Effects of Exogenous Nitric Oxide on Wheat Exposed to Enhanced Ultraviolet-B Radiation

doi:10.4236/ajps.2013.46159

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American Journal of Plant Sciences, 2013, 4, 1285-1290

http://dx.doi.org/10.4236/ajps.2013.46159 Published Online June 2013 (http://www.scirp.org/journal/ajps)

Effects of Exogenous Nitric Oxide on Wheat Exposed to

Enhanced Ultraviolet-B Radiation

Liyan Yang1, Rong Han1, Yi Sun2,3*

1Shanxi Normal University, Linfen, China; 2Biotechnology Research Centre, Shanxi Academy of Agricultural Sciences, Taiyuan,

China; 3Key Laboratory of Crop Gene Resources and Germplasm Enhancement on Loess Plateau, Ministry of Agriculture, Taiyuan,

China.

Email: *[email protected]

Received April 20th, 2013; revised May 20th, 2013; accepted June 10th, 2013

which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

We explored the use of exogenous nitric oxide (NO) on alleviating effects of UV-B light on winter wheat development.

Triticum aestivum L. cv. Linyou 7287 seeds were irradiated with UV-B (10.08 kJ·m–2·d–1) (enhanced UV-B) and wa-

tered with either water or 100 µmol·L–1 SNP solution. Plants were also watered with the SNP alone. The results showed

that enhanced UV-B produced negative effects on seedling development. Leaf length decreased and seedling biomass

dropped significantly compared with the control. Photochemical efficiency (Fv/Fm) dropped, and chlorophyll and caro-

tenoid content as well as the ATPase activity declined. Content of UV-absorbing compounds and activity of the POD

increased compared to the control. Application of the SNP, a NO donor partially protected wheat seedlings exposed to

elevated UV-B radiation in that their leaf lengths and biomass accumulation were enhanced compared to the UV-B

treatment alone. SNP also improved the contents of chlorophyll, carotenoid and UV-absorbing compounds in leaves.

ATPase activity was enhanced but no influence on POD activity. Furthermore, the application of SNP alone showed a

favorable ef fect on seedling growth compared with the control.

Keywords: Nitric Oxide; Seedling Development; UV-B Radiation; Wheat

1. Introduction

Plants are sessile photoautotrophic organisms and thus

must constantly adapt to surrounding environmental fac-

tors for optimal growth and development. Ultraviolet-B

(UV-B) radiation (wavelengths from 280 to 320 nm) is

an intrinsic part of the sunlight. There is evidence of ad-

verse effects of UV-B on plants including DNA damage

and biomass reduction [1-3], and enhanced UV-B radia-

tion has potentially harmful or even detrimental effects.

Chloroplast is th e photosynthesis organelle wh ich is very

sensitive to UV-B radiation, upon high dosage of UV-B

radiation, yellow spots or streaks appeared on the treated

leaf surfaces, which are attributed to decreased chloro-

phyll content and the possible injury on chloroplast [4].

Excessive radiation may lead to over-saturation of the

photosynthetic light reactions, which eventually cause

photo inhibitory damage to the photosynthetic apparatus

[5]. Photosystem II (PSII) and ATP synthase are two

kinds of proteins complex in thylakoid membrane, and

the later are abundantly located on plasma membrane,

inner mitochondrial membrane and thylakoid membrane

and play an important role in photosynthesis reaction.

The target of UV-B rad iation is the membrane [6] which

can be damaged by increased reactive oxygen species

(ROS) in the plant cell. UV-B exposure has shown to

increase ROS [7]. Higher plants have evolved different

mechanisms to resist the harm of ROS. These mecha-

nisms are based on metabolic compounds and enzymes,

including UV-absorbing substances and reactive oxygen

species.

Nitric oxide (NO) acts as a signaling molecule and

mediates multiple physiological processes in plants [8].

