know, these two proton pumps are present in all types of plant
vacuoles [6,4,7].
Organic compounds which typically accumulate in central
vacuoles are e.g. carbohydrates like mono- and disaccharides
(for details see below), linear and cyclic polyols, three types
of fructans with slightly different structures and various carboxylic acids [8–12]. Malate, citrate and fumarate enter the
vacuole via specific transport proteins and represent major carboxylic acids in plants [13–15]. For malate two distinct transport mechanisms have been identified: this dicarboxylic acid
enters the vacuole either by a anion channel specific for
malate2 [16], or by a recently identified solute carrier [17]
(Fig. 1). The latter carrier joins structurally the family of the
so called sodium-coupled carboxylate carriers as present in
the plasma membrane of animal cells [18]. Interestingly, the
absence of the Arabidopsis homolog AtTDT (Arabidopsis thaliana tonoplast dicarboxylate transporter) alters both, the
metabolism of organic acids and the regulation of the cytosolic
pH substantially [19] without affecting the phenotype of the
corresponding knock out mutant lines when compared with
wild-type plants [17].
Central vacuoles also play a critical role in plant nutrition
because they accumulate sulfate, phosphate and nitrate
[20,21]. Not only nitrate, which serves as the precursor for amino acid synthesis, but also the intermediate and toxic ammonia
molecule [22], and the final amino acids themselves are stored
in the central vacuoles [23,24]. The observation that the vacuolar concentration of several amino acids is lower than in the
surrounding cytosol [25] is, however, not consistent with the
facilitated diffusion mode of transport catalyzed by reconstituted tonoplastic amino-acid carrier activity [26]. The first candidate amino acid carriers have been identified in the proteome
of Arabidopsis mesophyll tonoplasts or as transporter-GFP
fusion proteins after transient transformation [27,28]. It will
be interesting to analyze the biochemical properties of corresponding recombinant proteins in the near future.
In addition to the compounds above, ecological relevant
solutes like anthocyans, flavonoids and a wide array of conjugated endogenously synthesized toxic- or xenobiotic compounds typically accumulate in the vacuole and several of
these substances cross the tonoplast via ABC-type carriers
[29–32]. Thus in sum, there is no other cellular compartment
harboring a comparable large number of different solutes
(see [33] for a recent complete overview).
In this review I will focus only on the transport of one class
of compounds, namely sugars in form of the disaccharide
0014-5793/$32.00 Ó 2007 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.febslet.2007.02.003
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Fig. 1. Sugar and malate transport processes across the tonoplast from
Arabidopsis vacuoles.
sucrose or in form of the monosaccharides glucose and fructose. This is because carriers involved in the vacuolar transport
of these compounds have been very recently identified on the
molecular level.
2. Transport of mono- and disaccharides across the tonoplast
The ability for net sugar synthesis represents a main feature
of plant physiology. Sugars fulfill a remarkable number of
essential functions as they are a general source for metabolic
energy, serve as a precursor for starch and cellulose synthesis,
and are a metabolic starting point of carboxylate- and amino
acid synthesis [34]. Therefore, it is not surprising that cells
from all types of organisms control the endogenous sugar levels and percept the actual concentrations via sophisticated
sensing systems [35–37].
The vacuole stores large concentrations of the disaccharide
sucrose, but also the monosaccharides glucose and fructose
are typically present in high levels [38]. In vacuoles from leaves
of C3- and CAM species sucrose import occurs by an ATP
independent mechanism solely driven by the existing concentration gradient between the cytosol and the vacuolar lumen
[39,40] (Fig. 1). In contrast, vacuoles from sugar beet taproots
seem to exploit the existing proton-motive force to import sucrose via an H+ antiport mechanism against the concentration
gradient [41] (Fig. 1).
Given that sucrose accumulation in the vacuoles is of high
importance for the control of photosynthesis [42] and for primary metabolism in storage tissues [38] it appears surprising
that no corresponding proteins have so far been characterized
on both, the functional and molecular level. A genome analysis
indicated that Arabidopsis harbours about ten disaccharide
transporter isoforms [51], but only a recent examination of
the proteome of vacuolar membranes purified from barley or
Arabidopsis cells provided first evidence on the molecular nature of a vacuolar sucrose carrier [43].
The barley carrier protein HvSUT2 and the Arabidopsis carrier AtSUT4 catalyze sucrose uptake into yeast cells expressing
the corresponding gene [44,45]. Interestingly, both of these
proteins, although able to mediate sucrose transport across
the yeast plasma membrane when heterologously synthesized
H.E. Neuhaus / FEBS Letters 581 (2007) 2223–2226
in yeast, are located in the plant tonoplast [43] (Fig. 1). This
location has been substantiated by two approaches: Firstly,
corresponding HvSUT4- and AtSUT4-GFP constructs, transiently expressed in either Arabidopsis- or onion cells, clearly
decorate the tonoplast and not the plasma membrane [43]. Secondly, transcripts coding for AtSUT4 specifically accumulate
in mesophyll cells and not in the smaller companion cells, or
in the chloroplast-free sieve element cells [43]. Mesophyll cell
vacuoles represent the main store for sucrose synthesized
during photosynthesis. However, since both, HvSUT4 and
AtSUT4 catalyze a H+/sucrose cotransport when recombinantly synthesized in yeast [44,45] we have to assume that
(due to the existing proton gradient, see above and Fig. 1)
these carriers are involved in sucrose export from the vacuole
into the cytosol.
