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Role of gibberellins in regulation of source-sink relations under optimal and

limiting environmental conditions

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REVIEW ARTICLE

Role of gibberellins in regulation of source–

sink relations under optimal and limiting
environmental conditions
Noushina Iqbal, Rahat Nazar, M. Iqbal R. Khan, Asim Masood and
Nafees A. Khan*
Department of Botany, Aligarh Muslim University, Aligarh 202 002, India

nutrients2. The integrated mechanisms induced by gibber-

Gibberellins (GAs) are plant growth regulators that
are known to stimulate physiological responses in plants ellic acid (GA3) enhance the source potential and redistri-
and alter the source–sink metabolism through their bution of photosynthates increases sink strength2. Plant
effect on photosynthesis and sink formation. GAs growth and development are normally limited by photo-
promote fructose-1,6-biphosphatase and sucrose phos- synthetic resources, i.e. ‘source-limited’. The source
phate synthase and stimulate phloem loading. Photo- activity drives the sink metabolism and in turn is related
synthate translocation from source to the developing to C and N metabolism. The supply of photoassimilate
sink is a major contributing factor towards increasing for growth and differentiation during plant development
the sink strength, and GAs are the key regulators of originates from leaves of the plants and the demand for
the process through which the extracellular invertase photosynthate changes as plants grow, mature and
involved in phloem unloading, carbohydrate partition- senescence. The regulatory role of phytohormones in selec-
ing and growth of sink tissues is induced. Gibberellic
tive ion uptake and distribution in plants through their ef-
acid is the major contributor in the process of source
and sink formation and is one of the most commonly fect on membrane properties and transport of assimilates
studied GAs. Recent studies indicate that GA signal- has been shown3. The role of GA has been shown in
ling is involved in adjustment of plants under limiting influencing the source–sink relationship by affecting
environmental conditions and maintains source–sink various plant processes4. GA3-mediated increase in photo-
relation. This adjustment could be mediated through synthesis and utilization of soil nitrogen (N) was the
the influence of GA on the regulation of salicylic acid cause of increase in source–sink relation in mustard5. The
biosynthesis. Here we focus on the developments and action of GA promotes sucrose synthesis within the leaf
understanding of integration of GA action with the through their positive effect on fructose-1,6-biphosphatase
metabolic process under optimal and limiting envi- and sucrose phosphate synthase. In addition, GA stimu-
ronmental conditions for maintaining source–sink lates phloem loading through its action on cell turgor,
relation. Further advances in the crosstalk between
apoplast pH and hormone concentration6. Moreover,
gibberellins and salicylic acid are discussed with ref-
erence to abiotic stress tolerance and source–sink rela- GAs also mediate assimilate translocation through
tion. increase in extracellular invertase which is responsible
for phloem unloading into the sink, thereby increasing the
strength.
Keywords. Gibberellins, invertase, phloem loading, sink, GAs are also known to induce various physiological
source, stress. responses in plants and alter plant metabolism under
stress. In addition to the role of GAs in the regulation of
GIBBERELLINS (GAs) constitute a group of tetracyclic plant responses to biotic stress, recently, their role in
diterpenes best known for their influence on seed germi- early plant abiotic stress responses has been documented
nation, leaf expansion, stem elongation, flower and in Arabidopsis through modulation of salicylic acid (SA)
trichome initiation, and flower and fruit development1. levels7. GAs probably increase SA level through a member
They play an important role in modulating diverse proc- of the Gibberellic acid stimulated in Arabidopsis (GASA)
esses throughout plant development and are known to gene family and thus show the existence of a crosstalk
improve the photosynthetic efficiency of plants through between these two plant hormones in Arabidopsis in the
their influence on photosynthetic enzymes, leaf-area alleviation of abiotic stress8. GA action in alleviating
index, light interception and enhanced use efficiency of oxidative stress generated due to the production of reac-
tive oxygen species under stress conditions has been
under focus recently9. GAs are found to enhance photosyn-
*For correspondence. (e-mail: naf9@lycos.com) thetic rate and invertase activity under stress10, favouring

