In plants, sugar production through the photosynthesis is a vital process. Sugars have an important role in different processes such as cell cycle progression, embryogenesis, seed germination, energy source, senescence etc. Sugar status modulates and coordinates internal regulators and environmental cues that govern growth and development. Plants have evolved a complex mechanistic system to sense different sugars, including sucrose, hexoses, and trehalose. Sugar sensing occurs at the level of individual cells and the responses of such cells must be integrated at the tissue, organ, and plant level. Sugar signalling is also a mechanism that plants use to integrate various internal and external cues to achieve nutrient homeostasis, mediate developmental programs, and stress responses (Li et. al, 2016). Plants have different type of sugar sensors which sense different form of sugars such as HXK (hexokinase) is a glucose sensor, FBP/FIS1 (fructose-1,6-bisphosphate) is a fructose sensor, RGS1 (regulator of G-protein) is a sucrose and hexose sensor, AtSUT2/SUC3 is a putative sucrose sensor etc. Two energy sensors i.e. SnRK1/AtKIN10 (sugar non-fermentation-related protein kinase) and TOR (target of rapamycin) kinase are also present downstream of sugar perception. Depending on the sugar type and function, four types of sugar signalling pathways are- a) Disaccharide signalling pathways, b) Hexose dependent pathways, c) Energy metabolite and sensors and d) Sugar signalling in the regulation of sugar transporters (Sakr et. al, 2018). The effect of sugars are regulated by different mechanisms at different level such as- a) epigenetic regulation by modifying the DNA methylation, histones modifications etc., b) transcription regulation in which genes are regulated by promoters and cis-acting elements like GC-box, G-box etc. and c) post-transcriptional level of regulation which involves the regulation of rate of mRNA turnover. Sugar signalling tightly interconnected with the hormones and nitrogen signalling (Ljung et. al, 2015 and Zhang et. al, 2017). Hormone and sugars show both synergistic and antagonistic effects with the each other. Sugars and auxin regulate the C/N ratio through PIF (phytochrome insensitive factor) response and they also regulate the cell cycle by regulating CDKs (cyclin dependent kinases). Similarly the other hormones regulate the different processes like photosynthesis, growth, anthocyanin accumulation etc. along with sugars. Sugars signalling also interact with the nitrogen. Sugar and nitrogen regulates the nitrogen assimilating enzymes like nitrate reductase (NR) and nitrite reductase (NiR). Nitrogen positively regulates the sugar uptake and assimilation, but it is negatively regulated the sugar assimilates. The study of sugar sensing and signalling is important because it influence many plant processes directly or indirectly by interacting with other molecules like hormone, nitrogen, phosphorus etc.

1. Sarita
CCS Haryana Agricultural University, Hisar

2. Introduction
15/11/2019 Essential roles of sugar in plants 2
Sugar act
as-
Substrate in carbon metabolism
Substrate in energy metabolism
Polymer biosynthesis
Signaling molecule
Precursor for primary and secondary plant
intermediates
Regulatory molecule

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Sugar involved in plant processes
SUGAR
Flower
development
Embryogenesis
Seed
germination
Energy
sources
Stress/defence
response
Regulation
Of gene
expressionLipid
regulation
metabolism
Fruit
development
Signaling
Molecule
Senescence
Cell cycle
progression

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Sensors and transporters
Proteins or
carriers
which
transport the
molecules
BvSUT1 (sucrose
transporter in
phloem)
SUT4-
tonoplast sucrose
transporter
AtSUT2/SUC3-
(plasma membrane
transporter)
Sensors
Proteins or
enzymes which
sense the changes
Transporters
SUT2-
putative sucrose
sensor
RGS1
External sugar
sensor
AtHXK1
Hexose sensor
SnRK1
serine/threonine
kinase
TOR kinase

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Disaccharide
Signaling
Pathway
Hexose
dependent
pathway
Energy and
Metabolite
Sensors
Sugar
signaling in
the regulation
of sugar
transporters
Sugar
signaling
pathways

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Sucose
Signalling
Trehalose-6-
phosphate

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Involvement
of Sucrose
signaling
Many metabolic processes
Plant growth
Plant defense mechanism
Regulation of
flowering
Differentiation of
vascular tissue
Development of storage organs
Anthocyanin
synthesis

8. 11/18/2019 Lemoine, 1999 8
The flow of sucrose from the source
organ (upper part) to the sink organs
(lower part) through the phloem
List of the sucrose transporter
sequences available in databases
Sucrose transport pathway