NO confers protection ag ainst the h erbicide diquat, drough t,

and salt stress [9-11]. When Arabidopsis thaliana were

exposed to UV-B irradiation, endogenous NO is gener-

ated, which indicated the involvement of NO in UV-B

stress [7] (Mackerness et al., 2001); flavonoid biosyn-

thetic pathway was systemically induced by UV-B in a

NO dependent way [12]; the NO is able to protect cells

from the deleterious effects of oxidative stress contribut-

*Corresponding a uthor.

Effects of Exogenous Nitric Oxide on Wheat Exposed to Enhanced Ultraviolet-B Radiation

1286

ing with the antioxidant response [13]. In the present

study, we examined the effects of the exogenous nitric

oxide on wheat seedling growth exposed to enhanced

UV-B radiation. We also investigated some physiological

characters among them those of pigments, intrinsic pho-

tochemical efficiency and ATPase activity, POD activity

was analyzed as well.

2. Materials and Methods

2.1. Plant Material and Treatments

Winter wheat (Triticum aestivum L. cv. Linyou 7287)

seeds were provided by the Wheat Research Institute,

Shanxi Academy of Agricultural Sciences (SAAS), Peo-

ple’s Republic of China. They were selected for uniform

size and sterilized for 10 min with 0.1% HgCl2 and

washed for 50 min with running water. Ninety seeds

were cultured on wet filter paper in each petri dish (di-

ameter 18 cm) and watered daily in a growth chamber at

25˚C and 70% relative humidity. There were 4 treat-

ments, with 3 replications. One day later, just as seeds

were germinating, irradiation treatment was applied accor-

ding to the light/dark period as given (Table 1). At the

same time, the seedlings were watered with 100 µmol·L–1

sodium nitroprusside (SNP, a NO donor) in S and SB

groups every day, and the same amount of distilled water

was applied in CK and B groups under same condition.

SNP solution was prepared immediately prior to use.

The UV-B radiation intensity was 10.08 kJ·m–2·d–1.

The spectral irradiance from the lamps was determined

with an Optronics spectroradiometer (Model 742 Op tronics

Laboratories, Orlando, FL, USA). The UV-B radiation

was generated by a filtered lamp (30 W, 297 nm, Qin

brand, Baoji Lamp Factory, Baoji City, China.). The

lamps were hung on the top of the petri dishes and the

desired irradiation was obtained by adjusting the distance

between the lamps and the petri dishes.

2.2. Plant Height and Biomass Measurement

Eight days after treatment, twenty seedlings per replica-

tion were randomly chosen from each treatment. A total

Table 1. Light/dark period of irritation treatments.

Light (hr·d–1)

Treatments White light UV-B irritation Dark (hr·d–1)

CK 8 - 16

B 8 8 16

S 8 - 16

SB 8 8 16

CK: distilled water without ultraviolet-B radiation; B: distilled water with

ultraviolet-B radiation; S: SNP without ultraviolet-B radiation; SB: SNP

with ultraviolet-B radiation.

of 60 seedlings were measured and means of leaf length,

fresh weight, and dry weight were recorded.

2.3. Chlorophyll, Carotenoid and

UV-Absorbing Compounds Content,

POD Activity Measurement

Eight days after treatment, 0.5g of leaves was frozen in

liquid nitrogen, grounded to a powder and extracted with

100% acetone. The pigment extracts were centrifuged for

3 - 5 min to make the extract transparent. The content of

chlorophyll and carotenoid were immediately assayed

spectrophotometrically according to Lee [14] and were

expressed in mg·g–1 fresh weight. UV-absorbing com-

pounds content was measured according to Smith et al

[15], sections were immersed in 5 ml methanol: conc.