998 CURRENT SCIENCE, VOL. 100, NO. 7, 10 APRIL 2011

 REVIEW ARTICLE
seedling growth under stress condition9. The present assisting in the change of rosette plants in long stem and
review focusses on the understanding of the develop- bolting.
ments in GA actions in the regulation of source–sink rela- In recent years, significant progress has been made in
tion in plants under optimal and abiotic stress conditions the identification of upstream GA signalling components
and its impact on overall physiology and metabolism of and trans and cis-acting factors that regulate downstream
plants. GA-responsive genes in higher plants. GAs appear to
derepress the signalling pathway by inducing proteolysis
of GA signalling repressors (the DELLA proteins).
Action of GAs in plants Recent evidence indicates that the DELLA proteins are
targeted for degradation by an E3 ubiquitin ligase SKP1–
GAs belong to a large family of diterpene acids. Over 136 CULLIN–F-box (SCF) complex through the ubiquitin-26S
naturally occurring GAs are known11. These are abbrevi- proteosome pathway27. KNOX homeodomain proteins
ated as GA with a subscript such as GA1, GA2, GA3, GA4 and MADS-box proteins (that determine plant architec-
and so on, of which GA3, commonly known as gibberellic ture during the vegetative and reproductive phase) are
acid, is the most important GA in plants. GAs and GA- transcription factors that preferentially accumulate in
like substances have been found in almost all the repre- indeterminate cells around the shoot apical meristem
sentatives of the plant kingdom ranging from bacteria (SAM), but not in determinate lateral organs such as
through fungi to angiosperms. They are produced in roots leaves28. KNOX proteins are considered to play a role in
and younger leaves, but have their highest concentration the maintenance of the indeterminate meristematic iden-
in seeds of higher plants. GA3 is the first widely available tity of cells that constitute SAM29. The KNOX protein
active form of commercial GAs. It is an economically NTH15 from tobacco was shown to bind to the promoter
important secondary metabolite12 formed as the end- sequence of the GA biosynthetic 20-oxidase gene Ntc12
product of the GA pathway13. GA3 acts as a hormone, (ref. 30), involved in the oxidation steps leading to the
regulating several processes of plant development13. It formation of the bioactive GA1 (ref. 17).
works with other hormones to promote rapid elongation
and division of cells.
Receptor and binding proteins on the plasma mem- GAs in source–sink relations under optimal
brane to perceive the hormones have been identified. GAs conditions
act on the outer face of the plasma membrane14. The
involvement of G protein in the early GA signalling event Several factors either endogenous or environmental con-
in aleurone cells has been reported by Jones et al.15. GAs ditions contribute to sink strength, but the sink activity
are synthesized from geranylgeranyl diphosphate produced can mainly be enhanced by GAs31. The influence of GA3
mainly through the plastidial methylerythritol phosphate on plant source is through increasing photosynthetic
pathway16. Geranylgeranyl diphosphate is converted to potential of plants, whereas its efficiency in assimilate
bioactive GAs through the activity of terpene cyclases, transport helps enhance the sink strength, thus establish-
P450 monooxygenases and 2-oxoglutarate-dependent ing its role in the source–sink system.
dioxygenases17. Among the latter class of enzymes, GA20- Sink potential is determined after growth and flower-
oxidase and GA3β-hydroxylase catalyse the last steps of ing, and phytohormones have a prominent role in modify-
the synthesis of GA4, the major GA in Arabidopsis ing it. Phytohormones might function in enhancing sink
