Salinity Effects on Leaf Anatomy: Consequences for Photosynthesis 1

Abstract

Increasing salinity led to substantially higher ratios of mesophyll surface area to leaf area (A(mes)/A) for Phaseolus vulgaris and Gossypium hirsutum and a smaller increase for Atriplex patula, a salt-tolerant species. The increase in internal surface for CO(2) absorption did not lead to higher CO(2) uptake rates, since the CO(2) resistance expressed on the basis of mesophyll cell wall area (r(cell)) increased even more with salinity. The differences among species in the sensitivity of photosynthesis to salinity in part reflect the different A(mes)/A and r(cell) responses.

Full text

Plant
Physiol.
(1979)
63,
700-703
0032-0889/79/63/0700/04$00.50/0
Salinity
Effects
on
Leaf
Anatomy
CONSEQUENCES
FOR
PHOTOSYNTHESIS'
Received
for
publication
August
31,
1978
and
in
revised
form
November
29,
1978
DAVID
J.
LONGSTRETH
AND
PARK
S.
NOBEL
Department
of
Biology
and
Division
of
Environmental
Biology
of
the
Laboratory
of
Nuclear
Medicine
and
Radiation
Biology,
University
of
California,
Los
Angeles,
California
90024
ABSTRACT
Increasing
salinity
led
to
substantially
higher
ratios
of
mesophyH
surface
area
to
leaf
area
(A"/A)
for
Phaseolus
vulgaris
and
Gossypium
hirsutum
and
a
smaller
increase
for
Atripkx
patuls,
a
salt-tolerant
species.
The
increase
in
internal
surface
for
CO2
absorption
did
not
lead
to
higher
CO2
uptake
rates,
since
the
CO2
resistance
expressed
on
the
basis
of
mesophyli
cell
wall
area
(r,,u)
increased
even
more
with
salinity.
The
differences
among
species
in
the
sensitivity
of
photosynthesis
to
salinity
in
part
reflect
the
different
A"/A
and
r<u
responses.
Increases
in
leaf
thickness
can
be
induced
by
exposure
of
roots
to
high
concentrations
of
NaCl
(6,
11,
17-20).
Such
salt-induced
succulence
could
lower
the
resistance
to
CO2
uptake
and
thus
increase
photosynthetic
rates
by
increasing
the
amount
of
internal
leaf
surface
area
across
which
gaseous
exchange
can
occur
per
unit
leaf
area.
However,
high
concentrations
of
substrate
NaCl
generally
reduce
photosynthesis
(2,
4,
12),
although
the
photosyn-
thetic
rates
of
some
species
from
saline
habitats
can
be
rather
insensitive
to
high
salinity
(1,
8,
10).
At
saturating
irradiance,
photosynthesis
is
generally
limited
by
the
rate
of
CO2
diffusion
into
the
leaf.
The
two
most
important
components
controlling
this
diffusion
are
stomatal
resistance
and
mesophyll
resistance
(9).
Using
the
ratio
of
mesophyll
surface
area
to
leaf
surface
area,
the
mesophyll
resistance
can
be
partitioned
into
effects
of
internal
leaf
anatomy
and
the
inherent
CO2
diffusion
resistance
of
the
mesophyll
cells
(14,
16).
Here,
the
interaction
between
salinity-induced
changes
in
leaf
anatomy
and
net
CO2
exchange
was
studied
for
Phaseolus
vulgaris,
Gossypium
hirsutum,
and
Atriplex
patula.
These
species
represent
a
wide
range
of
salinity
tolerance,
since
bean
is
salt-sensitive,
cotton
is
moderately
tolerant,
and
Atriplex
grows
in
saline
habitats
(4,
5,
19).
Using
plants
grown
under
different
NaCl
treatments,
the
relationship
between
NaCl-induced
anatomical
change
and
photosynthetic
response
at
the
mesophyll
cell
level
was
quanti-
tavely
analyzed
using
a
resistance
circuit
analogy.
MATERIALS
AND
METHODS
Seeds
of
P.
vulgaris
L.
cv.
Kentucky
Wonder,
G.
hirsutum
L.
var.
McNair
612,
and
A.
patula
ssp.
hastata
were
germinated
in
wet
sand
and
the
young
plants
were
transferred
to
nutrient
solution
after
10
days
(bean
and
cotton)
or
25
days
(Atriplex).
