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Source–sink regulation by sugar and stress
Thomas Roitsch
The regulation of carbon partitioning between source and
sink tissues in higher plants is not only important for plant
growth and development, but insight into the underlying
regulatory mechanism is also a prerequisite to modulating
assimilate partitioning in transgenic plants. Hexoses, as well
as sucrose, have been recognised as important signal
molecules in source–sink regulation. Components of the
underlying signal transduction pathways have been
identified and parallels, as well as distinct differences, to
known pathways in yeast and animals have become
apparent. There is accumulating evidence for crosstalk,
modulation and integration between signalling pathways
responding to phytohormones, phosphate, light, sugars, and
biotic and abiotic stress-related stimuli. These complex
interactions at the signal transduction levels and coordinated regulation of gene expression seem to play a
central role in source–sink regulation.
Addresses

Lehrstuhl für Zellbiologie und Pflanzenphysiologie, Universitaet
Regensburg,Universitaetsstrasse 31, D-93053 Regensburg, Germany;
e-mail: thomas.roitsch@biologie.uni-regensburg.de
Current Opinion in Plant Biology 1999, 2:198–206
http://biomednet.com/elecref/1369526600200198
© Elsevier Science Ltd ISSN 1369-5266

Introduction
Higher plants develop from an embryo which depends
on heterotrophic metabolism of storage products. During
the growth and differentiation of a plant, photosynthetically active source tissues (mature leaves) develop. They
export carbohydrates to photosynthetically less active or
inactive sink tissues such as roots, fruits or tubers, which
are characterised by a net import of sugars; however, this
physiological mosaic is not static. The plant life cycle is
accompanied by source–sink transitions as well as
changes with respect to the sink strength of individual
organs and the number of sink organs competing for a
common pool of carbohydrates. In addition, exogenous
factors such as abiotic stress or pathogen infection may

also influence carbohydrate partitioning. Thus, complex
mechanisms have to be assumed which integrate the
expression of enzymes involved in carbohydrate production in source tissues with utilisation in sink tissues.
These regulatory mechanisms ultimately determine the
pattern of carbon allocation between the different plant
organs and regulate source–sink transitions. The regulation of carbohydrate partitioning has attracted a lot of
attention in the past few years. Insight into these mechanisms is not only important for understanding plant
growth and development, but it is also a prerequisite for
the genetic manipulation of source–sink relations in
transgenic plants to increase crop yield.

This review will focus on two aspects of source–sink regulation which are of particular importance: metabolic
regulation by sugars, and the effect of stress-related exogenous stimuli. It has been recognised in the past ten years
that sugars not only function as substrate to sustain the
heterotrophic growth of sink tissues, but are also important
signalling molecules that regulate both source and sink
metabolism. In addition, both abiotic and biotic stressrelated stimuli have profound effects on plant growth and
development and are responsible for considerable loss of
crop yield. An increasing number of studies are focused on
the elucidation of the molecular mechanisms that link the

effect of diverse stress stimuli to source–sink regulation.

Source–sink regulation by sugars
Feedback inhibition of photosynthesis as a result of
decreased sink demand is a long known phenomenon.
Different experimental approaches have shown that sugars play a key role in this regulatory mechanism by
repressing the expression of photosynthetic genes [1].
The specific inhibitory effect of sugars on photosynthesis or on the expression of photosynthetic genes is
further supported by recent studies which included
some monocotyledonous species [2–4], whereas most
previous studies concentrated on dicotyledonous plants.
This feedback inhibition suggested that assimilates
function as link between source and sink tissues. Indeed,
sugars were shown to induce transcription of a number of
sink specific enzymes involved in sucrose breakdown
and metabolism and storage product synthesis [1,5•,6,7].
The co-ordinated and inverse regulation of mRNA levels
of a photosynthetic enzyme and a sink specific enzyme
in the same experiment has been demonstrated in glucose treated photoautotrophic cultures of Chenopodium
rubrum. The induction of the mRNA for the sink specific extracellular invertase by glucose showed the same

