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Potassium nutrition recover impacts on stomatal, mesophyll
1
and biochemical limitations to photosynthesis in Carya
2
cathayensis and Hickory illinoensis
3
4
Chao Shen1, Ruimin Huang1, Yiquan Tang1, Zhengjia Wang1*
5
1 State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Lin'an, Hangzhou 311300, China
6
Abstract
7
Potassium (K) influences the photosynthesis process in a number of ways; However, the
8
mechanism of photosynthetic response to the long-term supply of potassium is not yet clear.
9
Concurrent measurements of gas exchange and chlorophyll fluorescence were made to investigate
10
the effect of potassium nutrition on photosynthetic efficiency and stomatal conductance (gs),
11
mesophyll conductance (gm) in Pecan (Carya illinoensis K.Kock) and Hickory (Carya
12
cathayensis Sarg.) seedlings in a greenhouse. The results show that the photosynthetic capacity of
13
Pecan and Hickory plants was not limited when the leaves had potassium concentrations >1.4%
14
and 1.42% of dry weight. Most of limitation under potassium deficiency were dominated by MCL
15
for Pecan and Hickory. Both cultivars showed remarkable improvement in SL, MCL, J and Vc,max
16
with additional K supplies. However, effect from potassium deficiency on photosynthesis in plant
17
leaves was irreversible. All of SL, MCL, and BL nearly half down with recovery K supply in both
18
species. These results emphasize the important role of potassium on regulation of photosynthesis
19
by three limitations.
20
Key words: Carya cathayensis Sarg., Hickory illinoensis K.Koch., potassium deficiency, recover,
21
photosynthetic limitations.
22
Introduction
23
Pecan (Hickory illinoensis K.Koch), one of the world's efficient economic trees, can provides
24
high quality dried fruit, good wood and other products. In China, pecan has been introduced for
25
more than 100 years (Shi et al. 2013), and pecan have been grown in all parts of Zhejiang
26
Province. Fruit trees are potassium sensitive crops, and their normal growth and development need
27
adequate potassium supply. Potassium deficiency largely restricts the improvement of fruit quality.
28
(Zhang 2016, Shen et al. 2017). However, the total potassium content of this region is low,
29
resulting in less efficient potassium that can be absorbed and utilized by plants (Cong et al. 2016).
30
Potassium content in plant leaves is closely related to photosynthesis (Wood et al. 2016), most
31
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studies have focused on crops (Pettigrew et al. 2010, Lu et al. 2016, Sousa et al. 2010, Li et al.
32
2014), while few studies have been done on fruit trees.
33
Potassium is one of the three microelement of plant nutrition. It is different from nitrogen and
34
phosphorus, that exists mainly in the form of soluble inorganic salt in the cell fluid (Blevins et al.
35
1985), or adsorbed on the surface of the plasma colloid in the form of ions, and has no structural
36
purpose (Tester et al. 2001). K+ is an activator of more than 60 enzymes in plants (Berg et al., 2010;
37
Hu et al., 2015; Wang and Wu, 2013), including enzymes that alter carbohydrate metabolism and
38
nitrogen metabolism, and promote protein and nucleic acid synthesis (Amtmann et al., 2008;
39
Maathuis 1997). Potassium (such as potassium nitrate, potassium chloride and potassium citrate)
40
is the main regulator of vacuole osmotic regulation in vacuoles (Hsiao and Läuchli 1986),
41
regulating cell water potential and turgor pressure, thus affecting plant stomatal opening and
42
closing movement(Jordan et al., 2008; Peiter 2011). Therefore, potassium deficiency affects
43
various plant metabolism and osmotic adjustment, resulting in decreased leaf area, plant thin,
44
yellow leaf wilting, ultimately inhibit the plant growth and yield formation. (Severtson et al.,
45
2016).
