Plant aquaporins on the move: Reversible phosphorylation, lateral motion and cycling

Abstract

Aquaporins are channel proteins present in the plasma membrane and most of intracellular compartments of plant cells. This review focuses on recent insights into the cellular function of plant aquaporins, with an emphasis on the subfamily of Plasma membrane Intrinsic Proteins (PIPs). Whereas PIPs mostly serve as water channels, novel functions associated with their ability to transport carbon dioxide and hydrogen peroxide are emerging. Phosphorylation of PIPs was found to play a central role in the mechanisms that determine their gating and subcellular dynamics. Dynamic tracking of single aquaporin molecules in native plant membranes and the search for cell signaling intermediates acting upstream of aquaporins are now used to dissect their cellular regulation by hormonal and environmental stimuli.

Full text

Plant
aquaporins
on
the
move:
reversible
phosphorylation,
lateral
motion
and
cycling
Lionel
Verdoucq,
Olivier
Rodrigues,
Alexandre
Martinie
`re,
Doan
Trung
Luu
and
Christophe
Maurel
Aquaporins
are
channel
proteins
present
in
the
plasma
membrane
and
most
of
intracellular
compartments
of
plant
cells.
This
review
focuses
on
recent
insights
into
the
cellular
function
of
plant
aquaporins,
with
an
emphasis
on
the
subfamily
of
Plasma
membrane
Intrinsic
Proteins
(PIPs).
Whereas
PIPs
mostly
serve
as
water
channels,
novel
functions
associated
with
their
ability
to
transport
carbon
dioxide
and
hydrogen
peroxide
are
emerging.
Phosphorylation
of
PIPs
was
found
to
play
a
central
role
in
the
mechanisms
that
determine
their
gating
and
subcellular
dynamics.
Dynamic
tracking
of
single
aquaporin
molecules
in
native
plant
membranes
and
the
search
for
cell
signaling
intermediates
acting
upstream
of
aquaporins
are
now
used
to
dissect
their
cellular
regulation
by
hormonal
and
environmental
stimuli.
Addresses
Biochimie
et
Physiologie
Mole
´culaire
des
Plantes,
Unite
´Mixte
de
Recherche
5004,
CNRS/INRA/Montpellier
SupAgro/Universite
´
Montpellier
II,
F-34060
Montpellier,
Cedex
2,
France
Corresponding
author:
Maurel,
Christophe
(maurel@supagro.inra.fr)
Current
Opinion
in
Plant
Biology
2014,
22:101–107
This
review
comes
from
a
themed
issue
on
Cell
biology
Edited
by
Shaul
Yalovsky
and
Viktor
Z
ˇa
´rsky
´
For
a
complete
overview
see
the
Issue
and
the
Editorial
Available
online
6th
October
2014
http://dx.doi.org/10.1016/j.pbi.2014.09.011
1369-5266/#
2014
Elsevier
Ltd.
All
right
reserved.
Introduction
Aquaporins
are
channel
proteins
which
facilitate
the
passive
diffusion
of
water
and
small
neutral
molecules
across
biological
membranes.
Aquaporins
can
be
found
in
the
plasma
membrane
(PM)
and
in
most
intracellular
compartments
of
plant
cells.
They
are
involved
in
the
maintenance
of
the
whole
plant
water
status
by
mediating
osmoregulation
of
every
single
cell
and
trans-cellular
water
transport
in
roots
and
leaves.
In
the
past
decade,
numerous
integrative
studies
have
addressed
the
role
and
regulation
of
aquaporins
during
plant
response
to
the
environment
(reviewed
in
[1,2]).
The
identification
of
novel
aquaporin
substrates
in
addition
to
water,
such
as
boron
and
silicon,
has
also
broadened
the
physiological
spectrum
attributed
to
these
channel
proteins.
The
present
review
focuses
on
recent
insights
into
the
cellular
function
of
plant
aquaporins,
with
an
emphasis
on
the
subfamily
of
Plasma
membrane
Intrinsic
Proteins
(PIPs).
We
discuss
the
novel
functions
that
may
be
associated
with
their
ability
to
transport
carbon
dioxide
(CO
2
)
and
hydrogen
peroxide
(H
2
O
2
).
We
present
the
mechanisms
that
determine
their
subcellular
dynamics,
with
a
particu-
lar
focus
on
the
role
of
phosphorylation.
Besides
mech-
anisms
involved
in
aquaporin
trafficking
and
sorting,
linking
aquaporin
functions
to
signaling
cascades
now
represents
one
of
the
major
challenges
in
the
field.
Aquaporins
of
plants:
a
large
family
of
membrane
channels
with
diverse
cellular
roles
Plant
aquaporins
can
be
subdivided
into
up
to
eight
subfamilies
according
to
their
sequence
homology
[3].
These
proteins
have
been
reported
in
nearly
all
of
plant
cell
subcellular
compartments,
including
PM,
tonoplast,
endoplasmic
reticulum,
Golgi
apparatus
and
chloroplast
[4,5].
In
line
with
reports
on
animal
aquaporins,
a
local-
ization
in
mitochondria
was
also
proposed
for
Arabidopsis
TIP5;1
[6].
However,
a
recent
study
indicated
that
when
expressed
under
its
native
promoter,
AtTIP5;1
specifi-
cally
localizes
to
the
small
vacuoles
of
pollen
sperm
cells
[7].
This
study
also
showed
that,
in
the
former
work
[6],
ectopic
expression
of
AtTIP5;1
in
a
non-native
cell
(the
pollen
vegetative
cell)
and
the
use
of
low
resolution
of
imaging
and
co-localization
techniques,
had
led
to
an
erroneous
localization
in
mitochondria.
Interestingly,
some
PIP
and
Tonoplast
Intrinsic
Protein
(TIP)
homo-
logs
are
localized
in
the
chloroplast
envelope
and
thyla-
koids,
respectively,
but
these
observations
essentially
rely
on
proteomic
analyses
and
a
single
cell
biological
study
[8–10].
Therefore,
more
studies
are
needed
to
confirm
these
localizations
and
understand
the
mechanisms
that
drive
PIPs
and
TIPs
targeting
to
PM,
tonoplast
or
chlor-
oplast
membranes.
The
dual
localization
of
PIPs
in
the
PM
and
chloroplast
envelope
may
be
related
to
a
role
in
facilitating
CO
2
diffusion
toward
photosynthetic
carboxylation
sites
[8].
PIP-mediated
CO
2
transport
was
demonstrated
using
heterologous
expression
systems
(Xenopus
oocytes
and
yeast
cells)
for
Nicotiana
tabacum
NtAQP1
[11]
and
sub-
sequently
for
PIP
homologs
of
other
species
such
as
Arabidopsis
[12]
or
barley
[13].
In
complement
to
these
studies,
reverse
genetic
analyses
in
transgenic
tobacco,
Arabidopsis
and
poplar
(Populus
tremula
x
alba)
with
Available
online
at
www.sciencedirect.com
ScienceDirect
www.sciencedirect.com
Current
Opinion
in
Plant
Biology
2014,
22:101–107

