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by
Ismail CAKMAK
Sabanci University Istanbul, Turkiye
ROLE OF MINERAL NUTRITION IN ALLEVIATING DETRIMENTAL
EFFECTS OF ENVIRONMENTAL STRESSES ON CROP PRODUCTION
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HUGE INCREASES IN HUGE INCREASES IN
WORLD POPULATIONWORLD POPULATION
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FOOD SECURITYThe world population is expanding rapidly and will likely be 10 billion by the year 2050. Limited availability of additional arable land and water resources, and the declining trend in crop yields globally make food security a major challenge in the 21st century.
According to the projections, food production on presently used land must be doubled in the next two decades to meet food demand of the growing world population.
The projected increase in food production must be accomplished on the existing cultivated areas because the expansion of new land is limited.
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WORLD HUNGER
http://www.feedingminds.org/level1/lesson1/worldhungermap.htm
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Source: FAO, 1998
SOIL DEGRADATION INCREASES GLOBALLY
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ABIOTIC
STRESS
NUTRIENT DEFICIENY
CHILLING
HEAT
HIGH
LIGHT/UV FLOODING
OZONE
SALINITY
DROUGHT
NUTRIENT DEFICIENY
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CORN SOYBEAN WHEAT
Record Yield: (tons ha-1)
19.3 14.5 7.4
Losses by abiotic stress Present average yield Losses by biotic stress
10% 24%
66% 82%
13%5%
69%
22%9%
Decreases in Record Yield Capacity of Crop Plants by Abiotic and Biotic Stress Factors
Source: Bray et al., 2000, In Molecular Biology
and Biochemistry of Plants, ASPP
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Photooxidative
stress
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Photooxidative Damage a key process involved in cell damage and cell death in plants exposed to environmental stress factors
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Mineral nutritional status of plants greatly influences occurrence of photooxidative damage in plants by causing impairments in photosynthetic electron transport and CO2 fixation in various ways.
Photooxidative damage in nutrient
deficient plants can be more serious
when plants are simultaneously
exposed to an environmental stress.
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MEMBRANE DNA PROTEIN
FREE RADICAL DAMAGE TO CRITICAL CELL CONSTITUENTS
O2 h.v. e-
LIPID PEROXIDATION
PROTEIN DAMAGE
MUTATION
CHLOROPHYLL
CHLOROSIS
1O2 O2
._
H2O2 OH.
CELL DEATH
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Of the mineral nutrients
nitrogen plays a major role in utilization of absorbed light energy and photosynthetic carbon metabolism.
In N-deficient leaves an excess of non-utilized light energy can be expected leading to high risk for occurrence of photooxidative damage.
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Growth conditions
Chl Photosynthetic rate
Electron transport rate
(mmol m-2
) (µmol m-2
s-1
) (µmol m-2
s-1
)
DDeeffiicciieenntt NN 0.47 13 124
Adequate N 0.90 29 254
Photosynthetic characteristics in C. album leaves grown at high light
Kato et al., 2003, Plant Cell Physiol. 44:318-325
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To avoid occurrence of photooxidative damage in response to excess light energy, thylakoid membranes has a protective mechanism by which excess energy is dissipated as heat. Dissipation of excess light energy is associated with enhanced formation of xanthophyll pigment zeaxanthin.
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Violaxanthin
low
Antheraxanthin
light
Zeaxanthin Violaxanthin
high light
light
Antheraxanthin
high
light
low
Zeaxanthin
Zeaxanthin is synthesized from violaxanthin in the light-dependent xanthophyll cycle to avoid excess energy
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0
60
180
240
120
300
Leaf N (g m-2)
Z o
r V
(m
mo
l m
ol C
hl-
1)
Xanthophyll Cycle Composition in Relation to Leaf N of Fuji/M.26
Trees at Noon Under an Incident PFD of 1500 µmol m-2 s-1
1 2 3 4 5
Violaxanthin (V)
Zeaxanthin (Z)
Verhoeben et al., Plant Physiol.