shoots18. The genes encoding these enzymes were shown potential via increasing cell number and/or regulating cell
to be subjected to negative feedback regulation by the differentiation such as plastid biogenesis and DNA ampli-
action of GA itself17. fication, or by modifying the duration or rate of dry mass
GA is known to affect plant morphology19. GA3 in- accumulation of developing reproductive organs32.
creases shoot length by increasing its rate of elongation in Improvement in harvest index of many crops in response
majority of the plants, including Brassica campestris20 to phytohormones has been observed24. The source pro-
and red sanders21. Root length was also observed to duction is responsive to sink metabolism and this makes
increase by GA3 treatment in Lupinus albus22. GA3 optimum use of C and N resources33. Photosynthesis is
increased dry matter and leaf-area index in mustard the main driving force influencing dry matter partitioning
plant23, and photosynthetic rate in leaves of bean24,25 and and organ formation. GAs are important in influencing
wheat26. Khan et al.24 reported an increase in the activity the photosynthetic activity and consequently the source–
of carbonic anhydrase (CA) in mustard leaves following sink relations. Higher net photosynthesis in leaves has
the application of GA3 treatment. GA induces the aleurone been successfully attained by the exogenous application
cells of barley seeds to produce α-amylase which is of GA3 (ref. 2), through its stimulating effect on some
then transported to the endosperm, where it helps in the enzymes of dark reaction and nutrient transport5,24.
production of soluble sugars from starch. GA also Khan et al.5 reported that soaking of seeds in GA3
activates cell division in the intercalary meristem manifested its effect at an early stage but was not carried
CURRENT SCIENCE, VOL. 100, NO. 7, 10 APRIL 2011 999
REVIEW ARTICLE
to the reproductive stage, whereas the spray application Nutrient-use efficiency
of GA3, compensated the need for GA3 requirement at a
time when it was needed for photoassimilate formation, Studies indicate that GA increases the use efficiency of
thus enhancing the sink strength and its redistribution nutrients. Eid and Abou-Leila45 reported that GA treat-
towards seeds. ment increased the N, P, K, Mg, Fe, Zn, Mn and Cu con-
tent, thereby increasing the mineral nutrient status of the
plant. The increased nutrient content enhanced photosyn-
Role of GA3 in photosynthesis
thetic potential of leaves and source strength. GA3 treat-
ment increased the mineral nutrient levels of Vigna
Studies have shown that GA3 promotes growth23,34, photo-
unguiculata roots and shoots46. Khan et al. 25 have shown
synthesis23 and nitrogen utilization24,34. Plants treated with
that the increase in N uptake following GA3 application
GA contain more soluble carbohydrate than controls, but
was due to increase in shoot growth, which requires more
this accounts only for a small part of the increased carbon
utilization of soil N. GA3 N uptake results in increased
assimilation. The increase in glucose content by GA
photosynthetic efficiency through maintenance of photo-
application shows the efficiency of GA in increasing photo-
synthetic enzymes. They showed that application of GA3
synthesis35. Khan et al.34 have shown that GA3 spraying
at 10 μM increased carbon dioxide exchange rate, plant N
on mustard plants at the pre-flowering stage contributed
and seed N of plants grown at optimal N, but supra-
35.5% more leaf area and eventually led plants to have a
optimal N applied to crop was not utilized. At optimal N,
better chance of trapping sunlight and producing more
plants receiving GA3 made maximum use of available N
dry matter. The 35.5% increase in leaf area contributed to