altered
PIP
expression
have
revealed
defects
in
meso-
phyll
CO
2
conductance
(g
m
),
pointing
to
a
genuine
role
of
aquaporins
in
leaf
CO
2
transport
[12,14,15].
However,
the
molecular
bases
of
g
m
,
with
combined
contributions
of
cell
walls,
carbonic
anhydrases
and
plasma
and
chloroplastic
membranes
are
as
yet
unclear
and
the
strong
g
m
pheno-
type
of
some
aquaporin
mutant
plants
has
been
ques-
tioned
[16,17].
Thus,
the
possibility
remains
that
regulatory
mechanisms
altering
g
m
are
unmasked
in
plants
with
altered
aquaporin
functions.
Similar
to
CO
2
,
the
ability
of
plant
aquaporins
to
facilitate
H
2
O
2
transport
across
cellular
membranes
was
first
demonstrated
by
heterologous
expression,
using
toxicity
growth
and/or
uptake
assays
in
yeast
[18,19].
In
addition,
recent
work
in
maize
PIPs
showed
that
specific
isoforms
can
show
distinct
selectivity
with
respect
to
H
2
O
2
[20].
This
reactive
oxygen
species
(ROS)
is
per
se
a
potent
regulator
of
aquaporins
as
it
downregulates
plant
root
hydraulic
conductivity
in
many
plant
species
[21].
H
2
O
2
reduces
the
transcription
of
most
Arabidopsis
PIP2
genes
in
roots
[22],
and
affects
their
C-terminal
phosphorylation
and
subcellular
localization
[21,23,24].
However,
the
gap
between
H
2
O
2
transport
data
in
heter-
ologous
systems
and
whole
plant
responses
still
needs
to
be
filled.
Recently,
overexpression
of
a
wheat
PIP2
homolog
(TaAQP7)
in
transgenic
tobacco
was
shown
to
enhance
drought
stress
tolerance
by
reducing
ROS
accumulation
[25].
Whereas
this
study
suggests
a
role
of
aquaporins
in
ROS
detoxification,
PIP-mediated
H
2
O
2
transport
may
also
play
a
role
in
cell
signaling.
A
general
limitation
is
that,
up
to
now,
studies
on
H
2
O
2
membrane
transport
by
plant
aquaporins
were
performed
in
yeast
using
a
fluorescent
dye
(H
2
DCFDA)
which
is
not
specific
of
H
2
O
2
[18].
The
use
of
the
genetically
encoded
fluor-
escent
H
2
O
2
sensor,
HyPer
[26],
was
instrumental
to
show
that
human
AQP3
can
mediate
H
2
O
2
uptake
in
mammalian
cells,
thereby
contributing
to
intracellular
signaling
in
response
to
Epidermal
Growth
Factor
[27].
AQP8
was
also
shown
to
facilitate
diffusion
of
H
2
O
2
through
the
PM
of
erythro
megakaryocytic
cells
which
in
turn
induced
phosphorylation
of
both
PhosphatidylI-
nositol-4,5-bisphosphate
3-kinase
(PI3K)
and
p38
mito-
gen-activated
protein
kinase
(MAPK)
[28].
A
similar
approach
will
have
to
be
conducted
in
planta
to
unam-
biguously
establish
the
role
of
aquaporin-mediated
mem-
brane
diffusion
of
H
2
O
2
in
signaling
cascades
or
detoxification
processes.
The
tetramerization
of
PIPs:
an
expanding
array
of
functional
combinations
Aquaporins
assemble
as
tetramers
in
cell
membranes,
with
cytoplasmic
loop
B
and
extra-cytoplasmic
loop
E
delimiting
a
central
pore
in
each
monomer.
The
inter-
molecular
interactions
leading
to
PIP
oligomer
formation
are
as
yet
unclear.
In
maize
PIPs,
they
involve
loop
E
[29]
and
a
highly
conserved
cysteine
residue
of
loop
A