Besides sucrose the monosaccharides glucose and fructose
are typically present the vacuole [46]. In some tissue, e.g. grape
berries [47], glucose represents the main storage sugar and
both, facilitated diffusion as well as energized proton/sugar
antiport mechanisms have been described for glucose uptake
into isolated vacuoles, or into tonoplast vesicles prepared from
various plant species [48,49] (Fig. 1).
PCR amplification using primers directed against conserved
domains allowed to identify a so far unknown putative hexose
carrier from sugar beet [50]. By use of two independent peptide
specific antibodies it was possible to locate the corresponding
protein, exhibiting a calculated molecular mass of 54 kDa, in
enriched vacuolar membranes from both, transgenic tobacco
(expressing the sugar beet gene) and native sugar beet tissue
[50]. However, since all attempts to synthesize a functional recombinant transport protein in yeast failed unfortunately [50],
the exact transport activity of this carrier remains to be analyzed.
The Arabidopsis genome contains about 60 genes coding for
monosaccharide transporter isoforms and more than ten of
these proteins have been characterized as plasma membrane
located monosaccharide importers [51,52]. Within these large
monosaccharide family a small group comprising only three
isoforms exhibits unique structural characteristics. These carriers, named Arabidopsis thaliana tonoplast monosaccharide
transporter, AtTMT [53], exhibit about 12 predicted transmembrane domains, as known from other carriers belonging
to the major facilitator superfamily [54], but harbour an
extraordinarily long, hydrophilic loop connecting trans-membrane domains six and seven [53]. This loop comprises up to
320 amino acids in length and is therefore 4–5 times longer
than the corresponding loop domain in other so far known
monosaccharide transport proteins. A specific function of this
loop domain is so far unclear, but it appears remarkable that
in the central portion of this loop a strong negative cluster,
built up by 11 aspartate residues in a stretch of only 20 amino
acids, is present [53]. Interestingly, such negatively charged
clusters (also built by aspartate residues) of unknown function
are also present in a wide number of mitogen-activated protein
kinases (data not shown).
AtTMT-GFP fusion proteins of all three isoforms are directed into the vacuolar membrane after heterologous transient
expression in either tobacco- or onion cells and promoter–reporter data revealed that Attmt genes are active in sugar storing mesophyll cells [53] (Fig. 1). These results are completely in
line with proteomic data made on vacuolar membranes from
Arabidopsis mesophyll cells revealing the presence of AtTMT1
H.E. Neuhaus / FEBS Letters 581 (2007) 2223–2226
and AtTMT2 [27]. The absence of AtTMT3 in the detectable
proteome of Arabidopsis tonoplasts [27] concurs with the generally extremely low expression level of the third Attmt gene
under every condition tested [53].
A detailed expression analysis of all three Attmt genes
showed that both, Attmt1 and Attmt2 represent cold induced
genes, which are also responsive upon drought and salt stress
[53]. Interestingly, these three stress stimuli usually lead to an
accumulation of solutes, including sugars, in Arabidopsis
leaves [55–57] and since most of the sugars in mesophyll cells
accumulate in the vacuole [1,25], it is very likely that AtTMT
proteins contribute to the molecular response of Arabidopsis
upon osmotic stress. The observation that vacuoles isolated
from cold induced Arabidopsis wild type leaves exhibit a
markedly increased glucose transport rate when compared
with the properties of vacuoles from plants grown under moderate temperatures [53] further supports this assumption.
Clear evidence for the involvement of AtTMT proteins in
vacuolar monosaccharide transport has been gained by comparing the glucose uptake properties of vacuoles isolated from
either, wild type plants or from knock out lines. The absence of
a functional Attmt1 gene reduced the cold stimulated glucose
transport to about 1/3 of the transport observed on wild type
vacuoles [53]. As cold stimulated glucose transport into wild
type vacuoles is inhibited by fructose and the uncoupler compound ammonia it is very likely, that both types of monosaccharides are transported by AtTMT in a proton/sugar antiport
mode of transport.
The latter observations are somehow surprising given that
relatively close structural AtTMT homologs reside in the plasma membrane of cyanobacteria like Synechocystis spec. [58] or
Nostoc punctiforme (data not shown). The transporter from
Synechocystis spec., named SsGTR, is characterized to exert
a comparable high degree of specificity for glucose and to catalyze a proton coupled sugar import into the bacterial cell [58].
Thus, it will be interesting in the near future to identify the
structural determinants for such altered transport characteristics. However, in this context it has to be considered that even
small structural modifications in a transport protein might affect the mode of transport (e.g. antiport to uniport) drastically
[59].
3. What’s next to do?
As outlined above, first transport proteins involved in the
movement of monosaccharides across the tonoplast have been
identified. These transporters, belonging to the TMT group,
obviously mediate a proton-coupled antiport mechanism, but
the tonoplast contains in addition a glucose facilitator protein
of unknown molecular structure. On the basis of the available
proteomic information, this facilitator protein and further carbohydrate transport proteins might become identified in the
near future. Another challenging topic is the establishment
of a suitable recombinant system allowing the identification
of the biochemical properties of the carriers in more detail.
However, this aim seems currently difficult to approach since
the level of recombinant tonoplast proteins in heterologous
systems appear to be extremely low. Moreover, it is totally
unknown whether covalent modifications occurring in the
ER or Golgi compartment are required for function. A third
challenging task is the analysis of post-translational regulation
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of sugar transporters. Corresponding processes might involve
protein/protein interactions which have to be analyzed by
use of genetic and biochemical methods. It is very likely, that
research on the vacuolar membrane will lead to novel carrier
proteins and uncover so far unknown regulatory properties.
Acknowledgement: The author gratefully acknowledges the financial
support by the Deutsche Forschungsgemeinschaft.
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