Exogenous Glycinebetaine and Salicylic Acid Application Improves Water Relations, Allometry and...

DROUGHT STRESS

Exogenous Glycinebetaine and Salicylic Acid ApplicationImproves Water Relations, Allometry and Quality of HybridSunflower under Water Deficit ConditionsM. Hussain1, M. A. Malik1, M. Farooq1, M. B. Khan2, M. Akram1 & M. F. Saleem1

1 Department of Agronomy, University of Agriculture, Faisalabad, Pakistan

2 University College of Agriculture, Bahauddin Zakariya University, Multan, Pakistan

Introduction

Water paucity is a severe environmental constraint to

crop productivity worldwide. Drought-induced loss in

crop yield perhaps exceeds the loss from all other causes,

as both severity and duration of stress are critical (Farooq

et al. 2008a). Drought stress reduces crop growth rate

(CGR) and yield regardless of the growth stage at which

it occurs in arable crops including sunflower (Jensen and

Mogenson 1984).

Under severe water-deficiency, cell elongation of higher

plants can be inhibited by interruption of water flow

from the xylem to the surrounding elongating cells

(Nonami 1998). Impaired mitosis, cell elongation and

expansion result in reduced plant height, leaf area and

crop growth under drought (Nonami 1998, Kaya et al.

2006). Drought stress disturbs the plant water relations,

photosynthesis, assimilate translocation and economic

yield in filed crops (Siddique et al. 2000, Atteya 2003,

Farooq et al. 2008a,b, Hussain et al. 2008a,b). One of the

most common stress tolerance strategies in plants is the

overproduction of different types of compatible organic

solutes (Serraj and Sinclair 2002). Compatible solutes are

of low molecular weight, highly soluble compounds that

are usually non-toxic even at high cytosolic concentra-

tions. Generally, they protect plants from stress through

Keywords

drought stress; exogenous application;

glycinebetaine; growth; salicylic acid;

sunflower; water relations; water use

efficiency

Correspondence

Dr Muhammad Farooq

Department of Agronomy, University of

Agriculture, Faisalabad 38040, Pakistan

Tel.: +92 41 9200161-9/2917

Fax: +92 41 9200605

Email: [email protected]

Accepted November 12, 2008

doi:10.1111/j.1439-037X.2008.00354.x

Abstract

Limited water availability hampers the sustainability of crop production. Exog-

enous application of glycinebetaine (GB) and salicylic acid (SA) has been found

very effective in reducing the adverse effects of water scarcity. This study was

conducted to examine the possible role of exogenous GB and SA application in

improving the growth and water relations of hybrid sunflower (Helianthus

annuus L.) under different irrigation regimes. There were three levels of irriga-

tion, viz. control (normal irrigations), water stress at budding stage (irrigation

missing at budding stage) and water stress at flowering stage (FS) (irrigation

missing at FS). GB and SA were applied exogenously at 100 and 0.724 mm

respectively, each at the budding and FS. Control plants did not receive appli-

cation of GB and SA. Water stress reduced the leaf area index (LAI), leaf area

duration (LAD), crop growth rate (CGR), leaf relative water contents, water

potential, osmotic potential, turgor pressure, achene yield and water use

efficiency. Nevertheless, exogenous GB and SA application appreciably

improved these attributes under water stress. However, exogenous GB applica-

tion at the FS was more effective than other treatments. Net assimilation rate

was not affected by water stress as well as application of GB and SA. The

protein contents were considerably increased by water stress at different growth

stages, but were reduced by exogenous GB and SA application. The effects of

water stress and foliar application of GB were more pronounced when applied

at FS than at the budding stage. Moreover, exogenous GB application was only

advantageous under stress conditions.