time course and concentration dependence as the repression of the mRNA for the small subunit of the
ribulosebisphosphate-carboxylase [8•].
So far, most studies on source–sink regulation by sugars
have concentrated on the effect of exogenously added
sugars to protoplasts, suspension culture cells, and isolated tissues, or the analysis of transgenic plants with
modulated carbohydrate metabolism. An alternative
experimental approach was followed by Abdin et al. [9•]
who supplied exogenous sucrose into stems of soybean
plants continuously for almost their entire life cycle
using a modified pressurised injection technique. This
sucrose supplementation suppressed photosynthesis and
had positive effects on plant growth.
The elucidation of the underlying signal transduction
pathways of source–sink-regulation is currently the major

Source-sink regulation by sugar and stress Roitsch

focus of attention. A number of studies have shown that
hexoses and sucrose can elicit sugar responses [1]. The
studies involving sucrose, however, did not address the

question as to whether sucrose itself or the readily produced hexoses were the actual inducer. Recent studies on
the nature of sugar signal molecules have shown that, in
addition to hexose signalling, sucrose-specific pathways
may be differentiated. Chiou and Bush [10•] have shown
that sucrose specifically reduces the steady state mRNA
level of a proton–sucrose symporter thought to be involved
in phloem loading. Sucrose-specific signalling pathways
were also shown to be responsible for the repression of the
Arabidopsis ATBZ bZIP transcription factor [11•] and for
the modulation of phytochrome signalling [12•]. Studies
on starch synthesis in slices of potato tubers [13] and on
seed development in transgenic Vicia narbonensis [14•] support previous suggestions that sucrose specifically induces
differentiation and storage product synthesis. Hexose sugars are thought to be important primarily to regulate
growth and mitotic activity [15].
Several studies imply a possible role of hexokinase in
sugar signalling and Jang et al. [16•] have even proposed
that hexokinase functions as a sugar sensor in higher
plants [16•]. However, there is still a matter of debate
about the role of hexokinase in sugar sensing and signalling and it has been proposed that hexokinase
dependent and independent pathways are present in

higher plants [17–19]. Some of the conflicting suggestions stem from the differential effect of
non-phosphorylatable glucose-analogues in the individual experiment system analysed. In some laboratories it
has been found that 6-desoxyglucose or 3-O-methylglucose, that are not substrates for hexokinase, are able to
trigger gene regulation, whereas in other laboratories
these compounds are inactive and only the phosphorylatable glucose analogue 2-desoxyglucose is able to elicit
the same effects as glucose [17,18,19]. The fact that the
phosphorylatable glucose analogue is able to substitute
glucose is interpreted as a direct interaction with hexokinase and a regulatory role of this enzyme in the system
analysed. The observed differential effect of non-phosphorylatable glucose analogues on gene regulation,
however, may be completely independent of a direct
interaction of the different sugar compounds with hexokinase. This may rather reflect species specific differences
in the specificity of an extracellular or membrane bound
sugar binding protein. The function of such an extracellular sugar receptor would be in agreement with all
experimental data and does not even exclude a role of a
specific hexokinase isoenzyme in the corresponding
intracellular signalling pathway, which is suggested both
by transgenic approaches [16•] and inhibitor studies [20].
Although, so far, no direct experimental evidence exists
for this hypothesis, extracellular sugar recognition in
plants would be backed by the study of Herbers and

Sonnewald and co-workers [21]. Possible paradigms for
the extracellular sugar sensing molecules are extracellular