[30].
This
residue
stabilizes
PIP
dimers
through
a
disulfide
bridge
between
two
monomers,
but
has
limited
effects
on
their
functionality.
There
is
now
convincing
evidence
that
distinct
PIP
iso-
forms
can
physically
interact
and
likely
assemble
as
heterotetramers.
The
first
crucial
experiments
were
per-
formed
in
Xenopus
oocytes
with
PIPs
from
maize,
and
later
from
other
species
including
tobacco,
barley
and
strawberry
[29,31–33].
These
experiments
showed
that
homologs
of
the
PIP1
subclass
can
be
properly
targeted
at
the
PM,
only
when
co-expressed
with
PIP2
isoforms.
Direct
evidence
for
physical
interaction
between
PIP1s
and
PIP2s
was
obtained
in
planta
and
the
role
of
this
interaction
in
PIP1
trafficking
to
the
PM
was
nicely
extended
to
maize
protoplasts
[34].
However,
we
note
that
several
PIP1
and
PIP2
isoforms
are
co-expressed
in
most
other
plant
cell
types,
suggesting
that
in
these
cells
PIP2s
may
not
be
limiting
for
PIP1
targeting
to
the
PM.
Thus,
hetero-tetramerization
may
not
represent
a
ubiqui-
tous
regulatory
mechanism
of
PIP1
trafficking.
Recent
evidence
in
oocytes
and
yeast
indicate
that
this
process
can
also
affect
the
overall
tetramer
sensitivity
to
protons
[33]
or
the
substrate
specificity
and
specific
activity
of
individual
monomers
[33,35].
Thus,
combinatorial
regu-
lation
involving
multiple
PIP1s
and
PIP2s
(five
and
eight
in
Arabidopsis,
respectively)
may
provide
a
fine
adjust-
ment
of
PIP
functions
at
the
PM
(Figure
1).
PIP
trafficking,
cycling
and
partitioning:
how
to
cross
multiple
checkpoints
Even
though
PIPs
have
been
used
as
PM
markers
for
a
long
time,
it
is
only
recently
that
their
cellular
trafficking
was
studied
as
such.
A
diacidic
motif
(DxE)
found
at
the
N-terminus
of
some
maize
and
Arabidopsis
PIP2s
[36,37]
was
shown
to
act
as
an
endoplasmic
reticulum
(ER)
export
signal,
probably
by
recruiting
Sec24
and
inducing
COPII
vesicle
formation
(reviewed
in
[4]).
A
similar
sorting
mechanism
was
described
in
other
multimeric
membrane
proteins
such
as
Shaker-like
potassium
chan-
nels
[38].
This
suggests
that
oligomerization
likely
hap-
pens
at
the
ER
membrane
during
PIP
biogenesis
and
that
ER
sorting
would
act
as
a
regulatory
checkpoint
after
homotetramer
or
heterotetramer
formation.
Neverthe-
less,
we
note
that
ZmPIP2;1
or
ZmPIP2;2
can
reach
the
PM
even
in
the
absence
of
a
diacidic
motif,
whereas
ZmPIP1;2
carrying
such
motif
is
retained
in
the
ER
[36].
Thus,
additional
motifs
are
likely
present
in
PIPs
and
their
involvement
in
ER
export
or
retention
remains
to
be
identified.
The
regulated
trafficking
of
PIPs
also
seems
to
be
central
in
plant
cell
response
to
hormonal
and
environmental
stimuli.
For
instance,
a
reduction
in
PIP
abundance
at
the
PM
of
Arabidopsis
root
epidermal
cells
can
occur
in
the
few
tens
of
minutes
following
an
osmotic
or
salt
stress
[21,39,40].
This
phenomenon
is
dependent
on
protein
102
Cell
biology
Current
Opinion
in
Plant
Biology
2014,
22:101–107
www.sciencedirect.com