J. Agronomy & Crop Science (2009) ISSN 0931-2250

ª 2009 The Authors98 Journal compilation ª 2009 Blackwell Verlag, 195 (2009) 98–109

different means such as contribution towards osmotic

adjustment, detoxification of reactive oxygen species,

stabilization of membranes and native structures of

enzymes and proteins (Farooq et al. 2009). Glycinebetaine

(GB) and proline have been the most extensively studied

compatible organic solutes in this regard. Despite some

controversy, many physiological roles have been assigned

to free proline including stabilization of macromolecules,

a sink for excess reductant and a store of carbon and

nitrogen for use after relief of water deficit (Zhu 2002).

Proline contents were increased under drought stress in

pea cultivars (Alexieva et al. 2001).

Many studies demonstrate that GB plays an important

role in enhancing plant tolerance under a range of abiotic

stresses including drought (Quan et al. 2004). The intro-

duction of genes synthesizing GB into non-accumulators

of GB proved to be effective in increasing tolerance to

various abiotic stresses (Sakamoto and Murata 2002).

Naidu et al. (1998) reported that cotton cultivars adapted

to water-stress conditions accumulated higher GB than

the non-adapted ones under drought. In addition to

direct protective roles of GB either through positive

effects on enzyme and membrane integrity or as an

osmoprotectant, GB may protect cells from environmen-

tal stresses indirectly by participating in signal transduc-

tion pathways (Subbarao et al. 2000).

Glycinebetaine has been shown to protect functional

proteins, enzymes (e.g. Rubisco) and lipids of the photo-

synthetic apparatus and to maintain electron flow

through thylakoid membranes (Xing and Rajashekar

1999, Allakhverdiev et al. 2003). Furthermore, even high

concentration of it does not exert adverse effects on

protein structure, enzyme activities, membrane functions

and metabolic processes occurring within the cell (Rhodes

and Hanson 1993). GB-synthesizing transgenic plants can

accumulate GB to a level much lower than natural accu-

mulators, but confer tolerance to various abiotic stresses

including salt, drought, high and low temperatures

(Rhodes and Hanson 1993). It seems that protective role

of GB does not only depend on its osmoprotective role

but also on its other specific physicochemical and physio-

logical effects on the stress responses of plants.

All higher plants are unable to accumulate GB natu-

rally, but some transgenic plants capable of accumulating

GB have been made successfully (Sakamoto and Murata

2002) at lower levels. Exogenous application of GB to

GB-non-accumulators has been taken as an alternative to

improve the stress tolerance. For example, Ma et al.

(2006) reported that GB-treated plants maintained a

higher net photosynthetic rate during drought stress than

non-GB treated. Farooq et al. (2008b) reported that seed

priming with GB can improve the chilling tolerance in

hybrid maize by activation of antioxidant system. In

another study, exogenous GB application successfully

improved the drought tolerance in rice (Farooq et al.

2008a).

Although the role of endogenously produced salicylic

acid (SA) is still inscrutable, salicylic acid potentiates the

generation of reactive oxygen species in photosynthetic

tissues of Arabidopsis thaliana during osmotic stress

(Borsani et al. 2001). There are several reports available

highlighting the role of SA to induce drought stress toler-

ance in wheat (Singh and Usha 2003, Waseem et al. 2006,

Horvath et al. 2007). Recently, Hussain et al. (2008a)

found that exogenous application of SA can improve

yield and yield related traits in sunflower under drought

stress. While in another study, Farooq et al. (2008c)

reported that seed priming with SA can induce chilling

tolerance in hybrid maize mainly by the activation of

antioxidant system.

In view of gradually depleting irrigation water resources

throughout the world, it is highly imperative to investi-

gate the effects and mechanisms of drought in sunflower.

Although the general effects of drought in sunflower

growth are fairly well known, the primary effects of water

deficit on growth and water relations in sunflower are not

well-understood. It is hypothesized that exogenous GB

and SA application may alleviate the adversities of

drought stress, maintain plant tissue water status and

promote growth and allometric responses under drought

stress.