Plants
were
grown
hydroponically
in
aerated
nutrient
solution
(Hoagland
No.
'
This
investigation
was
supported
by
National
Science
Foundation
Grant
DEB
77-11128.
1,
Hoagland
minor
solution,
and
8
,ug
g-'
iron
in
sequestered
form
[71)
for
7
days.
Salinity
was
varied
by
adding
NaCl
(up
to
Q.4
molal)
to
the
nutrient
solution
to
yield
a
range
of
osmotic
poten-
tials
from
-0.05
MPa
to
-1.8
MPa
(1
MPa
=
10
bar).
Salinity
additions
were
made
in
daily
increments
of
0.025
molal
for
bean
and
0.05
molal
for
cotton
or
Atriplex
to
reach
the
indicated
levels.
Predawn
leaf
xylem
pressures
determined
with
a
PMS
Instruments
pressure
bomb
were
similar
to
the
osmotic
potentials
of
the
treatment
solutions.
Plants
were
maintained
in
environmental
chambers
using
a
12-h
day
at
27
C
with
300
,E
m
2
s-'
PAR
provided
by
warm-white
fluorescent
lamps
and
a
12-h
night
at
21
C.
Leaves
used
for
measurements
developed
under
a
particular
salinity
treatment
for
19
to
25
days
after
full
salinity
had
been
reached.
Rates
of
water
vapor
loss
and
CO2
uptake
were
deter-
mined
at
1,700
±
200
,uE
m
2
s-'
PAR
on
attached
leaves
of
at
least
two
plants
in
each
salinity
treatment
using
a
null
point,
closed
circuit
flow
system
with
circulating
air
containing
approx-
imately
1%
02
(15).
The
low
02
level
minimized
effects
of
respi-
ration
and
photorespiration
on
measured
CO2
fluxes
(9,
16).
Leaf
temperature
was
maintained
at
29
±
1
C
as
monitored
by
36-
gaugeiron
constantan
thermocouples
and
the
water
vapor
pressure
difference
between
leaf
and
air
was
1.5
±
0.2
kPa.
Net
CO2
exchange
(JCo2)2
was
represented
by
the
CO2
concen-
tration
difference
between
air
and
the
site
of
carboxylation
divided
by
a
stomatal
resistance
plus
a
mesophyll
resistance
(9,
14,
16).
Water
vapor
resistance
(r,,,)
was
used
as
a
measure
of
stomatal
resistance
and
was
set
equal
to
the
water
vapor
concentration
drop
from
leaf
to
air
divided
by
the
transpiration
rate
(the
water
vapor
concentration
in
the
leaf
was
assumed
to
be
the
saturation
value
at
the
measured
leaf
temperature).
Jco2
was
plotted
versus
the
CO2
concentration
in
the
intercellular
air
spaces
next
to
the
stomates
(co2),
which
was
equated
to
the
CO2
concentration
outside
the
leaf
minus
Jco,
X
1.56
%,
(14);
the
reciprocal
of
the
slope
of
the
line
connecting
the
CO2
compensation
point
(cM,
at
which
Jco2
equals
zero)
and
the
Jco,
value
at
ambient
CO2
concentration
(340
pl
I-)
was
designated
the
mesophyll
resistance
(rme9).
Since
Jco2
was
generally
linear
with
cc,
for
the
range
considered
here,
using
initial
slopes
to
estimate
rm.
would
have
had
little
effect
on
the
results.
Leaf
thickness
and
Am'/A
were
determined
for
each
leaf
used
in
the
gas
exchange
analysis.
Fresh
sections
cut
from
each
side
of
the
leaf
midvein
were
infiltrated
with
distilled
H20
and
examined
using
a
Zeiss
microscope
with
a
camera
lucida.
Cell
surface
areas
were
calculated
assuming
that
palisade
cells
were
cylindrical
with
2Abbreviations:
Am"/A:
surface
area
of
mesophyll
cells
per
unit
leaf
surface
area;
ceO2:
CO2
concentration
in
the
intercellular
air
spaces
next
to
the
stomates;
Jco2:
net
CO2
exchange
rate
per
unit
leaf
area;
rcen:
cellular
CO2
resistance
expressed
on
a
mesophyll
surface
area
basis;
rms:
CO2
mesophyll
resistance;
r,,:
water
vapor
resistance
(principally
stomatal).