1997, 113: 817-824
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High N Low N
Use of Absorbed Light Energy for Photochemistry
64% 36%
37% 63%
Verhoeben et al., Plant Physiol. 1997, 113: 817-824
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High N Low N
Conversion State of Xantophyll Cycle Pigments at Growth Irradiance in Spinach Leaves
V
Z A
A Z
V
82%
26 %
Verhoeben et al., Plant Physiol.
1997, 113: 817-824
Violaxanthin (V) Antheraxanthin (A) Zeaxanthin (Z)
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In plants suffering from N deficiency the conversion state of the xanthophyll cycle pigments zeaxanthin was enhanced together with chlorophyll bleaching particularly under high light intensity.
These results indicate impaired use of absorbed light energy in photosynthetic CO2 fixation and thus enhanced demand for protection against excess light energy in N-deficient plants.
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Nitrogen is involved in protection of plants from chilling stress
In studies with Eucalyptus seedlings it has been shown that seedlings with impaired N nutritional status were less susceptible to photooxidative damage in winter months.
Experiments were carried out to study the effect of low temperature stress on lipid peroxidation, antioxidants and defense enzymes in lemon that is very sensitive to low temperature.
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0
10
20
30
40
50
60
70L
ipid
Pero
xid
ati
on
(nm
ol M
DA
g-1
DW
)
low N medium N sufficient N
24 oC - 3.5 oC
Effect of Increasing Nitrogen Supply on Lipid Peroxidation at Normal and Low Temperature in Lemon
S. Eker, unpublished results Nitrogen Supply
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0
10
20
30
40
50
60
Pro
lin
(m
g g
-1 D
W)
low N medium N sufficient N
24 oC - 3.5 oC
Effect of Increasing Nitrogen Supply on Prolin Concentration at Normal and Low Temperature in Lemon
S. Eker, unpublished Results Nitrogen Supply
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0
500
1000
1500
2000
Su
pero
xid
e d
ism
uta
se
(Un
its g
-1 D
W)
low N medium N sufficient N
24 oC - 3.5 oC
Effect of Increasing Nitrogen Supply on Superoxide Dismutase at Normal and Low Temperature in Lemon
S. Eker, unpublished Results Nitrogen Supply
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Yield of transgenic alfalfa in 3 years of field trials. Cuttings were
planted in 1x3 m plots in replicated trials in spring 1992.
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0
20
40
60
80A
sco
rbate
pero
xid
ase
(µm
ol
g-1
DW
min
)
low N medium N sufficient N
24 oC -3.5 oC
S. Eker, unpublished Results
Effect of Increasing Nitrogen Supply on Ascorbate Peroxidase at Normal and Low Temperature in Lemon
Nitrogen Supply
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0
1
2
3
4
Glu
tath
ion
e r
ed
ucta
se
(µm
ol g
-1 D
W m
in)
low N medium N sufficient N
24 oC -3.5 oC
Effect of Increasing Nitrogen Supply on Glutathione Reductase at Normal and Low Temperature in Lemon
S. Eker, unpublished Results Nitrogen Supply
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0
1
2
3
4
5
6
Cata
lase
(µm
ol g
-1 D
W m
in)
low N medium N sufficient N
24 oC - 3.5 oC
S. Eker, unpublished Results
Effect of Increasing Nitrogen Supply on Catalase at Normal and Low Temperature in Lemon
Nitrogen Supply
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Catalase enzyme is highly sensitive to low
temperature. Improved N nutrition protects catalase from inhibition/inactivation by low temperature stress.
The activity of most antioxidant enzymes is
increased by low N supply, especially at low temperature. This lead to suggestion that N deficiency promotes increased production of reactive oxygen species.
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K
Water Regime
Protein Synthesis
Meristematic Growth
Phloem Export of Photosynthates
Photosynthesis
Enzyme Activation
Alleviation of Effects of Stress Factors
POTASSIUM IN CROP PRODUCTION
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K Deficiency-
Enhanced Sensitivity to
Fe toxicity
Diseases Low
Temperature
High Light
Salinity
Drought
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0
10
20
30
13 19 26
Effect of Varied K Supply on Photosynthesis in Cotton
Ph
oto
syn
the
sis
Ra
te
(µm
ol m
-2 s
-1)
K deficiency
Days
adequate K
Bednarz and Oosterhuis, 1999 ; J. Plant Nutr.
