African Journal of Biotechnology Vol. 8 (10), pp.

2004-2010, 18 May, 2009

Available online at
http://www.academicjournals.org/AJB ISSN 1684–5315
© 2009 Academic Journals

Review

Roles of plant soluble sugars and their responses to

plant cold stress
1 1 1 2,3,4
Ma Yuanyuan , Zhang Yali , Lu Jiang *, Shao Hongbo
1
The College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, China.
2
State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water
Conservation, Chinese Academy of Sciences, Yangling 712100, China.
3
Shandong Key Laboratory of Eco-environmental Science for the Yellow River Delta, Binzhou
University, Binzhou256603, China.
4
Institute for Life Sciences, Qingdao University of Science & Technology (QUST), Qingdao266042, China.
Accepted 17 March, 2009

Plants can enhance freezing tolerance by gradual exposure to low temperature known as cold
acclimation. Soluble sugars have been confirmed to play an important role during the process. This is
based on the fact they are most commonly detected in various species of terrestrial plants that have
undergone seasonal cold acclimation. Soluble sugars exert their positive effects to protect plant cells
from damage caused by cold stress through many ways including serving as osmoprotectants,
nutrients as well as interacting with the lipid bilayer. In addition to these functions, more focus is on
their important hormone-like functions as primary messengers in signal transduction nowadays. On the
other hand, higher sugar concentrations can trigger leaf senescence, which indicates that the
accumulation of soluble sugars during cold acclimation might impact on plants negatively. Further
study can be done to investigate the mechanisms by which soluble sugars are involved in the plants’
response to the cold signal by advanced molecular biology methodology to examine sugar-regulated
gene expression under cold condition.

Key words: Plants, sugars, cold acclimation, signal transduction,

biotechnology.

THE IMPACT OF SOLUBLE SUGARS ON THE COLD ACCLIMATION

Cold stress causes several dysfunctions at cellular level;
these include damage to membranes, generation of
reactive oxygen species, protein denaturation and
accumulation of toxic products etc (Bowers, 1994; Shao
et al., 2008). In nature, plants may exhibit cold tolerance
due to gradual exposure to low non-freezing tempera-
tures, and the process is known as cold acclimation
(Thomashow, 1999).
The advent of molecular biology has propelled research
in this area over the past two decades; today some of the
events of cold signal perception, transduction and cold
acclimation are defined at the molecular level (Shinozaki
et al., 2000; Shinozak et al., 2001; Zhu, 2001;
Thomashow, 2001; Shao et al., 2006, 2007). Cold
acclimation is associated with multiple mechanisms that
*Correspondence author. E-mail: shaohongbo@qust.edu.cn,
jiang.lu.cau@gmail.com. Tel: 86 532 84023984.
include changes in (a) gene expression (b) membrane
composi-tion and cryobehaviour (Orvar et al., 2000; Shao
et al., 2008) (c) elevation of ABA (Lang et al., 1994) (d)
antioxidants (Kang and Saltveit, 2002; Shao et al., 2008)
(e) accumulation of substantial amounts of compatible
solutes, such as soluble sugars (Ristic et al., 2003;
Wanner et al., 1999), amino acids (Lalk et al., 1985;
Wanner et al., 1999; Koster, 1991; Shao et al., 2006) and
glycine betaine (Kishitani et al., 1994), which are thought
to play a role in protection of cells from freezing injury
(Figure 1). Although so many changes occur during cold-
acclimation, soluble sugars have been confirmed to play
an important role based on the fact they are most
commonly detected in various species of land plants that
have undergone seasonal cold acclimation, including
angio-sperms, gymnosperms, and lower land plants such
as bryophytes (Saka and Larcher, 1987; Rutten and
Santarius, 1992). It has been reported that under natural
conditions, soluble sugars increase during the onset of
winter when plants are subjected to low temperatures;
 Yuanyuan et al. 2132
1321