700

SALINITY,
SUCCULENCE,
AND
PHOTOSYNTHESIS
hemispherical
ends
and
spongy
cells
were
spheres
(13,
16).
The
ratio
of
mesophyll
cell
surface
area
to
leaf
surface
area
(Am/A)
was
derived
from
the
leaf
anatomical
measurements
and
used
to
calculate
reell
(14):
rceU
=
rmes
X
Ame8/A
(1)
Fresh
and
dry
leaf
weights
were
also
determined,
and
fresh
weight/cm2
-
dry
weight/cm2
was
designated
succulence
(12,
17).
To
estimate
plant
dry
matter
production,
the
dry
weight
of
the
whole
plant
was
determined
30
days
after
full
salinity
had
been
reached.
RESULTS
Salinity
had
a
marked
effect
on
dry
matter
production
per
plant
(Fig.
IA).
Plant
biomass
of
the
salt-sensitive
bean
declined
sharply
with
salinity
up
to
0.1
molal,
cotton
biomass
declined
sharply
above
0.1
molal,
and
the
biomass
of
Atriplex,
the
salt-tolerant
species,
declined
gradually
from
0.0
to
0.4
molal
NaCl
(bean
and
cotton
did
not
survive
salinities
0.1
molal
above
those
indicated
in
Fig.
1).
Leaf
succulence
increased
with
increasing
NaCl
concen-
tration
for
all
three
species
(Fig.
IB).
Mesophyll
thickness
also
increased
with
salinity
in
all
three
species
(Table
I),
due
to
an
increase
in
length
of
palisade
cells
and
an
increased
number
of
spongy
cell
layers.
Diameters
of
palisade
cells
of
bean
and
cotton
remained
fairly
constant
in
all
salinity
treatments,
but
were
greater
in
the
A
triplex
palisade
cells
of
longer
lengths.
Spongy
cell
diameters
tended
to
increase
with
salinity
for
all
three
species
(Table
I).
The
surface
area
of
a
spongy
mesophyll
was
33
to
34%
of
the
total
Am0/A
for
bean,
was
37
to
40Y%
for
cotton,
and
increased
from
45
to
53%
as
the
salinity
was
raised
to
0.4
molal
for
Atriplex.
Greater
palisade
cell
lengths
and
more
spongy
layers
resulted
in
a
higher
Am0/A
for
bean
and
cotton
(Fig.
2).
Am0/A
for
Atriplex
varied
little
with
increasing
salinity,
because
palisade
cells
increased
in
diameter
as
well
as
length
(Fig.
2
and
Table
I).
c
25
20
1
20
I
0
_
ottnean
C
4
0
B
an
E
5
0
60
B
0
~~~~~~Afrip/ex
M
40
E
Cotton
0
0.0
0.1
0.2
0.3
0.4
NaCI
(molal)
FIG.
1.
Effects
of
NaCI
treatments
on
plant
dry
matter
production
(A)
and
leaf
succulence
(B)
for
bean
(0),
cotton
(A),
and
Atriplex
(l).
Standard
errors
averaged
5%
of
the
mean.
Net
CO2
exchange
retes
decreased
markedly
at
0.05
molal
NaCl
for
bean,
at
0.2
molal
for
cotton,
while
Atriplex
appeared
to
be
affected
only
at
0.4
molal
(Fig.
3A).
Correlated
with
salinity-
induced
reductions
in
net
CO2
exchange
rates
were
increases
in
resistance
to
water
vapor
diffusion
(Fig.
3B).
Over
the
ranges
of
NaCl
concentrations
used,
salinity
had
little
effect
on
rmes
for
bean,
a
small
effect
for
Atriplex,
and
an
appreciable
effect
for
cotton
(Fig.
3C).
Table
I.
Effects
of
NaCl
on
Leaf
Thickness
and
Mesophyll
Cell
7imen-
sions.
Epidermal
thickness
is
the
sum
of
both
lower
and
upper
epider-
mis;
mesophyll
thickness
is
the
sum
of
both
palisade
and
spongy
layers.
Each
entry
is
the
mean
of
16
measurements.
Standard
errors
averaged
3%
of
the
mean.