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0.0
1.0
2.0
3.0
normal CO2
high CO2
Assim
ilatio
n R
ate
[µm
ol C
O2 m
-2 s
-1]
Effect of Elevated CO2 on Photosynthesis
at Varied K Supply
Adequate K
Low K
+ K
- K - K
+ K
Barnes et al., 1995, Plant Cell Environ.
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PSII PSI
2H2
O
O2
LIGHT
THYLAKOID
CO2
O2
e-
STROMA
Sucrose
Phloem Export
O2-, H2O2, OH-
Reactive O2 Species
K Deficiency
CELL DAMAGE
Photosynthetic Electron Transport andSuperoxide Radical Generation
StomatalCO2 Flux
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Growth of bean plants with low K supply
under low and high light intensity
Low light
High light
Marschner and Cakmak, 1989, J. Plant Physiol.
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Enhancement of leaf chlorosis by high light
intensity is not related to differential K
concentration in leaves
Leaf K
concentration
0.15%
Leaf K
concentration
0.17%
Low light High light
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Enhancement of leaf
chlorosis in Mg-deficient
leaves by high light
intensity is not related to
Mg concentration in
leaves Partially shaded
bean leaf at low Mg
521 ppm
447 ppm
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Photooxidative damage to chloroplasts is a major contributing factor in development of K deficiency symptoms on leaves
Plants grown under high light intensity require more K than plants grown under low light
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Partially shaded K-deficient bean leaves
Enhancement of photooxidative damage in K-deficient leaves
SHADED
NON-SHADED
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CARBOHYDRATE ACCUMULATION AND CHLOROSIS
IN NUTRIENT-DEFICIENT LEAVES
Inhibitions in photosynthetic CO2 reduction and phloem
loading of sucrose play an important role in O2 activation and
occurrence of photooxidative damage, especially in Mg or K
deficient leaves
Control Low K Low Mg Low P
Leaf chlorosis and necrosis is common in Mg and K deficient leaves, but not in P deficient leaves
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PHLOEM TRANSPORT
K and Mg play critical role in phloem transport
K Mg Source
Sink
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Sucrose concentration (mg Glucose equiv. g-1 DW)
Control
12 76
K Deficiency
Accumulation of Phosynthates in K-Deficient Source Leaves
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Sucrose concentration in source leaves
(mg Glucose equiv. g-1 DW)
12 76 108 19
Control Low K Low Mg Low P
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Phloem Export of Sucrose (mg Glucose equiv. g-1 DW 8 h-1)
Control
3.4 1.6
K Deficiency
Decrease in Phloem Export of Sucrose by K-Deficiency
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Export of sucrose from bean leaves (mg Glucose equiv . g-1 DW . 8h-1)
3.4 ± 0.8 1.6 ± 0.3 2.8 ± 1.0 0.7 ± 0.3
Control Low K Low Mg Low P
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Relative distribution of total carbohydrates between shoot and roots (%)
Control K Deficiency
16 3
97 84
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Control Low Low Low K Mg P
16 3 1 23
84 97 99 77
Relative distribution of total carbohydrates between shoot and roots (%)
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H2O2
H2O MDAsA
AsA peroxidase
AsA
MDAsA reductase
NADH non-enzymatic
NAD+
DHAsA
GSSG
GSH
DHAsA reductase
Glutathione reductase
NADPH
NADP+
Enzymes involved in H2O2 detoxification in chloroplasts
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Ascorbate Peroxidase Activity of
Source Leaves
Control K Deficiency
4.7
(µmol Ascorbate g-1 FW min-1)
9.5
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Monodehydroascorbate Reductase
Activity of Source Leaves
Control K Deficiency
1.2
(µmol Ascorbate g-1 FW min-1)
3.5
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0
10
20
30
40
50
LOW MILD SEVERE
Ph
oto
syn
the
sis
(µm
ol C
O2 m
-2 s
-1)
Drought Stress
Low K
Adequate K
Potassium Improved Photosynthesis Under Drought Stress
Sen Gupta et al., 1988, Plant Physiol.
