全 文 ：第 49 卷 第 7 期
2 0 1 3 年 7 月
林 业 科 学
SCIENTIA SILVAE SINICAE
Vol. 49，No. 7
Jul．，2 0 1 3
doi:10．11707 / j．1001-7488．20130706
Received date: 2012 － 05 － 16; Revised date: 2013 － 02 － 19．
Foundation project: National Natural Science Foundation of China ( 30872004 ) ; Fundamental Research Funds for the Central Universities
(DC12010305，12010204) ．
* Yao Shanjing is Corresponding author．
盐胁迫下杨树质外体离子对气体交换参数的影响*
马金龙1，3 姜国斌2 姚善泾1 金 华2
(1. 浙江大学化学与生物工程系 杭州 310027; 2. 大连民族学院环境与资源学院 大连 116600;
3. 大连民族学院生命科学学院 大连 116600)
摘 要: 利用微透析技术，研究盐胁迫下吴屯杨和小胡杨嫩茎质外体中离子的动态变化对气体交换参数的影响。
杨树嫩茎质外体离子采用微透析与原子吸收联用进行监测，同时采用 Li － 6400 便携式光合仪进行气体交换相关参
数的测定。盐胁迫下，2 个杨树品种嫩茎质外体中 Na +积累的程度不同，吴屯杨经过一段时间后能够自我调节，减
少 Na +含量，而小胡杨质外体一直积累 Na +，从而造成细胞的渗透胁迫，抑制植物生长; 随着盐处理时间的增加，2
种杨树 K +浓度基本呈现下降的趋势。吴屯杨在 100 mmol·L － 1 NaCl 胁迫早期光合受抑制的主要原因是非气孔限
制，后期是气孔限制; 而小胡杨光合受抑制的主要原因是气孔限制。对 Na + 浓度、K + 浓度、Ca2 + 浓度、Na + /K +、Pn
进行相关性分析发现，2 个杨树品种 Pn 均与 Na
+浓度和 Na + /K +比值呈显著的负相关，与 K +浓度呈极显著的正相
关。以 Pn 为因变量，以 Na
+，K +，Ca2 +浓度和 Na + /K +为自变量，进行多元线性逐步回归分析得统计方程，其中只
有 Na + /K +对 Pn 的相关系数有显著意义，方程中只有 Na
+ /K +进入方程，其他 3 个离子都被剔除。盐胁迫下，吴屯
杨耐盐性强于小胡杨，统计方程说明盐胁迫下杨树嫩茎质外体离子变化和光合作用存在共线性关系，且Na + /K + 对
Pn 有显著的线性关系。
关键词: 盐胁迫; 杨树; 质外体; 离子; 光合作用
中图分类号: S718. 43 文献标识码: A 文章编号: 1001 － 7488(2013)07 － 0040 － 08
Effects of Apoplastic Ion Contents in the Tender Stems of Two Populus Cultivars
on Gas Exchange Parameters Under Salt Stress
Ma Jinlong1，3 Jiang Guobin2 Yao Shanjing1 Jin Hua2
(1. Department of Chemical and Biological Engineering，Zhejiang University Hangzhou 310027; 2. Environment and Resources College，
Dalian Nationalities University Dalian 116600; 3. Life Science College，Dalian Nationalities University Dalian 116600)
Abstract: In this paper we investigated effects of apoplastic ion dynamic changes in the tender stems of Populus
wutunenses and“P． simonii × P． euphratica”× P． sp． on gas exchange parameters under salt stress． The apoplastic ions
were monitored by microdialysis and atomic absorption，and the gas exchange parameters were determined with a portable
photosynthesis system． The net photosynthetic rates ( P n ) of the two poplar cultivars all decreased with increasing salt-
treated duration． The stomatal conductance (G n) and intercellular CO2 concentration (C i) of P． × wutunenses increased
and then decreased，whereas its stomatal limitation ( L s ) exhibited a contrary changing trend． The G n and C i of“P．
simonii × P． euphratica”× P． sp． gradually reduced，whereas its L s increased gradually． The results indicated that the
photosynthetic inhibition of P． × wutunenses under the stress of 100 mmol·L － 1 NaCl resulted from non-stomatal limitation
and stomatal limitation successively，whereas that of“P． simonii × P． euphratica”× P． sp． resulted from stomatal
limitation throughout the entire experiment． P n S of the two poplar cultivars were negatively correlated with Na
+
concentration and Na + /K + ratio significantly， however were positively correlated with K + concentration extremely
significantly． A multiple linear stepwise regression analysis was performed with P n as the dependent variable，and Na
+，
K +，Ca2 + concentrations and Na + /K + as the independent variables． P n was only significantly correlated with Na
+ /K +
aomg those independent variables． P． × wutunenses was more salt-tolerant than“P． simonii × P． euphratica”× P． sp．
第 7 期 马金龙等: 盐胁迫下杨树质外体离子对气体交换参数的影响
under salt stress． The statistical equation showed that apoplastic ion contents in the tender stems of poplar cultivars were
collinearly correlated with their photosynthesis performance under salt stress．
Key words: salt stress; Populus; apoplast; ion; photosynthesis