NaCl
(molal)
0.0
0.05
0.1
0.2
0.3
0.4
Epidermal
thickness
(um)
Bean
26
28
31
Cotton
31
35
33
Atriplex
27
--
44
Mesophyll
thickness
(uJm)
Bean
150
165
260
Cotton
209
256
329
Atriplex
210
--
210
Palisade
cell
length
(um)
Bean
88
103
129
Cotton
85
106
113
Atriplex
80
--
80
Palisade
cell
diameter
(umr)
Bean
19
18
20
Cotton
20
23
21
Atriplex
29
--
28
Spongy
cell
diameter
(uLM)
Bean
25
22
32
Cotton
28
23
27
Atriplex
36
--
41
37
36
41
41
373
422
212
260
118
124
82
87
23
20
23
34
33
34
41
42
51
340
115
43
63
Plant
Physiol.
Vol.
63,
1979
701

LONGSTRETH
AND
NOBEL
Resistance
per
unit
mesophyll
cell
surface
(rceu)
approximately
doubled
over
the
range
of
salinity
used
for
each
species
(Fig.
4).
The
rate
of
increase
in
rcell
was
inversely
correlated
with
salt
tolerance,
e.g.
from
0.0
to
0.1
molal
NaCl,
rce,l
increased
39%
for
bean,
28%
for
cotton,
and
13%
for
Atriplex.
The
minimum
cellular
resistance
of
38
s
cm-'
for
Atriplex
is
apparently
the
lowest
one
so
far
re?orted,
and
approaches
the
predicted
lower
limit
of
about
20
s
cm
for
rce,l(14).
To
see
whether
salinity
effects
on
AmeS/A
and
rcell
were
revers-
ible,
cotton
was
kept
in
0.0
molal
NaCl,
kept
in
0.3
molal
NaCl,
or
placed
in
0.3
molal
NaCl
and
then
transferred
to
0.0
molal
NaCl
after
the
normal
development
period
of
19
days.
Two
days
after
transfer,
Jco,
recovered
22%
of
the
salinity-induced
inhibition
and
after
6
days
recovered
59%
of
the
difference
between
0.0
and
0.3
molal
NaCl
(Fig.
3A).
The
increase
in
Jco2
upon
transfer
from
0.3
to
0.0
molal
NaCl
was
due
to
a
44%
decrease
in
rwv
and
a
35%
30F
to
E4
20
10
Bean
~_-
,Cotton
Atripo/ex
w
0.0
0.1
0.2
0.3
0.4
NaCI
(molal)
FIG.
2.
Mesophyll
cell
surface
area per
unit leaf
surface
area
versus
NaCI
treatments
for
bean
(0),
cotton
(A),
and
Atriplex
(0).
(A)
E
u
E
C
0
IA
3
0
2t
1
Bean
-,o
3
,
2
1I
I
0
6
E
4
a)
-t
"
EIV
0
L
0.0
B
Bean
Cotton
/~~
-/
ACtrp/'
C
Cotton
Bean
_
0~
A
trip/lex
0.1
0.2
0.3
0.4
NaCI
(molal)
FIG.
3.
Net
CO2
exchange
(A),
stomatal
resistance
(B),
and
mesophyll
resistance
(C)
for
bean
(0),
cotton
(A),
and
Atriplex
(Ol).
Jco2
and
rw,
were
determined
at
an
external
CO2
concentration
of
340
IlI
l-',
while
rm.,
was
calculated
from
curves
of
Jco2
versus
cCo2.
Bean
a)100
1
0~~~~
A
I
0.0
0.1
0.2
0.3
0.4
NaCl
(molal)
FIG.
4.
Influence
of
NaCl
treatments
on
cellular
resistance
for
bean
(0),
cotton
(A),
and
Atriplex
(l).
decrease
in
rm,,s,
which
was
accompanied
by
no
significant
change
in
Ames/A.
DISCUSSION
Raising
the
concentration
of
NaCl
in
hydroponic
solutions
resulted
in
greater
leaf
succulence
(mg
H20
cm-2)
and
greater
mesophyll
thickness
for
bean,
cotton,
and
Atriplex.
Similar
effects
on
succulence
and
leaf
thickness
have
been
reported
previously
for
bean
(1
1,
20)
and
cotton
(18),
as
well
as
other
species
(6,
12,
17).