cycling
between
the
PM
and
endosomes,
a
process
that
has
been
extensively
described
in
auxin
efflux
carriers
[41].
The
use
of
membrane
trafficking
inhibitors
and
co-
localization
approaches
have
shown
that
both
a
clathrin-
dependent
and
a
flotillin-associated
endocytosis
routes
may
contribute
to
cycling
of
AtPIP2;1
[39,40,42].
The
respective
role
of
these
pathways,
under
either
resting
conditions
or
environmental
stresses,
is
as
yet
unclear
and
complementary
genetic
approaches
will
be
needed
to
address
this
point.
In
these
respects,
the
recent
molecular
dissection
of
the
TPLATE
complex,
that
allows
recruit-
ment
of
the
clathrin
machinery
at
the
PM
[43],
opens
exciting
perspectives
to
explore
PIP
cycling
regulation.
As
recently
shown
for
plant
anion
channel
SLAH3
[44

]
and
NADPH
oxidase
RbohD
[45

],
membrane
protein
activity
can
also
be
regulated
by
partitioning
within
PM
micro-domains.
This
dynamic
equilibrium
is
intimately
linked
to
protein
diffusion
within
the
PM
plane.
The
use
by
Li
et
al.
[40]
of
Total
Internal
Reflection
Fluorescence
(TIRF)
microscopy
has
allowed
tracking
of
AtPIP2;1
particles
in
root
epidermal
cells.
This
study
revealed
a
relatively
low
lateral
motion
of
this
aquaporin
which
was
increased
by
about
twofold
during
salt
stress
[40]
(Figure
1).
It
was
speculated
that
this
effect
of
salt
may
be
associated
to
the
enhanced
recruitment
of
AtPIP2;1
into
the
endocytosis
machinery.
t-SNAREs
are
membrane-associated
proteins
involved
in
membrane
identity
and
vesicle
targeting,
that
form
submicrometer
clusters
within
the
PM
of
animal
cells
[46,47].
In
plants,
t-
SNAREs
are
emerging
as
central
players
of
membrane
protein
dynamics.
For
instance,
two
SNARE
proteins
of
Arabidopsis,
AtSYP61
and
AtSYP121,
were
recently
shown
to
form
a
complex
that
modulates
AtPIP2;7
post-Golgi
trafficking
thereby
fine-tuning
PM
water
permeability
[48

].
In
addition,
maize
ZmSYP121
was
shown
to
phy-
sically
interact
with
ZmPIP2;5
[49