due to enhancement of vegetative growth and develop-
a 27.1% increase in dry matter production. Spraying of
ment of pods25. The utilization of N and S has been found
plants with 10 μM GA3 caused more cells to differentiate.
to be interlinked, and GA3 influences the uptake of these
As a result, leaf area and photosynthesis were enhanced
elements2. It has been suggested that leaf N was not uti-
by 29.6% and 31.1% respectively, whereas the same con-
lized if mustard plants were grown with insufficient sul-
centration applied through seed soaking could enhance
phur5. GA3 increased carbon dioxide exchange rate,
leaf area and photosynthesis by 21.4% and 27.0% respec-
specific leaf area, leaf dry mass and dry mass of plants
tively36.
receiving 100 mg S kg–1 soil, and the gain in dry mass
Phytohormones have been employed to improve the
was associated with the increase in the efficiency of leaf.
physiological efficiency of plants by modifying the bal-
A two-fold increase in sulphur-use efficiency of GA3-
ance between photosynthesis and respiration37, affecting
treated plants was noted at sufficient S, i.e. 200 mg S kg–1
stomatal aperture or the activity of photosynthetic en-
soil (ref. 5). Thus optimum S is an essential requirement
zymes23. GA3 has been found to increase the photosyn-
for increasing N utilization and consequently photosyn-
thetic rate in leaves of plants26. It has been suggested that
thesis in GA3-treated plants to enhance the source–sink
GA3 treatment could lead to changes in plastid develop-
relationship.
ment and chloroplast structure38. Contradictory reports
are available showing the stimulatory39 or inhibitory40
effect of GA on ribulose-1,5-biphosphate carboxylase Sucrose synthesis and phloem loading
oxygenase (Rubisco) activity. Yuan and Xu41 reported
that the stimulatory effect on photosynthesis was due to GAs have a strong influence on phloem loading and regu-
increase in Rubisco content and activity, and GA3 stimu- lation of sucrose synthesis47,48, and consequently on photo-
lates the synthesis of Rubisco protein at translational synthetic activity. GA-dependent activation of sucrose
rather than transcriptional level. GAs were identified as phosphosynthase has been shown49, which is involved in
one of the possible signals in the regulation of sucrose the synthesis of sucrose. Sucrose symporter, a key player
phosphate synthase (SPS) activity in soybean and spinach in apoplastic phloem loading, is regulated by the changes
leaves. SPS plays an essential role in regulation of photo- in level of sucrose in leaf. The sucrose-dependent trans-
synthetic sucrose formation42. El-Shraiy and Hegazi43 duction pathway is an important regulatory step in re-
also found decrease in chlorophyll content with GA source allocation. Sucrose is arguably the most important
application. Application of GA3 to red clover increased metabolite in this system of resource allocation, as it is
Rubisco activity and improved photosynthesis44. GA3 has generally the major end-product of photosynthetic carbon
been found to increase the N-use efficiency and activities metabolism and, in most plants it is the predominant form
of nitrate reductase (NR) and CA of plants23. In a study of carbon transported to the heterotrophic tissues50.
on mustard, Khan et al.24 reported that plants which were Moreover, in many plants energy-dependent sucrose
fed with sufficient N and treated with GA3 showed higher accumulation in the phloem generates high hydrostatic
activities of CA and NR, photosynthesis and leaf-area pressure that drives the long-distance flow of resources.
index. Increased N utilization by plants helped in The proton-coupled sucrose symporter mediates phloem
increased photosynthesis. loading, the key transport step in assimilate partitioning

