Scientia Horticulturae 127 (2010) 1–15
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Molecular approaches for enhancing sweetness in fruits and vegetables
Akula Nookarajua, Chandrama P. Upadhyayaa,∗∗, Shashank K. Pandeya, Ko Eun Younga,
Se Jin Hongb, Suk Keun Parka, Se Won Parka,∗
aDepartment of Molecular Biotechnology, Konkuk University, 1, Hwayang-dong, Gwangin-gu, Seoul 143 701, Republic of Korea
bDepartment of Applied Plant Science, Gangneung-Wonju National University, Gangneung 210 702, Republic of Korea
a r t i c l e i n f o
Received 20 May 2010
Received in revised form
11 September 2010
Accepted 14 September 2010
a b s t r a c t
The quality of fruits and vegetables is mainly dependant on the sweetness determined by the level of
soluble sugars such as glucose, fructose and sucrose. Other fruit quality parameters include Brix content,
acidity, aroma, color, size and shape. Total sugar content in fruits and vegetables is a function of genetic,
nutritional, environmental and developmental factors. Understanding the factors controlling sweetness
is important to design strategies for enhancing quality of fruits and vegetables. Modifying the activity
of enzymes in carbohydrate metabolism such as sucrose synthase (SuSy), acid invertase, ADP-glucose
pyrophosphorylase (AGPase), sucrose phosphate synthase (SPS) and sucrose transporters were found to
influence carbohydrate partitioning and sucrose accumulation in sink tissues of several food crops. Plant
and thaumatin have potential application for developing transgenic plants to improve the sweetness and
quality of fruits and vegetables. The present review envisages various cultural, breeding and molecular
approaches used for enhancing sugar content and sweetness in fruits and vegetables.
© 2010 Elsevier B.V. All rights reserved.
Modeling approaches to predict sugar content in fruits and vegetables..............................................................................
Strategies to increase sweetness in fruits and vegetables.............................................................................................
3.1. Cultural practices...............................................................................................................................
3.2.Breeding strategies .............................................................................................................................
3.3. Biotechnological approaches...................................................................................................................
3.3.1. Sucrose phosphate synthase (SPS; EC 22.214.171.124) ......................................................................................
3.3.2. Invertase (?-fructosidase) (AI; EC 126.96.36.199)..........................................................................................
3.3.3. Sucrose synthase (SuSy or UDPG: d-fructose 2-glucosyl-transferase; EC 188.8.131.52) .................................................
3.3.4. ADP-glucose pyrophosphorylase (AGPase; EC 184.108.40.206) .............................................................................
3.3.5.Pyrophosphate d-frucrose-6-phospahte 1-phosphotransferase (PFP; EC 220.127.116.11) .................................................
3.3.6.Sorbitol-6-phosphate dehydrogenase (S6PDH; EC 18.104.22.168) .......................................................................
3.3.7. Fructose-1,6-bisphosphatase (FBPase; EC 22.214.171.124)..................................................................................
3.3.8. Sucrose phosphorylase (SuP; E.C 126.96.36.199) ............................................................................................
3.3.9.Phosphoglucomutase (PGM; EC 188.8.131.52) .............................................................................................
3.3.10.Sucrose:sucrose 1-fructosyltransferase (1-SST; EC 184.108.40.206).......................................................................
3.3.11. S-adenosylmethionine hydrolase (SAMase or AdoMetase; EC 220.127.116.11) ............................................................
Abbreviations: AA, acetaldehyde; AGPase, ADP-glucose pyrophosphorylase; AI, acid invertase; EIN3, ethylene insensitive 3; FBPase, fructose-1,6-biphosphatase; FRK,
fructokinase; GLK, glucokinase; HXK, hexokinase; Pdc, pyruvate decarboxylase; PFP, pyrophosphate d-frucrose-6-phosphate 1-phosphotransferase; PGM, phosphoglucomu-
tase; SAMase, S-adenosyl methionine hydrolase; SI, sucrose isomerase; snRK1, SNF1-related protein kinase; SoSUT1, spinach sucrose transporter 1; SPS, sucrose phosphate
synthase; 1-SST, sucrose:sucrose-1-fructosyl transferase; SuP, sucrose phosphorylase; SuSy, sucrose synthase; SUT, sucrose transporter; S6PDH, sorbitol-6-phosphate
dehydrogenase; SXD1, sucrose export defective 1; TSS, total soluble sugars; UDPase, uridine diphosphate-glucose pyrophosphorylase.
∗Corresponding author. Tel.: +82 2 450 3739.
∗∗Co-Corresponding authors. Tel.: +82 2 049 6256.
E-mailaddresses:firstname.lastname@example.org (C.P. Upadhyaya), email@example.com (S.W. Park).
0304-4238/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
A. Nookaraju et al. / Scientia Horticulturae 127 (2010) 1–15
Sucrose transporters and binding proteins ....................................................................................................
Sweet proteins/taste modifying proteins.....................................................................................................
3.5.1. Brazzein .............................................................................................................................
3.5.2. Curculin and neoculin...............................................................................................................
3.5.5. Miraculin ............................................................................................................................
3.5.7. Pentadin .............................................................................................................................
Conclusions and perspectives ........................................................................................................................
Sucrose isomerase (SI; EC 18.104.22.168)................................................................................................
Fructokinase (FRK; EC 22.214.171.124) ......................................................................................................
Pyruvate decarboxylase (Pdc; EC 126.96.36.199)...........................................................................................
mainly on type and composition of sugars present, which is pri-
marily a genotype dependent. Sugar content is also dependent on
total solids, pH, titratable acidity and fruit size (Georgelis, 2002). In
most of the fruits, glucose and fructose form the major proportion
of soluble sugars (Baldwin et al., 1991), while in few wild species of
tomato (Lycopersicon chmielewskii, Solanum habrochaites) and mel-
ons, sucrose is the major sugar. The amount of total soluble sugars
changes with fruit maturity showing a maximum score at ripening
(Cho et al., 1993). The accumulation of sugars was also found to dif-
fer between mesocarp and locular tissues of tomato fruit (Mounet
et al., 2009). In addition, sugar content varies with plant nutrition,
thetically fixed carbon is partitioned between sugars and starch
in higher plants. The starch being a major carbohydrate reserve
material is partly synthesized in the chloroplasts of photosynthetic
The carbohydrate partitioning and relative composition of sugars
in sink tissues is dependent on the relative expressions of enzymes
tions in sucrose metabolism in the sink tissues of higher plants is
depicted in Fig. 1.
The transcriptome analysis of high Brix introgression lines of a
cross between Solanum pennellii and Solanum lycopersicum showed
a coordinated up-regulation of enzymes in sucrose metabolism,
glycolysis and TCA cycle (Baxter et al., 2005). During tomato
(Lycopersicon esculentum L., renamed as S. lycopersicum L.) fruit
development, sucrose levels showed a reduction with correspond-
ing increase in the levels of glucose and fructose (Carrari et al.,
2006) with exception of sucrose accumulating species such as S.
habrochaites and Solanum chmielewskii. The progressive increase
in hexoses and decline in sucrose with tomato fruit maturity is
attributed to a decrease in sucrose synthase (SuSy), glucokinase
(GLK) and fructokinase (FRK) activities and a high invertase activ-
ity (Yelle et al., 1991; Carrari et al., 2006; Steinhauser et al., 2010).
Abundance of invertase isoforms was also observed during matu-
with developmental changes in the activities of key enzymes of the
sucrose-to-starch metabolic pathway such ADP-glucose pyrophos-
phorylase (AGPase) (Schaffer and Petreikov, 1997). In addition to
sucrose metabolizing enzymes, sucrose transporters and sucrose
and subsequent accumulation (Delú-Filho et al., 2000; Williams et
al., 2000; Leggewie et al., 2003; Hofius et al., 2004).