Approximately 1 /3 of earth lands are covered with
saline soils， which seriously affect agricultural
production and vegetation distribution (Munns et al．，
2008) ． There are nearly 2. 5 × 106 hm2 of various
saline soils in China，and the situation still deteriorates
every year ( Zheng et al．，2008 ) ． Therefore， it is
imperative to investigate the salt-tolerance mechanism
of plants． Apoplast of higher plants is a dynamic space
in which many important physiological and biochemical
processes and reactions such as solute transportation，
nutrient activation，adversity resistance and etc． occur
(Bartels et al．，2005; Saglam et al．，2010 ) ． The
dynamic changes of ions in apoplast not only directly
affect the salt tolerance of plants，but also are closely
associated with many physiological mechanisms such as
plant transpiration， signal transduction， ion
compartmentation in cells and etc． (Tuteia，2007) ．
Oertli ( 1968 ) hypothesized that salt stress
decelerated the ions in the apoplast of plant tissues
before entering symplast， which resulted in the
substantial accumulation of ions in apoplast that then
dehydrated cells， eliminated turgor and damaged
membrane structures，thereby inhibiting the growth and
development of plants． However， this hypothesis is
hardly proven． Sun (2000) reported that the apoplast
is an essential part of plants in which different organs，
tissues and cells interact and communicate that affect
the physiological functions of cells as soon as they
confront in vivo and in vitro biological or non-biological
environmental changes． The reduced photosynthesis
under salt stress commonly results from water potential
and decreased stomatal conductance induced by
osmotic stress，which thus prevents the movement of
CO2 ( Zhu et al．，1999 ) ． Meanwhile， the increased
Na + content in leaves lowers stomatal conductance and
prevents CO2 from being transported to the chloroplast，
and CO2 assimilation was blocked as a result (Wei et
al．，2004) ． The apoplast in tender stems，which are
similar to those in leaves，are close to the growing
point of plants． The roots，stems and leaves are closely
related，and ions absorbed by roots will be transported
to leaves through stems． The dynamic changes of
apoplastic ions in tender stems will also indirectly affect
photosynthesis． Therefore， clarifying the effects of
apoplastic ion changes on gas exchange parameters
under salt stress may reveal the relationship between
apoplastic changes and photosynthetic physiology． On
the other hand，photosynthesis provides fundamental
materials and energy for the growth and development of
plants ( Rhors-Richey et al．，2011 ) ． However， the
underlying reason accounting for the decrease of
photosynthetic capacity ( stomatal or non-stomatal
limitation) is still controversial (Xia et al．，2005) ．
Thus far，crops including barley，rice，cotton and
etc． have been mainly employed as the salt tolerance
models (Chaves et al．，2009)，whereas economic trees
have seldom been studied． Meanwhile，the functions of
symplast have been more frequently studied than those
of apoplast． Moreover，apoplastic ions in the roots and
leaves of plants have been most frequently accessed
(Cuin et al．， 2010; 2011; Zeng et al．， 2009 ) ．
However， the previous studies on apoplast in plants
suffer from several drawbacks ( Narendra， 2007 )，
which are in need of a rapid，convenient and accurate
method． The micro-dialysis sampling technique that
has been widely applied in different parts of animals
and human is feasible to remedy the deficiency．
Notably，micro-dialysis (MD) is a non-invasive，in
situ sampling，real-time and online dialysis technology