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Sucrose Signaling
1. Increase no. of cells
2.Faster vegetative
growth
3. Changes
developmental stages
SuSy protein targets the
nuclei of photosynthetic cells
Increase the photosynthetic
efficiency
Abundance of sucrose
Stimulate WUSCHELL
(WUS) and CycD3
Shoot apical meristem
develoment
sucrose-phosphate synthase
(SPS)
sucrose-phosphatase (SPP)
Sucrose synthase (SuSy)
Triose phosphate (TP)

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T6P signaling modulates transcription, hormone signals and cell wall biogenesis to
coordinate growth, development and stress responses with carbon availability.
T6P- Trehalose-6-
phosphate
TPS- Trehalose-6-
phosphate Synthase
TPP- Trehalose-6-
phosphate phosphatase
EXO- Exordium
Trehalose-6-phosphate Signaling

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2.
Hexose -
Dependent
pathways
Glucose

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Glucose
sensors
RGS1
(regulator of G-protein
signaling1)
AtHXK1
(Hexokinase1 in
Arabdopsis)
External Sensors on plasma membrane intracellular glucose sensor

13. 11/18/2019 Rolland et. al, 2002 13
 Glcucose (and Fructose) can be
transported into the cell by
hexose transporters or mobilized
from cytosolic and vacuolar
Sucrose and plastid starch.
 The HXK sugar sensor, as a
cytosolic protein or associated
with mitochondria or other
organelles could activate a
signaling cascade through HXK-
interacting proteins (HIPs) or
affect transcription directly after
nuclear translocation.
Possible Sugar Signals and Sensing Sites in
Plant Cells
Possible Sugar Signals and Sensing Sites in Plant Cells

14. 11/18/2019 Jen Sheen, 2014 14
Arabidopsis glucose-signaling networks
Glucose-signaling networks
Sourse
(sucrose/glucose)
Sink (cell prolification,
expansion, maintain
energy and metabolic
homeostasis)
Glucose
Master regulators
HXK1
KIN10/KIN11
TOR

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Glucose-signaling networks
HXK1 nuclear signaling
AtHXK1
VHA-B1
19S RPT5B
Hetero-
multimeric
complex
Gene
expression
Regulatory particle
of proteasome subunit
Vacuolar H+-ATPase B1

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3.
Energy and
Metabolite Sensors
SnRK1
TOR kinase

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SnRK1(Sucrose Non-Fermenting Related Protein Kinase 1)
SnRK1
 Growth
 Development
Reprogramming
of metabolism
 Biotic and
abiotic stresses Chromatin remodling
Post translational
regulation
Gene expression

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Role of SnRK1 in germination and seedling growth
 Role of SnRK1 in
sugar signaling as –
 Sugar inhibits the
SnRK1(activator of
MYBS1) or it directly
inhibit the MYBS1.
No transcription of α-
amylase so there is
inhibition of germination
and seedling growth.
Lu et.al, 2007

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 SnRK1 is activated
during the sugar starvation
.
It phosphorylates many
TFs in nucleus and
cytoplasm which regulates
the transcription of SnRK1
regulated genes.
These transcripts
regulates the metabolism in
different organelles like
chloroplast and
mitochondria.
Wurzinger et. al, 2018
Metabolism regulated by SnRK1

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Regulation of seed maturation and
germination by sugars through T6P and
SnRK1
An increase in ABA level during
mid-embryogenesis, partly through
the B3 domain FUS3, positively
regulates SnRK1 by PP2C
inactivation.
T6P inhibits SnRK1 in vitro possibly
to reset SnRK1 activity after ABA
levels decline.
ABA in turn positively regulates
FUS3, ABI3, and ABI5 through
transcriptional and/or post-
translational regulation.
SnRK1 regulates seed germination
also through chromatin remodelling.
Tsai and Gazzarrini, 2014

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TOR
TOR (A target of Rapamycin) Kinase
Stress inputs
Diverse Nutrient
Energy
Hormone
Modulate
Stress responses
Cell proliferation
Growth
Metabolism

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Role of TOR in different processes.
Shi et. al, 2018
Role of TOR kinase

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TOR Kinases in growth response
 A high metabolic status is
reflected by sucrose
availability, which is
correlated with plant T6P
levels.
Under these conditions,
T6P inhibits SnRK1, and the
active TOR kinase stimulates
translation and growth.
SnRK1 strongly regulates
the C/S1-bZIP TF which
inhibit the growth.
Sucrose inhibits the
translation of S1-group bZIP
mRNAs.
LST8 – part of TOR complex
in plants
RAPTOR- Regulatory-
associated protein of TOR
SnRK1- α subunit-
catalytic, β & γ-
regulatory Subunits
Xiong and Sheen, 2015

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Sugarsignalingin the
Regulation of Sugar
Transporters