]
to
favor
its
targeting
to
the
PM.
This
syntaxin
acts
similarly
on
several
Shaker-
like
potassium
channels
[50,51].
The
ability
of
SYP121
to
form
tripartite
complexes
at
the
PM
bringing
together
potassium
channels
and
aquaporins
is
as
yet
unknown
but
could
critically
contribute
to
cell
turgor
regulation.
Mem-
brane
shape
is
also
a
key
determinant
of
transmembrane
protein
targeting.
Recent
studies
in
giant
unilamellar
liposomes
showed
that
whereas
concentration
of
mam-
malian
AQP0
was
similar
in
flat
and
curved
membranes,
the
potassium
channel
KvAP
accumulated
in
tubular
membranes,
with
the
greatest
enrichment
in
most
highly
Plant
aquaporins
on
the
move
Verdoucq
et
al.
103
Figure
1
Heterotetramerization
ENDOPLASMIC RETICULUM
Sorting
PLASMA MEMBRANE
Micro-
domain
Partitioning within
the PM plane
H
2
O, CO
2
, H
2
O
2
, ...
P
PP
Post-translational
modifications
Sequestration
Degradation
Hormonal & environmental stimuli
VESICLE
Current Opinion in Plant Biology
Schematic
representation
of
aquaporin
function
and
regulation
in
plant
PM.
Hetero-tetramerization
of
PIP1s
(white)
with
PIP2s
(gray)
is
thought
to
be
crucial
for
proper
sorting
of
the
former
to
the
PM.
The
transport
specificity
of
individual
PIP
isoforms
and
their
ability
to
transport
water
and/or
CO
2
and
H
2
O
2
was
mostly
inferred
from
expression
studies
in
heterologous
systems.
The
figure
shows
that
multiple
stimuli
(hormones,
light
and
stresses)
can
act
on
several
facets
of
PIP
functionality:
their
post-translational
modification
profile,
their
lateral
diffusion
at
the
PM
and
their
rate
of
cycling/
endocytosis.
The
latter
phenomenon
is
thought
to
be
crucial
for
regulating
PIP
density
at
the
PM
and
thereby
cell
water
permeability.
Note
that,
depending
on
modified
site,
phosphorylation
of
PIPs
can
affect
their
intrinsic
activity
or
subcellular
localization.
www.sciencedirect.com
Current
Opinion
in
Plant
Biology
2014,
22:101–107

curved
regions
[52,53].
The
mobility
of
these
two
mem-
brane
proteins
was
crucially
dependent
on
the
membrane
deformations
that
are
self-generated
around
the
protein
and
that
can
be
tuned
according
to
membrane
tension
[53].
These
recent
advances
suggest
that
much
remains
to
be
learnt
from
the
dynamic
tracking
of
single
aquaporin
molecules
in
native
plant
membranes,
to
dissect
their
cellular
regulation
by
hormonal
and
environmental
stimuli.
Post-translational
modifications
(PTM)
of
aquaporins:
phosphorylation
makes
its
marks
While
various
PTM
such
as
methylation
[54,55],
ubiqui-
tination
[56],
deamidation
[23]
and
phosphorylation
[23,24,57,58

]
have
been
reported
in
PIPs,
most
func-
tional
studies
have
focused
on
the
role
of
the
latter.
PIP2s
carry
several
conserved
phosphorylation
sites
in
their
cytosolic
loop
B
and
C-terminal
tail
[59].
X-ray
crystal-
lography
structure
of
a
spinach
PIP2
(SoPIP2;1)
indicated
that
phosphorylation
of
these
sites
can
play
an
important
role
in
pore
gating
[60].
Phosphorylation
of
C-terminal
Ser-274
would
act
on
an
adjacent
SoPIP2;1
monomer
to
prevent
its
transition
to
a
closed-pore
conformation.
Phosphorylation
of
loop
B
Ser-115
would
disrupt
an
anchoring
network
between
cytosolic
loop
D
and
the
N-terminal
tail,
releasing
the
loop
D
and
causing
the
water
channel
to
open.
Yet,
functional
reconstitution
in
proteoliposomes
of
SoPIP2;1
forms
mutated
in
loop
B
failed
to
confirm
this
model
[61].
By
contrast,
heter-
ologous
expression
in
Xenopus
oocytes
of
SoPIP2;1
or
tulip
TgPIP2;2
indicated
that
phosphorylation
of
Ser-
115
or
Ser-274
increases
channel
activity
[59,62].
This
discrepancy
may
arise
from
different
phospholipidic
environments.
The
functionality
of
intrinsic
membrane
proteins
is
indeed
very
sensitive
to
the
lipid
membrane
characteristics,
as
was
shown
for
water
permeability
of
mammalian
AQP4
and
AQP0
[63