In general, sugar content of many present day fruits and veg-
etables changed to a great extent owing to continuous selection
and breeding efforts. Modern apples taste sweeter than older culti-
vars and popular tastes in apples have varied over time. Evolution
of apple cultivars in a region is also dependant on people prefer-
ence. Most North Americans and Europeans favor sweet, subacid
apples, while extremely sweet apples with barely any acid flavor
are preferred in Asia and India (Tarjan, 2006). Cultivated varieties
of tomatoes are less sweet than some of its wild relative such as
L. chmielewskii (Yelle et al., 1988). Fruits of modern tomato culti-
vars accumulate hexoses while few wild cultivars (L. chmielewskii,
Lycopersicon hirsutum, S. habrochaites) accumulate sucrose relative
to hexoses (Yelle et al., 1988; Miron and Schaffer, 1991). Efforts
were made to enhance sucrose accumulation in relation to hexoses
in tomato through genetic engineering (Klann et al., 1996). As fruc-
tose is two times sweeter to glucose, efforts were made to develop
the overall fruit sweetness and flavor in tomato through classical
and beet sugars have been used as the major sweeteners in food
industry. As the conventional sugars, sucrose, glucose and fructose
are calorie rich, people today prefer less calorie sugar substitutes
such as xylitol, erythritol, isomaltulose, aspartame, and sucralose.
Transgenic plants were developed producing enhanced levels of
isomaltulose in potato (Börnke et al., 2002; Hajirezaei et al., 2003)
and sugarcane (Wu and Birch, 2007).
Apart from imparting sweetness to fruits and vegetables, sugars
polymer biosynthesis. High levels of glucose are associated with a
(Tsai et al., 1970; Weber et al., 1998). Similarly, exogenous supply
of glucose increased glycolytic metabolites in potato tuber discs
whereas feeding of sucrose led to a stimulation of starch synthesis
(Geiger et al., 1998). In addition, sugars have also been reported to
have important hormone-like functions. They act as primary mes-
sengers in signal transduction and play a key role in the regulation
of both physiological and metabolic events in plants (Koch, 1996;
Lalonde et al., 1999). In developing seeds, it has been suggested
that sucrose regulates differentiation and storage, whereas hex-
oses control growth and metabolism (Weber et al., 1997; Wobus
and Weber, 1999). It has been also proposed that glucose has a
regulatory role in many plant developmental processes such as
germination, seedling development, root, stem, and shoot growth,
photosynthesis, carbon and nitrogen metabolism, flowering, and
senescence (Rolland et al., 2006).
Progress has been made in sugar signaling with the discovery of
hexokinase (HXK) as a glucose sensor that modulates gene expres-
A. Nookaraju et al. / Scientia Horticulturae 127 (2010) 1–15
Fig. 1. Schematic diagram showing sucrose metabolism in higher plants. Plants synthesize sucrose by photosynthesis and sucrose is transported to amyloplasts by sucrose
transporters where it will be converted to storage form, starch. Partly starch is synthesized in chloroplasts. Sucrose is also stored in vacuole. AGPase: ADP-glucose pyrophos-
phorylase; AI: acid invertase; CeSy: cellulose synthase; HK: hexokinase; FRK: fructokinase; FBPase: fructose-1,6-biphosphatase; N/AI: neutral or alkaline invertase; PFP:
pyrophosphate d-frucrose-6-phospahte 1-phosphotransferase; PGM: phosphoglucomutase; SoSUT1: spinach sucrose transporter 1; SPP: sucrose phosphate phosphatase;
sion and multiple plant hormone-signaling pathways (Sheen et
al., 1999; Smeekens, 2000). The HXK1 glucose sensor is primar-
ily associated with mitochondria as part of a glycolytic metabolon.
In addition, HXK1 is found in high-molecular-weight complexes
in the nucleus where it controls transcription and proteasome-
In the nucleus, several types of TFs are involved in sugar-regulated
transcription (Rolland et al., 2006). The HXK1 loss-of-function glu-
cose insensitive2-1 (gin2-1) and gin2-2 have been isolated through
a mutant screen based on a high glucose (6%) repression assay,
displaying inhibition of cotyledon expansion, chlorophyll accumu-
in Arabidopsis (Moore et al., 2003). Similarly, at high concen-
trations of glucose, HXK1-dependent glucose signaling interacts
positively with ABA, but negatively with ethylene signaling (Cho
et al., 2010). Thus diverse sugar signals activate multiple HXK-
dependent and HXK-independent pathways and use different
molecular mechanisms to control transcription, translation, pro-
tein stability and enzymatic activity. Important and complex roles
for Snf1-related kinases (SnRKs), extracellular sugar sensors and
2. Modeling approaches to predict sugar content in fruits
Time of fruit harvest is crucial for maintaining high total sol-
uble sugar (TSS) content, good color and overall fruit quality.
In many fruits, carbohydrate content, firmness and flesh color
are important indicators of maturity, thus assessment of these
parameters is indispensable. Many methods (both destructive and
non-destructive) have been developed for assessment and pre-
diction of firmness and TSS content in fruits. The TSS measured
by refractometer and the firmness detected by touch or by hand-
held penetrometer are both destructive methods and the results
vary greatly with the skill and care taken by the operator. Appli-
cation of a non-destructive optical method, near infra-red (NIR)
spectroscopy for assessment of fruit firmness and TSS content has
attracted great attention in recent days. Several studies have been
reported on using near-infrared (NIR) spectroscopy in the spectral
region between 400nm and 2500nm to measure the sugar con-
tent of many fruits including apples, kiwifruits, melons, peaches,
pears, tangerines, cucumbers, sweet cherries, and mandarins (Dull
et al., 1992; Kawano et al., 1992, 1993; Slaughter, 1995; Ventura
et al., 1998; Choi et al., 1997; Lammertyn et al., 1998; Moons et
al., 1997; Peiris et al., 1999; Lu, 2001; McGlone et al., 2002; Ying
et al., 2005; Liu and Ying, 2005; Liu et al., 2007; Ariana et al.,
2006; Fu et al., 2008). However, a greater spectral region beyond
1100nm appears to give improved prediction results in sugar con-
tent and other quality attributes (Moons et al., 1997; Lu et al.,
Lammertyn et al. (2000) established a relationship between the
reflectance spectra (at 880–1650nm) and the SSC of apples by
means of the partial least square (PLS) technique. Lu and Ariana
(2002) investigated an NIR sensing technique in interactant mode
for rapid acquisition of spectral information to predict the sugar
content and possibly firmness of Empire and Red Delicious apples.
transmission mode to predict the total sugar content of a variety
of fruit juices. Subedi et al. (2007) used short wave near infrared
(SWNIR) (400–1100nm) spectroscopy for assessment of mango
A. Nookaraju et al. / Scientia Horticulturae 127 (2010) 1–15
Fig. 2. Sugar sensing mechanism in plants mediated by hexokinase. The HXK1 glucose sensor is primarily associated with mitochondria as part of a glycolytic metabolon.
In addition, HXK1 is found in high-molecular-weight complexes in the nucleus where it controls transcription and proteasome-mediated degradation of the EIN3 TF. In the
nucleus, several types of TFs are involved in sugar-regulated transcription (a). Sucrose appears to be sensed at the plasma membrane, possibly by transporter homologs
(b). G-protein coupled receptor signaling by RGS1 and GPA1 is involved in glucose control of plant processes possibly in a hexokinase-independent way (c). SnRK1 proteins
play an important role in plant sugar signaling (d). Important regulatory effects are reported for trehalose (Tre) and T6P, apparently downstream of SnRK1 (e). The concept
is taken from Rolland et al. (2006). AP2: APETALA2-type TF; bZIP: basic leucine zipper; EIN3: ethylene insensitive 3; GCR1: G-protein coupled receptor1; GPA1: G-protein
?-subunit; RGS1: regulator of G-protein signaling1; TPS1: trehalose-6-P synthase; TPP: trehalose-6-P phosphatase; snRK1: SNF1-related protein kinase; B3 domain protein;
CCT domain protein; MYB protein; WRKY TF.