46
K+ as the main regulator of guard cell permeability, its richness affects stomatal function
47
(Shavala, 2003; Lebaudy et al. 2008; Andrés et al. 2008), thereby affecting the exchange process
48
of the blade and outside the water and gas. Therefore, stomatal limitation was thought to be the
49
primary cause of the decrease in leaf photosynthetic rate due to potassium deficiency (Bednarz et,
50
al. 1998).But the research in apricot showed that leaf photosynthetic rate decreased significantly
51
under potassium starvation (Basile et al. 2003; Oosterhuis et al. 2014; Quentin et al. 2013; Flexas et
52
al. 2015), but the stomatal conductance is not affected, and the biochemical disorders caused by
53
inadequate supply of potassium is the main reason that limit the photosynthetic rate (Basile et al.
54
2003; Flexas et al. 2012). Potassium deficiency decreased leaf chlorophyll content, decreased
55
Rubisco activity, accelerate the generation of reactive oxygen species (ROS), may also lead to the
56
accumulation of photosynthetic products and feedback inhibition of leaf net photosynthetic rate
57
(Paul et al. 2003; Cakmak 2005; Araya et al., 2006; Battie-Laclau et al. 2013; Vislap et al. 2012).In
58
recent decades, with the in-depth research on the mesophyll conductance (Bernacchi et al., 2010;
59
Flexas et al., 2007; Galmés et al., 2007; Xiong et al., 2016), people gradually realize that
60
potassium plays an important role in the regulation of mesophyll conductance under potassium
61
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deficiency leads to reduced mesophyll conductance on leaf photosynthetic rate limit as due to
62
stomatal function limited (Song et al., 2011; Battie-Laclau et al., 2014).Thus, the dominant
63
limiting factor of potassium deficiency on photosynthesis has a significant effect on the surface,
64
this effect is based on the three factors in proportion to the size of the plant, but is regulated by
65
internal features, including changes in the degree of stress and porosity, the resulting mesophyll
66
layer and the physiological and biochemical characteristics.
67
Recently, a quantitative limitation analysis for the RuBP-limited phase of photosynthesis was
68
proposed (Chen et al., 2013; Christian et al., 2014; Wang et al., 2015; Song et al., 2013; Wang et al.,
69
2012). In this way, the quantitative analysis of photosynthesis limitation was conducted by
70
combining stomatal conductance and mesophyll conductance (Song et al., 2011; Tosens et al.,
71
2012), the total photosynthesis limitation of leaves can be divided into three components:
72
AL=SL+ML+BL, SL, ML, BL, stomata, mesophyll, and biochemical limitation, respectively. To date,
73
most studies on quantitative analysis of photosynthetic restriction have focused on crops (Sagardoy
74
et al., 2010; Pettigrew et al., 2010; Lu et al., 2016; Sousa et al., 2010), and most of them compare
75
genetically modified species and genotypes with large variation in leaf structure. Nevertheless, the
76
information related to the influence of nutrient deficiency on quantitative limitation analysis for
77
photosynthesis is missing. Previous study showed a relationship between potassium and
78
photosynthesis in plant leaves of Pecan and Brassica napus, but do not involve the effect of
79
potassium deficiency time on photosynthesis of leaves. For this reasons, it is desirable to develop
80
a better understanding of the mechanisms which K supply affects photosynthesis of leaves.
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Materials and methods
82
Plants materials and growth conditions
83
Two-year-old pecan seedlings (Hickory illinoensis K.Koch) were transplanted into 30.5 cm
84
tall plastic pots with a top diameter of 25 cm, containing full-strength nutrient solution. The
85
composition of the standard nutrient solution was as follows: 2.5 mM Ca(NO3)2, 0.5 mM
86
Ca(H2PO4)2, 1.0 mMK2SO4, 0.5 mM MgSO4, 12.5 µM H3BO3, 1.0 µM MnSO4,1.0 µM ZnSO4,
87
0.25 µM CuSO4, 0.1 µM (NH4)6Mo7O24 and10 µM EDTA-Fe. The seedlings were grown in a
88
greenhouse with natural sunlight during the day. The mean daytime maximum and minimum
89
temperatures in the greenhouse were 28 and 20°C, with a constant relative humidity of 60%. After
90
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2 months, the composition of the nutrient solution was altered to one of three K concentrations:0,
91
2.0 and 5.0 mM K, respectively. In all cases, Ca(OH)2 and HCl were used to adjust the pH of the
92
nutrient solution to 5.7. The nutrient solution was changed every 7 days. All the treatments had 10
93
replicates with a completely random design.