Figure 1. The well known changes during the process of cold acclimation.
2142 Afr. J.
1421 Biotechnol.
conversely, soluble seasonal cold acclimation of freezing tolerance to 0
sugars decrease in in woody plants, along levels so high that some 6
spring when plants are with development plants can even tolerate )
deacclimating (Sakai, to freezing in liquid .
1962; Siminovitch, nitrogen without Up to now, researchers
1981). Sugar content also cryoprotectants (Sauter have isolated several
increases during cold et al., 1996). mutant lines of
acclima- tion under Arabidopsis that are
artificial conditions impaired in their freezing
(Koster and Lynch, 1992; VARIOUS STUDIES tolerance after cold
Sasaki et al., 1996; Shao INVOLVED IN THE acclimation, such as the
et al., 2006-2008). EFFECT OF SOLUBLE sfr (sensi- tivity to
SUGARS freezing) mutants. These
mutants have provided
DIFFERENT SUGARS Aside from the researchers a good
INVOLVED IN THE accumulation in insight into the
COLD ACCLIMATION endogenous sugars, it relationship between the
has been revealed that sugars and freezing
It has been proved that exogenous application of resistance in the plants.
many kinds of soluble soluble sugars resulted in The freezing tolerance in
sugars are included in the an increase in freezing these plants before cold
course of cold tolerance in various acclimation is unaffected
acclimation. For instance, higher plant species. which allows the freezing
European habitats which There has been report sensitivity of the sfr
possess substantial that pre-incubation with mutants to be specifically
degrees of freezing glucose increased attributed to defects in
tolerance have exhibited survival after the
higher degrees of cryopreservation of
freezing tolerance in cabbage leaf cells
winter than in summer. (Jitsuyama et al.,
Increase in freezing 1997), and pre-incubation
tolerance in these with sucrose enhanced
mosses appeared to be survi- val Jerusalem
associated with artichoke cells after
accumulation of soluble cryopreservation (Harris
sugars, espe- cially that et al., 2004). Moreover,
of sucrose (Rutten and improved freezing tole-
Santarius, 1992). Also, rance in Arabidopsis
chilling of muskmelon thaliana protoplasts
plants led to the occurred after the
accumulation in the exogenous application
source leaves of large of sucrose (Uemura et
amounts of starch, al.,
sucrose, and hexoses, as 2
has been reported 0
previously for many plant 0
species (Paul, 1991; 3
Paul, 1990). In addition, it ;
has been demonstrated
that the levels of a few L
oligosac- charides i
increase during cold
acclimation, typically in e
cereals and woody t
plants, both of which
develop high degrees of a
freezing tolerance in l
winter. Galactosyl- .
sucrose oligosaccharides ,
such as raffinose and
stach- yose are
2
commonly found to
0
accumulate during
Yuanyuan et al. 2152
1521
2162 Afr. J.
1621 Biotechnol.
acclimation process, Columbia ecotype, shows cryostability of cellular that they may function as
rather than generalized greater freezing tolerance membranes. Increased nutrients which make
debilitation. Using than that of the Columbia membrane cryostability plants survive the
electrolyte leakage ecotype (Klotke et al., is a prerequisite for decreased temperature
assay, the quantitative 2004). freezing tolerance and dryland condi- tions
exami- nation of freezing because freeze-induced as well as recover from
tolerance of all the sfr destabilization of cellular freezing-stress (Eagles
mutants was achieved. THE FUNCTIONAL membranes is the et al., 1993; Trunova;
The results showed all ROLES OF SOLUBLE primary cause of injury 1982; Shao et al., 2008).
the sfr mutants actually SUGARS DURING in
increased their freezing COLD ACCLIMATION plants
tolerance during cold (Steponkus et al., MORE FOCUS ON
acclimation, but to a less All of these facts suggest 1993; Shao et al., THE ROLES OF
extent than the wild type. critical roles for these 2008). SOLUBLE SUGARS AS
The deficit was greatest sugars as compatible An additional role of SIGNALING
in the sfr4 mutant, solutes in freezing sugars during cold MOLECULES
according to its high tolerance. The mecha- acclimation is
degree of sensitivity in nisms by which Although there have been
survival tests on intact sugars act to many functional soluble
plants (Warren et al., influence freezing sugars that act as