199

sugar binding proteins in bacteria [22] and plasmamembrane bound sugar transporters in yeast [23].
Different screens have yielded a number of Arabidopsis
mutants that are affected in sugar sensing and signalling
and in feedback inhibition of photosynthesis
[19,24•,25•,26]. So far, the corresponding target gene has
been identified only from the highly pleiotropic mutant
prl1 (pleiotropic regulatory locus-1) that causes sugar hypersensitivity [25•]. The prl protein was shown to be imported
into the nucleus and to interact with a nuclear import
receptor protein. Also the other mutants isolated to date
are also characterised by pleiotropic phenotypes, and this
indicates an interaction between different signalling pathways that will be discussed further below.
Transgenic plants overexpressing a heterologous invertase
from yeast, or other enzymes to modulate carbohydrate
metabolism, have greatly stimulated progress in understanding source–sink regulation [27]. Sugars accumulate to
unphysiologically high levels in these plants, however, and

the target genes are regulated by stress related stimuli and
thus are also expected to be regulated by osmotic stress
resulting from sugar accumulation (see discussion below).
It may be difficult, therefore, to differentiate between
sugar and stress responses. These problems, inherent to
the use of constitutive promoters, have been circumvented
by the use of an ethanol inducible promoter [28•].
Different components of sugar signal transduction pathways have been identified. There is increasing evidence
that mitogen-activated protein (MAP) kinase pathways are
important in plants to regulate the response to various
exogenous and endogenous stimuli [29]. Work in our group
has shown that MAP kinases are also involved in sugar signalling pathways [8•]. It has been demonstrated that in
autotrophic suspension culture cells of Chenopodium
rubrum a myelin basic protein phosphorylating protein
kinase is rapidly and transiently activated in response to
the metabolic stimulus glucose. This finding indicates that
different plant signalling pathways may have a common
origin and the apparent parallels to pathogen activated
pathways may also help to unravel the components of
sugar related signalling pathways. The importance of protein phosphorylation in regulating sink specific

metabolism is also demonstrated by the identification of a
calcium-dependent protein kinase in maize which is active
only in sink tissues [30•]. It has also been shown that a calcium-dependent protein kinase of tobacco that is
associated with the plasma membrane is inducible by
sucrose [31]. The latter two studies further suggest that
calcium may be involved in source–sink regulation as a
secondary messenger which has also been suggested on
the basis of pharmacological studies (summarised in [18]).
Parallels of plant sugar signalling pathways to the well
characterised catabolite repression system in yeast are suggested by the identification and function of SNF-1-related
protein kinases in plants [32,33]. Antisense repression of

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SNF-1-related protein kinases was shown to result in loss
of sugar inducibility of sucrose synthase [34•]. These studies indicate that proteins homologous to the SNF-1 kinase
of yeast may have a function in sugar signalling of higher
plants. However, future studies will be required to prove

the speculations that plant SNF-1 related proteins are
global regulators of carbon metabolism in plants [35] and
that they even integrate cytokinin, light, glucose and
brassinosteroid signalling [36].
By functional dissection of sugar regulated promoters it has
been possible to identify cis-acting regulatory sequences
required for sugar regulated gene expression
[37,38,39•,40]. These results will be important to elucidate
whether positively and negatively regulated promoters
share the same regulatory sequences and thus are regulated by the same transcription factors. Furthermore, the
identified regulatory sequences may be a valuable tool to
isolate such regulatory proteins.

Source–sink regulation by stress
Stress related stimuli may be both of abiotic and biotic origin. Despite the dramatic effect of stress related stimuli on
yield in agriculture, only few studies have focused on the
regulation of enzyme activities and transcriptional regulation of genes in response to these stimuli. Therefore, it is
difficult to compare the mostly unrelated studies on
source-sink regulation by stress related stimuli and this
section lists the recent advances sorted by the nature of the