94
Leaf gas exchange and fluorescence measurements
95
Measurements were made on the youngest fully expanded leaf from 6–8 randomly selected
96
seedlings on the 60th day of the treatment, using leaves developed after the initiation of the K
97
nutrition treatment. Leaf gas exchange and chlorophyll fluorescence were measured
98
simultaneously using a portable infrared gas analyser system (Li-6400, Li-Cor, Lincoln, NE, USA)
99
equipped with an integrated leaf chamber fluorometer (Li-6400-40) at a concentration of 380
100
µmol mol−1 CO2, 21% O2 and 50% relative humidity. Leaf chamber temperature was maintained
101
at 28 °C. All measurements were carried out at 1200 µmol m−2 s−1, with 90% red light and 10%
102
blue light, which we previously determined to be just above light saturation for pecan seedlings.
103
Once a steady state was reached (~20 min at a photosynthetic photon flux density (PPFD) of 1200
104
µmol m−2 s−1), a CO2 response curve (A–Ci curve) was performed. The ambient CO2 concentration
105
(Ca) was lowered stepwise from 380 to 50 µmol mol−1, and then returned to 380 µmol mol−1 to
106
re-establish the initial steady-state value of photosynthesis. Ca was then increased stepwise from
107
380 to1800 µmol mol−1. At each Ca, photosynthesis was allowed to stabilize for 3–4 min until gas
108
exchange was steady, so that each curve was completed in 35–50 min. Corrections for the leakage
109
of CO2 in and out of the Li-6400 leaf chamber, as described by Perez-Martin et al. (2009), were
110
applied to all gas-exchange data.
111
The actual photochemical efficiency of photosystem II (
Φ
PSII) was determined by measuring
112
steady-state fluorescence (Fs) and maximum fluorescence during a light-saturating pulse (Fm
′
)
113
following the procedure of Genty et al. (1989):
114
Φ
ୗ୍୍
୫
ᇱ
௦
/
୫
ᇱ
(1)
115
The rate of electron transport estimated from chlorophyll fluorescence is given by the equation
116
(Bilger and Björkman1994)
117
Φ
ୗ୍୍
PPFD α β
(2)
118
where PPFD is the photosynthetic photon flux density,
α
is leaf absorptance and
β
is the
119
proportion of quanta absorbed by photosystem II.
α
⋅
β
was determined for each treatment from the
120
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slope of the relationship between
Φ
PSII and
Φ
CO2 (i.e., the quantum efficiency of gross CO2
121
fixation), which was obtained by varying light intensity under non-photo respiratory conditions in
122
an atmosphere containing <1% O2 (Valentini et al.1995).
123
Measurement of mitochondrial respiration rate in the light (Rd) and intercellular CO2
124
compensation point (Ci*)
125
Rd and Ci* were determined according to the method of Laisk (1977). A–Ci curves were
126
measured using an open gas-exchange system (Li-6400, Li-Cor Inc.) equipped with an integrated
127
light source (Li-6400-02) at three different photosynthetically active PPFDs (50, 200 and 500
128
mmol m−2 s−1) at six different CO2 levels ranging from 300 to 50 mmol CO2 mol−1 air. The curves
129
intersected at the point where A is the same at different PPFDs; therefore, A at that point represents
130
Rd, and Ci represents Ci*.
131
Estimation of gm
132
From combined gas-exchange and chlorophyll fluorescence measurements, the mesophyll
133
conductance for CO2 (gm) was estimated according to Harley et al. (1992) as
134
A/
Γ
כ
8
ௗ
/ 4
ௗ
(3)
135
where A, Ci, Rd and J were determined as previously described for each treatment.
Γ
* is the
136
chloroplastic CO2 photocompensation point calculated from the Ci* and Rd measurements
137
according to the method of Warren et al. (2007) using a simultaneous equation with gm:
138
כ
כ
ௗ
/
(4)
139
Equation (4) was then substituted into (3) and the value of gm was found; then
Γ
* was calculated.