( Simon et al．， 2009 )， which functions in plant
detections in limited previous literatures ( Eklund，
1991; 1993; Eklund et al．，1991) ． In addition，our
group has demonstrated that microdialysis could
acquire pure apoplastic sap of plants rapidly and easily
(Wang et al．，2009) ．
In this paper，Populus × wutunenses is a novel
salt-resistant and drought-resistant tree species
distributed in Liaoning Province that was developed
and cultivated by our group，and “P． simonii × P．
euphratica”× P． sp． is a traditional salt-tolerant and
drought-tolerant tree species widely planted， which
were used to investigate the effects of apoplastic ions in
14
林 业 科 学 49 卷
the tender stems of Populus cultivars on gas exchange
parameters under the salt stress of 100 mmol·L － 1 NaCl
and to explore the mechanisms of apoplast in
photosynthetic physiology，which will be conductive to
improving the salt tolerance of plants． Micro-dialysis in
the physiological and biochemical examinations of plant
stress resistance to preliminarily study the changes of
apoplastic ions under salt stress， to reveal the
correlations between them by combining traditional
instruments，and to interpret the experimental results
by data processing and previous literatures，aiming to
allow timely， online and non-invasive measurements
practically．
1 Materials and methods
1. 1 Treatment of plant materials
Eighty cutting woods of P． × wutunenses and“P．
simonii × P． euphratica”× P． sp． collected from Yaopu
Township，Xinmin Country，Liaoning Province were
put into pots ( inner diameter: 20 cm; height: 16 cm;
each pot: 1 strain) in April． Forest humus soils were
used in the pots (Zeng et al．，2009) ．
After 40 days， three uniformly grown strains
(height: 12 ～ 15 cm; leaves: 12 ～ 16 pieces) of each
type were selected． The plants were irrigated every four
days with a 100 mmol NaCl solution depending on the
humid conditions of the soils． It is necessary to irrigate
more water than that held in soil in order to ensure a
constant NaCl concentration ( Brinker et al．，2010 ) ．
The plants were sampled by microdialysis and gas
exchange parameters were determined after 1，5，9，13
and 17 days of salt processing． Only the mature and
recent fully-unfolded leaves were used for tests． Every
test was repeated in triplicate．
1. 2 Determination methods
The color， salt spot and falling of leaves were
observed on the 1 st，5 th，9 th，13 th，17 th and 20 th day of
salt processing．
1. 3 Microdialysis sampling
A MD probe (340 μm OD; polyacrylonitrile with
a molecular weight cutoff of 30 000 Da; BASi，
Sweden) was connected to a pumping system and a
fraction collector (Model FC203b，Gilson，Middleton，
WI，USA) by an FEP tubing (CMA /MD，Stockholm，
Sweden) ． The perfusate was delivered at a flow rate of
1. 0 μL·min － 1 by a MD infusion pump ( CMA 102;
CMA /MD AB，Stockholm，Sweden ) equipped with
three 1 mL gastight syringes (Hamilton，Reno，NV，
USA) ． Considering that poplar tender stems are harder
than animal tissues，a guide wire forming an angle of
30° to 45° with the tender stem was first inserted into
the sampling part to prevent potential damages of the
probe ( Simon et al．，2009 ) ． To prevent the loss of
perfusion fluid，complete dry mono-methylmethacrylate
( MMA )， which was prepared by mixing auto-
coagulating powders and a denatured base resin fluid，
was used to seal the margin of the probe． Millipore-Q
hyper-pure water was used as the perfusion fluid ( flow
rate: 1 μL·min － 1 ) ． All the tests were performed at
ambient temperature． The system was allowed to
equilibrate for at least 20 min after eliminating the dead
volume in the tubing． Then the dialysis fluid was