Materials and Methods

The study was conducted at the Agronomic Research

Area, University of Agriculture, Faisalabad (31.25�N,

73.09�E and 183 m a. s. l.), during two consecutive years

viz. 2006 and 2007. Experimental soil was well drained,

sandy clay loam, with pH 7.8, 0.32 mS cm)1 total

exchangeable salts and 0.75 % organic matter and the soil

belongs to Lyallpur soil series [aridisol-fine-silty, mixed,

hyperthermic Ustalfic, Haplarged in the United States

Department of Agriculture (USDA) classification and

Hyplic Yermosols in the Food and Agriculture Organiza-

tion (FAO) classification].

Sunflower hybrid Hysun-33 was used as experimental

material. The experiment was laid out in randomized

complete block design with split plot arrangement and

was replicated three times with net plot size of

3 m · 5 m. Irrigation levels and GB and SA applications

were randomized in main plots and sub-plots respec-

tively.

Irrigation levels included in the study were standard

[CKI = normal irrigations (no water stress), vegetative

stage (VS) = water stress at budding stage (irrigation

missing at budding stage) and FS = water stress at flower-

Sunflower under Water Deficit Conditions

ª 2009 The AuthorsJournal compilation ª 2009 Blackwell Verlag, 195 (2009) 98–109 99

ing stage (irrigation missing at FS)]. GB was applied at

100 mm each at budding (VGB) and FSs (FGB), while SA

was applied at 0.724 mm each at budding (VSA) and

flowering stage (FSA). In control plots (CKF), neither GB

nor SA was applied. The measured amount of water was

applied using cut-throat flume according to following

formulae given by Buland et al. (1994):

QT = AD

where Q is discharge rate from flume, T is time, A is area

to be irrigated and D is depth of irrigation water applied.

Under well-watered conditions, 300 mm (four irriga-

tions, 1 = 75 mm) and under both stressed conditions,

225 mm (three irrigations, 1 = 75 mm) water was

applied. Weather data during the whole course of study

in both the years are given in Table 1. No rainfall was

received during stress period in both years.

Prior to seedbed preparation, pre-soaking irrigation of

10 cm was applied. When soil reached a workable mois-

ture level, the seedbed was prepared by cultivating the

field for 2–3 times with tractor-mounted cultivator each

followed by planking. Sunflower hybrid Hysun-33 was

sown on 14 and 17 February during 2006 and 2007

respectively. Sowing was done with the help of dibbler

using seed rate of 8 kg ha)1 maintaining row to row

distance of 75 cm and plant to plant distance of 25 cm.

Fertilizers were applied at 150 kg N and 100 kg P2O5 ha)1

in the form of urea and diammonium phosphate (DAP).

Half of nitrogen and whole of phosphorus were applied

at sowing, whereas the remaining nitrogen was applied

with first irrigation. Field was kept weed-free by hoeing

and manual weeding. Earthing up was done 30 days after

sowing (DAS).

Data on water relations traits were recorded at 87 DAS

(20 days after the water stress at FS and exogenous appli-

cation of GB and SA at FS). Leaf water potential (ww)

was determined using pressure chamber (Soil Moisture

Equipment Corp., Santa Barbara, CA, USA) from penulti-

mate leaf. Frozen leaf tissues were thawed, sap expressed,

centrifuged at 5000 g and osmotic potential (ws) deter-

mined using an osmometer (Digital Osmometer, Wescor,

Logan, UT, USA). Leaf pressure potential (wp) was com-

puted as a difference of ww and ws. To determine relative

water contents (RWC), fresh leaves (0.5 g) (Wf) were

weighed to get fresh weight. Later, these leaves were

floated on water for 4 h and saturated weight (WS) was

determined. These leaves were dried for 24 h at 85 �C

to determine dry weight (Wd). RWC (%) were calculated

as:

RWC ¼ (Wf �WdÞ=ðWS �WdÞ � 100%

Water use efficiency (WUE) was calculated as the ratio

between achene yield and water applied (Viets 1962).