140
The value of
Γ
* was found to be slightly higher for the K0-treated plants (53.9 ± 9.6 µmol mol−1),
141
compared with the four other treatments (47.3 ± 7.5, 44.9 ± 7.8, 44.7 ± 5.1 and 44.6 ± 8.6 µmol
142
mol−1 for K1, K2, K3 and K4 treatments, respectively). Changes in
Γ
* derived using the method
143
of Laisk (1977) have been frequently observed under stress conditions such as drought (Galmés et
144
al. 2007); therefore, we re-calculated gm using the non-stressed
Γ
* values (44.6 µmol mol−1),
145
which is a reasonable assumption as
Γ
* is an intrinsic property of Rubisco and thus varies only by
146
a small amount within a species under different growing conditions. The CO2 concentration in the
147
chloroplast stroma (Cc) was calculated using the equation
148
A/
(5)
149
Quantitative limitation analyses
150
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The limitations (stomatal limitation, SL; the mesophyll conductance limitation, MCL; and the
151
biochemical limitation, BL) imposed by K deficiency on A were investigated following Grassi and
152
Magnani (2010). Because the fluorescence derived linear electron transport rate (J) is tightly
153
coupled with the maximum rate of Rubisco-catalysed carboxylation (Vc,max) (Galmés et al. 2007;
154
Gallé et al. 2009), a minor modification was adopted when calculating BL using J instead of Vc,max
155
(Gallé et al. 2009). Relative changes in light-saturated assimilation are expressed in terms of
156
relative changes in stomatal, mesophyll conductance and biochemical capacity as showed in Eqn
157
6:
158
dA/A
௦
d
௦
/
௦
d
/
d/
(6)
159
where ls, lmc and lb are the corresponding relative limitations calculated as Eqns 7–9 and gsc is
160
stomatal conductance to CO2 (gs/1.6).
161
௦
௧௧
/
௦
∂A/∂Cc/
௧௧
∂A/∂Cc
) (7)
162
௧௧
/
∂A/∂Cc/
௧௧
∂A/∂Cc
) (8)
163
௧௧
/
௧௧
∂A/∂Cc
) (9)
164
Where the gtot is the total conductance to CO2 from the leaf surface to carboxylation sites
165
determined in Eqn 10.
∂
A/
∂
Cc was calculated as the slope of A/Cc response curves over a Cc range
166
of 50–100
μ
mol mol1 (Tomás et al. 2012).
167
௧௧
1/1/
௦
1/
(10)
168
Then, the relative change of A, gsc, gm and J in Eqn 6 can be approximated by the following (Chen
169
et al. 2013):
170
dA # A
௫
A/A
௫
(11)
171
d
௦
/
௦
#
௦
௦
/
௦
(12)
172
d
/
#
/
(13)
173
d/ #
௫
/
௫
(14)
174
where
A
௫
,
௦
,
and
௫
are the reference values. Reference maximum values of net
175
CO2 assimilation rate, stomatal and mesophyll conductance and the rate of electron transport were
176
obtained in +K treatments; therefore, its parameters were defined as standard.
177
Statistical analysis
178
Descriptive statistical analyses were used for the obtained parameters to assess the range of
179
variability and standard error (SE). All data were subjected to a two-way analysis of variance
180
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(ANOVA) with SPSS 18.0 software (SPSS, Chicago, IL, USA). The difference between mean
181
values was compared using Duncan’s multiple range test at P < 0.05. Graphics and regression
182
analysis were performed using the GraphPad Prism 7.0 software (GraphPad, San Diego, CA).