1000 CURRENT SCIENCE, VOL. 100, NO. 7, 10 APRIL 2011

 REVIEW ARTICLE
for many plants51. Chiou and Bush52 provided evidence tissues57. Extracellular invertase has been shown to be
that this pivotal activity was regulated by a response specifically expressed under conditions that require a
pathway sensitive to sucrose levels in leaf. These charac- high carbohydrate supply such as pathogen infection or
teristics are consistent with a sucrose-dependent signal- wounding, and upregulated by a number of stimuli that
ling pathway that dynamically regulates phloem loading affect source–sink relations58. GAs play an important role
by responding to the sucrose levels in the phloem. Ele- in expressing higher acid invertase activity during the
vated sink demand would decrease sucrose levels in the rapid elongation phase, enabling the cleavage of imported
phloem. This would upregulate transport activity and thus sucrose to hexoses that are utilized in elongating cells59.
increase the capacity for phloem loading. Enhanced Tymowska-Lalanne and Kreis57 have shown that GA3
phloem loading would draw down the sucrose levels in plays a significant role in regulating invertase levels.
the mesophyll, perhaps stimulating photosynthetic activ- Invertase mRNA from shoots of dwarf P. sativum was
ity and also increasing the percentage of recently fixed induced after GA3 treatment, indicating that the expression
carbon directed to sucrose synthesis versus starch accu- of the pea shoot cell-wall invertase gene could be regu-
mulation52. In the source–path–sink continuum, phloem lated by GA3 at transcriptional and/or translational levels56.
loading of organic solutes is a crucial step subject to In suspension cultured tomato cells (Lycopersicon escu-
regulation by phytohormones. lentum L.), the addition of GA3 had no effect on the
mRNA for the two invertase genes expressed in flower
organs. This finding suggests that the function of GAs in
Induction of extracellular invertase and phloem
flower induction seems to be unrelated to sucrose meta-
unloading
bolism60. However, a solely tissue-specific GA induction
of the corresponding invertase genes cannot be ruled out.
Extracellular invertase is the key enzyme of an apoplas-
The long-term GA3 exposure might enhance growth in
mic phloem unloading pathway and catalyses the hydro-
the sink leaf (symplastic unloading), where sucrose is
lytic cleavage of sucrose released into the apoplast. This
rapidly utilized in growth and metabolism. Here, GA may
mechanism contributes to long-distance assimilate trans-
enhance export to the sink leaf by increasing the assimi-
port, helps the substrate sustain heterotrophic growth and
late concentration gradient between source and sink leaf.
generates metabolic signals known to affect various pro-
GAs increase sink demand by the enhancement of phloem
cesses of primary metabolism and defence responses53.
unloading or/and metabolism of carbon assimilates61.
Extracellular invertase is particularly suited as a key
regulator of apoplasmic phloem unloading due to its
enzymatic activity. The Km value of hexose transporters is Assimilate partitioning and sink strength
in the micro-molar range, and the Km value of extracellu-
lar invertase is in the millimolar range and thus are limit- The assimilate partitioning to sink organ increases the
ing in phloem unloading. In addition, extracellular sink strength. Sink strength is defined as the competitive
invertase catalyses the only irreversible step of the ability of an organ to receive or attract assimilates62, and
apoplasmic phloem-unloading pathway. An increase in is regulated by phytohormones through stimulating nutri-
acid invertase activity in response to exogenous GA has ent transport and increasing phloem unloading, or acting
been observed in many elongating plant tissues such as on metabolism and compartmentalization of sucrose and
Avena internodes54, Phaseolus vulgaris internodes55 and sorbitol31. The systemic distribution of photosynthate is
elongating dwarf Pisum sativum shoots56. Increased acid known as ‘assimilate partitioning’, and it is a major
invertase activity in response to GAs in these tissues was determinant of plant growth and productivity63. Phyto-
also accompanied by increased hexose concentrations and hormones have been found to be engaged in the assimi-
rapid elongation growth. Wu et al.56 showed an increase late translocation towards reproductive parts of plants24.
in acid invertase mRNA levels within 4 h after GA treat- They enhance the partitioning of carbon assimilates to
ment in dwarf pea seedling. This indicated that enhanced developing fruits by several mechanisms. GAs likely
invertase expression was an initial response to GAs caus- enhance either cell division or enlargement, and increased
ing increased hexose sugar availability and growth elon- cell numbers or size results in more sites for assimilate
gation. Since unloading of sucrose from the phloem into deposition increasing dry matter accumulation. Photosyn-
the apoplast follows the concentration gradient and thate translocation in phloem controlled by the pressure
hexose transport into the sink cells is mediated by high- gradient between source and sink is driven through osmo-
affinity monosaccharide transporters, extracellular inver- sis64, or the active process of phloem loading or unload-
tase with a high Km value in the millimolar range is ing65. Partitioning of photosynthetic metabolites between
expected to be the limiting step for phloem unloading and leaf and stem is an important factor in yield determina-
thus a potential target for regulation. Studies demonstrate tion66. Komor67 reported that total plant productivity
an essential function of extracellular invertase for phloem relied on appropriate C assimilation rate and the export of
unloading, carbohydrate partitioning and growth of sink C from source leaves. Moreover, phytohormones have