collected in 1. 5 mL Eppendorf vials at appropriate time
intervals (Fig． 1) ． Three different probes were used to
ensure that the results were independent of the probe
type． In order to perform microdialysis and to interpret
the results correctly，it is also necessary to calibrate
the microdialysis probes prior to the experiments．
1. 4 Determination of the concentrations
and recoveries
The dialysis fluids were diluted by 10 times with
Millipore-Q ultrapure water to determine Na + and K +
concentrations by the atomic absorption spectrophotometer
(AAS) ( Jiang et al．，2010 ) ． The standard storage
solution ( 1 000 mg·L － 1 ) was provided by the
National Standard Material Research Center． AAS
analysis was performed using a Hitachi Z2000 ( Japan)
atomic absorption spectrophotometer system equipped
with Potassium， Sodium hollow cathode lamp． The
conditions of AAS are listed in Tab． 1．
In vitro relative recovery: The microdialysis probe
was inserted into Na + standard solution with known
concentration． 100 μL of dialysis fluid was collected
30 min after inserting the probe to determine Na +
concentration． The in vitro relative recovery of Na +，
which is the ratio of the measured concentration to the
standard concentration，was determined as 8% ．
24
第 7 期 马金龙等: 盐胁迫下杨树质外体离子对气体交换参数的影响
Fig． 1 Microdialysis system and tender stem of poplar with a probe
Tab． 1 Working conditions of AAS
Element
Wave length /
nm
Silt
width /
nm
Lamp
current /
mA
Time
constant /
s
PMT
voltage /
V
Na 589. 0 0. 4 10. 0 0. 1 376
K 766. 5 1. 3 10. 0 0. 1 294
Ca 422. 7 1. 3 5. 5 0. 1 396
C = C1 × 10 /0. 08
where C represents the concentration of a certain ion;
C1 represents the concentration determined by AAS; 10
is the dilution factor; 0. 08 is the in vitro relative
recovery．
1. 5 Determination of gas exchange parameters
The gas exchange parameters of recent fully
unfolded leaves (4 th － 5 th leaf from the top)，including
net photosynthetic rate ( P n )， stomatal conductance
(G n) and intercellular CO2 concentration (C i )，were
determined with a portable photosynthesis system (LI-
COR，6400 ) during 10: 00—11: 00 AM． Stomatal
limiting value (L s) can be expressed as (1 － C i / Ca)
(Ca: CO2 concentration in the sampling chamber) ．
The conditions of 6400 － 02B LED source were set at:
intensity: 800 μmol·m － 2 s － 1; temperature: 20 ℃ ;
flow rate: 350 μmol · s － 1; atmospheric CO2
concentration: 370 μmol·mol － 1 ．
1. 6 Data analysis
All the data of each cultivar were measured in
triplicate， and all the data were processed by
correlation analyses ( software: SPSS) and Duncan’s
new multiple range test． The effects of apoptotic ions
on P n were analyzed by the multiple linear regression，
and the variables were screened by the stepwise method
(α include = 0. 05，α exclude = 0. 10) ．
2 Results
2. 1 Growth status of the two populus cultivars
under salt stress
The two populus cultivars grew healthily holding
dark green leaves after being treated with salt stress for
1d． Salt spots began to appear on the leaves of“P．
simonii × P． euphratica”× P． sp． and P． × wutunenses
on the 5 th day and 13 th day of salt processing，which
were accompanied by falling leaves． Thereafter， the
salt spots already existed on the leaves enlarged，and
the leaves at higher positions were also subject to salt
spots． Meanwhile，the leaves began to fall off from the
bottom up． Accordingly，it has been initially verified
that“P． simonii × P． euphratica”× P． sp． suffered
from more severe salt damage than P． × wutunenses did
(Tab． 2) ．
2. 2 Effects of salt stress on the contents of
apoplastic ions
With increasing salt processing time， Na +
concentrations in the apoplasts of the tender stems of