Plant height was recorded at maturity. Leaf area was mea-

sured using a leaf area meter (DT Area Meter, model

MK2) at a regular interval of 15 days. Leaf area index

(LAI) was calculated using the formula given by Watson

(1947). CGR and net assimilation rate (NAR) were

calculated using the formulae of Hunt (1978).

The crop was harvested when fully ripe to determine

achene and biological yields and harvest index. The

achene yield was adjusted to 10 % moisture content and

presented in kg ha)1. Achene yield data are taken from

Hussain et al. (2008a). For achene protein estimation,

nitrogen was determined according to Kjeldahl method

(Bremner 1964). Crude proteins were estimated from the

nitrogen contents.

The data were statistically analysed using the computer

software mstat-c (Department of Plant and Soil Sciences,

Michigan State University, East Lansing, MI, USA).

Analysis of variance technique was employed to test the

overall significance of the data, while the least significant

difference (LSD) test (at P = 0.05) was used to compare

the differences among treatment means.

Results

Plant water relations and WUE

Drought stress at both the stages i.e. budding (vegetative)

and FSs had negative effects on plant water relation

parameters and WUE (Table 2), but these attributes were

appreciably improved by the foliar application of GB and

SA (Table 3) under stress conditions during both years.

Table 1 Weather data during the course of

study

Months

Mean monthly

temperature (�C)

Mean monthly

relative humidity (%)

Total monthly

rainfall (mm)

2006 2007 2006 2007 2006 2007

February 20.28 15.5 52.36 67.07 14.6 55.90

March 21.00 19.35 57.00 46.97 37.00 41.30

April 25.00 35.13 57.00 35.13 0.00 0.00

May 29.50 24.97 57.00 24.97 24.00 16.10

Hussain et al.


Table 2 Effect of drought stress levels on crop water relations and water use efficiency in sunflower

Treatments

RWC (%)

Water potential

()MPa)

Osmotic potential

()MPa)

Turgor potential

(MPa) WUE (kg m)3)

2006 2007 2006 2007 2006 2007 2006 2007 2006 2007

CKI 82.44 a 82.12 a 0.71 c 0.75 c 1.27 c 1.29 c 0.56 a 0.54 a 0.73 ab 0.77 b

VS 75.30 b 75.62 b 0.90 b 0.91 b 1.35 b 1.36 b 0.45 b 0.44 b 0.77 a 0.83 a

FS 72.84 c 73.33 b 1.07 a 1.09 a 1.45 a 1.47 a 0.38 c 0.38 c 0.69 b 0.74 b

LSD at 0.05 2.318 4.63 0.057 0.046 0.042 0.016 0.042 0.016 0.045 0.032

CKI, normal irrigations (no drought stress); VS, irrigation missing at budding stage (drought stress at budding stage); FS, irrigation missing at

flowering stage (drought stress at flowering stage); WUE, water use efficiency; LSD, least significant difference. Values with similar alphabets in a

column do not differ significantly at P = 0.05.

Table 3 Effect of exogenous application of GB and SA on water relations and water use efficiency in sunflower

Treatments

RWC (%)

Water potential

()MPa)

Osmotic potential

()MPa)

Turgor potential

(MPa) WUE (kg m)3)

2006 2007 2006 2007 2006 2007 2006 2007 2006 2007

CKF 74.66 b 76.21 0.94 a 0.97 a 1.31 b 1.32 c 0.37 c 0.35 c 0.69 0.75 e

VGB 77.39 a 76.89 0.88 b 0.92 b 1.36 a 1.38 b 0.48 b 0.46 b 0.72 0.79 b

FGB 78.32 a 78.73 0.86 b 0.88 c 1.37 a 1.40 a 0.52 a 0.51 a 0.76 0.83 a

VSA 76.96 a 77.16 0.88 b 0.90 bc 1.38 a 1.38 b 0.48 b 0.48 b 0.73 0.77 d

FSA 76.97 a 76.12 0.89 b 0.92 c 1.36 a 1.38 b 0.48 b 0.46 b 0.73 0.77 c

LSD at 0.05 1.748 ns 0.043 0.038 0.036 0.014 0.039 0.025 ns 0.009

CKF, control (no application); VGB, exogenous application of 100 mm GB at budding stage; FGB, exogenous application of 100 mm GB at flower-