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0
20
60
80
40
100
K supply to growing medium (mM)
Liv
e r
oo
t (
%)
0 2.5 10
Non-drought stressed
Drought Stressed
Effect of increasing K Supply on Percentage of Live Roots Under Varied Drought Treatments
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0
10
20
30
0 42 84
Le
af D
am
age
Ca
use
d
by F
rost
(%
)
K supply (kg ha-1)
Alleviation of Frost Damage by K Supply in Potato
Grewal, and Singh, 1980
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Ch
loro
ph
yll
(g
kg
-1 F
W)
0.0
0.5
1.0
1.5
2.0
0
20
40
60
Me
mb
ran
e D
am
ag
e (%
)
Control NaCl + K supply NaCl
Alleviation of Salt Stress by K Supply
Kaya et al., 2001, J. Plant Nutr.
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Activity of NADPH-
oxidizing enzymes
play an important role in
generation of
superoxide radical
production under
drought, chilling, Zn
deficiency, UV light,
wounding, pathogenic
infection, etc.
O2– - Generating
NADPH - Oxidase
NADPH
e-
Flavin ox Flavin red
O2·– O2
CELL DAMAGE
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Stress stimulated NADPH oxidase and NADPH-dependent superoxide radical generation
Cakmak, 2003, in press
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Increases in NADPH-Dependent O2-
Generation by K Deficiency in Bean Roots
K supply O2.- generation
(µmol)
10 45 (124)
25 42 (117)
50 50 (139)
100 49 (136)
200 44 (122)
2000 (control) 36 (100)
(nmol O2.- FW min-1)
S. Eker, unpublished results
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0
50
100
150
200
10 25 50 100 200 2000
NA
DP
H o
xid
as
e
(µm
ol g
-1 F
W m
in-1
)
K supply (µM)
K Deficiency-Induced Marked Increases in NADPH Oxidase Activity of Bean Roots
S. Eker, unpublished results
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0
4
8
12
16
CHILLING CONTROL
0
20
40
60
80
CHILLING CONTROL
NA
DP
H o
xid
ation
(nm
ol m
g p
rote
in-1
min
-1)
O2- P
roduction
(nm
ol m
g p
rote
in-1
min
-1)
Chilling-Induced NADPH-Oxidation and NADPH-Dependent O2
- Generation in Leaves of Cucumber
Shen et al., 2000; Plant Physiol.
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0
10
20
30
K-Deficiency Control
AB
A C
on
ce
ntr
ati
on
(ug
g-1
FW
ro
ot)
K Deficiency-Induced Biosynhesis of ABA
(Abscisic Acid) in Roots
Peuke et al., 2002, J. Exp. Botany
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0
4
8
12
16
control ABA drought
NADPH oxidase
O2- nm
ol m
in-1
(m
g p
rote
in)-
1
0.0
0.4
0.8
1.2
control ABA drought
O2- production
nm
ol m
in-1
(m
g p
rote
in)-
1
NADPH oxidase and O2- Production in
Plants Treated with ABA and Drought
ABA: Abscisic Acid Jiang and Zhang, 2002; Planta
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Zn and B deficiencies also affect photosynthetic activities of plants in various ways. • Both micronutrients exert marked influences on photosynthetic CO2 fixation and translocation of photosynthates. • Any disturbance in the adequate supply of plants with Zn and B is, therefore, potentially capable of inducing photooxidative damage
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ALSO ZINC-DEFICIENT PLANTS ARE
HIGHLY PHOTOSENSITIVE
Increases in light intensity rapidly cause development of
chlorosis and necrosis in Zn-deficient plants
Growth of Zn deficient bean plants
at different light intensities
22 W m-2 127 W m-2 53 W m-2
Light
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Growth of Citrus Trees on a Zn-Deficient Soil
NORTH
SOUTH
Cakmak et al., 1995
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Sufficient B Supply Deficient B Supply
Low
light
Low
light
High
light
High
light
High light-induced damage in B-deficient plants
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Photooxidative damage to
membrane and chlorophyll
can be expected in B-deficient
leaves as a result of enhanced
photogeneration of toxic
oxygen free radicals caused
by impaired utilization of light
energy in photosynthesis
Shaded Unshaded
Superoxide Generation and
Photooxidative Damage
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0
2
4
6
100 200 600
Light Intensity, µE m-2
sec-1
nm
ol N
O2
- 30 m
in-1
4 leaf
dis
ks
+B
-B
-B, +SOD
O2- - Production in Leaf Disks from
B-Deficient Plants
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Activity of NADPH-oxidizing enzymes play an important role in generation of superoxide radical under drought, chilling, Zn deficiency, UV light, wounding, pathogenic infection, etc.