stimuli. Future work will require to focus on the effect of
different stimuli on specific target proteins or genes to be
able to better compare the results of different studies.
Water has long been recognised as a crucial abiotic determinant of carbon allocation [41] and drought is a major
factor limiting plant distribution and productivity. Water
stress induces large alterations in source–sink relations due
to a modification of growth priorities and to a reduction of
the performance of photosynthetic organs. With respect to
the effect of water deficiency on whole plants, source limitations such as a reduced photosynthetic capacity,
resulting in a decreased export of assimilates seem to be
responsible for decreased crop load [42]. Variations in
stomatal conductance resulting in decreased water loss due
to transpiration were found to be important in stress tolerant cultivars [43,44]. A few studies have addressed the
regulation of source and sink specific enzymes in response
to drought. It has been shown that as water deficit is
increased in discs of potato tubers, there is a progressive
inhibition of starch synthesis [45]. This was also observed
in peach seedlings where it appears to be caused by the
inhibition of photosynthesis [46]. Different studies
demonstrated an effect of water stress on soluble acid
invertase that is thought to mobilise sucrose stored in the
vacuole. It has been shown that induction of male sterility
in wheat by meiotic stage water deficit is preceded by a
decline in vacuolar invertase activity [47]. In contrast, mild
water stress in maize leaves produced an early and large
stimulation of vacuolar invertase activity which was tightly

related to the mRNA concentration for a specific vacuolar
invertase gene [48,49,50•]. The conflicting data on the regulation of vacuolar invertase may reflect tissue specific
responses as well as differences in the time point, duration
time and severity of the applied water stress which need to
be addressed in future studies. In parallel to the analyses
of the regulation of mRNA for vacuolar invertase in
response to water stress, the genetic analysis of quantitative traits associated with DNA markers in segregating
near isogenic lines has been applied to the drought
response fo maize leaves [50•]. Several quantitative trait
loci (QTLs) were detected for invertase activity in control
plants and in stress conditions, respectively. The finding
that only two QTLs were located close to the corresponding invertase gene locus indicates that other genes are also
likely to be involved in the invertase stress response and
some of them were found to form ‘stress clusters’.
Salinity is another important environmental factor resulting in suboptimal growth. Despite the far-reaching impact
in agronomic terms, however, only limited information
about the effect on plant metabolism and source–sink relations are available. It has been shown that salt stress not
only alters photosynthesis and carbohydrate levels, at least
transiently, but also alters the types of carbohydrates that
are synthesised and exported by the source tissues
[51•,52]. The proposal that alterations in the type of carboyhdrate transported in response to salt stress may act as
a (novel) sugar signalling system for acclimation responses
in the sink tissues [51•] is an interesting extension of the
concept of sugar signalling in plants but still lacks any
experimental evidence.
An important biotic stress for plants is the infection by
viruses. It has been shown that viral infection or expression
of different viral movement proteins in transgenic plants
influences photosynthesis, carbohydrate accumulation and
assimilate partitioning (reviewed in [53]).
Infection by phytopathogenic fungi may be mimicked by
the use of fungal elicitors which proved to be useful in
numerous studies to analyse early, elicitor-induced
defence responses of plant cells. The use of photoautotrophic cultures made it possible to analyse
simultaneously the effect of elicitors on defence responses
as well as source–sink relations [8•]. It has been shown that
in photoautotrophic cultures of Chenopodium rubrum the
regulation of mRNAs for representative enzymes of
defence response and source and sink metabolism are coordinately regulated. Induction of the mRNAs for the
sink-specific and defence-related enzymes, and the repression of the mRNA for the photosynthetic enzymes showed
the same time course and concentration dependence to the
fungal elicitor chitosan and two other stress stimuli.
Wounding is an other severe environmental stress to which
plants may be subjected and may come about through such
diverse causes as mechanical injury and herbivore attack.
Wounding of source leaves of Chenopodium rubrum plants

Source-sink regulation by sugar and stress Roitsch

201

Figure 1
Model for the regulation of sink metabolism,
photosynthesis and defence responses by
sugars and stress-related stimuli. Sugars and
stress-related stimuli activate different signal
transduction pathways that are ultimately
integrated to co-ordinately regulate gene
expression. Intracellular signalling may involve
hexokinase and MAP kinases and is
modulated by other signal transduction
pathways. Any signal that upregulates
extracellular invertase will be amplified and
maintained via the sugar-induced expression
of this enzyme.