ing; VSA, exogenous application of 0.724 mM SA at budding stage; FSA, exogenous application of 0.724 mM SA at flowering stage; WUE, water

use efficiency; LSD, least significant difference. Values with similar alphabets in a column do not differ significantly at P = 0.05.

Table 4 Interactive effect of irrigation levels and exogenous application of GB and SA on water relations and water use efficiency in sunflower

Treatments

RWC (%)

Water potential

()MPa)

Osmotic potential

()MPa)

Turgor potential

(MPa) WUE (kg m)3)

2006 2007 2006 2007 2006 2007 2006 2007 2006 2007

CKICKF 80.00 81.29 0.73 b 0.77 ab 1.25 a 1.28 a 0.52 bc 0.51 bc 0.72 0.76 h

CKIVGB 82.43 81.09 0.72 ab 0.75 ab 1.29 a 1.29 a 0.57 a 0.55 ab 0.72 0.76 h

CKIFGB 84.12 84.21 0.68 a 0.73 ab 1.27 a 1.31 ab 0.59 a 0.59 a 0.75 0.79 e

CKIVSA 81.94 81.38 0.72 ab 0.72 a 1.29 a 1.30 ab 0.57 a 0.58 a 0.71 0.77 g

CKIFSA 83.72 82.61 0.71 ab 0.78 b 1.26 a 1.29 a 0.55 ab 0.51 bc 0.75 0.79 e

VSCKF 73.38 74.59 0.95 d 0.97 d 1.29 a 1.29 a 0.35 f 0.32 e 0.71 0.78 f

VSVGB 76.85 76.77 0.88 c 0.91 c 1.34 b 1.37 c 0.46 d 0.46 c 0.76 0.86 b

VSFGB 76.22 75.35 0.87 c 0.89 c 1.36 bc 1.37 c 0.49 cd 0.49 c 0.79 0.88 a

VSVSA 74.92 76.80 0.89 c 0.92 cd 1.37 bc 1.39 c 0.48 cd 0.47 c 0.81 0.81 c

VSFSA 75.14 74.60 0.89 c 0.88 c 1.37 bc 1.35 bc 0.48 cd 0.47 c 0.75 0.80 d

FSCKF 70.59 72.75 1.15 f 1.16 g 1.39 c 1.39 c 0.24 g 0.23 f 0.64 0.70 k

FSVGB 72.90 72.81 1.04 e 1.11 f 1.45 d 1.49 d 0.40 e 0.38 d 0.68 0.73 j

FSFGB 74.64 76.63 1.02 e 1.04 e 1.50 e 1.51 d 0.48 cd 0.47 c 0.73 0.81 c

FSVSA 74.01 73.31 1.05 e 1.06 ef 1.45 d 1.45 d 0.40 e 0.39 d 0.68 0.73 j

FSFSA 72.04 71.17 1.06 e 1.09 ef 1.46 d 1.49 d 0.40 e 0.40 d 0.70 0.74 i

LSD at 0.05 ns ns 0.037 0.050 0.042 0.053 0.045 0.053 ns 0.002


flowering stage (drought stress at flowering stage); CKF, control (no application); VGB, exogenous application of 100 mM GB at budding stage;

FGB, exogenous application of 100 mM GB at the flowering; VSA, exogenous application of 0.724 mM SA at budding stage; FSA, exogenous

application of 0.724 mM SA at flowering stage; LSD, least significant difference. Values with similar alphabets in a column do not differ

significantly at P = 0.05.