HCl: water solution, at the end of the extractio n period, a

absorbance of the solution at 280 - 320 nm was deter-

mined using a UV/Visible scanning spectrophotometer,

and the area under the curve integrated to give total ab-

sorbance in the UV-B wavelength band. POD activity

was determined by measuring the increase rate in absor-

bance at 470 nm of a mixture containing 1 ml of 50 mM

sodium phosphate buffer (pH7.0), 0.95 ml of 0.2% 2-me-

thoxyphenol, 1 ml of 0.2% hydrogen peroxide and 0.05

ml of enzyme extract or disti lled water as negat ive control.

2.4. Chlorophyll Fluorescence Measurement

The chlorophyll fluorescence was determined by a port-

able pulse-modulated fluorometer (PAM-2000, Walz, Ef-

feltrich, Germany) with a far-red source adapter. The

maximum photochemical efficiency of PSII was deter-

mined from the ratio of variable (Fv) to maximum (Fm)

fluorescence (Fv/Fm = (Fm – F0)/Fm) in leaves that had

been dark-adapted for 30 min. The minimal fluorescence

level (F0) with all PSII reaction center open was deter-

mined by measuring modulated light of 735 nm, which

was sufficiently low not to induce any significant vari-

able fluorescence. The maximal fluorescence level (Fm)

with all PSII reaction center closed was determined by a

saturating pulse of 8000 µmol·m–2·d–1 in the dark-adapt-

ed leaves.

2.5. ATPase Activity Measurement

Eight days after treatment, activity of ATPase located in

thylakoid membrane of leaves as well as in plasma mem-

brane of root cell was measured according to Chen [16].

2.6. Statistical Analysis

Statistical significance was estimated at P < 0.05 ac-

cording to Duncan’s multiple range test. All data give

mean ± SD.

Effects of Exogenous Nitric Oxide on Wheat Exposed to Enhanced Ultraviolet-B Radiation

1287

3. Results

3.1. The Effect of SNP on Chlorophyll,

Carotenoid and UV-Absorbing Compounds

Content in Seedlings under UV-B

Significant declined chlorophyll (chlorophyll a and b)

and carotenoid contents appeared in B group compared

to those in the control (P < 0.05), but they increased at

the presence of SNP under UV-B radiation compared to

UV-B alone. Application of SNP resulted in higher con-

tent of chlorophyll and carotenoid than the control though

there was no significant difference. Content of UV-ab-

sorbing compounds in B group was significant higher (P

< 0.05) than the contro l, but lower (P > 0.05) than th at in

SB group. Application of SNP alon e induced higher gen-

eration of UV-absorbing compounds than the control (P

< 0.05) but less than that in B group (P > 0.05) (Table

2).

3.2. The Effects of the SNP on Chlorophyll

Fluorescent in Seedlings Exposed to

Enhanced UV-B

Photosynthesis is very vulnerable to UV-B treatment. To

study the effect of SNP on photosynthesis under the UV-

B treatment, we measured the maximum efficiency of

PSII photochemistry Fv/Fm (Figure 1). After 8 days of

UV-B radiation, Fv/Fm significantly declined (P < 0.05)

compared with that of the control. Application of SNP

could reverse the inhibition on PSII photochemistry

where Fv/Fm was enhanced significantly compared with

that in the B group (P < 0.05); the highest Fv/Fm was

observed in the S group.

3.3. The Effect of SNP on ATPase Activity in

Seedlings under Enhanced UV-B

The highest ATPase activity was observed in the S group

either for that in thylakoid membrane of leaves or plasma

membrane of roots (Figure 2); the lowest ATPase active-

ity was showed in the B group which was significantly

lower than that of th e control (P < 0.05). ATPase located

in thylakoid membrane was more sensitive to ultravio-

let-B radiation in that its activity was 27.6% lower than

control versus 11.94% decreased in plasma membrane of

root cell. Application of SNP showed a favorable effect

on ATPase activity in both thylakoid membrane and

plasma membrane of root cell under UV-B exposure.