CURRENT SCIENCE, VOL. 100, NO. 7, 10 APRIL 2011 1001

REVIEW ARTICLE
been proposed as mobilizers of assimilates to fruits and determinants of sink capacity by generating a sucrose
modulators for many of the rate-limiting components in gradient to support unloading of sucrose from the
the overall process of C partitioning31. Recently, it has phloem. Thus, the sink strength can be increased through
been suggested that apoplasmic phloem unloading existed GA, which increases extracellular invertase and sucrose
in developing apple fruit and invertase was critical for gradient through the conversion of sucrose to glucose.
this process68. Studies on the activity of NAD+-dependent This helps in phloem unloading of carbohydrate in sink
sorbitol dehydrogenase (NAD-SDH) and invertase in organ, subsequently increasing plant yield. Hence, the
‘Kousui’ fruit after GA application also confirmed the enzymes responsible for the first metabolic reaction of
above finding69. The mechanism of GA action seems to sucrose are probably critical links between photosynthate
be more complex than the stimulation of assimilate trans- production in source leaves and growth capacity of sink
port, i.e. phloem loading and unloading. GA-dependent organs73.
stimulation of SPS activity, a key enzyme in sucrose syn-
thesis, as well as invertases degrading sucrose has been
defined70. GA and kinetin influence assimilate transport GAs in source–sink relations under limiting
at the site of hormone application71. GA affected the environmental conditions
source–sink relationship in trans-location and carbohy-
drate storage in alfalfa72. Sucrose concentration in the Phytohormones are active members of the signal com-
elongating internodes fell substantially after treatment pounds involved in the induction of plant stress responses69.
with GA3, whereas the concentration of hexose sugars They not only regulate plant growth and development,
increased. It has been suggested that GA3 stimulated acid but also increase plant resistance to various environ-
invertase synthesis in the elongating internodes, and mental stress conditions74. Partitioning of assimilates and
established a more favourable sucrose gradient between its effect on dry matter distribution is influenced by
sink and source72. Under source-limiting conditions this, several environmental factors such as temperature,
in turn, will lead to a reduced rate of assimilate transloca- drought, salinity and nutrient availability70. The photoas-
tion to competing sinks in the root system. GA3 promo- similates produced under salt stress are used to support
tion of photosynthate accumulation by the pith tissues is a crucial processes such as growth and osmotic adjustment.
minor contributing factor to GA3 regulation of phloem In general, salinity causes a reduction in sink enzyme
translocation. The GAs may stimulate the photosynthetic activities, leading to an increase in sucrose in source
activity from the beginning of shoot growth and are thus leaves, with a decrease in photosynthesis rate by feed-
responsible for the enhancement of yield49. The possible back inhibition75. Application of GA is found to induce
role of GA in increasing source–sink relation is depicted extracellular invertase, which acts on sucrose to form
in Figure 1, where it is shown that GA affects SPS- hexose. The hexose formed is easily transported to the
enhancing sucrose synthesis and is involved in phloem sink, thereby increasing sink strength (Figure 2). The
loading of sucrose. Further, apoplastic unloading is also induction of extracellular invertase by both abiotic and
under the influence of GA, through its role in increasing biotic stress stimuli supports the suggestion that extracel-
invertase activity. Invertase converts sucrose to hexose, lular invertase is not only a key modulator of assimilate
forming a concentration gradient that favours the unload- partitioning, but is also an important component of vari-
ing of sucrose into the sink cell. The hexose in the sink ous stress responses. Similarly, GA increases photosyn-
cell is responsible for sink strength. Thus GA indirectly thetic rate under stress and thus enhances the source
affects sink strength through this pathway and directly potential (Figure 2).
through cell expansion that governs sink size. Besides, Reduced plant growth under stress conditions could
the phytohormones may stimulate transport of nutrients result from an altered hormonal balance and phytohor-
through the phloem and modify the sink strength by mone application provides an attractive approach to cope
stimulating its growth and increasing the ability for sugar with stress9. An intimate relationship has been suggested
unloading from the phloem. GA increases sink demand to exist between GA levels and the acquisition of stress
by the enhancement of phloem unloading or/and metabo- protection in barley (Hordeum vulgare)9. Overexpression
lism of C assimilates. A larger fruit size and increased of Dwarf and Delayed Flowering 1 (DDF1) causes a
sink demand were closely correlated with changes in the reduction in GA4 content and dwarfism in Arabidopsis76.
activity of sugar-metabolizing enzymes induced by GA There is a correlation among the survival of salt toxicity
application. Also, Zhang et al.61 found that increased sink and the function of DELLA proteins77. These results sug-
demand by GA application was closely related to the acti- gest that the salt-inducible DDF1 gene is involved in
vation of invertase cell wall (Inv-CW) bound in the core growth responses under high salinity conditions in part
and invertase neutral (Inv-N) and NAD-SDH in the pulp through altering GA levels and improves seed germina-
during rapid growth in fruits. The supply of the transport tion78. Kumar and Singh79 reported increased growth and
sugar, sucrose, is a limiting step for the growth of sink grain yield under saline condition on GA treatment.
tissues73 and sucrose-metabolizing enzymes are important Archard et al.77 reported that salt-treated Arabidopsis
1002 CURRENT SCIENCE, VOL. 100, NO. 7, 10 APRIL 2011
 REVIEW ARTICLE