the two populus cultivars gradually increased．
Apoplastic Na + concentration in P． × wutunenses
slightly decreased and differed apparently with that in
“P． simonii × P． euphratica”× P． sp． after 17 days of
salt processing ( Fig． 2 ) ． Moreover，apoplastic Ca2 +
content in P． × wutunenses continuously decreased
34
林 业 科 学 49 卷
until the 17 th day，whereas that in “P． simonii × P．
euphratica” × P． sp kept decreasing throughout the
whole experiment． Furthermore， Na + /K + ratio of
P． × wutunenses increased initially (5 th day: ＞ 1; 17 th
day: ～ 4) and slightly decreased on the 17 th day of
salt processing． In general，the contents of all the ions
in the two populus cultivars differed significantly，and
the ion contents in P． × wutunenses changed less than
those in“P． simonii × P． euphratica”× P． sp． ．
Fig． 2 Effects of salt stress on apoplastic ion contents in the tender stem of two Populus cultivars
Tab． 2 Effects of salt stress on the growth status of the two Populus cultivars
P． × wutunenses P． simonii × P． euphratica × P． sp．
1 th Dark green leaves，healthy growth Dark green leaves，healthy growth
5 th Dark green leaves，healthy growth Some leaves of low had brown salt spots and fallen
9 th Dark green leaves，healthy growth Brown salt spots enlarged many leaves of lower fallen
13 th Some leaves of lower had brown salt spots and fell Some leaves of middle and lower had brown salt spots and fallen
17 th Some leaves of lower had brown salt spots and fell
Leaves of middle and low almost fell some leaves of middle
and upper had brown salt spots
20 th Many leaves of lower had brown salt spots and fell Many leaves of middle and upper fell，shoot tip wilting
Fig． 3 Effects of salt stress on gas exchange parameters in the leaves of two Populus cultivars
2. 3 Effects of salt stress on the gas exchange
parameters of leaves
The photosynthetic rates of plants will decrease
under salt stress (Guo et al．，2001; Hui et al．，2004;
Zhou et al．，2005)，which is commonly attributed to
stomatal and non-stomatal limitations ( Zhu et al．，
1999) ． Fig． 3 shows that P n of the two Populus
cultivars decreased with elapsed salt processing time．
P n of P． × wutunenses and “P． simonii × P．
euphratica”× P． sp． began to sharply decrease after
17 and 9 days of salt processing． G n of P． × wutunenses
increased and then conversely reduced，and that of
44
第 7 期 马金龙等: 盐胁迫下杨树质外体离子对气体交换参数的影响
“P． simonii × P． euphratica”× P． sp． continuously
decreased． L s of P． × wutunenses decreased initially
and increased subsequently，and that of“P． simonii ×
P． euphratica” × P． sp． kept increasing． On the
contrary，C i of P． × wutunenses increased at first and
then decreased， and that of “P． simonii × P．
euphratica” × P． sp． gradually reduced． Generally
speaking， the drastically changed gas exchange
parameters of the two Populus cultivars all differed
significantly．
Tab． 3 Results of relativity analysis①
Na + K + Ca2 + Na + /K + Pn
Na + 1
K + － 0． 948(＊＊) 1
Ca2 + － 0． 789(＊＊) 0． 802(＊＊) 1
Na + /K + 0． 977(＊＊) － 0． 962(＊＊) － 0． 753(＊＊) 1
P n － 0． 865(＊＊) 0． 878(＊＊) 0． 689(＊＊) － 0． 929(＊＊) 1
①＊＊: Correlation is significant at the 0. 01 level (2-tailed) ．
2. 4 Relationship between apoplastic ions and Pn
The correlations between the concentrations of
Na +，K +，Ca2 +，Na + /K + and P n were analyzed by
SPSS． Table 3 exhibits that P n of P． × wutunenses is
negatively correlated with Na + concentration and
Na + /K + as well as is positively correlated with the
concentrations of K + and Ca2 +， and P n of
“P． simonii × P． euphratica”× P． sp． is negatively
correlated with Na + concentration and Na + /K +
