Biotechnological

Communication

Biosci. Biotech. Res. Comm. 9(3): 439-444 (2016)

Photochemical ef cacy analysis using chlorophyll

 uorescence of

Dicranopteris linearis

in response to

desiccation and rehydration stress

Kavitha C H

and K Murugan

Department of Botany, St. John’s College, Anchal, Kollam

Plant Biochemistry and Molecular Biology Laboratory, Department of Botany, University College,

Trivandrum, 695 034, Kerala, India

ABSTRACT

Exploring the mechanism of desiccation tolerance is critical in order to unravel the position of ferns in tropical region

of the earth. Desiccation in plants induces morphological deformities, ROSs formation, oxidation of protein, nucleic

acids, peroxidation of cell membranes, antioxidants machinery and photosynthetic ef cacy. The present study is

planned to analyze the pigment and  uorescence responses of the forked fern - Dicranopteris Linearis (Burm.F.)

Underw. against desiccation and rehydration stress with a view to select drought tolerant marker species. Fronds of

the fern were subjected to various regimes of desiccation rehydration stress ((a) 2 (b) 4 (c) 6 (d) 8 and (e) 10 days).

Initially chlorophyll a and b pigments were decreased (2

day) followed by an increase indicating the physiological

resurrection of the stressed plants during subsequent days of desiccation phase. Meanwhile, carotenoids showed a

steady increase till 6th day followed by a decrease. The quantum yield potential of photosystem II (F

) was 0.61,

0.77, 0.79, 0.80 and 0.76 respectively, when subjected to 2, 4, 6, 8 and 10 days of desiccation. The F

ratio, Fm,

, Fo the potential parameters of chlorophyll  uorescence can be used in the early detection of desiccation stress in

the fern. Further, the quantum yields (F

), photosynthetic quenching and ERT and non-photochemical quenching

were maintained remarkably in the fronds till the 8 d of desiccation stress. Further studies are warranted at molecular

levels to unravel the mechanism of desiccation tolerant ability in the fern.

KEY WORDS: CHLOROPHYLL FLUORESCENCE; CHLOROPHYLL; CAROTENOIDS; PHOTOSYNTHETIC EFFICACY

439

ARTICLE INFORMATION:

*Corresponding Author: harimurukan@gmail.com

Received 16

July, 2016

Accepted after revision 5

Aug, 2016

BBRC Print ISSN: 0974-6455

Online ISSN: 2321-4007

Thomson Reuters ISI ESC and Crossref Indexed Journal

NAAS Journal Score 2015: 3.48 Cosmos IF : 4.006

reserved.

Online Contents Available at: http//www.bbrc.in/

440 PHOTOCHEMICAL EFFICACY ANALYSIS USING CHLOROPHYLL FLUORESCENCE BIOSCIENCE BIOTECHNOLOGY RESEARCH COMMUNICATIONS

Kavitha and Murugan

INTRODUCTION

Desiccation is the most alarming stress faced by plants.

The loss of water in the tissues leads to the denaturation

of essential biomolecules and subsequently, degenera-

tion of cell organelles (Alpert, 2006). Animals actively

avoid desiccation by movements, while plants are static

and therefore subjected to water loss and recover back

slowly during rehydration (Alpert, 2006). Resurrection

plants such as Myrothamnus  abellifolius, Xerophyta

viscose, andSporobolus stap anus were proven drought

tolerant species (even up to 90% water loss) (Alpert,

2006). Adaptation to desiccation is based on the ability

of the organism to equilibrate its internal water potential

with the desiccating environment, and also their dras-

tic ability to regain normal activities after rehydration

(Alpert, 2000).

Compared to vascular plants (Vicre et al., 2004), the

mechanisms involved in desiccation among lower plants

like ferns is poorly understood. Most of the drought stress

initiates the activation of antioxidant enzymes such as cat-

alase, superoxide dismutase, ascorbate peroxidase and glu-

tathione reductase (GR) etc. (Burrittet al., 2002) to counter

balance desiccation-mediated oxidative stress. Similarly,

many macro algae resist desiccation tolerance through the

photosynthetic system including chloroplast (Zou and Gao,

2002a,b). Fucus vesiculosus was evaluated by molecular

approaches to unravel the responses to desiccation via the

genes encoding photosynthetic and ribosomal proteins

(Pearsonet al., 2010 Maghsoudi et al., 2015).

The photosystem II reaction center was critical in pho-

tosynthetic pathway against drought stress (Wen et al.,

2005) i.e., desiccation stress reduces the photosynthetic

electron transport activity and also the  uorescence of

photosystem II (PSII). Inactivation of PSII leads to derail-

ment of the water-splitting complex, disturbance of pig-

ment protein complexes in thylakoids, which further

in uences regulation of energy transfer and  nally, the

photochemical reaction center of PSII was deactivated

(Wise et al., 2004). Impact of plants exposed to desicca-

tion stress was drastic but, its recovery was gradual or

ceased due to the injury to PSII components (Sinsawat et

al., 2004 and Kifah and Jaroslav, 2015).