3.4. The Effect of SNP on POD Activity

The POD activity was the highest in the S group, and it

was significantly higher (P < 0.05) than that in the rest

groups. Application of SNP didn’t induce a higher activ-

ity of POD compared to B group, but they were signifi-

cantly higher than that of the control (P < 0.05) (Figure 3).

3.5. Effects of SNP on Leaf Length and Biomass

of Seedlings under UV-B

Leaf length was severely inhibited under UV-B radiation

compared with that of the control (P < 0.05); the inhibit-

tion on leaf length was significantly alleviated at the

presence of SNP under ultraviolet-B radiation compared

to that under UV-B alone. SNP alone showed more fa-

vorable effect than the control. Same tendency was also

observed for the plant biomass in that fresh and dry

weights were significantly decreased under ultraviolet-B

radiation compared with those of control (P < 0.05), and

they increased at the presence of SNP (Table 3).

4. Discussion

Plants use inducible mechanisms to defend themselves

from environmental concerns, including metabolic and

morphological changes. When maize seedlings were ex-

posed to enhanced ultraviolet-B, shoot height was dwarfed

[17], and in the present study, leaf growth of wheat seed-

ling was inhibited significantly. A decrease in leaf elon-

gation might well serve to decrease UV-B exposure, but

might influence photosynthesis and reduce photosyn-

thetic accumulation. SNP application partially alleviated

the adverse effects of UV-B on leaf growth. Moreover,

SNP alone resulted in favorable impact on leaf growth

compared to that of the control.

Table 2. Content of chlorophyll, caro te noid and UV-B absorbing compounds in seedlings exposed to UV-B.

Treatment Chlorophyll a content

(mg·g–1 FW) Chlorophyll b c ontent

(mg·g–1 FW) Carotenoid content

(mg·g–1 FW) Content of UV-absorbing

compounds (% )

CK 1.87 ± 0.20 ab 2.16 ±0.19

ab 4.87 ± 0.45ab 0.32 ± 0.02 c

S 2.01 ± 0.23 a 2.36 ±0.20

a 4.98 ± 0.50 a 0.51 ± 0.04 ab

B 1. 2 0 ± 0 .10 c 0.86 ± 0.07 c 2.58 ±0.24

c 0.64 ± 0.04 a

SB 1.32 ±0.11 c 0.98 ± 0.08 c 2.77 ± 0.26 c 0.71 ± 0.06 a

CK: distilled water without ultraviolet-B radiation; B: distilled water with ultraviolet-B radiation; S: SNP without ultraviolet-B radiation; SB: SNP with ultra-

violet-B radiation. Values are means ± SD (n = 3), and values in the same column followed by different letters are significantly different at P < 0.05.

Effects of Exogenous Nitric Oxide on Wheat Exposed to Enhanced Ultraviolet-B Radiation

1288

CK: distilled water without ultraviolet-B radiation; B: distilled water with

ultraviolet-B radiation; S: SNP without ultraviolet-B radiation; SB: SNP

with ultraviolet-B radiation. Each bar is the mean ± SD (n = 3) for each

treatment. Bars with different letter are significantly different at P < 0.05.

Figure 1. The value of Fv/Fm in various treatments.

Antioxidative system is another inducible system upon

UV-B radiation. Flavonoids and related phenolics are

probably the most important UV-induced antioxidants

which can ab sorb UV-B. In the present study, much mor e

UV-absorbing substances were generated under UV-B

radiation compared to control, SNP application induced

more UV-B absorbing compounds, which means the more

protection from UV-B, and SNP alone resulted in more

antioxidant production. POD activity did not change with

the SNP application compared to UV-B treatment alone.

SNP alone induced improved POD activity which was

consistent with the study of Costa and Shi [18,19] and

microarray studies where NO induces a large number of

genes at transcriptional level; among them those of fla-

vonoids related genes and antioxidant enzymes genes

[20].