Sucrose
Pathogen
infection

Abiotic
stress

D-Glucose

Cell wall

+ HXK?
MAP-kinase

MAP-kinase
STAU
Crosstalk

CHX
Nucleus
Induction

Sinkspecific
genes

Pathogenresponsegenes

Repression

Photosynthetic
genes

Extracellular
invertase
Current Opinion in Plant Biology

was shown to result in the same co-ordinated regulation of
source–sink relations and defence responses as elicitor
treatment of suspension culture cells. These studies
involving both tissue culture cells as well as plants demonstrate that different stress related stimuli result in the same
regulatory pattern of mRNAs for enzymes involved source
and sink metabolism and defence reactions. This indicates
that defence responses are tightly linked to the upregulation of sink metabolism to satisfy the energy requirements
of the activation of the cascade of defence reaction.
Under natural conditions plants are simultaneously affected by a variety of both biotic and abiotic stress related
stimuli and other environmental factors. The presence of
one stress may change plant responses to other stresses,
thus creating additive or synergistic interactions. This fact
is neglected when usually only the effect of a single stress
or other environmental factor is analysed. Three recent
studies provide some preliminary results about such naturally occurring interactions or multistress situation on
source–sink relations. By combining elevated levels of the

air pollutant ozone and mild drought, the ozone-induced
responses of all parameters, such as the disequilibrium of
the carbon transfer between roots and shoots, were significantly amplified [54]. Elevated levels of CO2 were shown
to enhance the growth inhibitory effect of powdery mildew
infection in barley [55] and to ameliorate ozone effects on
biomass and leaf area in soybean [56•].
Fluorescence imaging has been suggested only recently as a
diagnostic tool to analyse plant stress responses [57]. The
relationship between laser-induced chlorophyll fluorescence
and photosynthesis in drought and ozone stressed plants has
been evaluated with respect to quantitative interpretation of
the measurements and further practical applications of this
method [58]. The available data indicate that this powerful
noninvasive technique, which allows the measurement of
both the photosynthetic activity as well as the sink status of
the tissues analysed, could complement and extend molecular studies on the co-ordinated regulation of sink and source
specific genes. In addition, this method may help to compare
the effect of different types of stress related stimuli.

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Physiology and metabolism

Figure 2
Sieveelements

Pathogen
infection
Elicitors

Brassinosteroids
Sink-cell

SUC
Wounding

Cytokinin
+

+

+

Gene regulation
• Photosynthetic genes
• Sink genes
• Defence genes

+
Ethylene
+

Suc

–

Extracel.
invertase

Suc
TP

Model for apoplastic phloem unloading in sink
tissues and regulation of extracellular
invertase. Sucrose is unloaded from the sieve
elements of the phloem into the apoplast by a
sucrose transporter (Suc TP), the
disaccharide (Suc) is cleaved by an
extracellular invertase and the hexose
monomers (Fru and Glc) are taken up from
the sink cell by monosaccharide transporters.
Extracellular invertase is regulated by glucose,
as well as by phytohormones and stressrelated stimuli. Sugars are substrates for
heterotrophic growth and function as signals
for gene regulation.