(Mangifera indica L.) fruit maturation and TSS content. Recently,
Fu et al. (2009) investigated the potential of NIR spectroscopy in
diffuse reflectance mode for determining the SSC and acidity of
intact loquats and their models gave relatively good predictions of
the SSC of loquats. Although a general trend of correlation exists
between NIRS measurements and fruit firmness, this technique
still cannot predict fruit firmness accurately and reliably due to
light reflection and scattering by surface and internal components,
respectively. These limitations may be overcome by using meth-
ods based on light scattering principle. Birth (1978, 1986) first time
explored the potential of using light scattering for analyzing agri-
cultural products for firmness. Lu (2004) evolved a multispectral
imaging technique based on light scattering for predicting firm-
on the activity of key regulatory enzymes was used to predict the
sugar accumulation in sugarcane culms (Zhu et al., 1997; Rohwer
and Botha, 2001).
3. Strategies to increase sweetness in fruits and vegetables
3.1. Cultural practices
Few cultural and agronomic practices applied in the field were
nutrition showed to influence metabolite accumulation in spinach
soybean seeds (Robinson, 1996). However, high nitrogen applica-
limitation resulted in increased accumulation of nonstructural car-
to the fact that nitrate redirects the flow of carbon away from
sucrose and towards amino acid synthesis by activating cytoso-
lic protein kinases (Champigny and Foyer, 1992). Application of
prohexadione-calcium (400ppm) at 10 days after transplantation
significantly improved leaf sugar content and compactness of Chi-
nese cabbage (Kang et al., 2010). In a study, pre-harvest spraying
of acetaldehyde (AA) was found effective in hastening fruit ripen-
ing, increasing respiration and accumulation of sugars in figs (Hirai
et al., 1968). The AA is an aroma constituent in most plant tis-
sues (Janes and Frenkel, 1978) and the endogenous levels of AA
were found to be elevated during fruit ripening (Fidler, 1968) lead-
ing to sugar accumulation. Spraying of peach plants with 50mgl−1
abscisic acid (ABA) at 90 days after full bloom increased the accu-
The increase in sucrose accumulation in their study was attributed
to the increased generation of glucose from elevated sorbitol flux
through enhanced activity of sorbitol oxidase by ABA treatment. In
another study, application of 100mgl−1para-chlorophenoxyacetic
acid (p-CPA) at 25 days after anthesis significantly improved the
sucrose content in relation to glucose and fructose in muskmelon
fruit (Hayata et al., 2001). The highest increase in sucrose content
was observed when p-CPA was applied to pollinated fruits com-
pared to parthenocarpic fruits.
Sucrose content of fruits and vegetables is found to depend
on the environmental conditions prevailing during fruit devel-
A. Nookaraju et al. / Scientia Horticulturae 127 (2010) 1–15
opment. Dorais et al. (1996) observed decreased CO2 fixation,
increased leaf starch and sugar contents in tomato plants grown
under continuous light. Similar results were observed by Demers
and Gosselin (2002) where they reported increased accumulation
of sucrose and starch in pepper leaves under continuous light
attributed to decreased sucrose export. This strategy may be uti-
lized in green leafy vegetables such as spinach, cabbage and lettuce
for increasing sucrose accumulation in leaves. Up-regulation of
the photosynthetic enzymes coincided with a reduction in leaf
stomatal conductance, transpiration and leaf water use efficiency
(WUE) by CO2enrichment in sugarcane led to enhanced leaf area,
biomass accumulation and sucrose production (Vu et al., 2006).
at 20–25 days after anthesis (DAA) were found to inhibit sucrose
increased sucrose accumulation in fruits (Wang et al., 1993). High
(Georgelis, 2002). These reports suggest that manipulation of crop
microenvironment may be an alternative to modulate the sugar
composition for increasing the quality of fruits and vegetables.
In addition to cultural practices followed in the field, posthar-
vest treatment of fruits and vegetable was also reported to affect
the accumulation of sucrose and hexoses but at normal to high
temperatures the sugars recondensed to form starch (Isherwood,
1973). In general, low temperatures promote the production of AA
leading increased sucrose accumulation. Exposure of fruits to AA
vapors improved the organoleptic property of table grapes (Pesis
and Frenkel, 1989), strawberries (Morris et al., 1979), blueberries
and tomatoes (Paz et al., 1981). The AA treatment also caused
reduced fruit acidity due to accelerated respiration and stimula-
tion of gluconeogenesis (Halinska and Frenkel, 1991). Treatment of
sugar beet root tissue discs and cell cultures with synthetic growth
regulators (Pix and BAS 106W) significantly improved the sucrose
application of certain growth regulators and organochemicals to
fruits and vegetables during storage may enhance the sugar con-
3.2. Breeding strategies
There are few reports on breeding programs aimed at increas-
ing fruit sugar content and for identification of molecular markers
linked to sugar content in fruits and vegetables. During breeding
of blue berries, the type of pollen parent has shown to affect the
cinium corymbosum L.) (Kobashi et al., 2002). The sugar content
in fruits of this cultivar showed a significant increase when arti-
ficially cross-pollinated with ‘Northland’ pollen. There are several
potential sources of high sugar among the wild species of tomato,
L. chmielewskii, L. hirsutum and Lycopersicon pimpinellifolium. Theo-
retically these lines could be crossed to large fruited tomatoes that
have a low sugar level and through backcrossing the sugar level
cherry tomato accession PI270248 (L. esculentum var. cerasiforme)
significantly lower sugar levels in the fruit (Georgelis, 2002). This
study identified six random amplified polymorphic DNA (RAPD)
markers linked to high sugars among which five are dominant
and one is co-dominant. Combination of markers for breeding pur-
poses was also tested and the results from this could be useful for
designing breeding strategies for evolving cultivars with improved
lines originating from a cross between the green-fruited L. pennellii
and the cultivated tomato (cv. M82) revealed at least 23 quantita-
tose to glucose ratio would be desirable to increase the overall fruit
sweetness and flavor. Schaffer et al. (1999) evolved genotypes with
high fructose to sucrose ratio in mature fruits through backcross
breeding program based on initial inter-specific cross between
L. esculentum and L. hirsutum. On further analysis of backcross
progenies with high fructose to glucose ratio (>1.5:1) identified
two inter simple sequence repeat (ISSR) sequences which were
alleles to each other (Levin et al., 2000). Their study identified
L. hirsutum-derived dominant allele (FgrH) that was found to be
responsible for higher fructose to glucose ratio. Recently, Obando-
(NILs) of melon derived from a Spanish cultivar Piel de Sapo (PS)
and the exotic Korean accession Shongwan Charmi (PI 161375).
Recently, introgression lines of cultivated tomato harboring the
wild species (S. habrochaites) allele for the regulatory large subunit
(L1H) of AGPase were developed (Petreikov et al., 2009).
In a study, crossing of low sucrose melon cv. Faqqous (Cucumis
melo subsp. melo var. flexuosus) with a high sucrose melon cv.
Noy Yizre’el (C. melo subsp. melo var. reticulatus) showed that low
accumulation in melon fruit is conferred by a single recessive gene
suc gene, sucrose content in melon fruits is also affected by addi-
tional genetic factors. In another study, Kim et al. (2002) reported
a melon (C. melo) cultivar with high soluble sugars (15–17% TSS)
and multiple disease resistance, ‘Busan 926’ through backcross and
pedigree breeding. Cowpea line evolved by Institut de la Recherche
Agronomique pour le Developpement (IRAD), Cameroon cowpea
tained higher sucrose content as compared to commercial cowpea
cultivars (Kitch et al., 1998). Another sweet cowpea breeding line,
‘KV×61-1’ was recently developed by the National Breeding Pro-
gram in Burkina Faso (Issa Drabo, unpublished) with an average
sucrose content of 5% (L.L. Murdock, unpublished). High sucrose
content in cowpea also enhanced the flavor of the grain also.