The use of  uorescence parameters permit to ana-

lyze the reduction in electron transport disorder via the

emission of heat in the form of IR radiation or by  uo-

rescence. This technique is based on the light kinetics

absorbed by antenna pigments and the excitation energy

transferred to the reaction centers of photo system I and

II (Zhani et al., 2012).

Contreras-Porcia et al., (2011) analyzed the interrela-

tionship between F

m and F0 in Porphyra columbina col-

lected from the different intertidal regions. Generally, in

the optimal conditions the proportion of radiant energy

emitted as  uorescence is decreased. Meanwhile, during

stressed conditions, the chlorophyll  uorescence will be

altered (Kadir and Von Weihe 2007). So, in vivo  uores-

cence of chlorophyll pro vides an early sign of photosyn-

thetic malfunc tion and can be used as marker to localize

the possible sites of damage induced by stress within the

cells. In this juncture, the present study is aimed to ana-

lyze the photosynthetic pigments and their ef ciency in

the fern against different duration of desiccation and

rehydration.

MATERIAL AND METHODS

QUANTIFICATION OF PHOTOSYNTHETIC

PIGMENTS

Photosynthetic pigments were estimated in 80% ace-

tone extract. 1 g tissue was homogenized with 1.5 ml

of 80% chilled acetone. The homogenate was centri-

fuged at 3000 rpm for 5 min. The aliquots were made

up to 3 ml by using 80% acetone and the absorbance

was read at 470, 648 and 664 nm spectrophotometrically

against 80% acetone as blank. Total chlorophyll as well

as chlorophyll a and b concentrations and carotenoids

were calculated according to the protocol of Arnon

(1949).

Chlorophyll  uorescence emission from the upper

and lower surface of the leaves of the fern was meas-

ured by a modulated  uorometer (OS 500;Opti

Sciences;Inc;Tyngsboro;Mass). Maximum  uorescence

yield (F

) was determined during saturating  ash (3000

mol m

-2

)

The actual  uorescence level (F) was moni-

tored to ensure that it was stable. To obtain the maximal

 uorescence yield under illumination (F

), the leaf was

exposed to a saturating  ash during exposure to actinic

light (210 mol m

-2

-1

). To determine the minimal level of

 uorescence during illumination (F

), the leaf was con-

tinuously illuminated with far-red light (730 nm) to rap-

idly reoxidize the PSII centers. All measurements were

conducted at 25ºC (Demmig-Adams et al., 1996).

The minimal  uorescence level (F

) with all PSII reac-

tion centers open and the maximal  uorescence level

) with all PSII reaction centers closed were determined

on dark-adapted leaves. Then the leaves were continu-

ously illuminated with a white actinic light at an irra-

diance of 180 µmol m

-2

-1

to measure the steady-state

value of  uorescence (F

), which occurred at about 6 min

after the initiation of white actinic light. The maximal

 uorescence level in the light-adapted state (F

’) was

recorded after subjecting the leaf to a second saturating

pulse at 8000 µmol m

-2

-1

BIOSCIENCE BIOTECHNOLOGY RESEARCH COMMUNICATIONS PHOTOCHEMICAL EFFICACY ANALYSIS USING CHLOROPHYLL FLUORESCENCE 441

Kavitha and Murugan

The minimal  uorescence level in the light-adapted

state (F

) was determined by exposing the leaf to far-red

light for 3s.Using both light and dark  uorescence data,

the following parameters were calculated:

- F

(maximum variable chlorophyll  uorescence

yield in a dark-adapted state) was calculated fol-

lowing Maxwell and Johnson (2000): F

= F

- F

(the maximal ef ciency of PSII photo-

chemistry in the dark-adapted state) was calcu-

lated as: F

= (F

- F

)/F

- qP (the photochemical quenching coef cient):

qP = (F

´ - F

) / ( F

´ - F

´)

- qN (non-photochemical quenching coef cient):

qN = 1 - (F

´ - F

´) / (Fm - F0).

PSII (the actual quantum yield of PSII electron

transport in the light-adapted state):

PSII = (F

´ - F

)/ F

´, which was equal to the prod-

uct of qP and F

´ /F

´. Thus,  PSII depends on the

degree of closure of PSII reaction centers and the

ef ciency of excitation energy capture in PSII.

- ETR (Apparent photosynthetic electron transport

rate): Apparent electron transport rates (ETR) are

derived from effective quantum yields of pho-

tosystem II (∆F/F

´ or Y(II)) according to ETR =

Y(II) x PAR x 0.42. In this equation, the PAR cor-

responds to the quantum  ux density of photo-

synthetically active radiation, and the 0.42 is the

product of light absorptance by an average green

leaf (0.84) times the fraction of absorbed quanta

available for photosystem II (0.5).