183
Results
184
The leaf potassium (K) concentration (%), net CO2 assimilation rate (AN) and chloroplastic
185
CO2 concentrations (CC) of daily potassium supplied plants (control) remained mostly unchanged
186
throughout the experiment (Fig. 1a,b,d,e), but, slightly different between species, Pecan had a little
187
larger K and CC but lower AN compared with Hickory. After withholding potassium from plants,
188
K and AN decreased progressively in two treatment (K0 and K2), reaching minimum values of 0.5%
189
and < 5
μ
mol CO2 m-2 s-1, respectively, while CC increased in both two cultivars, with similar
190
trends during severe potassium stress (Fig. 3). Compare with K0 treatment, K, AN and CC of K2
191
recovered more quickly and closer to K5 (control, daily potassium supplied) throughout the
192
recovery period of potassium supply. K, AN of K2 rose 41.24% and 26.98% after restoring
193
potassium supply 7 days after in Pecan, which were significantly larger than those (18.92% and
194
16.16%) in Hickory.
195
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196
Fig.1. Leaf potassium percentage (%) of dry weight (K), net CO2 assimilation rate (AN),
197
chloroplastic CO2 concentrations (CC) of Pecan and Hickory as affected by different K levels
198
during seedling stage. The vertical dashed lines indicate the beginning of the beginning of
199
recovering potassium supply. Data points represent means and standard errors of at least four
200
replicates.
The width of green, purple and red ribbons is the standard deviation.
201
202
After withholding potassium from plants, Mesophy
conductance for CO2 (gm), stomatal
203
conductance for CO2 (gs), electron transport rate (J) and maximum velocity of carboxylation
204
(Vc,max) decreased progressively in all treatments of Pecan and Hickory, reaching minimum values
205
of 0.0265 mol CO2·m-2·s-1, 0.0457 mol·m-2·s-1, 99.94
μ
mol e-1·m-2·s-1 and 47.5904
μ
mol CO2·m-2·s-1
206
after severe potassium stress for 80d, respectively. After recovering potassium supply, the large
207
restoration of gm, gs, J and Vc,max were observed in the K0 and K2 treatments in two cultivations.
208
The gm of K0 and K2 recovered 55.16% and 71.54% to control values (0.09684 mol CO2·m-2·s-1)
209
of Pecan (Fig. 2a), respectively; gm of K0 and K2 recovered 55.65% and 81.93% to control values
210
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(0.09938 mol CO2·m-2·s-1) of Hickory (Fig. 2b), respectively; gs recovered 76.80% and 90.64% to
211
control values (0.1082 mol·m-2·s-1) of Hickory (Fig. 2f) respectively, which were nearly 10
212
percentage points more than of Pecan. The restoration of J and Vc,max under both K0 and K2
213
treatments were reached to control values after recovering potassium supply for 40d (Fig. 2c, d, g
214
h), respectively. However, slightly different levels of recovery time of gm gs and Vc,max were
215
observed in K2 treatments, with the three photosynthetic parameters show faster recovery speed
216
after recovering potassium supply. Under K5 treatment, gm, gs, J and Vc,max of Pecan and Hickory
217
almost unaltered throughout the experiment, while those photosynthetic parameters of Hickory
218
were slightly larger than Pecan.
219
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g
m
(
m
o
l
C
O
2
·
m
-
2
·
s
-
1
)
G
S
(
m
o
l
·
m
-
2
·
s
-
1
)
J
(
μ
m
o
l
·
e
-
1
·
m
-
2
·
s
-
1
)
0 20406080100120
20
40
60
80
100
0 20406080100120
220
Fig.2. Mesophy
conductance for CO2 (gm), stomatal conductance for CO2 (gs), electron transport
221
rate (J) and maximum velocity of carboxylation (Vc,max) of Pecan and Hickory as affected by
222
different K levels during seedling stage. The vertical dashed lines indicate the beginning of the
223
beginning of recovering potassium supply. Data points represent means and standard errors of at
224
least four replicates. The width of green, purple and red ribbons is the standard deviation.
225
226
227
228
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When plotting all K content (consisting all of K5, K2 and K0 under potassium stress and
229
recover, respectively) against the corresponding calculated AN, J, gs and gm, highly significant
230
positive correlation relationships were obtained pooling potassium supply and potassium stress
231
data together, although two different functions were derived for the Pecan and Hickory (Fig. 3a-d).