Efforts were also made to develop first strawberry F1-hybrids with
improved vitamin-C and enhanced sugar content through classical
breeding (Bentvelsen and Bouw, 2002).
3.3. Biotechnological approaches
As discussed earlier, the total carbohydrates synthesized in the
photosynthetic organs are partitioned between sucrose, starch and
other sugars due to the action of enzymes in sugar metabolism. So
far, many enzymes in sucrose metabolism and sugar transporters
have been expressed either in sense or antisense orientation in
transgenic plants which showed a significant change in the sucrose
altering the metabolic flux towards sugars by manipulation of the
activity of specific enzymes in biosynthetic pathways is reported
3.3.1. Sucrose phosphate synthase (SPS; EC 188.8.131.52)
It catalyzes the synthesis of sucrose 6-phosphate from UDP-
glucose and d-fructose 6-phosphate. Its activity was highly
correlated with the sucrose content in fruits of L. hirsutum (Miron
and Schaffer, 1991) and Lycopersicon peruvianum (Stommel, 1992).
It increases the rate of sucrose accumulation in tissues by main-
taining the hexose gradient between the apoplast and cytosol.
sutum sp. humb. and bonpl. was coincided with reduced activity of
A. Nookaraju et al. / Scientia Horticulturae 127 (2010) 1–15
List of accomplishments for altering sugars in fruits and vegetables by manipulating the expression of sugar metabolic enzymes.
Gene modified Plant species Metabolic changeReference
Sucrose phosphate synthase
Tomato-OEEnhanced synthesis of sucroseWorrell et al. (1991)
Increased sucrose unloading
Enhanced leaf sucrose
Enhanced fruit sucrose, reduced fruit size
Altered carbohydrate partitioning
Lower sucrose accumulation in tubers, delayed
Increased fruit sucrose accumulation,
degradation of chloroplast membrane
Decreased starch content and tuber yield
Nguyen-Quoc et al. (1999)
Haigler et al. (2007)
Klann et al. (1996)
Tang et al. (1999)
Hajirezaei et al. (2003)
Acid invertase (AI)
Muskmelon-OE Yu et al. (2008)
Sucrose synthase (SuSy)Potato-DR Zrenner et al. (1995),
Fernández et al. (2009)
Tang and Sturm (1999)
D’Aoust et al. (1999),
Chengappa et al. (1999)
Müller-Röber et al. (1992),
Leidreiter et al. (1995)
Reduced sucrose utilization
Decreased sink strength and dry matter
Reduced starch, increased tuber number and
tuber fresh weight
Increased starch synthesis
Increased sucrose accumulation
No significant change in sugar and starch
Sweetlove et al. (1996)
Park et al. (2006)
Hajirezaei et al. (1994)
Enhanced sucrose accumulation in taproots
Kovacs et al. (2007)
Gao et al. (2001) Sorbitol-6-phosphate
Increased sucrose accumulation
Decreased starch content coincided with
enhanced accumulation of soluble sugars
Accumulation of 3-PGA, triose phosphate and
FBP with subsequent reduction in sugar and
Enhanced levels of glucose and fructose at
green and late ripening stage
Decreased sucrose accumulation
Increased sucrose breakdown and decreased
starch accumulation in potato tubers
Decreased starch accumulation in tubers and
Increased leaf sucrose and decreased tuber
Reduction in ethylene biosynthesis and
increased soluble sugars
Increased starch breakdown and respiration
Delayed flowering (LeFRK1), reduction in stem
and root growth; number of fruits, flowers and
Reduced utilization of sucrose in vascular
tissues leading to poor xylem development,
reduced plant growth and wilting
Increased leaf acetaldehyde and tolerance to
Kanamaru et al. (2004)
Kossmann et al. (1994) Fructose-1,6-bisphosphatase
Zrenner et al. (1996)
Tomato-DR Obiadalla-Ali et al. (2004)
Sucrose phosphorylase (SuP)Potato-OE
Trethewey et al. (2001)
Fernie et al. (2002b)
Phosphoglucomutase (PGM)Potato-DR Lytovchenko et al. (2002),
Fernie et al. (2002a)
Lytovchenko et al. (2005) Potato-OE
Sucrose isomerase (SI)
Cantaloupe melon-OEClendennen et al. (1999)
Börnke et al. (2002)
Hajirezaei et al. (2003)
Odanaka et al. (2002)
German et al. (2003)
Pyruvate decarboxylase (Pdc) Potato-OE
Tadege et al. (1998)
OE: overexpressed; DR: down-regulated.
(SPS) (Miron and Schaffer, 1991). Transgenic tomato overexpress-
ing maize SPS showed enhanced synthesis and accumulation of
sucrose relative to starch (Worrell et al., 1991). Similarly, Nguyen-
Quoc et al. (1999) reported that the overexpression of SPS could
increase sucrose unloading in transgenic tomato fruits up to 60%
as compared to the untransformed controls which indicated that
overexpression of SPS increased the sink strength in transgenic
tomato fruits. It also enhances partitioning of carbohydrates to
sucrose in preference to starch (Haigler et al., 2007). In addition to
enhanced sucrose synthesis, SPS activity enhances carbon assim-
ilation as observed in transgenic tobacco, which was reflected by
ber of flowers (Baxter et al., 2003). Apart from these affects, the
SPS has also been shown to improve plant developmental pro-
tobacco and Arabidopsis due to increased photosynthesis in SPS
overexpressing plants (Baxter et al., 2003; Strand et al., 2003). The
activation of SPS in leaf tissues may function to facilitate sucrose
formation for osmoprotection under low temperature stresses.
3.3.2. Invertase (ˇ-fructosidase) (AI; EC 184.108.40.206)
Acid invertase catalyzes the conversion of sucrose to glucose
and fructose. It is one of the most important enzymes involved in
sucrose metabolism in fruits. Sucrose hydrolysis by acid invertase
may determine the rate and extent of sucrose storage in tomato
fruit (Dali et al., 1992; Walker et al., 1978). Acid invertases were
reported to be primary determinants of sucrose levels in tomato
(Klann et al., 1993, 1996), cucumber (Burger and Schaffer, 2007)
and hexose levels in grapes (Davies and Robinson, 1996). The acid
invertase and SuSy catalyze the cleavage of sucrose in rapidly
growing tomato fruit. Higher accumulation of sugars preferentially
A. Nookaraju et al. / Scientia Horticulturae 127 (2010) 1–15
sucrose than glucose and fructose in the sweet tomato species L.
chmielewskii was attributed to the inherent down-regulation of
acid invertase gene in the fruits (Yelle et al., 1988). Similarly, high
levels of sucrose accumulation were associated with low levels of
acid invertase coupled with high levels of SPS activity in L. hirsu-
as sucrose has half the osmolarity as that of glucose and fructose
(Steingrover, 1983) and is less accessible to metabolic and respira-
tory loss than hexoses (Salerno and Pontis, 1978).
Attempts were made to modify the activity of invertase gene
in transgenic plants of tomato, carrot, potato and muskmelon that
resulted in altered sugar composition in fruits and tubers (Klann
et al., 1996; Tang et al., 1999; Hajirezaei et al., 2003; Yu et al.,
2008). Expression of tomato invertase (TIV1) gene in antisense
orientation resulted in higher sucrose accumulation coupled with
smaller fruits in tomato (Klann et al., 1996). Similarly, antisense
inhibition of vacuolar and cell wall invertase altered carbohy-
drate partitioning and enhanced sugar and starch accumulation in
mature leaves as well as taproots of transgenic carrot (Tang et al.,
cific expression of invertase in potato resulted in inhibited sucrose
accumulation. In addition, the transgenic tubers showed delayed
sprout growth indicating the impairment of phloem transport of
sucrose to growing bud. Recently, Yu et al. (2008) reported trans-
genic muskmelon plants down-regulated for soluble acid invertase
showed substantial increase in sucrose accumulation in fruits. Fur-
ther, the transgenic fruits showed accelerated ripening correlated
with elevated production of ethylene.