Maximum relative leaf water contents (LRWC) were

observed in CKI (normal irrigation) against the minimum

from FS (water stress at FS) (Table 2) during both years.

Nevertheless, GB and SA application improved LRWC.

Maximum LRWC were recorded in FGB (foliar applica-

tion of GB at FS), but it was statistically at par with all

other treatments except CKF (control) having minimum

LRWC during 2006. In 2007, foliar application of GB and

SA had no significant effect on LRWC (Table 3). The

interaction between the two factors was also non-signifi-

cant (Table 4).

Irrigation levels considerably affected leaf water poten-

tial and osmotic potential during both years and statisti-

cally maximum water potential and osmotic potentials

were recorded under well-watered conditions (CKI),

whereas a minimum was recorded from water stress at

FS (Table 2). Exogenous applications of GB and SA

appreciably affected leaf water potential and osmotic

potential during both years. Maximum leaf water poten-

tial was recorded from exogenous application of GB at

FS (FGB), which was statistically at par with all other

treatments except control (CKF i.e. no application)

having minimum water potential during 2006. In 2007,

almost the same trend was found, where maximum leaf

water potential was found in FGB (exogenous applica-

tion of GB at FS), but it was statistically similar with

VSA (exogenous application of SA at vegetative (bud-

ding) stage) and FSA (exogenous application of SA at

FS) (Table 3). Interactive effect of I · F was significant

during both years. During 2006, maximum leaf water

potential was observed in CKIFGB (normal irrigations;

exogenous application of GB at FS), but it was at par

with CKIVGB, CKIVSA and CKIFSA against the mini-

mum in FSCKF (water stress at FS; no application of

GB and SA). In 2007, maximum leaf water potential was

observed in CKIFSA (normal irrigations; exogenous

application of SA at FS), but it was statistically at par

with CKICKF, CKIVGB, CKIFGB and CKIVSA against

the minimum in FSCKF (water stress at FS; no applica-

tion of GB and SA) (Table 4). Maximum negative osmo-

tic potential was observed from applications of GB at FS

(FGB) in both years, but it was statistically at par with

all other treatments except control (CKF) in 2006

(Table 3). Interactive effect of irrigation levels (I) and

exogenous applications of GB and SA (F), I · F, was

significant during both years. Statistically more negative

leaf osmotic potential was observed in FSFGB (water

stress at FS; exogenous application of GB at FS) and less

negative leaf osmotic potential was recorded in CKICKF

(normal irrigations; no application of GB and SA), but it

was statistically at par with CKIVGB, CKIFGB, CKIVSA,

CKIFSA and VSCKF during both years (Table 4).

Water stress considerably affected leaf turgor potential

during the years 2006 and 2007. Statistically more leaf

turgor potential was recorded when crop faced no water

stress (CKI) and less leaf turgor potential resulted when

crop faced water stress at FS (Table 2). Maximum leaf

turgor potential resulted when crop was grown under the

application of GB at FS (FGB) and minimum leaf turgor

potential resulted when crop did not receive any exoge-

nous applications of GB and SA at any growth stage

(CKF) during both years (Table 3). Interactive effect of,

I · F, was significant during both years. During 2006,

maximum leaf turgor potential was observed in CKIFGB

(normal irrigations; exogenous application of GB at FS),

but it was statistically at par with CKIVGB, CKIVSA and

CKIFSA against the minimum turgor potential, which

was recorded in FSCKF (water stress at FS; no application

of GB and SA). In 2007, maximum leaf turgor potential

was observed in CKIFGB (normal irrigations; exogenous

application of GB at FS), but it was statistically at par

with CKIVGB and CKIVSA (normal irrigations; exoge-

nous application of SA at budding stage) against the

minimum in FSCKF (water stress at FS; no application of

GB and SA) (Table 4).