232
In these four figures, slightly steep slope was determined for the Pecan data set, however, less
233
clear difference was observed between two cultivars. Moreover, K content on AN, J, gs and gm
234
values resulted in almost similar slopes of linear regression for both two cultivars, respectively.
235
236
Fig.3. The relationships between leaf potassium percentage(%) of dry weight (K) and net CO2
237
assimilation rate (AN), electron transport rates (J), stomatal conductance for CO2 (gs) and
238
mesophy
conductance for CO2 (gm) derived from data of the whole experimental periods. Circles
239
and diamonds denote Pecan and Hickory data, respectively. Data points represent means and
240
standard errors of at least four replicates.
241
242
The AN correlated negatively with chloroplastic CO2 concentrations (CC), while, AN in
243
Hickory was slightly higher Pecan. When plotting all AN (consisting all of K5, K2 and K0 under
244
potassium stress and recover potassium, respectively against the corresponding calculated J and
245
gm, highly significant positive correlation relationships were obtained pooling potassium supply
246
and potassium stress data together, although two different functions were derived for the Pecan
247
and Hickory (Fig. 4b,c).In addition, AN on J and gm values resulted in almost similar slopes of
248
linear regression for both two cultivars, respectively.
249
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140 150 160 1 70 180 190
2
4
6
8
10
C
C
(μmol CO
2
·mol
-1
)
80 1 00 120 140 160 180 200
J
(μmol ·e
-1
·m
-2
·s
-1
)
250
Fig.4. The relationships between leaf potassium percentage (%) of dry weight (K) and net CO2
251
assimilation rate (AN), electron transport rates (J), stomatal conductance for CO2 (gs) and
252
mesophy
conductance for CO2 (gm) derived from data of the whole experimental periods. Circles
253
and diamonds denote Pecan and Hickory data, respectively. Data points represent means and
254
standard errors of at least four replicates.
255
When analyzing the effects of potassium on photosynthesis different indicators of stress
256
intensity can be used. In order to enhance the comparability of our data with other experiment, we,
257
therefore expressed relative limitations in terms of both of both K (% of dry weight) (Fig. 5)and
258
day of experiment (Fig. 6).what the stress index adopted, small differences between Pecan and
259
Hickory. With increasing potassium stress intensity MCL, BL and SL increased significantly, and,
260
the increase rate of MCL is greater than that of BL and SL. At mild-to-moderate potassium stress
261
levels (corresponding to values of K >0.9% of dry weight), about half of the decline in AN was
262
attributable to mesophy
resistance.
263
264
Fig.5. The relationships between photosynthetic limitations and leaf potassium percentage (%) of
265
dry weight (K) of Pecan (a) and Hickory (b).SL MCL BL denote stomatal, mesophy
conductance
266
and biochemical limitation respectively. Each point in the same shape represents a calculation (42
267
values were calculated for each limitation)
268
269
Quantitative limitation analysis of photosynthesis underlined the above-described changes
270
during potassium stress and recovery after subsequent recover potassium. In all three experiments,
271
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MCL play a major role of the total limitation under severe potassium stress. In K0 and K2
272
treatments, MCL made up >40% and >50% of the total limitation under severe potassium stress in
273
Pecan and Hickory, while SL accounted for only up to 20%. Furthermore, BL did not exceed 10%
274
of the total limitation. As already observed for the AN, gs, and gm data during stress and recovery,
275
almost no limitation of SL and BL during potassium stress and after recover potassium (Fig. 6c,f).
276
Limitation of photosynthetic recovery of the K0 and K2 plants was mainly driven by a still high
277
MCL and somewhat lower SL and BL (Fig. 5a, b, d, e).The delayed recovery of photosynthesis in
278
the K0 plants was mainly due to a maintained high proportion of MCL and SL (Fig. 5d) during
279
several days of recover potassium (Fig. 6a, d), while SL contributed only partially to the total
280
limitation in the initial phase of re-watering. The recovery of photosynthesis in the K2 plants is
281
due to a rapidly decreasing MCL during the recover potassium period, while SL is nearly equaled
282
MCL in the later phase of recover potassium (Fig. 6b, e).