3.3.3. Sucrose synthase (SuSy or UDPG: d-fructose
2-glucosyl-transferase; EC 220.127.116.11)
Sucrose synthase is a glycosyl transferase that converts
reversibly sucrose into UDP-glucose and fructose in the presence
of UDP. In mature tissues of muskmelon, the activity of SuSy was
suggested as the predominant sucrose-cleaving enzyme by pro-
viding UDP-Glu for complex carbohydrates production (McCollum
et al., 1989). Also, SuSy is responsible for the cleavage of newly
imported sucrose and the rate of starch synthesis (Wang et al.,
late the import and compartmentation of sucrose in the early stage
of tomato fruit development (Demnitz-King et al., 1997). There are
two isoforms of SuSy (SS I and SS II) reported in Japanese pear fruit
(Tanase and Yamaki, 2000). The isoform SS I plays a role in degra-
dation of translocated sucrose in young fruit, whereas SS II plays a
role in sucrose synthesis in mature fruit as SS II has higher affinity
influence sucrose accumulation in Japanese pear but SuSy activity
contributed more than SPS activity (Moriguchi et al., 1992).
Transgenic potatoes with reduced SuSy activity exhibited a
marked decrease in the starch content of tubers and overall tuber
yield (Zrenner et al., 1995) confirming the earlier findings by Sun et
al. (1992). Similar to potato, antisense inhibition of SuSy in carrot
showed reduced utilization and increased accumulation of sucrose
in sink organs (Tang and Sturm, 1999). Similar inhibition of SuSy in
tomato resulted in decreased sink strength and reduced dry mat-
ter accumulation in fruits (D’Aoust et al., 1999). The reduced SuSy
expression also led to the decreased activity of SPS in the trans-
genic tomato fruits in their study. Similarly, a transient increase
in SuSy activity during early stages of tomato fruit development
correlated with fruit growth and sink strength suggesting the reg-
ulatory role of SuSy in controlling the sugar import (Chengappa et
al., 1999). Recently, Fernández et al. (2009) reported an increased
accumulation of tuber starch at the expense of sucrose in trans-
genic potato plant overexpressing SuSy gene. A reverse correlation
was observed in transgenic plants, indicating a balance between
SuSy- and acid invertase-mediated sucrolytic pathways determin-
ing sugar–starch inter-conversion in potato tubers.
3.3.4. ADP-glucose pyrophosphorylase (AGPase; EC 18.104.22.168)
It catalyzes the key step of starch biosynthesis by generat-
ing ADP-glucose and inorganic pyrophosphate (Pi) from glucose
1-phosphate and ATP. Maize mutants (bnttle-2 and shrunken-
2) with reduced AGPase activity contained only 25–30% of the
total starch content in their endosperm (Tsai and Nelson, 1996;
Dickinson and Preiss, 1969). Similar observations were reported
in rb embryo mutant of pea, adgl and adg2 mutants of Arabidop-
sis with reduced levels of AGPase activity (Lin et al., 1988a,b;
Smith et al., 1989). Reduced activity of AGPase in two starch-
deficient mutants of Arabidopsis TL25 and TL46 showed enhanced
sucrose accumulation and reduced starch accumulation in leaves
(Sun et al., 1999) indicating the role of AGPase in carbohydrate
partitioning and sucrose–starch conversion. Antisense repression
of AGPase in potato resulted in increased accumulation of glucose
and sucrose with concomitant increase in tuber number and tuber
fresh weight (Müller-Röber et al., 1992). In another study, trans-
genic potato plants down-regulated for AGPase showed reduced
leaf starch content while sucrose content was unaltered (Leidreiter
et al., 1995) owing to increased translocation of photo-assimilates
from source leaves to tubers. Similarly, overexpression of AGPase
showed increased rate of starch turnover in transgenic potato
tubers (Sweetlove et al., 1996). In a recent study, fruit specific sup-
pression of AGPase in transgenic strawberries showed decreased
fruit starch content to 27–47% and increased total soluble sugar
content to 16–37% (Park et al., 2006). All these studies suggested
the antisense down-regulation of AGPase in transgenic plants may
increase sucrose accumulation in fruits and vegetables.
3.3.5. Pyrophosphate d-frucrose-6-phospahte
1-phosphotransferase (PFP; EC 22.214.171.124)
evidence for the role of PFP in glycolysis, gluconeogenesis or catal-
ysis of a metabolite cycle between hexose phosphates and triose
in transgenic potato tubers (Hajirezaei et al., 1994) did not affect
plant growth, respiration and/or sucrose or starch pools signifi-
cantly. Whereas, down-regulation of PFP in transgenic sugarcane
odes due to elevated hexose-phosphate levels (Groenewald and
Botha, 2001, 2008; Groenewald, 2006; Van der Merwe et al., 2010)
indicating an inverse correlation between PFP activity and intern-
ode sucrose content confirming the earlier reports by Whittaker
and Botha (1999). These results suggested that PFP plays a role in
glycolytic carbon flux and carbohydrate partitioning as observed
in immature metabolically active sugarcane internodes (Van der
Merwe et al., 2010). Also, the decreased PFP expression led to a
reduction in inorganic pyrophosphate (PPi) levels in older intern-
odes indicating its role in gluconeogenesis. In contrary to earlier
reports, Kovacs et al. (2007) reported enhanced sucrose accumu-
lation in carrot taproots expressing PFP under cold and drought
unfavorable environmental conditions by PFP through promoting
the re-synthesis of transportable sucrose in taproots. These studies
indicated the dual role of PFP in sucrose–starch metabolism.
3.3.6. Sorbitol-6-phosphate dehydrogenase (S6PDH; EC 126.96.36.199)
alyzes the reduction of d-sorbitol 6-phosphate in the presence of
NAD+to produce d-fructose-6-phosphate, NADH and H+. Overex-
pression of apple S6PDH resulted in accumulation sorbitol sugar in
A. Nookaraju et al. / Scientia Horticulturae 127 (2010) 1–15
contained increased sorbitol and showed dwarf phenotype (Gao
et al., 2001). Higher accumulation of sorbitol in transgenic plants
resulted in either leaf necrosis or dwarfism due to the interference
of sorbitol with inositol biosynthesis leading to osmotic imbalance
and affecting carbohydrate allocation and transport. Transgenic
apple plants overexpressing S6PDH showed modified S6PDH activ-
than the untransformed control (Kanamaru et al., 2004). This study
further showed that S6PDH is a key enzyme regulating partitioning
of carbohydrates between sorbitol and sucrose and their accumu-
lation in apple leaves.
3.3.7. Fructose-1,6-bisphosphatase (FBPase; EC 188.8.131.52)
bisphosphate (FBP) into fructose-6-phosphate and inorganic
phosphate (Pi) with regeneration of primary CO2 acceptor,
ribulose-1,5-bisphosphate. The promotive role of FBPase in
sucrose synthesis was evidenced in transgenic Arabidopsis where
decreased expression of cytosolic FBPase led to decreased sucrose
synthesis, increased accumulation of phosphorylated intermedi-
ates with subsequent increase in starch synthesis (Strand et al.,
2000). So far, transgenic potato and tomato plants were developed
down-regulated for FBPase (Kossmann et al., 1994; Obiadalla-Ali
et al., 2004). Leaves of transgenic potato plants expressing plastid
localized cpFBPase showed increased synthesis of starch and
expression of transcripts encoding starch biosynthetic enzymes
when cultured on sucrose medium (Kossmann et al., 1992, 1994).
Also the transgenic potato plants with inhibited FBPase activity
below 15% of wild-type leaves showed reduced photosynthesis
leading to dramatic decrease in starch content coincided with
higher accumulation of soluble sugars (Kossmann et al., 1994).