+

+
Fru
+
Glc

Metabolism

Hexoses
Hexose
TP
H+

Current Opinion in Plant Biology

Signalling pathways: crosstalk and integration
Interaction between different phytohormones is well
established and best exemplified by the effect of
auxin/cytokinin ratio on plant morphogenesis [59].
There are several studies that demonstrate interactions
between sugar and phytohormone signalling pathways
which further support the significance of sugar signalling
in plant growth and development. Modulation of sugar
responses by phytohormones or vice versa, or cross talk
between the underlying signalling pathways has been
determined for gibberellins [60•], ethylene [24•], auxin
[61] and cytokinin [25•]. Inorganic ions such as phosphate and nitrogen were also shown to modify
sugar-mediated gene regulation in a gene specific manner [62,63]. Interactions between the environmental
stimulus light and sugar has been reported by Dijkwel et
al. [12•]. These studies demonstrate that sugar regulation in higher plants is linked to the effect of a number
of other signals and that complex interactions exist
between the underlying signal transduction pathways.
Based on the sugar inducibility of a number of defence
related enzymes it has been proposed that regulation of
defence related enzymes in response to pathogen infection
is indirectly mediated via the initial induction of an extracellular invertase and the resulting increased sugar
concentration [64]. The study of Ehness et al. [8•], however, shows that sugar and stress related stimuli
independently activate different signalling pathways
which are ultimately integrated to regulate source and sink
metabolism and activate defence responses as depicted in

Figure 1. Thus, sugars may function as an extracellular
indicator for pathogen infection, as suggested before [64],
but the corresponding genes are under dual control and
directly regulated both by the metabolic stimulus glucose
as well as in response to stress related stimuli. Based on the
pleiotropic phenotype of the prl1 mutation in Arabidopsis
[25•], a connection between glucose and stress signalling
has also been proposed [36].

Invertase: a key enzyme in source–sink
regulation
Supplying carbohydrates to sink tissues via an apoplastic
pathway involves the release of the transport sugar
sucrose into the apoplast by a sucrose exporter, cleavage
of the disaccharide by an extracellular invertase and
uptake of the hexose monomers by monosaccharide
transporters (Figure 2). The regulation of extracellular
invertase by a number of different stimuli indicates that
extracellular invertase is not only important for supplying carbohydrates to sink tissues — experimental data
suggest that this sucrose cleaving enzyme also plays a
crucial role to mediate source–sink regulation in
response to a variety of stimuli via sugar regulation of
invertase expression. Extracellular invertase may be considered as a central modulator of assimilate partitioning
and defence response based on the following four different functions: firstly, supplying carbohydrates to sink
tissues; secondly, regulation of source–sink transitions;
thirdly, amplification of signals that regulate source–sink
relations; and finally, integration of signals that regulate
source–sink relations and defence responses.

Source-sink regulation by sugar and stress Roitsch

Supplying carbohydrates to sink tissues

A number of studies demonstrate an essential function of
extracellular invertase for phloem unloading, carbohydrate
partitioning and growth of sink tissues (reviewed in [65,66•])
Regulation of source–sink transitions

The fast upregulation of extracellular invertase expression
after the induction of metabolism in autotrophic cultures
of tomato and Chenopodium rubrum [5•,67], and the induction of sink metabolism in source leaves of transgenic
plants by overexpression of a yeast invertase [27] indicate
a role of extracellular sucrose cleavage in regulating
source–sink-transitions and establishing sink metabolism.
Amplification of signals that regulate
source–sink relations

As unloading of sucrose from the phloem into the apoplast
follows the concentration gradient, and hexose transport
into the sink cells is mediated by high affinity monosaccharide transporters, extracellular invertase with a high
Km-value in the millimolar range is expected to be the limiting step for phloem unloading and thus a potential target
for regulation. Indeed, extracellular invertases were shown
to be specifically expressed under conditions that require a
high carbohydrate supply and upregulated by a number of
stimuli that affect source–sink relations (Figure 2).
Extracellular invertase was shown to be specifically
expressed in sink tissues. The corresponding gene was
induced by growth stimulating phytohormones such as
cytokinin and brassinosteroids ([68 •], M Goetz and
T Roitsch, unpublished observations), as well as elicitors,
pathogen infection and wounding that lead to the requirement for additional energy to elicit defence responses
[8•,69]. In contrast, ethylene, that is associated with fruit
ripening and thus terminates fruit growth, represses the
expression of extracellular invertase [70]. Extracellular
invertases from different species were also shown to be
transcriptionally induced by sugars [5•,67,71] and a higher
extracellular invertase activity will increase the sugar concentration; therefore, any signal that upregulates
extracellular invertase will be amplified and maintained by
the positive sugar feedback circuit (Figures 1 and 2).
Integration of signals that regulate source–sink
relations and defence responses

Since extracellular invertase is regulated by a number of
different stimuli that influence source–sink relations, the
corresponding signals are integrated via this enzyme.
Elevated hexose levels brought about by an upregulated
extracellular invertase expression have been suggested to
be important in defence responses and systemic acquired
resistance [21].