Data were statistically analyzed using ANOVA followed

by Tukey’s test (SPSS 14.0; SPSS Chicago, IL, USA). Sig-

ni cant differences were analyzed based on P < 0.05

and P < 0.01. Percentage data were subjected to arc sine

transformation prior to statistical analysis.

RESULTS AND DISCUSSION

Generally, desiccation tolerance was evaluated as the

capacity of the plants to mitigate the excess ROS formed

and thereby attenuating the oxidative stress within the

plant. Photosynthetic components such as enzymes,

chlorophylls, and carotenoids levels depend on the

severity and duration of stress.

In the present analysis,

the total chlorophyll content was maintained by the fern

during the different periods of desiccation stress (4 to

day) i.e., showed an increase from 0.352 (in control)

to 0.353 mg/g at 10

day of desiccation treatment in the

fern (Table-1). The optimal maintenance of chlorophyll

content directly re ects the functional status of the fern

against the desiccation stress management. Chlorophyll

a/b ratio showed an initial increase (2

day) followed

by an decrease with the degree of desiccation till the

day 10 of treatment. Carotenoids, the major accessory

pigments showed steady increase up to 6

day and then

decreased marginally (10

day) (Table-1). The pigments

are effective antioxidants and therefore, protect the cells

from oxidative stress by mitigating ROSs formed during

photo-oxidative stress.

Chlorophyll  uorescence emission is a versatile tool for

quick and non-intrusive estimation of the photosynthetic

activity and photoinhibition in the leaves against environ-

mental stresses. Initially, after 2 d desiccation the F

level

increased whereas, the F

value decreased in the frond

when compared to control. This leads to a decline in the

maximum quantum yield of PSII (F

) to 0.61. From 4

to 8

day of desiccation F

, F

and F

values were

maintained. The effective quantum yield of PSII (PSII) and

photochemical quenching (qP) also showed a similar trend.

In contrast, the non-photochemical quenching (qN) was

increased at 2 d desiccated fronds with improvement in

apparent photosynthetic electron transport rate (ETR) also.

ratio, known as the basal quantum yield displayed a

range from 0.198 to 0.38 (Table – 2). Rehydration applica-

tion regained these parameters of desiccation stressed ferns

compared to the stressed plants. A signi cant correlation

was observed in 2 d desiccated ferns compared with in

terms of marginal necrosis in the fronds.

Generally, the chlorophyll  uorescence parameters

are ideal markers of PSII and photosynthetic activity

in stressed plants (Kifah and Jaroslav, 2015). Maximum

quantum ef cacy of PSII (F

) refers the photosynthetic

ef ciency of the leaf (Maghsoudi et al., 2015). Thus, F

is widely used to evaluate stress-induced impairment in

Table 1: Pigment content in the fern treated with desiccation and rehydration stress (D - desiccated; R- rehydrated)

Control 2D 2R 4D 4R 6D 6R 8D 8R 10D 10R

Chl a(mg/g) 0.226 0.197 0.261 0.240 0.285 0.237 0.309 0.284 0.325 0.21 0.226

Chl b(mg/g) 0.126 0.109 0.123 0.136 0.142 0.166 0.217 0.191 0.224 0.128 0.127

Chl a/chl b 1.79 1.8 2.12 1.76 2.00 1.42 1.42 1.48 1.45 1.64 1.78

Total chl 0.352 0.306 0.384 0.376 0.427 0.403 0.526 0.475 0.549 0.338 0.353

Carotenoids(mg/g) 0.051 0.057 0.066 0.062 0.059 0.083 0.113 0.070 0.088 0.075 0.089

Tot chl/tot car 6.9 5.37 5.81 6.06 7.23 4.85 4.65 6.78 6.23 4.50 3.97

442 PHOTOCHEMICAL EFFICACY ANALYSIS USING CHLOROPHYLL FLUORESCENCE BIOSCIENCE BIOTECHNOLOGY RESEARCH COMMUNICATIONS

Kavitha and Murugan

the chloroplast. The present results revealed that desic-

cation stress resulted an initial reduced F

(Table – 2)

which may be due to the decreased ef ciency of energy

transfer from the antennae to the reaction centers and /

or inhibition of the activity circumscribed around PSII

reaction centers (Abdeshahian et al., 2010). The decline

in F

suggests the possible damage occurred to PSII

(Yamane et al., 2008). Amirjani (2010) reported that the

decline in F

might retard the rate of photosynthesis,

thereby inhibiting plant growth and development.