O2– - Generating
NADPH - Oxidase
NADPH
e-
Flavin ox Flavin red
O2·– O2
CELL
DAMAGE
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Ca2+ (mM)
NA
DP
H o
xid
as
e a
cti
vit
y
70
0
NADPH Oxidase Activity in Isolated Tomato and Tobacco Membranes
2 4 6 8 10
60
50
40
30
20
10
0
Sagi and Fluhr,2001, Plant Physiol. 126: 1281-1290
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There is increasing evidence suggesting that Ca is involved in expression of high tolerance to heat stress in plants.
• Jiang and Huang (2001) showed that Ca treatment protects
cool-season grass species from heat injury expressed as
increased lipid peroxidation and chlorophyll degradation.
• Exposure of seedlings to heat stress at 40 oC induced lipid
peroxidation and reduced survival of seedlings, and these
effects of heat stress could be inhibited very significantly by Ca
treatment.
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0.00
0.02
0.06
0.08
0.04
0
20
60
80
40
100
Unheated Heated
(light)
Heated
(dark)
µg
MD
A g
-1 F
W
% s
urv
iva
l
Unheated Heated
(light)
Heated
(dark)
Oxidative Damage and Survival in Response of Heating in Arabidopsis
Larkindale er al., Plant Physiol. 2002, 128: 682-695
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0.00
0.03
0.09
0.12
0.06
0
20
60
80
40
100
Control CaCl2
Pe
rox
ida
tio
n
nm
ol g
-1 F
W
% s
urv
iva
l
20 oC 40 oC
Control CaCl2
Oxidative Damage and Survival in Response of Heating in Arabidopsis with and without Ca supply
Larkindale er al., Plant Physiol. 2002, 128: 682-695
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0
10
40
60
20
0.0
0.5
1.5
2.0
1.0
2.5
Blo
sso
m-e
nd
(%
)
Lip
id p
ero
xid
ati
on
(nm
ol g
-1 F
W)
Control Low Ca Foliar
Ca spray
Effect of Foliar Application of Ca on Lipid Peroxidation and Blossom-end
Control Low Ca Foliar
Ca spray
30
50
Schmitz-Eiberger et al., J. Plant Physiol. 2002, 159: 733-742
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CONCLUSIONS
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The existing data indicate that
improving mineral nutritional status of
plants under marginal environmental
conditions is indispensable for sustaining
survival and high yield.
Impairment in mineral nutritional status
of plants, therefore, exacerbates adverse
effects of environmental stress factors on
plant performance.
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Mineral at adequate levels nutrients supplied are essentially required for maintaining photosynthetic activities and utilization of light energy in CO2 fixation.
Improving mineral nutrition of
plants is, therefore, a major contributing factor to the protection of plants from photooxidative damage under marginal environmental conditions.
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Remaining challenges include the better understanding the roles of mineral nutrients in i) ROS formation during photosynthesis and
plasma membrane-bound NADPH oxidase, ii) signaling pathways affecting adaptive
response of plants to environmental stresses and
iii)expression and regulation of genes induced by mineral nutrient deficiency.