Figure 1. Phloem loading in sieve element and apoplastic phloem unloading mediated by regulation of extracellular invertase. Sucrose is loaded
into the sieve element by proton sucrose co-transport and the apoplastic unloading occurs by the action of extracellular invertase on sucrose to form
hexose. Hexose is transported through hexose transportor. TP, Transportor; SPS, Sucrose phosphate synthase; Comp cell, Companion cell;
Photosyn., Photosynthetic; +, Positive effect; –, Negative effect.

the regulation of source–sink metabolism. Mohammed83

suggested that the multiple effects of GA3 which could be
involved in alleviating the adverse effect of salinity on
mungbean seedlings include the stimulation of growth pa-
rameters, increase in photosynthetic pigments concurrent
with the marked increase in reducing sugars and sucrose,
increase in protein synthesis, including de novo synthesis
of proteins and accumulation of certain existing proteins,
increase in the activities of catalase and peroxidase and
decreases in the activities of the ribonuclease and poly-
phenol oxidase. The promoting effect of GA3 on seed
germination may be attributed to an increase in α-amylase
activity, thus increasing soluble sugars, and this might
Figure 2. Action of gibberellins on source–sink relation under stress. enable the embryo to germinate and accelerate the mobi-
Extracellular invertase is regulated by both gibberellins and stress, and lization of reserves from the endosperm84. Siddique
invertase acts on sucrose to form hexose that increases sink strength.
The increase in photosynthetic rate by gibberellin under stress increases et al.85 found ameliorating effect of GA3 and N in Bras-
source potential. sica juncea salinity stress. The ameliorative effect of GA
and N was on the primary growth potential, activities of
plants contain reduced levels of bioactive GAs, support- NR and CA enzymes, membrane permeability and N-use
ing the idea that salt slows down the growth by modulat- efficiency. The available nutrients in the growth medium
ing the GA metabolism pathway. were absorbed more rapidly as reflected by increased leaf
Salt stress generally decreases the GA content. How- N and K concentration, and this led to maximum utiliza-
ever, a remarkable increase in GA3 content was reported tion of absorbed nutrients, resulting in enhancement of
in the leaves of salt-tolerant wild tomato, L. pennellii80. vegetative growth and development of more pods (sink).
Exogenous application of GAs overcomes the effect of Similarly, heavy metals alter the hormone content in
salinity stress and improves seed germination under plants and the application of phytohormones to heavy-
saline conditions78. GA3 has also been shown to alleviate metal stressed plants reduces the uptake of these metals86.
the effects of salt stress on pigment content, Hill acti- GAs strongly inhibited Cd and Ni incorporation into
vity81 and water-use efficiency82. GA3 treatment of salt- plants43. Picazo et al.87 found that GA increased the sugar
stressed wheat plants resulted in an increased photosyn- content in roots, second and third leaves, and also modi-
thetic capacity, which was discussed as a major factor for fied the carbohydrate distribution pattern of rice plants
greater dry matter production23. The increase in pigment grown with Cd or Ni. GA3 probably reverses the effect of
content, photosynthetic capacity and growth through GA Ni stress in soybean seedlings by decreasing the Ni
treatment under salinity stress indicates its potential in uptake by roots to some extent and by enhancing