,64].
In
addition
to
gating,
PIP
phosphorylation
affects
their
subcellular
localization
(reviewed
in
[5]).
In
AtPIP2;1,
phosphoryla-
tion
of
Ser-283,
but
not
of
Ser-280,
is
required
for
target-
ing
of
newly
synthesized
proteins
to
the
PM
[24].
This
mark
also
provides
an
intracellular
sorting
signal
for
directing
internalized
AtPIP2;1
to
specific
spherical
bodies
under
salt
stress
[24].
Although
recent
phosphoproteomic
analyses
have
pro-
vided
a
good
inventory
of
phosphorylation
sites
present
in
PIPs
of
Arabidopsis
and
Oryza
sativa
[23,65–67],
only
a
few
studies
have
established
the
role
of
PIP
phosphorylation
in
regulating
water
transport
in
planta.
In
support
of
quantitative
phosphoproteomics,
expression
studies
of
phosphomimetic
and
phosphorylation
deficient
forms
of
AtPIP2;1
in
transgenic
Arabidopsis,
demonstrated
that
phosphorylation
at
Ser-280
and
Ser-283
was
necessary
for
mediating
leaf
hydraulic
conductivity
enhancement
under
darkness
[68

].
More
generally,
a
large-scale
pro-
teomics
analysis
of
aquaporins
in
Arabidopsis
roots
under
various
water,
oxidative
or
nutritional
constraints
showed
that
the
overall
phosphorylation
status
of
PIPs
was
posi-
tively
correlated
with
root
hydraulic
conductivity
across
the
whole
set
of
treatments
[23].
Characterization
of
specific
protein
kinases
involved
in
printing
phosphorylation
marks
on
multiple
aquaporin
isoforms
will
undoubtedly
boost
our
understanding
of
regulation
networks
involved
in
aqua-
porin
regulation.
For
instance,
a
large-scale
analysis
of
sucrose-induced
protein
phosphorylation
recently
led
to
the
identification
of
SIRK1,
a
Leucine-Rich
Repeat
Re-
ceptor-Like
Kinase
(LRR-RLK),
that
phosphorylates
the
C-terminal
tail
of
several
PIP2s
following
sucrose
resupply
to
starved
plantlets
[58

].
Large-scale
interactome
studies
[69]
are
also
expected
to
reveal
novel
regulatory
proteins
acting
on
aquaporin
function.
Conclusion
Recent
studies
have
shed
new
light
on
PIP
functions
and
regulation
in
specific
cell
types
(Figure
1).
For
instance,
combined
physiological
and
genetic
approaches
have
shown
that
PIPs
are
regulated
in
leaf
veins
(bundle
sheath
cells)
by
both
the
stress
hormone
abscisic
acid
(ABA)
[70]
and
the
light
regime
[68

].
Furthermore,
phosphoryla-
tion
of
a
single
aquaporin
isoform
(AtPIP2;1)
in
this
tissue
was
sufficient
to
account
for
light-dependent
regulation
of
leaf
hydraulics
[68

].
Hormonal
regulation
of
PIPs
has
also
established
novel
roles
during
plant
development.
Auxin,
which
orchestrates
root
growth
and
development,
was
found
to
inhibit
aquaporin
gene
expression
during
lateral
root
formation
in
Arabidopsis
root
[71

],
to
down-
regulate
turgor
of
overlaying
cortical
cells
and
favor
the
emergence
of
the
lateral
root
primordium.
These
studies
delineate
highly
relevant
contexts
in
which
to
investigate
cellular
regulation
of
aquaporins.
Whereas
phosphorylation
is
now
established
as
an
import-
ant
mark
of
PIPs
that
affect
both
their
activity
and
subcellular
localization,
the
next
challenge
will
be
to
identify
the
protein
kinases
and
phosphatases
and
the
transduction
pathways
that
determine
PIP
phosphoryla-
tion
profiles
in
specific
cell
types.
We
anticipate
that
recent
advances
in
microscopic
techniques
that
allow
tracking
of
single
aquaporin
proteins
and
a
better
un-
derstanding
of
membrane
heterogeneities
will
also
bring
novel
insights
into
PIP
regulation
at
the
PM.
These
processes
are
definitely
of
great
agronomic
relevance
for
the
control
of
plant
water
homeostasis
in
plants,
but
also
for
cell
signaling
(H
2
O
2
transport)
or
carbon
fixation
(CO
2
transport).
References
and
recommended
reading
Papers
of
particular
interest,
published
within
the
period
of
review,
have
been
highlighted
as:

of
special
interest

of
outstanding
interest
1.
Chaumont
F,
Tyerman
SD:
Aquaporins:
highly
regulated
channels
controlling
plant
water
relations.
Plant
Physiol
2014,
164:1600-1618.
104
Cell
biology
Current
Opinion
in
Plant
Biology
2014,
22:101–107
www.sciencedirect.com