Conclusions and perspectives
Although there is accumulating evidence that stress related stimuli are important exogenous factors that regulate
source–sink relations, it is still not known how these
exogenous signals are sensed. Only scattered information

203

is available about the intracellular transduction of these
signals and about the molecular and cellular mechanisms
that contribute to the physiological responses. To further
elucidate the effect of plant stress on source–sink regulation, it will be important to consider naturally occurring
multistress situations. That is, to say, it will be important to
determine possible additive, synergistic and compensating
effects between different stress related stimuli and other
environmental factors.
Sugars have been identified as important signal molecules
that regulate source–sink relations. There is accumulating
evidence that several independent sugar signal transduction pathways, both specific for hexoses and sucrose,
operate in parallel. The identified components of the
underlying signal transduction pathways suggest homologies as well as distinct differences to well characterised
signal transduction pathways in yeast and mammals.
Interactions and crosstalk between sugar and hormones,
phosphate and light signal transduction pathways are evident. There is experimental evidence that sugar and stress
related signal transduction pathways are integrated to regulate defence reactions as well as source–sink relations.
To elucidate the mechanisms that regulate source–sink
relations, complementing experimental approaches are
required. Protoplasts and suspension culture cells are suitable experimental systems to study signal transduction,
and photoautotrophic cultures have proven to be particularly suitable. Photosynthesis is usually repressed in
heterotrophic cultures that also require a sugar depletion
period which may cause artefacts. Studies involving whole
plants will be required to assess source–sink relations, and
controlled manipulation of pathways using regulated promoters seems to be very promising.
Parallels of plant signal transduction pathways to well characterised pathways in yeast will possibly allow cloning by
complementation of yeast mutants, but the isolation and
analysis of plant mutants will be necessary to identify components unique to plants. The analysis of signal
transduction and response mutants was indispensable for
the rapid and significant progress in the field of phytohormone signal transduction and the regulation of source–sink
relations. To dissect the moleuclar basis for the apparent
interaction and crosstalk between sugar and other signal
transduction pathways it will be necessary to determine
branch points, such as common second messengers or regulatory proteins, by identifying corresponding upstream
and downstream mutants; such mutants would be expected to be characterised by either pleiotropic or more
specific phenotypes, respectively.
An alternative approach to identify key genes controlling and
co-ordinating acclimative reactions is the use of molecular
marker technologies. Quantitative trait loci analysis has been
applied to several key enzymes in carbohydrate metabolism
[50•,72]. The QTL method is a powerful approach to dissect

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Physiology and metabolism

and understand the complex regulation of processes taking
place at the whole plant level and thus may be also a valuable
tool to study the regulation of source–sink relations.
Understanding the complex interactions between different
signals at the level of signal transduction pathways is likely to be the key for understanding source–sink regulation
at the molecular level. Future studies should also consider
possible interactions between carbohydrate, nitrogen and
phosphate metabolism.
One driving force to study source–sink regulation was the
projected practical application to manipulate assimilate
partitioning in transgenic plants and to increase the partitioning of fixed carbon into harvestable sinks — however,
the numerous approaches taken by many laboratories to
modify carbon fluxes through modifying individual enzymatic steps have been largely unsuccessful [73]. This
insight and the available literature on source–sink regulation indicate that plants may display an enormous and
underestimated metabolic flexibility and crosstalk
between different signal transduction pathways. The challenge remains, therefore, to unravel the underlying
sophisticated network of highly flexible regulatory circuits
to get insight into the fascinating biology of source–sink
regulation. This will allow predictable genetic engineering
of plants via manipulating signal transduction pathways
rather than specific enzymatic reactions.