CURRENT SCIENCE, VOL. 100, NO. 7, 10 APRIL 2011 1003

REVIEW ARTICLE
antioxidant enzyme activities88, thereby promoting of tobacco93. However, the mechanisms of molecular
growth. The enhancement of growth rate by GA might signalling and their regulation of plant resistance to unfa-
result in an increase in leaf area, stimulation of photosyn- vourable environmental conditions induced by SA are
thetic rate, modified partitioning of photosynthates, or still not clear. Generally, deficiency or a high level of SA
their combination10. GA-mediated elongation of shoots of increases the plant susceptibility to abiotic stress94, and
various plants results from activation of cell division probably GA functions in inducing stress tolerance
and/or cell elongation. The GA3-mediated invertase acti- through its influence on SA. Notably, SA also induces
vity in elongating shoots could result in significant accu- genes encoding GA biosynthetic enzymes. These obser-
mulation of hexoses required for primary cell-wall vations indicate that SA promotes seed germination under
biosynthesis11, thus favouring seedling growth under high salinity by modulating biochemical and molecular
stress condition9. mechanisms signalling a crosstalk with GA95.
GA applications effectively promoted the development
of flowers during normally inhibitory high temperatures.
This was due to the promotion of longitudinal growth of Conclusion
the flower primordium by GA application50. Treatment of
Phalaenopsis flowering shoots with GA at warmer tem- GA3 enhances source and sink potential through increas-
peratures increased the levels of the active GA required ing photosynthetic enzymes, increasing leaf area for
for the promotion of flower development to the same higher interception of photosynthetically active radiation
extent as that found in flowering shoots grown in cool and enhancing nutrient use efficiency. The integrated
temperatures89. mechanisms enhance the source potential and redistribu-
Recently, it has been reported that GAs interact with tion of photosynthates by GA3 results in increased sink
other phytohormones such as salicylic acid, abscisic acid strength. GAs are known to induce extracellular inver-
and jasmonic acid and influence various plant develop- tase, and phloem loading and unloading. It activates SPS
mental processes7,8,90. resulting in sucrose formation, which is loaded into the
The regulation of source–sink relations under abiotic phloem and is acted upon by invertase before being
stress could be attributed to GA-enhanced SA production. unloaded into the sink. The whole process is under the
Transgenic plants overexpressing a GA-responsive gene control of GA.
from beechnut (Fagus sylvatica), coding for a member of Besides increasing source–sink potential under opti-
the GASA family (FsGASA4), showed reduced GA mum growth conditions, the role of GA in increasing
dependence for growth and improved responses to salt, source–sink relations under limiting environmental condi-
oxidative and heat stress at the level of seed germination tions is equally important. The exogenous application of
and seedling establishment7. This finding was further GA helps the plant to ameliorate the abiotic stress condi-
substantiated by the reversal of inhibitory effect of salt, tions. GAs increase the photosynthetic potential of plants
oxidative and heat stress by the exogenous application under stress resulting in more photosynthate production
of GA3 in the germination and seedling establishment of (source) and this in turn enhances the sink strength.
Arabidopsis thaliana. This effect of GA3 was accompa- Extracellular invertase also increases under stress. Thus,
nied by an increase in SA levels8. GAs and the overex- there could be a role for extracellular invertase in increas-
pression of a GA-responsive gene were able to increase ing source–sink potential under various abiotic stress
not only the endogenous levels of SA, but also the expres- conditions. Extracellular invertase may be considered as a
sion of ics1 and npr1 genes involved in SA biosynthesis central modulator of assimilate partitioning and defence
and action respectively. Furthermore, this hypothesis is response based on the following four different functions:
supported by the finding that sid2 mutants, impaired in supplying carbohydrates to sink tissues; regulation of
SA biosynthesis, are more sensitive to salt stress than the source–sink transitions; amplification of signals that
wild type and are not affected by exogenous application regulate source–sink relations, and integration of
of GA3. signals that regulate source–sink relations and defence
In contrast, Hamayun et al.90 reported that SA content responses.
decreased under the influence of elevated GA3, whereas it Exogenous application of growth hormones may be
increased in NaCl-treated plants. It suggested that SA useful to return metabolic activities to their normal lev-
biosynthesis was upregulated to strengthen the systemic els. At a certain concentration GA3 has been shown to be
acquired resistance mechanism under stress conditions. beneficial for the physiology and metabolism of many
As GA3 application relieved plants from salt stress, a plants under abiotic stress, since it may provide a mecha-
decline in endogenous SA content was observed. The role nism to regulate the metabolic process as a function of
of SA as an anti-stress hormone is evident from SA- sugar signalling and antioxidative enzymes. There also
induced synthesis of heat shock proteins in tobacco exists a crosstalk between GAs and SA in the regulation
plants91, accumulation of wheat lectins92, and fast activa- of source–sink relation under abiotic stress. Although
tion of 48-kDa protein kinase in suspension cell culture GA3 is the most studied GA, the importance of other GAs
1004 CURRENT SCIENCE, VOL. 100, NO. 7, 10 APRIL 2011
 REVIEW ARTICLE
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