2.
Li
G,
Santoni
V,
Maurel
C:
Plant
aquaporins:
roles
in
plant
physiology.
Biochim
Biophys
Acta
2014,
1840:1574-1582.
3.
Abascal
F,
Irisarri
I,
Zardoya
R:
Diversity
and
evolution
of
membrane
intrinsic
proteins.
Biochim
Biophys
Acta
2014,
1840:1468-1481.
4.
Hachez
C,
Besserer
A,
Chevalier
AS,
Chaumont
F:
Insights
into
plant
plasma
membrane
aquaporin
trafficking.
Trends
Plant
Sci
2013,
18:344-352.
5.
Luu
DT,
Maurel
C:
Aquaporin
trafficking
in
plant
cells:
an
emerging
membrane-protein
model.
Traffic
2013,
14:629-635.
6.
Soto
G,
Fox
R,
Ayub
N,
Alleva
K,
Guaimas
F,
Erijman
E,
Mazzella
A,
Amodeo
G,
Muschietti
J:
TIP5;1
is
an
aquaporin
specifically
targeted
to
pollen
mitochondria
and
is
probably
involved
in
nitrogen
remobilization
in
Arabidopsis
thaliana.
Plant
J
2010,
64:1038-1047.
7.
Wudick
MM,
Luu
DT,
Tournaire-Roux
C,
Sakamoto
W,
Maurel
C:
Vegetative
and
sperm
cell-specific
aquaporins
of
Arabidopsis
highlight
the
vacuolar
equipment
of
pollen
and
contribute
to
plant
reproduction.
Plant
Physiol
2014,
164:1697-1706.
8.
Uehlein
N,
Otto
B,
Hanson
DT,
Fischer
M,
McDowell
N,
Kaldenhoff
R:
Function
of
Nicotiana
tabacum
aquaporins
as
chloroplast
gas
pores
challenges
the
concept
of
membrane
CO
2
permeability.
Plant
Cell
2008,
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9.
Ferro
M,
Brugiere
S,
Salvi
D,
Seigneurin-Berny
D,
Court
M,
Moyet
L,
Ramus
C,
Miras
S,
Mellal
M,
Le
Gall
S
et
al.:
AT_CHLORO,
a
comprehensive
chloroplast
proteome
database
with
subplastidial
localization
and
curated
information
on
envelope
proteins.
Mol
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2010,
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10.
Beebo
A,
Mathai
JC,
Schoefs
B,
Spetea
C:
Assessment
of
the
requirement
for
aquaporins
in
the
thylakoid
membrane
of
plant
chloroplasts
to
sustain
photosynthetic
water
oxidation.
FEBS
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587:2083-2089.
11.
Uehlein
N,
Lovisolo
C,
Siefritz
F,
Kaldenhoff
R:
The
tobacco
aquaporin
NtAQP1
is
a
membrane
CO
2
pore
with
physiological
functions.
Nature
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12.
Heckwolf
M,
Pater
D,
Hanson
DT,
Kaldenhoff
R:
The
Arabidopsis
thaliana
aquaporin
AtPIP1;2
is
a
physiologically
relevant
CO
2
transport
facilitator.
Plant
J
2011,
67:795-804.
13.
Mori
IC,
Rhee
J,
Shibasaka
M,
Sasano
S,
Kaneko
T,
Horie
T,
Katsuhara
M:
CO
2
transport
by
PIP2
aquaporins
of
barley.
Plant
Cell
Physiol
2014,
55:251-257.
14.
Secchi
F,
Zwieniecki
MA:
The
physiological
response
of
Populus
tremula
x
alba
leaves
to
the
down-regulation
of
PIP1
aquaporin
gene
expression
under
no
water
stress.
Front
Plant
Sci
2013,
4:507.
15.
Flexas
J,
Ribas-Carbo
M,
Hanson
DT,
Bota
J,
Otto
B,
Cifre
J,
McDowell
N,
Medrano
H,
Kaldenhoff
R:
Tobacco
aquaporin
NtAQP1
is
involved
in
mesophyll
conductance
to
CO
2
in
vivo.
Plant
J
2006,
48:427-439.
16.
Kaldenhoff
R,
Kai
L,
Uehlein
N:
Aquaporins
and
membrane
diffusion
of
CO
2
in
living
organisms.
Biochim
Biophys
Acta
2014,
1840:1592-1595.
17.
Evans
JR,
Kaldenhoff
R,
Genty
B,
Terashima
I:
Resistances
along
the
CO
2
diffusion
pathway
inside
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2009,
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18.
Bienert
GP,
Moller
AL,
Kristiansen
KA,
Schulz
A,
Moller
IM,
Schjoerring
JK,
Jahn
TP:
Specific
aquaporins
facilitate
the
diffusion
of
hydrogen
peroxide
across
membranes.
J
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2007,
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19.
Dynowski
M,
Schaaf
G,
Loque
D,
Moran
O,
Ludewig
U:
Plant
plasma
membrane
water
channels
conduct
the
signalling
molecule
H
2
O
2
.
Biochem
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2008,
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20.
Bienert
GP,
Heinen
RB,
Berny
MC,
Chaumont
F:
Maize
plasma
membrane
aquaporin
ZmPIP2;5,
but
not
ZmPIP1;2,
facilitates
transmembrane
diffusion
of
hydrogen
peroxide.
Biochim
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2014,
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Y,
Boudet
J,
Postaire
O,
Luu
DT,
Tournaire-Roux
C,
Maurel
C:
Stimulus-induced
downregulation
of
root
water
transport
involves
reactive
oxygen
species-activated
cell
signalling
and
plasma
membrane
intrinsic
protein
internalization.
Plant
J
2008,
56:207-218.
22.
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C,
Rhee
JY,
Kwak
KJ,
Chung
GC,
Horie
T,
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M,
Kang
H:
Hydrogen
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permeability
of
plasma
membrane
aquaporins
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Pietro
M,
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J,
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GW,
Hem
S,
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K,
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M,