1996). Subsequently, it resistance are just documented above,
was detected that sfr4, beginning to be nowadays, more and
alone among the deciphered. Sucrose more attention has been
mutants, showed levels of glucose, fructose and put on the important
freezing tolerance similar oligosaccharides such as hormone- like functions of
to those of wild-type raffinose as well as soluble sugars as primary
(WT) plants when grown stachyose are messengers in signal
at ambient temperatures commonly found in transduction. The
but, unlike WT plants, soluble sugars that pivotal role of sugars
underwent a reduction in accumulate along with as signaling molecules is
its Suc and Glc contents, development of freezing well illustrated by the
in contrast to the increase tolerance in higher plants. variety of sugar sensing
shown by wild type during It has been suggested and signaling
cold acclimation that these sugars not mechanisms discovered
(McKown et al., 1996; only serve as in free-living
Uemura and Steponkus, osmoprotectants but also microorganisms such as
2003). play a role in protecting bacteria and yeast
In addition to these cellular membranes from (Rolland et al., 2001;
mutants, there have damage caused by Stulke and Hillen, 1999;
existed many studies dehydration and freezing Wang et al., 2008; Xiao
indicating that transgenic through interacting with et al., 2009).
plants over-accumu- the lipid bilayer Based on the
lating raffinose have (Anchordoguy et al., biochemical, molecular,
higher degrees of 1987; Shalaev and and genetic experiments,
freezing resistance than Shalaev, 2001; Shao et it has been concluded
do wild-type plants (Taji al., 2006). It is also that soluble sugars play
et al., 2002; proposed that the role of a central role in the
Pennycooke et al., some oligosaccharides is control of plant
2003). Perennial to prevent crystallization metabolism, growth, and
ryegrass plants which of sucrose, thus development. Moreover
were transgenic to facilitating glass formation many researches have
express wheat fructosyl- within the cell, leading to revealed interactions that
transferase genes protection of membrane integrate light, abiotic and
accumulate increased phospholipids biotic stress, and
amounts of fructan and (Anchordoguy and hormone signaling
acquire enhanced Leopold, (Roitsch, 1999; Sheen,
resistance on a cellular 1989; Crowe et al., 1999; Smeekens, 2000;
level to freeze (Hisano et 1988). Generally Gazzarrini and McCourt,
al., 2004). It has also speaking, the 2001; Finkelstein and
been reported that the accumulation of Gibson, 2002) and
Arabidopsis ecotype C24, soluble sugars coordinate carbon and
which accumulates more contributes to the nitrogen metabolism (Stitt
raffinose than does the increase in the and Krapp, 1999; Coruzzi
 Yuanyuan et al. 2172
1721
and Bush, 2001; Coruzzi 2).
and Zhou, 2001; Uddin et As mentioned above,
al., 2008; Wang et al., sugar-sensing and
2008; Xiao et al., 2009). sensing of the
Abiotic and biotic stress environment appear to be
stimuli, such as drought, part of a complex
salinity, wounding, and regulatory web (Gibson,
infection by viruses, 2000). In relation to cold,
bacteria, and fungi, can high sugar supply
modulate source-sink
activities. Because
extracellular invertase, a
key enzyme for
hydrolyzing Suc (Sturm,
1999), is regulated by
stress stimuli and hor-
mones, it has been
proposed to be a central
modulator of assimilate
partitioning, integrating
sugar, stress, and
hormone signals
(Roitsch, 1999). In
addition, many
jasmonate-, ABA-, and
stress-inducible genes
are co- regulated by
sugars (Reinbothe et al.,
1994; Sadka et al.,
1994; Shao et al., 2005-
2008; Uddin et al., 2008;
Wang et al., 2008).
How plants sense
cold is unknown. A
fall in temperature can
reduce the fluidity of
membranes, and this
appears to be an
effective direct sensor of
cold in cyanobacteria.
Another possibility is that,
in light, photosynthetic
cells may sense cold
through an effect on
photosystem 2
excitation pressure
(Gray et al., 1997;
Huner et al., 1998).
Molecular studies have
shown that cold
acclimation in higher
plants is complex
involving multiple
regulatory pathways
(Fowler and
Thomashow,
2002), furthermore while
some of the signal
transduction pathways
interact, others are
independent (Xin and
Browse, 2000). Thus
more than one sensor of
cold is possible (Figure
2182 Afr. J.
1821 Biotechnol.