Lepedu et al., (2012) reported a reduction in photo-

chemistry among drought-stressed cowpea plants but,

its overall photosynthetic ef ciency remained unaf-

fected. The desiccation induced suppression noticed

initially (2d after desiccation) with the apparent pho-

tosynthetic electron transport rate (ETR) revealing the

initial imbalance of the fern against drought stress with

an increase of qN. This may be to counter balance the

excessive light energy with reduction in photosynthetic

rate. Thus, the photochemical down-regulation related

with the stress payway to reduction in ETR (Arabzadeh,

2013).

In this study, 2 day desiccation increased the non-

photochemical quenching (qN) but later qN was main-

tained at optimal level. Yamane et al., (2008) reported

chloroplast damage in rice due to photo-inhibition that

was induced by high salinity condition. Photo-inhibi-

tion may also retard and reverse the reduction in pho-

tosynthetic ef cacy that partially impairs transforma-

tion of radiation energy into net assimilatory products.

Hazem et al., (2011) reported the effect of salt stress on

photosystem II ef ciency and CO

assimilation of two

Syrian barley landraces. Further, the excessive light

energy could be dissipated as heat through qN. Cha-um

(2013) suggested that adequate supply of CO

for car-

bon reactions may prevent photoinhibition, which has

been re ected as signi cantly higher F

value in the

cowpea plants and others against salinity stress. In the

present study, desiccation initially reduced the F

val-

ues, but was subsequently maintained signi cantly in

the fern during 4, 6, 8

days of desiccation.There were

different interpretations regarding the variation in the

level of F

such as an estimation of the relative size of

the antenna pigment complexes of the PSII (Kadir and

Von Weihe, 2007).

Contreras-Porcia et al., (2011) also suggested that in

Porphyra columbina an increase in F

leads to symp-

tom of damage to the PSII reaction center, resulting in

a reduction in absorbed light and a subsequent increase

in unused emitted light. The results of present study

showed that desiccation stress reduced F

initially, but

maintained the photosynthetic quenching. Maghsoudi

et al., (2015) also showed a reduction in F

but an

increase in F

in wheat seedlings under water de -

cit stress. Additionally, De Lucena et al., (2012) reported

in mango that a reduction in F

ratio, under stress

conditions, is often an indicator of photoinhibition or

injury to PSII complex. Therefore, the increase in non-

photochemical quenching can be expected under desic-

cation stress as a result of decrease in the utilization

of light energy due to a drought-induced reduction in

PSII activity (F

). This might explain the increase in

the value of F

in silicon treated wheat under water-

de cit conditions (Maghsoudi et al., 2015).

Several studies have reported stress-induced increases

in the values of F

and qN and decreases in F

qP, F

, and cpPSII (Pellegrini et al., 2011; De Lucena

et al., 2012; Contreras-Porcia et al., 2011). In the fern,

D. linearis, under desiccation stress at 4, 6, 8 days sig-

ni cantly increased the value of F

as well as that

of qP (Table – 2). Reductions in the values of F

and

qN and increases in F

, qP, F0, and  PSII have been

reported in many plants under abiotic stress conditions

(Pellegrini et al., 2011; De Lucena et al., 2012; Contreras-

Porcia et al., 2011). Similarly, Al-aghabary et al., (2004)

have reported in tomato that addition of silicon to the

root growing medium of salt-stressed plants enhanced

as well as improved the photochemical ef ciency

of PSII through antioxidant machineries.

CONCLUSION

The present results revealed that the ferns can withstand

desiccation via maximum quantum yield of PSII and pho-

tochemical quenching. The chlorophyll  uorescence and

photosynthetic pigments suggest enhanced drought toler-

ance of the ferns. The fern alleviate the adverse effects of

desiccation through the pigments and also effective ROSs

scavenging mechanism. Further studies are warranted at

molecular level to analyze the antioxidant enzymes and

stress protein up regulation in the fern.

Table 2: Chlorophyll  uorescence parameters

control 2 D 4D 6D 8D 10D

121 158 133 127 125 123

612 410 584 610 629 512

491 252 451 483 504 389

0.80 0.61 0.77 0.79 0.80 0.76



0.67 0.50 0.62 0.67 0.68 0.60

qP 0.82 0.71 0.8 0.83 0.84 0.78

NPQ 0.68 0.76 0.65 0.66 0.65 0.70

ERT 78 66 75 78 79 70

0.198 0.38 0.22 0.208 0.199 0.24

BIOSCIENCE BIOTECHNOLOGY RESEARCH COMMUNICATIONS PHOTOCHEMICAL EFFICACY ANALYSIS USING CHLOROPHYLL FLUORESCENCE 443

Kavitha and Murugan

ACKNOWLEDGEMENT

The authors thank the University Grant Commission

regional of ce, Bangalore for providing FDP status to

the teacher fellow for completing the Ph.D. work (Order

No.F.No.FIP/12th plan/KLKE021 TF 06).

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