Water stress at vegetative (budding) stage had the high-

est WUE during both years, but statistically at par with

control (CKI) in 2006 against the minimum WUE in case

of water stress at FS, but it was statistically at par with

normal irrigations (CKI) during both years (Table 2).

Table 5 Effect of drought stress on net assimilation rate, yield and quality in sunflower

Treatments

NAR (g m)2)

Plant height at

maturity (cm)

Achene yield

(kg ha)1)

Biological yield

(kg ha)1)

Harvest index

(%)

Achene protein

contents (%)

2006 2007 2006 2007 2006 2007 2006 2007 2006 2007 2006 2007

CKI 7.91 7.46 191.9 a 199.9 a 2736 a 2771 a 13 120 a 12 540 a 20.88 a 21.32 21.93 c 22.85 c

VS 7.22 7.58 175.7 c 184.0 b 2294 b 2337 b 10 320 c 9880 b 22.25 a 23.12 23.32 b 23.99 b

FS 7.02 7.21 184.3 b 197.0 a 2075 c 2095 c 10 720 b 10 060 b 19.37 b 19.72 24.85 a 24.71 a

LSD at 0.05 ns ns 1.86 6.53 72.73 79.59 329.5 1026 1.38 ns 1.06 0.35


flowering stage (drought stress at flowering stage); WUE, water use efficiency; LSD, least significant difference. Values with similar alphabets in a

column do not differ significantly at P = 0.05.

Hussain et al.


Exogenous application of GB and SA had non-significant

effect on WUE in 2006 and significant effect during the

year 2007. During 2007, maximum WUE was observed

with GB application at flowering (FGB) against the mini-

mum WUE in CKF (control) (Table 3). Interactive effect

of irrigation levels (I) and exogenous applications of GB

and SA (F), I · F, on WUE was non-significant during

2006 and was significant in 2007. Maximum WUE was

recorded in VSFGB (water stress at budding stage; foliar

application of GB at budding stage) against the minimum

WUE recorded in FSCKF (Table 4).

Achene yield

Maximum achene yield was obtained with no stress CKI

(no water stress), whereas minimum achene yield was

noted from water stress at flowering (FS) during both

years (Table 5). In the years 2006 and 2007, maximum

achene yield was produced with GB application at flower-

ing (FGB), which was statistically at par with SA applica-

tion at flowering (FSA) in 2006, whereas minimum

achene yield was recorded from CKF (control) during

both years (Table 6). Interactive effect of irrigation levels

Table 6 Effect of exogenous application of GB and SA on net assimilation rate, yield and quality in sunflower

Treatments

NAR (g m)2)

Plant height at

maturity (cm)

Biological yield

(kg ha)1)

Achene yield

(kg ha)1)

Harvest index

(%)

Achene protein

contents (%)

2006 2007 2006 2007 2006 2007 2006 2007 2006 2007 2006 2007

CKF 7.91 7.48 184.2 193.6 10 680 c 10 660 c 2255 c 2301 c 21.10 21.60 24.52 a 25.10 a

VGB 6.95 7.41 183.8 193.0 11 530 ab 11 270 b 2343 b 2404 b 20.34 21.39 22.50 b 23.84 b

FGB 7.50 6.85 183.1 194.4 11 820 a 11 690 a 2472 a 2533 a 20.97 21.73 23.49 ab 23.52 bc

VSA 7.48 7.44 184.8 194.1 11 440 b 11 354 bc 2378 b 2379 b 20.83 21.00 22.47 b 23.41 c

FSA 7.41 7.75 183.9 193.0 11 464 b 11 260 bc 2394 ab 2387 b 20.93 21.22 23.83 ab 23.39 c

LSD at 0.05 ns ns ns ns 316.6 266 85.35 38.96 ns ns 1.96 0.395

CKF, control (no application); VGB, exogenous application of 100 mM GB at budding stage; FGB, exogenous application of 100 mM GB at

flowering; VSA, exogenous application of 0.724 mM SA at budding stage; FSA, exogenous application of 0.724 mM SA at flowering stage; WUE,

water use efficiency; LSD, least significant difference. Values with similar alphabets in a column do not differ significantly at P = 0.05.