extremely as well as is positively correlated with K +
concentration extremely． L s of P． × wutunenses is not
significantly with any ion concentrations，whereas L s of
“P． simonii × P． euphratica”× P． sp． is positively
correlated with Na + concentration and Na + /K +
extremely as well as is negatively correlated with K +
concentration extremely． Furthermore， a multiple
linear stepwise regression analysis was performed to
obtain the corresponding equation utilizing P n as the
dependent variable and Na +，K +，Ca2 + concentrations
and Na + /K + as the independent variables，
respectively．
The fitting equations can be expressed as follows:
P． × wutunenses: Y = 5. 306X + 4. 714 ( R2 =
0. 580) ．
Y-P n，X- K
+，F = 24. 866，P = 0. 000 ＜ 0. 005，
t = 0. 000 ＜ 0. 005 ( indicate K + and P n are correlated
significantly) ．
“P． simonii × P． euphratica”× P． sp: Y = －
1. 819X + 13. 495 (R2 = 0. 952) ．
Y-P n，X- Na
+ /K +，F = 170. 533，P = 0. 000 ＜
0. 005，t = 0. 000 ＜ 0. 005 ( Na + /K + is correlated
with P n significantly) ．
Only Na + /K + ratio is included in the equation，
and the concentrations of the three ions are excluded，
which may be attributed to they are collinearly
correlated．
3 Discussion
The apoplast of higher plants consists of the outer-
cell-membrane fibers and micro-crystal space that
compose the cell wall，the intercellular space full of
water and air，and the completely differentiated xylem
(Cuin et al．，2011) ． Although apoplast only accounts
for a small proportion of plant tissues (8% － 15% )，it
plays essential roles in plant physiology． Many
reactions take place in the apoplastic space under salt
stress ( Mengle et al．，1988; Speer et al．，1991 )
responding to the changes of symplast ( Ntsika et al．，
1986) ． Oertli (1968) found that the accumulation of
apoplastic Na + under salt stress destroys the balance
between intracellular and extracellular water potentials，
which leads to the dehydration of numerous protoplasts
and thus results in osmotic stress of cells． In this
study， apoplastic Na + concentrations in the tender
stems of the two Populus cultivars accumulated in
different ways． The apoplastic Na + concentration in
P． × wutunenses decreased by self-regulation，but that
in“P． simonii × P． euphratica”× P． sp． accumulated
continuously，leading to the osmotic stress of cells and
growth inhibition． Moreover，when the external salt
concentrations increased，K + flowed from the roots into
the ambient medium or got replaced by Na +，thereby
decelerating photosynthesis． The results are
inconsistent with those reported previously (Cramer et
al．，1985; Sulian et al．，2012 ) ． In this study，K +
concentration declined with increasing salt processing
54
林 业 科 学 49 卷
time，which may result from the increase of Na +
concentration． As a result，the growth of plants was
inhibited．
Photosynthesis，which is an essential metabolic
process in plants，remarkably affects plant growth and
stress resistance ( Hui et al．，2003 ) ． Photosynthetic
inhibition may originate from stomatal or non-stomatal
limitation． The relationship between P n，C i，G s and L s
determines whether a decrease of the photosynthetic
rate results from stomatal limitation． Only when C i，G s
and P n all decrease while Ls increases can it safely be
concluded that photosynthetic inhibition is mainly
induced by the decrease of stomatal conductance． In
contrast， if P n， G s and L s all decrease while C i
increases， photosynthetic inhibition is primarily
triggered by a reduced photosynthetic activity
(Farquhar et al．，1989) ． Therefore，the results in our
study show that the photosynthetic inhibition of P． ×
wutunenses is induced by stomatal limitation under a