Their experiments concluded that a little decrease of FBPase
resulted in increased photosynthesis and carbon assimilation
while a high FBPase repression impaired the both. Transgenic
potato plants expressing cytosolic FBPase activity below 20% of the
wild type activity led to the accumulation of 3-phosphoglyceric
acid (3-PGA), triose phosphate, and FBP (Zrenner et al., 1996). This
subsequently led to reduction in photosynthesis and sugar and
starch synthesis. Transgenic tomato fruits overexpressing a potato
FBPase under fruit specific fashion showed enhanced levels of
glucose and fructose at green and late ripening stage (Obiadalla-Ali
et al., 2004). Based on these studies on FBPase manipulation
in transgenic plants, it seems clear that altering FBPase levels
provokes dramatic effects on transgenic plants in terms of rate of
photosynthesis, starch accumulation, carbohydrate partitioning,
plant growth and yield.
3.3.8. Sucrose phosphorylase (SuP; E.C 184.108.40.206)
lation of other metabolic intermediates. It catalyzes the conversion
of sucrose to d-fructose and ?-d-glucose-1-phosphate. Expression
of bacterial SuP in transgenic potato tubers resulted in decreased
levels of glucose and fructose (Trethewey et al., 2001). Further,
the transgenic tubers showed higher accumulation of glycolytic
metabolites due to enhanced activity of key enzymes of glycolysis,
phosphofructokinase, trios phosphate isomerase, glyceraldehydes
Fernie et al. (2002b) reported increased sucrose breakdown and
decreased starch accumulation in potato tubers expressing SuP. A
strategy to increase sucrose accumulation in sink tissues by anti-
sense down-regulation of SuP may be exploited.
3.3.9. Phosphoglucomutase (PGM; EC 220.127.116.11)
It catalyzes the transfer of phosphate group between glucose-
1-phosphate and glucose-6-phosphate. Transgenic potato plants
down-regulated for cytosolic isoform of PGM showed decreased
starch accumulation in tubers (Lytovchenko et al., 2002) and
decreased tuber yield (Fernie et al., 2002a). While overexpression
of a bacterial PGM gene in potato resulted in increased leaf sucrose
et al., 2005). The transgenic tubers showed delayed rate of sprout-
ing and enhanced respiration.
3.3.10. Sucrose:sucrose 1-fructosyltransferase (1-SST; EC
Sucrose (Suc):Suc 1-fructosyltransferase is the key enzyme in
plant fructan biosynthesis, since it catalyzes de novo fructan syn-
thesis from sucrose and responsible for the modification of sugar
composition in plants. Sucrose:sucrose 1-fructosyltransferase (1-
SST) and sucrose:fructan 6-fructosyltransferase (6-SFT) were
involved in fructan accumulation during cold hardening of win-
ter wheat (Kawakami and Yoshida, 2002) and Patagonian grass
(del Viso et al., 2009). The results on wheat and Patagonian grass
showed the potential of 1-SST and 6-SFT for developing transgenic
plants with cold tolerance through modulating sugar composition
towards fructan synthesis. Isozyme studies suggested a close rela-
tionship between fructosyl transferases and acid invertases which
determine the sucrose accumulation (Luscher et al., 2000).
3.3.11. S-adenosylmethionine hydrolase (SAMase or AdoMetase;
This enzyme belongs to the family of hydrolases, catalyzing the
hydroxylation of S-adenosyl-l-methionine to form l-homoserine
and methylthioadenosine. Antisense down-regulation of SAMase
in Cantaloupe melon resulted in a significant reduction of ethy-
lene biosynthesis and increased soluble sugars’ accumulation in
transgenic fruits (Clendennen et al., 1999). The increased sugar
accumulation was attributed to delayed fruit slip by 1–3 days,
ilarly, Defilippi et al. (2004) observed a modulation in the cellular
ethylene regulation on sugar accumulation.
3.3.12. Sucrose isomerase (SI; EC 18.104.22.168)
It catalyzes the conversion of sucrose to isomaltulose and is also
referred as isomaltulose synthase. Purified sucrose isomerase was
found to mediate sucrose conversion into several other products
like isomaltose, trehalulose, glucose, fructose and isomelezitose
substitute. It is digested slowly than sucrose and thus has health
benefits for diabetics. Tuber-specific expression of an apoplasm-
targeted SI resulted in partial conversion of the low soluble sucrose
expression of Erwinia rhapontici SI in potato resulted in a quanti-
tative shift of sucrose to palatinose (other name for isomaltulose)
(Hajirezaei et al., 2003). The transgenic potato tubers were char-
acterized by accelerated respiration and starch breakdown during
storage suggesting that low sucrose levels trigger starch mobiliza-
tion in stored potato tubers. Wu and Birch (2007) developed trans-
genic sugarcane with vacuole specific expression of SI that resulted
in remarkable increase in total sugar levels along with a high value
sugar isomaltulose without significant depletion in stored sucrose.
The transgenic sugarcane lines with enhanced sucrose accumula-
tion was attributed to increased photosynthesis by delayed leaf
senescence, increased sucrose transport and sink strength.
A. Nookaraju et al. / Scientia Horticulturae 127 (2010) 1–15
3.3.13. Fructokinase (FRK; EC 22.214.171.124)
starch synthesis in sink tissues in conjunction with SuSy activity.
In sink tissues of potato and tomato, the activities of FRK and SuSy
parallel starch content (Ross et al., 1994; Schaffer and Petreikov,
1997). In addition, the localization of mRNA of both enzymes is
closely associated with starch-accumulating cells in young tomato
fruits (Wang et al., 1994; Kanayama et al., 1998). The expression
is high in young tomato fruit (Kanayama et al., 1997). Suppression
of tomato fructokinase 1 (LeFRK1) resulted in delayed flowering
while suppression of LeFRK2 resulted in reduction in stem and root
growth, number of fruits, flowers and seeds in tomato (Odanaka
et al., 2002). The retarded growth in earlier case was attributed to
had prevented utilization of sucrose in vascular channels for xylem
development leading to the inhibition of plant growth and wilting
of young leaves (German et al., 2003).
3.3.14. Pyruvate decarboxylase (Pdc; EC 126.96.36.199)
in the cytoplasm. A cDNA isoform of Pdc from strawberry (Fapdc1)
was found to be involved in fruit ripening and aroma biogenesis
under stressed conditions (Moyano et al., 2004). Transgenic potato
plants over expressing Zymomonas mobilis Pdc gene showed 5–12-
folds increase in leaf acetaldehyde and exported 2–10-folds higher
regulatory role of Pdc as sucrose exporter to sink tissues (Tadege et
3.4. Sucrose transporters and binding proteins
The long-distance transport of sugars in organisms depends
on a family of proteins that act as sugar carriers called sugar
transporters. Sugar transporters in different organisms including
human, plants and yeast belong to a major facilitator superfamily
(MFS) (Lalonde et al., 2004). There are at least 69 sugar trans-
porter homologues reported in Arabidopsis and were classified into
8 large families depending on the type of sugar they transport
(Shiratake, 2007). Among these, the sucrose transporters (SUT) are
the major sugar transporters in higher plants (Chang et al., 2004).
Sucrose transporters function in cellular proton-coupled sucrose
uptake and are thought to involve in loading sucrose into the
phloem of source leaves and uptake of sucrose into the cells of
sink tissues (Williams et al., 2000). Riesmeier et al. (1992) isolated
then many sucrose transporter genes have been identified and
characterized in different plant species (The Arabidopsis Genome
Initiative, 2000; Delú-Filho et al., 2000).