Figure 2. Sugars-involved into the events occurring in plants under cold stress (Shao et
al., 2008).
 Yuanyuan et al. 2192
1921
induces fructan genes are also induced Uddin developing organs
accumulation, which is by dehydration (due to et al., (Smart, 1994; Smart et
also a usual res- ponse water deficit or high salt) 2008; al., 1995; Williams et al.,
of grasses to cold and ABA, and can be Wang 1997).
(Winter, 1994; Wang et collectively called cold- et al., Although senescence
al., responsive 2008) occurs in an age-
2 genes. Cold-responsive . dependent manner in
0 genes are regulated many species (Noode`n,
0 through C- 1988), its initiation and
8 repeat/dehydration- progression can be
THE INVOLVEMENT OF
; responsive elements modulated by a variety of
SUGARS IN LEAF
(CRT/DRE) and abscisic environ-
SENESCENCE
X acid (ABA)-responsive
i elements (cis elements),
a C-repeated binding Soluble sugars help
o factors/dehydration- ensure an adequate
responsive element supply of building
e binding proteins materials and energy to
t (CBFs/DREBs) and carry out specific
basic leucine zippers developmental programs.
a (bZIPs) (SGBF1), For example, in-vivo and
l respectively. It has been in- vitro experiments
. reported that expression suggest that in some
, of key regulators of plant species, increasing
abiotic stress responses sugar levels delay seed
2 such as CBF3, COR15A, germination and stimulate
0 and RD29A was induced the induction of flowering
0 by both glucose and and senescence. In other
9 ABA. Constitutive words, it may be
) expression of CBF3 in beneficial for plants to
. transgenic Arabidopsis adjust the timing with
New insights into the plants induces expression which nutrient-intensive
mechanisms by which of target COR (cold- events occur to supply
sugar- response regulated) genes to enough materials and
pathways interact with enhance freezing energy for successful
cold response pathways tolerance in non- completion of those
have been supported by acclimated plants. events. Levels of sugars,
micro-array experiments Expression of COR15A such as sucrose, have
exami- ning sugar- and RD29A is regulated been postulated to
regulated gene by CBF3, suggesting that affect the timing at
expression under glucose may contribute to which some plant species
different conditions. the regulation of cold flower (Bernier et al.,
Based on the fact, it has stress tolerance (Yunhai 1993). Soluble sugar
been elucidated that et al., 2006; levels have also been
many sugar-regulated shown to affect other
genes are involved in phase changes, such as
the cold- induced gene the onset of senescence
expression. (Paul and Pellny, 2003).
Cold acclimation is Endogenous leaf sugar
accomplished by the levels tend to increase
expression of many cold- during senescence.
regulated genes Similarly, application of
(Thomashow, 2001; exogenous sugars
Zhu, stimulates the early
2001). In Arabidopsis, stages of senescence.
these genes are called rd Leaf senescence is the
(respon- sive to last step in the life cycle
dehydration), erd (early of plants. During the
responsive to process, materials used
dehydration), lti (low- to build up leaves during
temperature induced), kin vegetative growth are
(cold induced) and cor remobilized and
(cold-regulated). These transported into the
2202 Afr. J.
2022 Biotechnol.
 Yuanyuan et al. 2212
2122
mental factors such as leaves. A possible source the induction of freezing tolerance in the
temperature, mineral of hexoses is the senescence by sugar plants. What roles of
deficiency, and drought breakdown of starch. In accumulation (Zhao et sugars play during cold
conditions, as well as addition, Jongebloed et al., 2008; Shao et al., acclimation is