long-term salt stress ( 100 mmol )， which can be
attributed to the stomatal contraction of leaves and the
decrease of stomatal conductance that limited the
transmission of CO2 into chloroplast and disrupted
photosynthesis． Besides，the non-stomatal limitation of
P． × wutunenses at the early stage probably results from
the lowered activity of RuBP carboxylase under a short-
term salt stress ( Chen et al．，2006 ) ． However，the
photosynthetic inhibition of “ P． simonii × P．
euphratica”× P． sp． primarily results from stomatal
limitation． Moreover，P n of the two populus cultivars
decreased through apparently different ways． In
summary， it has been demonstrated that the salt
tolerance of P． × wutunenses is stronger than that of
“P． simonii × P． euphratica”× P． sp． ．
It is well known that ion damage (damage induced
by excessive or insufficient ions) is one of the reasons
inhibiting photosynthesis． Ion redundancy and ion
insufficiency refer to excessive Na + and Cl － and
insufficient K + and Mg2 +，respectively ( Chen et al．，
2010) ． The above experimental results and statistical
analyses reveal that the variations of apoplastic ions in
the tender stems of Populus under salt stress might
influence the photosynthetic rate in leaves，which may
be ascribed to the accumulation of apoplastic Na + rather
than K + and Ca2 + ． As a result，the concentrations of
K + and Ca2 + lowered， and the photosynthesis of
populus was inhibited． A multiple linear stepwise
regression reveals that only K + concentration is included
in the equation for P． × wutunenses and only Na + /K +
ratio is included in the equation for“P． simonii × P．
euphratica”× P． sp． The results indicate that K + of P．
× wutunenses is linearly correlated with Pn significantly，
and Na + /K + of P． simonii × P． euphratica × P． sp． is
linearly correlated with Pn significantly． The final fitting
equation is expressed as:
Y = － 1. 819X + 13. 495 (R2 = 0. 952)
Y － Pn，X － Na
+ /K +，F = 170. 533，P = 0. 000 ＜
0. 005，t = 0. 000 ＜ 0. 005．
Only Na + /K + ratio is included in the equation，
and the concentrations of the three ions are excluded，
indicating that they are collinearly correlated with P n ．
4 Conclusions
Under salt stress，the apoplastic Na + concentration
in P． × wutunenses decreased by self-regulation，but
that in “P． simonii × P． euphratica” × P． sp．
accumulated continuously，leading to the osmotic stress
of cells and growth inhibition． K + concentrations in the
two Populus cultivars both decreases with increasing
salt processing time． The changes of the four
photosynthesis indexes of their leaves suggest that the
photosynthesis of P． × wutunenses decreased owing to
non-stomatal limitation ( initially ) and stomatal
limitation successively，whereas that of“P． simonii ×
P． euphratica” × P． sp． reduced due to stomatal
limitation throughout the whole experiment．
The concentrations of ions and the corresponding
photosynthesis indexes of the two Populus cultivars all
varied． The concentrations of almost all the ions
( except for Ca2 + concentration in the tender stem of
“P． simonii × P． euphratica” × P． sp． ) were
correlated with P n values significantly． A multiple
linear stepwise regression reveals that K + of P． ×
wutunenses is linearly correlated with P n significantly，
and Na + /K + of“P． simonii × P． euphratica”× P． sp．
is linearly correlated with P n significantly． Only Na
+ /
K + ratio is included in the equation， and the
concentrations of the three ions are excluded，
indicating that they are collinearly correlated with P n ．
64
第 7 期 马金龙等: 盐胁迫下杨树质外体离子对气体交换参数的影响
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