The SUC/SUT family was further divided into 3 subfamilies
namely SUC2/SUC1, SUC3/SUC2 and SUC4 based on the homol-
ogy. In most plants, more than one sucrose transporters exist. In
plants, sucrose transport activities were reported for isolated vac-
uoles and vacuolar membrane vesicles from different plant organs
such as taproots of sugar beet (Getz and Klein, 1995) and tomato
fruits (Milner et al., 1995). Few sucrose transporter genes belong to
et al., 1997) and pea (PsSUT1, Tegeder et al., 1999). It has also been
tive and seed tissues. The second subfamily of sucrose transporters
called SUT2 is structurally different from SUT1 having extended
domains at N terminus (30 amino acids longer than in SUT1). The
SUT2 genes were identified in tomato, potato (Barker et al., 2000)
and grape wine (Davies et al., 1999) though their exact function
is not well known. However, a potato SUT2 maps close to a major
as low-affinity sucrose transporter in veins of source leaves (Weise
et al., 2000). This StSUT2 was localized in bundle sheath cells of
in all green tissues and is diurnally regulated (Shakya and Sturm,
1998), where as DcSUT2 was mostly restricted to tap root. Their
studies suggested that DcSUT1 is responsible for phloem loading
and DcSUT2 responsible for sucrose uptake by storage parenchyma
cells. The SUT4 subfamily consists of low-affinity sucrose trans-
porters and these were identified in vegetables and fruit crops
such as carrot (Shakya and Sturm, 1998), fava beans (Weber et
al., 1997), grape berry (Manning et al., 2001), tomato and potato
(Weise et al., 2000). The expressions of LeSUT4 and StSUT4 tran-
scripts were detected in source and sink leaves, green tomatoes
and ovaries of flowers. In higher plants, the duplication of sucrose
transporter genes might have adaptive significance for multiple
roles and to enhance the sucrose transport capacity. Some of the
genes were expressed in crop species that showed altered sucrose
accumulation in sink tissues (summarized in Table 2).
Antisense suppression of sucrose transporter protein (P62) in
transgenic potato caused a reduction of carbohydrate efflux from
source leaves leading to an inhibition of root growth and photo-
synthetic rate and an increase in accumulation of carbohydrates
in leaves (Riesmeier et al., 1994). Similar results were reported in
potato with sucrose transporter (SUT1) by Kiihn et al. (1996). Seed
specific expression of potato SUT1 in pea led to increased sucrose
uptake by parenchyma cells of developing seeds (Rosche et al.,
2002). Overexpression of a spinach sucrose transporter (SoSUT1) in
potato resulted in decreased leaf sucrose content due to increased
sucrose transport to tubers (Leggewie et al., 2003). The trans-
genic tubers accumulated significantly higher levels of all soluble
sugars (sucrose, glucose and fructose) with insignificant effect on
starch content. These results together with the localization of SUT1
in sieve elements indicate that phloem loading occurs in sieve
elements by transmembrane uptake of sucrose directly from the
to be localized in sink tissues also (Riesmeier et al., 1994) though
its function in sink tissues was not clear. Antisense tuber specific
suppression of SUT1 in potato showed disturbed tuber physiol-
ogy and delayed tuber development (Kühn et al., 2003) confirming
the importance of sucrose transport for sink development. Studies
on transgenic maize plants overexpressing sucrose export defective
(SXD1) indicated the role of SXD1 protein in sucrose accumulation
in leaf mesophyll cells (Provencher et al., 2001). Similar manipula-
tion of SXD1 expression in transgenic leafy vegetables like lettuce
may increase the sugar content in leaves. However, silencing of
SXD1 by RNAi approach in potato resulted in enhanced accumu-
lation of total soluble sugars and starch in leaves due to impaired
photoassimilate export from source leaves to tubers (Hofius et al.,
2004). In addition, the transgenic plants showed reduced synthe-
sis of tocopherol indicating that potato SXD1 ortholog codes for
functional tocopherol cyclase (TC) in plants.
as mesophyll cells of young sink leaves, companion cells of mature
phloem and cells of cotyledon (Grimes et al., 1992; Overvoorde and
Grimes, 1994). Several lines of evidence suggest that sucrose bind-
ing protein (sbp) is also involved in sucrose uptake and transport
in plants (Overvoorde et al., 1997). Transgenic tobacco cell lines
overexpressing a sbp homologue from soybean (S-64) showed an
cell-wall invertase activity in addition to increased sucrose uptake
(Delú-Filho et al., 2000). These results indicate the potential for
manipulating sbp gene in transgenic plants to enhance sucrose
A. Nookaraju et al. / Scientia Horticulturae 127 (2010) 1–15
List of sucrose transporters and sucrose binding proteins influencing sucrose accumulation in transgenic plants.
Gene modifiedPlant species Metabolic change Reference
Sucrose transporter protein P62
Sucrose transporter protein SUT1
Sucrose export defective 1 (SXD1)
Spinach sucrose transporter (SoSUT1)
Inhibition of root growth and photosynthesis
Increased accumulation of carbohydrates in leaves
Enhanced production of sucrose in leaf mesophyll cells
Decreased leaf sucrose with corresponding increase in all soluble
sugars in tubers
Enhanced accumulation of soluble sugars and starch in leaves
Increased SuSy activity and decreased cell-wall invertase activity
Riesmeier et al. (1994)
Kiihn et al. (1996)
Provencher et al. (2001)
Leggewie et al. (2003)
Sucrose binding protein (S-64)
Hofius et al. (2004)
Delú-Filho et al. (2000)
OE: overexpressed; DR: down-regulated.
accumulation in fruits and other sink tissues of important food
3.5. Sweet proteins/taste modifying proteins
Sweet proteins and taste-modifying proteins are natural pro-
teins produced in plant and are natural alternatives to artificial
sweeteners and flavor enhancers. These proteins impart peculiar
sweet taste and flavor to the fruits. Presently, nine kinds of sweet
proteins have been identified. Out of them, eight proteins are from
plant origin (brazzein, curculin mabinlin, miraculin, monellin, pen-
the plant proteins, only mabinlin is stored in seeds and the others
are accumulated in fruits. Thaumatin and monellin are the most
potent sweet proteins and the amino acid sequence analysis of
these sweet proteins showed few similarities in their sequences
(Gibbs et al., 1996). Some of these proteins have been expressed
in crop plants like potato, tomato, lettuce, pear and cucumber to
produce sweeter fruits and other edible plant parts (Table 3).
inally isolated from the fruit of an African plant Pentadiplandra
brazzeana Baillon (Assadi-Porter et al., 2000a). This protein con-
tains 54 amino acid residues and is reported to be 500–2000 times
sweeter than sucrose (Izawa et al., 1996). Recombinant brazzein
protein was first expressed in Escherichia coli using synthetic gene
in maize and the protein was highly expressed (up to 4% of total
protein) in seeds (Lamphear et al., 2005). Recently, Yin et al. (2009)
expressed brazzein driven by AGPL1 promoter in tomato to pro-
3.5.2. Curculin and neoculin
Curculin was first extracted from Curculigo latifolia, a wild
plant that grows in West Malaysia and is considered to be a
high-intensity sweetener, with a reported relative sweetness of
et al., 1990). It consists of two identical 114 amino acid residue
subunits (Shirasuka et al., 2004). The sweet-tasting and taste-
modifying activities are exhibited solely by the heterodimer of
curculin 1 and curculin 2 isoforms (Suzuki et al., 2004). Neoculin
is a sweet modifying protein from the same source (C. latifolia). It
is approximately 500 times sweeter than sucrose by weight basis
(Yamashita et al., 1990) and the sweetness of neoculin is enhanced
in the presence of any acid (Yamashita et al., 1995). Immunohisto-
fruit especially at the basal portion (Okubo et al., 2008). Curculin
is a homodimeric form composed of the basic subunit (NBS) while
neoculin is the heterodimeric form composed of the acidic sub-
unit (NAS) and a basic subunit (NBS). Neoculin elicits a sweet-taste
response but curculin does not (Shirasuka et al., 2004; Suzuki et
al., 2004). Recently, neoculin has been heterologously expressed
in Aspergillus oryzae (Nakajima et al., 2006). So far no transgenic
studies were reported in plants for overexpression of curculin or
Lysozyme from egg white is one of the most thoroughly charac-
terized enzymes, and the sweetness of lysozyme is widely known
The lysozyme from hen egg white belongs to the c-type lysozymes,
and those from goose and ostrich egg white belong to the g-type
lysozymes. Goose egg lysozyme consists of a single amino acid
chain of 185 residues and has a molecular weight of 20,500. While
List of taste-modifying sweet proteins expressed in transgenic plants.