by internal factors such al. (2004) showed that 2008; Bressan et al., complicated by the fact
as plant growth phloem blockage by 2009). that sugars can act by
regulators (Grbic and callose deposition could affecting osmotic
Bleecker, lead to an age-dependent potentials as well as by
CONC
1995; Buchanan- sugar accumulation. functioning as signaling
LUSIO
Wollaston, 1997; Nam, molecules. On the other
N
1997; Weaver et al., hand, sugars affect
THE DUAL ROLES OF AND
1997; Dai et al., 1999; developmental programs
SUGARS POSSIBLY PERS
Uddin et al., 2008; Wang ranging from
INVOLVED IN PECTI
et al., embryogenesis to
ENCOUNTERING COLD VES
2 senescence, which
0 STRESS makes the research
Alterations in the levels
0 of soluble sugars, such more complex. On the
During cold acclimation,
8 basis of the fact that
soluble sugars as glucose and sucrose
) leaves which have
accumulated which could have been shown to
. developed in the cold do
theoretically have affect the
Since senescence can not display the typical
adverse impact on photo-
be induced by a large down-regulation of
synthesis as well as
number of different photosynthesis in
induce senescence.
conditions, and several response to sugar
Nevertheless, cold-
signaling pathways are accumulation, it is
acclimated leaves do not
involved in the regulation possible that induction of
show the typical
of senescence the cold acclimation
repression of
(Buchanan- Wollaston, pathway have resulted in
photosynthesis by sugars
2003), it is possible that decreased sugar
(Strand et al., 1997; Li
environmental signals are sensitivity and thus
and Huang, 2008). On the
integrated by sugar delayed senescence.
other hand, it has been
signaling. For example, Further studies about
hypothe- sized that
experi- ments on sugar the actual roles that
photosynthetic activity is
regulated senescence sugars play in plants’
regulated in a feedback
indicate that leaf response to cold stimuli
manner by soluble
senescence can be can be done by scanning
sugars. The
induced by growing lists of sugar-regulated
photosynthetic machinery
Arabidopsis plants in the genes expression under
might be down-regulated
presence of 2% glucose cold condition using
by sugars due to the
in combination with low various advanced
cold-girdling petioles to
nitrogen supply (Pourtau technologies such as
prevent sugar export out
et al., 2004; Wingler et microarray experiments.
of the leaf. Also, in these
al., On the basis of these
cases, genes related to
2004). Affymetrix research investigations,
photosyn- thesis were
GeneChip data confirmed we might get new insight
repressed, including
that changes in gene into mechanisms by
those for chlorophyll
expression during which sugar-response
binding protein and
glucose-induced pathways interact with
Rubisco (Smeekens,
senescence are other response pathways
2000).
characteristic of in the cold-triggered
However more
developmental response. At the same
complicated it is, there
senescence. Simi- larly, time, we will have a
have been studies
Stessman et al. (2002) promising perspective by
showing increased flux
found that hexoses accu- bioengineering plant
through the Suc biosyn-
mulate in senescing responses to cold stress
thetic pathway that
Arabidopsis leaves. by sugar functions.
reduces inhibition of
However, the question
photosynthesis in the cold
remains as to what
(Strand et al., 2003). It A
causes the strong
was therefore conceiv- C
accumulation of hexoses
able that cold acclimation K
despite the decline in
could interact with N
photosyn- thetic carbon
metabolic regulation of O
assimilation in senescing
senescence by inhibiting
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