Maurel
C,
Santoni
V:
Coordinated
post-translational
responses
of
aquaporins
to
abiotic
and
nutritional
stimuli
in
Arabidopsis
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2013,
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Prak
S,
Hem
S,
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J,
Viennois
G,
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N,
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M,
Maurel
C,
Santoni
V:
Multiple
phosphorylations
in
the
C-
terminal
tail
of
plant
plasma
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Role
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sub-cellular
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AtPIP2;1
in
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2008,
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Zhou
S,
Hu
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X,
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Z,
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C,
Wang
C,
Wang
J,
He
Y,
Yang
G
et
al.:
Overexpression
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the
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Belousov
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Miller
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CJ:
Aquaporin-3
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K,
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V,
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MC,
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D,
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M,
Chaumont
F:
A
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in
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formation
between
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T,
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S,
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M,
Katsuhara
M:
Mechanisms
of
water
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mediated
by
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aquaporins
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Drought
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Yaneff
A,
Sigaut
L,
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M,
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K,
Pietrasanta
LI,
Amodeo
G:
Heteromerization
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34.
Zelazny
E,
Borst
JW,
Muylaert
M,
Batoko
H,
Hemminga
MA,
Chaumont
F:
FRET
imaging
in
living
maize
cells
reveals
that
plasma
membrane
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interact
to
regulate
their
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B,
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Macadam
X,
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M,
Lachnit
M,
Pede
N,
Priem
N
et
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Aquaporin
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36.
Zelazny
E,
Miecielica
U,
Borst
JW,
Hemminga
MA,
Chaumont
F:
An
N-terminal
diacidic
motif
is
required
for
the
trafficking
of
maize
aquaporins
ZmPIP2;4
and
ZmPIP2;5
to
the
plasma
membrane.
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Sorieul
M,
Santoni
V,
Maurel
C,
Luu
DT:
Mechanisms
and
effects
of
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of
over-expressed
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AtPIP2;1
in
the
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move
Verdoucq
et
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105
www.sciencedirect.com
Current
Opinion
in
Plant
Biology
2014,
22:101–107

38.
Mikosch
M,
Hurst
AC,
Hertel
B,
Homann
U:
Diacidic
motif
is
required
for
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mechanical/structural
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AR,
Hem
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2013,
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Using
quantitative
(phospho)proteomic
analyses
and
expression
in
trans-
genic
Arabidopsis
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106
Cell
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Current
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Plant
Biology
2014,
22:101–107
www.sciencedirect.com

of
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Y,
Xu
M,
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RS,
Ho
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S,
You
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Bundle-sheath
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M
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aquaporin-dependent
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www.sciencedirect.com
Current
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2014,
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