A
substantial
increase
in
Am'/A
also
occurred
with
increased
salinity
for
bean
and
cotton,
but
not
for
Atriplex
(Fig.
2).
Palisade
cell
length
increased
and
diameter
remained
relatively
constant
with
salinity
for
bean
and
cotton
(Table
I),
accounting
for
the
increases
in
Ames/A.
Both
length
and
diameter
of
A
triplex
palisade
cells
increased,
resulting
in
little
change
in
Armes/A
with
salinity.
Thus
Ames/A
increased
more
rapidly
with
salinity
as
the
salt
tolerance
of
the
species
decreased.
Salinity
can
affect
photosynthesis
at
stomatal
and/or
mesophyll
levels,
depending
on
type
of
salinity,
duration
of
treatment,
spe-
cies,
and
plant
age
(2,
4,
5,
8,
10,
12).
Here,
stomatal
closure
substantially
reduced
photosynthesis
for
bean,
while
for
cotton
and
Atriplex
increases
in
both
r.,
and
rmes
were
responsible
for
the
decreases
in
photosynthesis.
Although
the
major
focus
of
this
study
was
on
anatomical
changes
and
their
impact
on
mesophyll
resistance,
a
significant
effect
of
salinity
was
on
stomatal
resist-
ance.
The
increase
in
Ames/A
with
salinity
could
have
reduced
rmes
because
there
is
then
more
internal
cell
surface
for
gas
exchange.
Such
a
relationship
has
previously
been
shown
for
illumination
effects
on
Plectranthus
parviJlorus
and
Hyptis
emoryi
(13,
14,
16).
The
increases
found
in
rme.
(Fig.
3C)
together
with
the
increases
in
Am'/A
(Fig.
2)
showed
that
resistance
on
a
mesophyll
cell
surface
basis
(rceu)
increased
substantially
with
salinity,
especially
for
the
less
salt-tolerant
species
(Fig.
4).
The
influence
of
increas-
ing
salinity
on
CO2
uptake
at
the
mesophyll
cell
level
would
not
have
been
apparent
if
only
mesophyll
resistance
had
been
meas-
ured,
since
the
increases
in
Am`/A
compensated
for
much
of
the
increases
in
rcell.
Lowering
substrate
salinity
after
a
high
Ames/A
had
developed
could
result
in
a
lower
rme,
if
rceu
declined
in
response
to
the
reduction
in
salinity
and
there
was
no
change
in
Am'/A.
Indeed
Am'/A
here
did
not
change
upon
transferring
cotton
from
0.3
to
0.0
molal
NaCl
after
leaf
development
and
rcel,
did
decline.
However,
it
went
only
from
200
to
130
s
cm-'
after
6
days,
and
hence
did
not
reach
the
low
value
of
78
s
cm-'
appropriate
for
a
plant
maintained
in
0.0
molal
NaCl
(Fig.
4).
The
photosynthetic
rate
of
the
transferred
plant
was
not
increased
above
that
of
the
702
Plant
Physiol.
Vol.
63,
1979

SALINITY,
SUCCULENCE,
AND
PHOTOSYNTHESIS
plant
maintained
continuously
in
0.0
molal
NaCl,
although
most
of
the
salinity
inhibition
was
overcome.
Components
of
rcelt
(14)
are
both
physical
(cell
walls,
mem-
branes,
intracellular
distances)
and
chemical
(reactions
of
photo-
synthesis).
Although
the
methods
used
here
do
not
allow
quanti-
tative
assessment
of
each
component,
calculations
based
on
known
ranges
of
some
cellular
properties
(14)
indicate
that
physical
dissimilarities
probably
could
not
account
for
the
changes
in
rr,,e
with
salinity
or
the
differences
in
rcell
among
species
(Fig.
4).
The
constancy
of
rcell
for
A
triplex
over
a
wide
NaCl
range
as
compared
to
the
variation
for
bean
and
cotton
presumably
indicates
differ-
ences
among
species
at
the
chemical
level.
Such
differences
in
the
response
of
rcell
may
reflect
different
degrees
of
shielding
of
the
photosynthetic
mechanism
from
harmful
NaCl
effects,
rather
than
inherent
dissimilarities
in
enzyme
properties
(3).
Acknowledgments-We
thank
R.
S.
Alberte
and
D.
T.
Patterson
for
helpful
comments
on
the
manuscrpt.
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