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1. Monosaccharide transporters (MSTs)
2. Sucrose transporters (SUTs)
3. SWEETs (Sugars Will Eventually be
Exported Transporters).
Sugar signaling in the Regulation of Sugar Transporters
Sugar
transporter
families
Sugar influx
Efflux and
bidirectional
sugar transport

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 SWEET (in purple) are key
components for sucrose export
likely from parenchyma cells .
SUT1 is proposed between
companion cell and enucleate
sieve elements.
Sucrose is unloaded to
connected sink organs via SUTs
(in red) and cleaved by sucrose-
splitting enzymes (light blue) to
yield glucose (Glu) and fructose
(Fru) that are taken up by MSTs
(in blue).
Sugar Transporters in plant
Doidy et. al, 2012

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Sugar transporters: SUTs (in red),
MSTs (in blue) and SWEETs (in purple).
SWEETs and SUFs are energy-
independent uniporters
At the vacuolar membrane the MST
subfamilies, VGT and TMT function as
sugar/H+ antiporters
Two families play a role in efflux of
sugars from plastids are- SUT4 and
MST subfamily, pGlcTs (plastid glucose
transporters
Finally, the MST subfamily
transporters, INTs (inositol transporters)
localize to both plasma and vacuolar
membranes they transport myo-inositol,
an important precursor in a number of
metabolic pathways.
Cellular model of Transporters
Doidy et. al, 2012

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Sugar
Transporter
genes
Light
AtSTP13 & AtSTP14 genes

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Sugar metabolism & Signaling
 Glucose sensors (HXK: OGT: O-
Glucose N-acetyl
transferase); fructose sensors (i.e.,
FBP/FIS1), sucrose and hexose
sensors
(RGS1), and putative sucrose sensors
(SUSY, SUcrose SYnthase,
putative sucrose transporter
AtSUT2/SUC3).
 Downstream of sugar perception are
two energy sensors: AtKIN10/SnRK1
and TOR-kinase. CWI: cell wall
invertase; GS/GOGAT:
glutamine synthetase/ glutamate
oxoglutarate aminotransferase; INV,
invertase; STP: Sugar transport
protein; SUT: sucrose transporter; TPS:
T6P synthase; TPP: trehalose 6P
phosphatase; UDPGlc-NAC:
UDP N-acetylglucosamine
Schematic representation of Sugar
metabolism & Signaling
Sakr et. al, 2018

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30
Molecular
mechanism
of Sugar
regulation
Epigenetic
Regulation
Transcriptional
Regulation
Post-
Transcriptional
Level
Translational
and Post-
Translational
Regulation

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Epigenetic Regulation
Epigenetic
Mechanism
DNA Methylation
Post-translational
modification of histone
Small RNAs
Chromatin
remodeling
Gene
regulation

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Epigenetic regulation of Flowering genes
Plant
hac1 gene
Plant
hac1 gene
Timely
Flowering
Late Flowering
Expression of
FLC (Flowering
Locus C)
Expression of FLC
(Flowering Locus C)
hac1 mutant

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Phenotypes of hac1 mutants
Delay in Flowering
Total no. of leaves
Less fruiting

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Histone Modification
H2B
112 Serine
UDP-
GlcNAc
H2B
UDP-
GlcNAc
O
O- linked UDP-GlcNAc
OGT
Extracellular glucose
Hexosamine
biosynthetic
pathway
Sense
Gene
regulation
uridine diphosphate N-aetylglucosamine (UDP-
GlcNAc)
O-GlcNAc transferase (OGT)

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Transcriptional regulation
Promoter
Cis-acting elements
Gene expression
GC-box
(GGAGAACC
GGG), G-
box
(CTACGTG),
TA-box
(TATCAA),
Sugar
starvation
(promote
α-
amylase 3)
B-box
(GCTAAACAAT)
, CGACG
element,
TGGACGG
element, W-
box (TGACT),
S box
(CACCTCCA),
and TTATC
element
Sugar
signaling
Regulation

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Post-transcriptional level
Gene expressionRegulationmiRNA
Juvanile Arabidopsis
Adult ArabidopsismiRNA156A &
miRNA156C
Sugars

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Crosstalk between Sugar and Hormones

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Sugar and Auxin
Auxin
+
Sugar
seed
development
Hypocotyl
elongation
Cell
prolification
cell
expension
Sucrose
Auxin level
And distribution
Glucose
+
Auxin
Sugar + Auxin

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Sugar and Auxin mediate C/N ratio:-
Light (yellow arrow) and CO2
(blue arrow) elevate
endogenous Sucrose and thus
carbon (C) levels (Before).
Sucrose then stimulates both
PIF-dependent and -
independent auxin responses
(Response), promoting
hypocotyl and root elongation.
 These elongated roots
acquire nitrogen (N) from the
soil, and the carbon-nitrogen
balance is restored(After).
So, they maintain the C:N
ratio in plants.
A model of a PIF- and auxin-mediated
carbon-sensing pathway.