283
0
1
2
2
1
2
8 4
3 5
0 60
69
80
8
7
9
8
1
0
8 1
16
1
20
0
1
2 2
1 28
43
50
6
0
6
9
8
0
8
7 9
8 10
8
1
1
6
1
2
0
0 12
21
2
8
4
3
5
0
6
0
6
9
8
0
87
98
1
0
8
1
1
6 1
2
0
284
Fig.6. Quantitative limitation analysis of photosynthetic CO2 assimilation during potassium stress
285
and subsequently recovering. The shaded areas represent the percentage of stomatal (SL),
286
mesophyll (ML), and biochemical (BL) limitation based on control values of AN, gs, gm, and Vc,max
287
and J. Calculations were done with mean values of at least five measurements per treatment and
288
day. The vertical dashed lines indicate the beginning of the beginning of recovering potassium
289
supply. Data points represent means and standard errors of at least four replicates.
290
Discussion
291
In the present study, the same experimental design was applied to Brassica napus under four
292
different potassium treatments, followed by a potassium stress period and a recover after recover
293
potassium. The most important difference between the four potassium treatments was observed:
294
the rate of photosynthetic recovery was the slowest under K0 treatment and the quickest under K2
295
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treatment of Pecan. Then, extremely low photosynthetic limitation in plant leaves of Pecan and
296
Hickory under K5 treatment. A positive relationship between K supply and AN had reported in
297
numerous previous studies. However, photosynthesis rates may not have changed as a response to
298
K treatment due to relatively higher leaf K concentration, which were far more than the values
299
(1.04% and 1.28 % of dry weight) proposed by Gierth (2007)and Zhifeng Lu (2016) respectively,
300
as are the values ( 1.4 % and 1.42%) in this study.
301
Withholding potassium resulted in a closure of stomata, which was accompanied by a marked
302
decrease of net photosynthesis (AN) in K0 and K2 treatment of Pecan and Hickory (Fig. 2).
303
Throughout periods of potassium stress imposition, stomatal conductance (gs) and AN followed
304
the same course, indicating a strong correlation between them, which has been shown elsewhere
305
(Medrano et al., 2002). Moreover, plants under K5 treatment displayed a inequable course for
306
stomatal conductance (gs) of Pecan and Hickory. In addition, mesophyll conductance (gm) showed
307
a similar trend with stomatal conductance (gs) under all three potassium supply in Pecan and
308
Hickory. These results are in line with previous studies, where a decrease of gm has been observed
309
during potassium stress (Song et al., 2011; Lu et al., 2016; Wang et al., 2012; Battie-Laclau et al.,
310
2014). The rapid restoration of J and Vcmax to control values during prolonged recover potassium,
311
while the restoration of gs and gm is could not reach the level of the control value, especially under
312
K0 stress of Pecan and Hickory. These results are indicating restored J and Vcmax during prolonged
313
recover potassium presumably facilitated photosynthetic recovery after the beginning of
314
re-watering, because AN and J , Vcmax were immediately restored to control values within the initial
315
phase.
316
Lots of previous studies have shown total photosynthetic dramatically decreased with
317
decreasing K supply. (Bednarz et al.1998; Jin et al. 2011; Wang et al. 2012; Battie-laclau et
318
al.2014; erel et al. 2015). And the results of quantitative analysis revealed that the three
319
components contributing to total photosynthetic limitation, namely, SL, MCL, and BL varied at
320
varying K concentrations. The decline of Pn with the decrease of potassium concentration in
321
leaves, while all of SL, BL and MCL were decreased, BL was markedly lower and MCL was higher,
322
especially at lower treatment in both cultivars (Fig. 6). This can be attributed to prioritization of
323
allocation of excess K to the cytosol for metabolic activity rather than to reduce the transmission
324
resistance of CO2 in the chloroplast. (Reich et al., 1997; Pettigrew 1999; Zhao et al., 2001;
325
Battie-Laclau et al., 2013; Tomás et al., 2016). Then our quantitative limitation analysis showed
326
that SL was always higher than BL under three treatments in both species. This pattern of response
327
is consistent with that decried by other authors (Tanaka et al., 2005; Christian et al., 2014; Peiter et
328
al., 2011). Although several studies have reported that stomatal closure (SL) plays by far the main
329
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role in the decline of photosynthesis, even at rather severe levels of potassium stress (Bednarz
330
1998; shavala ,2003; Lebaudy ,208; Andrés, 2014), but our study draw different conclusions that
331
MCL is the dominant factor in the AN reduction rather than the SL in both species. This striking
332
discrepancy is explained by the fact that potassium stress increases the transmission distance of
333
CO2 in the chloroplast (Zhao et al., 2001; Battie-Laclau et al., 2014 ).