Acknowledgements
I would like to gratefully acknowledge the help of Rainer Ehneß, Markus
Hofmann, Georgine Stühler and Doris Urbaneck for their help during the
course of the preparation of this review and thank Marc Götz and Anja
Stadler for critically reading of the manuscript.

References and recommended reading

Papers of particular interest, published within the annual period of review,
have been highlighted as:

• of special interest
•• of outstanding interest
1.

Koch KE: Carbohydrate-modulated gene expression in plants.
Annu Rev Plant Physiol Plant Mol Biol 1996, 47:509-540.

2.

Morcuende R, Pérez P, Martínez-Carrasco R: Short-term feedback
inhibition of photosynthesis in wheat leaves supplied with
sucrose and glycerol at two temperatures. Photosynthetica 1997,
33:179-188.

3.

Felitti SA, Gonzalez DH: Carbohydrates modulate the expression
of the sunflower cytochrome c gene at the mRNA level. Planta
1998, 206:410-415.

4.

Winder TL, Sun J, Okita TW, Edwards GE: Evidence of the
occurrence of feedback inhibition of photosynthesis in rice. Plant
Cell Physiol 1998, 39:813-820.

5.
•

Godt DE, Roitsch T: Regulation and tissue-specific distribution of
mRNAs for three extracellular invertase isoenzymes of tomato
suggests and important function in establishing and maintaining
sink metabolism. Plant Physiol 1997, 115:273-282.
This study demonstrates that extracellular invertases of tomato are encoded
by four differentially expressed and regulated genes. Specific isogenes are
specifically expressed in sink tissue and/or induced in response to signals
that require a high carbohydrate supply such as growth stimulating phytohormones, elicitors and wounding.
6.

Ehness R, Roitsch T: Differential effect of D-glucose on the level of
mRNAs for three invertase isoenzymes of Chenopodium rubrum.
J Plant Physiol 1997, 150:514-519.

7.

Ismail I, De Bellis L, Alpi A, Smith SM: Expression of glyoxylate
cycle genes in cucumber roots responds to sugar supply and can
be activated by shading or defoliation of the shoot. Plant Mol Biol
1997, 35:633-640.

8.
•

Ehness R, Ecker M, Godt DE, Roitsch T: Glucose and stress
independently regulate source and sink metabolism and defense
mechanisms via signal transduction pathways involving protein
phosphorylation. Plant Cell 1997, 9:1825-1841.
The effect of sugar and stress-related signals on photosynthesis, sink metabolism and defense response was studied in photoautotrophic cultures of
Chenopodium rubrum by analysing the regulation of mRNAs for representative enzymes. All stimuli resulted in the induction of the genes encoding the
sink specific extracellular invertase and the defense responsive PAL, whereas the photosynthetic gene RbcS was repressed. The differential effect of
the kinase inhibitor staurosporine demonstrated that glucose and stress
independently activate different intracellular signalling pathways that are ultimately integrated to co-ordinately regulate source–sink relations and
defense mechanisms. Both glucose and stress-related stimuli triggered the
rapid and transient activation of protein kinases that specifically phosphorylate the MAP kinase substrate myelin basic protein.
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Abdin OA, Zhou X, Coulman BE, Cloutier D, Faris MA, Smith DL:
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for a potato sucrose transporter is not regulated by sucrose.
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13. Geiger M, Stitt M, Geigenberger P: Metabolism in slices from
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Expression of a yeast-derived invertase in developing cotyledons
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To change the sugar status during seed development, a yeast-derived invertase was expressed in Vicia narbonensis under the control of a LeguminB4
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novel carbohydrates. The authors provide the novel and interesting suggestion that alteration in the type of carbohydrate may act as a signalling system
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