Gene cloned Promoter used Plant speciesMetabolic expression Reference
Brazzein Embryo preferred
Brazzein highly expressed (up to 4% of total protein) in seeds
Accumulated miraculin protein (33.7–43.5?gg−1FW) in leaves
Lamphear et al. (2005)
Yin et al. (2009)
Sun et al. (1997)
Sun et al. (2006)
TomatoAccumulated miraculin protein (102.5 and 90.7?gg−1FW) in
leaves and fruits
Accumulated miraculin protein (0.5–2.0?gg−1FW) in fruits
Sun et al. (2007)
5?UTR of psbA
StrawberrySugaya et al. (2008)
Accumulated monellin (23.9?gg−1FW) in fruits
Lower accumulation of monellin protein
Enhanced accumulation of monellin in chloroplasts
Imparted sweet taste
Penarrubia et al. (1992)
Penarrubia et al. (1992)
Roh et al. (2006)
Demonstrated taste modification
Low levels of sweetness expression
Increased fruit sweetness and generated a liquorice aftertaste
Enhanced tolerance to Botrytis cinerea fruit rot
Lebedev et al. (2002)
Szwacka et al. (2002)
Bartoszewski et al. (2003)
Schestibratov and Dolgov
ND: no details available.
A. Nookaraju et al. / Scientia Horticulturae 127 (2010) 1–15
the molecular weight of hen egg lysozyme was about 14,500. Egg
white lysozyme is an acceptable food protein and has potential
application in transgenic technology for enhancing the quality of
fruits and vegetables.
Mabinlin is another major sweet protein stored in the seeds
of Capparis masaikai Lévl. possessing the highest known thermo-
stability (Guan et al., 2000). It consists of an A chain with 33 amino
acid residues and a B chain composed of 72 residues and is esti-
mated to be about 100–400 times sweeter than sucrose on weight
plants (Hu et al., 2009). So far, attempts were made to express
mabinlin protein in transgenic potato (Sun et al., 1997).
Miraculin is a taste-modifying protein originally extracted from
Richadella dulcifica, a shrub native of West Africa by Kurihara and
Beidler (1968). The protein is a single polypeptide with 191 amino
acid residues (Theerasilp et al., 1989). The taste-modifying protein
miraculin has the unusual property of being able to modify a sour
taste into a sweet taste. This protein is highly accumulated in ripe
fruit of miracle fruit and its content can reach up to 10% of the total
soluble protein in the fruits (Sun et al., 2006). Immunocytolocal-
ization studies revealed that miraculin protein is secreted in the
intercellular spaces of miracle fruits and transgenic tomato fruits
(Hirai et al., 2010). A synthetic gene encoding miraculin protein
when expressed in transgenic lettuce resulted in the accumulation
of significant amount of miraculin protein in the leaves (Sun et al.,
2006). Recently, the miraculin protein was also expressed in trans-
genic tomato plants (Sun et al., 2007) and strawberry (Sugaya et
al., 2008) although the miraculin content in these plants was at
least two times lower than in miracle fruit (Sun et al., 2007). The
accumulation of the miraculin protein in transgenic tomato fruit
increased with fruit development and reached its highest level at
the overripe stage (Kim et al., 2010).
Monellin was first purified from the African berry Discoreophyl-
(Edens and van der Wel, 1985). It consists of two non-covalently
and a B chain of 50 amino acid residues (Ota et al., 1999). This
protein when expressed in Candida utilis under glyceraldehydes-3-
phasphate decarboxylase promoter showed monellin accumulation
A single-chain monellin was introduced to enhance the flavor and
sweetness of tomato and lettuce (Penarrubia et al., 1992). Unfor-
tunately the transgene showed lower expression in the transgenic
plants. This limitation was overcome by expressing the monellin
gene under psbA 5?UTR which resulted in enhanced accumulation
of monellin in the transformed tobacco chloroplasts (Roh et al.,
a shrub found in tropical forests of few African countries (van der
Wel et al., 1989). The protein was reported to be around 500 times
sweeter than sucrose on a weight basis. It is a 12-kDa protein con-
sisting two subunits coupled by disulfide bonds (Faus and Sisniega,
2004). So far, no transgenic studies were attempted to overexpress
pentadin protein in transgenic plants.
The thaumatins are a class of intensely sweet proteins iso-
lated from the fruit of the tropical plant Thaumatococcus danielli.
It consists of 207 amino acid residues with eight intramolecular
disulfide bonds and contains no free cysteine residues. The pro-
tein is about 10,000 times sweeter than sugar (Ogata et al., 1987).
Thaumatin was first time cloned among the sweet proteins in E.
coli (Edens et al., 1982). Tattersall et al. (1997) observed accu-
mulation of thaumatin-like protein in high levels at the onset of
sugar accumulation and berry softening in Vitis vinifera cv. Mus-
cot of Alexandria. Accumulation of this protein conferred tolerance
in berries to fresh infection of Botrytis fungus. This protein was
also successfully introduced in potato hairy roots (Witty, 1990),
pear (Lebedev et al., 2002), cucumber (Szwacka et al., 2002) and
tomato (Bartoszewski et al., 2003). The transgenic potato hairy
roots, pear leaves, cucumber and tomato fruits showed increased
sweetness by sensory analysis indicating the potential of produc-
plants overexpressing thaumatin II protein showed enhanced tol-
erance to Botrytis fruit rot (Schestibratov and Dolgov, 2005, 2007)
confirming the earlier reports by Tattersall et al. (1997) in grapes.
Production of these recombinant taste-modifying sweet proteins
in transgenic plants will open up the exciting area of metabolic
engineering of fruits and vegetables with enhanced sweetness and
4. Conclusions and perspectives
sweetness and flavor determined by the amount and relative com-
position of soluble sugars and organic acids. Sugars are also being
recognized as regulatory molecules having signaling functions in
plants and other organisms. However plant sugar signaling is con-
interactions and the intimate integration of a web-like signaling
network governed by plant hormones, nutrients, and environmen-
energy transfer (FRET) based imaging will hopefully circumvent
this limitation and provide critical information to facilitate the
elucidation of intracellular sugar signal transduction pathways.
Changes in the activity of enzymes in sugar metabolism determine
the carbohydrate partitioning and sugar accumulation in fruits.
Engineering of plants for manipulating the expression of sucrose
metabolic enzymes in the transgenic plants resulted in significant
changes in the accumulation of sucrose and other sugars. As fruc-
tose is twice as sweet as glucose the modification of the fructose
to glucose ratio without changing the overall sugar level through
flavor. Manipulation of the expression of sucrose transporter pro-
teins is another potential alternative to increase the sucrose export
from source leaves to sink tissues. This strategy may be appli-
cable to tissue specific accumulation of carbohydrates (sucrose)
by either expressing or down-regulating sucrose transporter pro-
teins. Being thousands of times sweeter than sucrose and with low
cation in quality enhancement of fruits and vegetables through
metabolic engineering. Present review will be extremely useful to
plant biotechnologist and plant breeders in designing strategies for
developing plants bearing sweeter fruits.
Authors thank Konkuk University for granting Brain Pool Post-
Doctoral fellowship to Dr. Nookaraju. Authors also thank Mayank
A. Gururani for critical review of the manuscript. Work in our labo-
A. Nookaraju et al. / Scientia Horticulturae 127 (2010) 1–15
ratory focusing on the topic of this review is funded by 2010 Brain
Pool program of Konkuk University.
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