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Glucose and auxin signal in cell cycle regulation
Glucose and auxin signal in cell cycle regulation
1
2
3
4
5
6
7
8
9
10
Wang and Ruan, 2013

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Sugar and Gibberellins (GAs)
GAs
Elongation of intact stems
Bolting
Dormancy
Seed Germination
Flowering
in LDP
DELLASucrose
Stabilize
GAs
Anthocyanin
biosynthesis
Sucrose genes

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In the wild-type
endosperm, sugar
repression of α-amylase
expression is inhibited by
MYBGA, which interacts
with the GARE in α-
amylase gene promoters.
In the gamyb-2 mutant
endosperm, the absence
of MYBGA leads to the
sugar repression of α-
amylase expression.
Role of GAs and Sugar in Seedling Development
Interactions among Sugars, GAs, MYBGA,
and α-Amylases
Chen et. al, 2006

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Sugar and Cytokinin (CKs):-
CKs
Cell prolification
Source/sink relationship
Leaf senescence
Root growth
Nutritional
signaling
Antagonistic
effects
sensitivity to sugar
hxk1/gin2 mutant
sensitivity to CKs
Sucrose
CKs
WPK1
Putative Protein
kinase
Of SnF1 family

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Sugar and Cytokinin (CKs):-
Synergistic effects
Sucrose
CKs Root
Growth
AHK- Arabidopsis
Histidin kinase 4
ARR- Arabidopsis
Response regulators
Glucose
CKs Anthocyanin
accumulationMYB75/PAP1 by HY5

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Sugar and Ethylene:-
Ethylene
+ Sugar
Inhibition
of stem
And root
elongation
Senescence
Fruit
ripening
Flowering
Glucose
Degradation
EIN3
Ethylene response
Ethylene

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Model for glucose and ethylene signaling.
Model for glucose and ethylene
signaling
 Ethylene regulates the
germination, cotyledon
greening, expansion ,
root hair initiation and
triple response but sugar
negatively regulates
these effects.
 Sugar regulates these
processes by activation
of GIN1, which also
repress the
photosynthetic gene
expression.

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EIN3
Ethylene
Sugars
Circadian
rhythm in
evening
Circadian
rhythm in
night
by stabilizing the GIGANTEA (GI) protein
depending on the activity of the F-Box
protein ZEITLUPE (ZTL)

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Sugar and Abscisic Acid (ABA):-
ABA
Bud dormancy
Flowering
Senescence
Release of Ethylene
Inhibition of
other hormones
ABA + Sugars
Photosynthesis
SnRK1
ABA
Sugar
Root development

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 Perception of low WP, via an
unknown mechanism, induces signalling
events which lead to increased ABA
synthesis and accumulation,
osmoregulatory changes, and changes in
ABA response and/or other ABA-
independent regulation (indicated by
dashed lines).
 Bold up arrows indicate an increase in
Pro or ABA content.
ABI1 and ABI2 are regulators of ABA
content via a feedback mechanism which
may act on ABA catabolism or
conjugation (indicated by the
dashed line).
 ABI4 is a negative regulator of Pro
accumulation at low WP and serves to
connect Pro accumulation to sugar
sensing.
Model of the interaction of low WP, ABA,
and sugar
Paul E Verslues, 2006
Sugar and Abscisic Acid (ABA):-

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Overview of sugar and hormones
Schematic representation of crosstalk between sugar and hormone
signaling pathways (orange) in regulation with certain physiological
processes (green).
Sakr et. al, 2018

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Crosstalk between Sugar and
nitrogen

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Interaction between sugar and nitrogen
Nitrate
 Sugar uptake
Assimilation
Assimilates like Glutamate

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Nitrate
Uptake
CO2
C/N ratio
Nitrate reductase(NR)
Nitrite reductase(NiR)
Sugar and nitrogen uptake

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• Sugar acts as a signaling molecule and it influence many plant
processes like growth, development, flowering etc.
• There are many sugar sensors which sense different forms of sugar
like- RGS1, SUT2, SnRK1, TOR etc.
• Some metabolic sensors also sense the sugar like O-GlcNAc
transferase.
• Sugar signaling mediates the balance between the anabolic and
catabolic metabolisms through epigenetic reprogramming,
transcriptional/post-transcriptional regulation, ribosome
biogenesis, translational activity, and protein modifications.
• Sugar signal transduction pathways are tightly interconnected with
the hormones and nitrogen signaling networks.
Summary

55. SYMBOL OF TRUST