(a) (b)

(a) Activity of ATPase that located in plasma membrane of seedling root; (b) Activity of ATPase that located in thylakoid membrane of wheat l eaves. CK: d is-

tilled water without ultraviolet-B radiation; B: distilled water with ultraviolet-B radiation; S: SNP without ultraviolet-B radiation; SB: SNP with ultraviolet-B

radiation. Each bar is the mean ± SD (n = 3) for each treatment. Bars with different letter are significantly different at P < 0.05

Figure 2. ATPase activity in various treatments.

Each bar is the mean SD (n = 3) for each treatment. Bars with different

letters are significantly different at P < 0.05. CK: distilled water without

ultraviolet-B radiation; B: distilled water with ultraviolet-B radiation; S:

SNP without ultraviolet -B radiation; SB: SNP with ultraviolet-B radiation.

Figure 3. POD activity in various treatments.

Table 3. Leaf length and biomass in various treatments.

Treatment Leaf length ( cm)

(means ± SD) Fresh weight (g)

(means ± SD) Dry weight (g)

(means ± SD)

CK 12.03 ± 0.08a 1.64 ± 0a 0.21 ± 0.01a

S 12.13 ± 0.07a 1.66 ± 0.02a 0.22 ± 0.01a

B 9.24 ± 0.01c 1.50 ± 0.01b 0.17 ± 0.003b

SB 10.35 ± 0.02b 1.56 ± 0.04b 0.19 ± 0.007b

CK: distilled water without ultraviolet-B radiation; B: distilled water with

ultraviolet-B radiation; S: SNP without ultraviolet-B radiation; SB: SNP

with ultraviolet-B radiation. Values are means ± SD (n = 60), and values in

the same column followed by different letters are significantly different at P

< 0.05.

Effects of Exogenous Nitric Oxide on Wheat Exposed to Enhanced Ultraviolet-B Radiation 1289

Enhanced ultraviolet-B caused reduction of chlorophyll

content and resulted in adaptive changes on photosynthetic

apparatus such as thylakoid membrane, PSII system [4,

12]. In the present study, we found not only chlorophyll

but also carotenoid content decreased under UV-B radia-

tion. Carotenoid plays a vital role in the photosynthetic

reaction centre where, it provides a mechanism for photo

protection against auto-oxidation and they also participate

in the energy-transfer process. The loss of carotenoid

might negatively influence the photosynthesis. Measure-

ment of the maximum efficiency of PSII photochemistry

(Fv/Fm) revealed that it decreased under UV-B radiation.

The ATP synthase of chloroplasts is an anabolic enzyme

which is the prime producer of ATP, using the proton

gradient generated by photosynthesis. ATP synthase

activity of chloroplasts was significantly inhibited under

UV-B radiation compared to that of the control, which

implied that the ATP generation might be hampered

accordingly. At the presence of SNP, the values of

Fv/Fm were higher than that of UV-B treatment alone, so

were the contents of chlorophyll and carotenoid, as well

as ATPase activity. We attribute those favorable effects

of SNP to following: NO, an important signaling molecule,

involved in UV-B transduction pathway and plants may

use exogenous NO as a protection strategy against ele-

vated doses of UV-B. NO may fulfill this function by

inducing more antioxidant to absorb UV-B. Decreased

UV-B irradiation and peroxidant damage on photosyn-

thetic apparatus as PSII and ATPase partially alleviated

the inhibition on them caused by UV-B. We also con-

clude ATPases of root cell membrane was less sensitive

to UV-B, but their activity was declined too, SNP alone

showed a more favorable effects compared to the control.

5. Acknowledgements

This research project was supported by the Shanxi Scho-

larship Council of the People’s Republic of China (2011-

061) and the National Nature Science Foundation of

Shanxi Normal University (SMYKZ-18).

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Abbreviation

NO: nitric oxide; UV-B: Ultraviolet B; POD: peroxidase; SNP: sodium nitroprusside; ROS: reactive oxygen species;

PSII: Photosystem II; ATPase: ATP synthase.