334
An even clear picture of the potassium effects emerges when the different limitations are
335
plotted against potassium stress and subsequent recovering (Fig. 6). In both species, all the
336
limitations increased with increasing potassium stress and duration of treatment, but their relative
337
contribution changed. Moreover, in the early stage of potassium treatment (0-21d), all the three
338
limitations under k0 and K2 rapidly risen. In the middle and late period (21-80d), all the
339
limitations maintained their high level and changed little under K0 treatment, this could be the
340
acclimation of plants to severe potassium deficiency, a similar situation had been appeared in the
341
plant drought test (Galle et al., 2009). After recover potassium, obvious decline could be observed
342
of all the three limitations under K0 and K2 treatment in both species. However, SL and MCL were
343
not hopely recovered to the control level (K5), they remain at a high level until the end of the
344
experiment. The most likely explanation for this discrepancy might be derived from the effect of
345
potassium stress on the irreversible structural effects of plant leaves. In this sense, potassium
346
deficiency induced the increase of with leaf dry mass per area (MA)(Reich et al., 1997; Pettigrew,
347
1999; Zhao et al., 2001; Song et al., 2011), reducing the leaves thickness and the volume of cell
348
gap in the leaves, thus reducing the gas conduction ability of CO2 (Battie-Laclau et al., 2014).
349
In conclusion, AN of Pecan and Craya plants declined by increasing SL, MCL, and BL under
350
prolonged severe potassium stress. Pecan, needed K (1.4% of dry weight less than that of Hickory)
351
to avoid the decline of AN. All of SL, MCL, and BL had a sharp decline under K0 and K5treatment
352
in both species. In summary, the present study strongly reinforces the important role of gs, gm, J
353
and Vc,max during recovery from potassium stress induced inhibition of photosynthesis, and shows
354
for the first time that such a role depends on the Long-term processing.
355
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539
540
.CC-BY-NC-ND 4.0 International licenseIt is made available under a
(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
The copyright holder for this preprint. http://dx.doi.org/10.1101/425629doi: bioRxiv preprint first posted online Sep. 24, 2018;
.CC-BY-NC-ND 4.0 International licenseIt is made available under a
(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
The copyright holder for this preprint. http://dx.doi.org/10.1101/425629doi: bioRxiv preprint first posted online Sep. 24, 2018;
.CC-BY-NC-ND 4.0 International licenseIt is made available under a
(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
The copyright holder for this preprint. http://dx.doi.org/10.1101/425629doi: bioRxiv preprint first posted online Sep. 24, 2018;
.CC-BY-NC-ND 4.0 International licenseIt is made available under a
(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
The copyright holder for this preprint. http://dx.doi.org/10.1101/425629doi: bioRxiv preprint first posted online Sep. 24, 2018;
.CC-BY-NC-ND 4.0 International licenseIt is made available under a
(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
The copyright holder for this preprint. http://dx.doi.org/10.1101/425629doi: bioRxiv preprint first posted online Sep. 24, 2018;
.CC-BY-NC-ND 4.0 International licenseIt is made available under a
(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
The copyright holder for this preprint. http://dx.doi.org/10.1101/425629doi: bioRxiv preprint first posted online Sep. 24, 2018;
.CC-BY-NC-ND 4.0 International licenseIt is made available under a
(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
The copyright holder for this preprint. http://dx.doi.org/10.1101/425629doi: bioRxiv preprint first posted online Sep. 24, 2018;