Table 7 Interactive effect of irrigation levels and exogenous application of GB and SA on net assimilation rate (NAR), yield and quality of

sunflower

Treatments

NAR (g m)2)

Plant height at

maturity (cm)

Biological yield

(kg ha)1)

Achene yield

(kg ha)1)

Harvest index

(%)

Achene protein

contents (%)

2006 2007 2006 2007 2006 2007 2006 2007 2006 2007 2006 2007

CKICKF 7.90 8.10 191.7 202.2 12 425 12 418 2704 ab 2715 c 21.78 21.88 22.49 23.32 e

CKIVGB 6.66 7.96 191.3 195.0 13 115 12 858 2695 ab 2717 c 20.56 21.13 21.25 23.21 e

CKIFGB 7.94 7.11 192.3 203.1 13 688 13 455 2809 a 2846 a 20.53 21.16 21.87 22.42 f

CKIVSA 7.68 7.78 195.0 200.3 13 018 13 151 2645 b 2759 bc 20.36 20.99 21.04 22.08 f

CKIFSA 7.14 8.63 189.3 198.9 13 346 13 154 2827 a 2817 ab 21.18 21.42 23.00 23.21 e

VSCKF 7.71 7.32 175.0 181.7 9453 9605 2126 ef 2206 f 22.50 22.99 25.38 25.19 b

VSVGB 7.28 7.01 178.7 187.4 10 507 10 246 2288 cd 2436 d 21.76 23.78 22.74 23.71 de

VSFGB 7.61 6.62 173.7 182.5 10 707 10 582 2370 cd 2481 d 22.14 23.45 23.66 23.45 de

VSVSA 7.40 7.59 176.7 185.0 10 820 10 143 2440 c 2311 e 22.58 22.79 21.80 24.19 d

VSFSA 7.90 7.57 174.3 183.4 10 096 9964 2247 de 2250 ef 22.26 22.58 23.00 23.43 de

FSCKF 7.67 7.03 186.0 197.1 10 172 9953 1934 g 1983 h 19.02 19.92 25.70 26.79 a

FSVGB 6.90 7.26 181.3 196.7 10 957 10 703 2048 fg 2060 g 18.70 19.26 23.50 24.59 bc

FSFGB 6.96 6.79 183.3 197.7 11 057 11 039 2237 de 2271 ef 20.24 20.57 24.94 24.69 bc

FSVSA 7.34 6.96 182.7 197.0 10 477 10 748 2048 fg 2065 g 19.56 19.21 24.58 23.96 cde

FSFSA 7.19 7.05 188.0 196.6 10 942 10 660 2110 ef 2094 g 19.36 19.65 25.50 23.54 de

LSD at 0.05 ns ns ns ns ns ns 148 67.47 ns ns ns 0.685

CKI, normal irrigations (no drought stress); VS, irrigation missing at budding stage (drought stress at budding stage); FS, irrigation missing at flow-

ering stage (drought stress at flowering stage); CKF, control (no application); VGB, exogenous application of 100 mM GB at budding stage; FGB,

exogenous application of 100 mM GB at flowering; VSA, exogenous application of 0.724 mM SA at budding stage; FSA, exogenous application

of 0.724 mM SA at flowering stage; LSD, least significant difference; NAR, net assimilation rate. Values with similar alphabets in a column do not

differ significantly at P = 0.05.



(I) and exogenous applications of GB and SA (F) was sig-

nificant during both years. During 2006, maximum

achene yield was obtained in CKIFGB (normal irrigations;

exogenous application of GB at FS), but it was statistically

at par with CKICKF, CKIVGB and CKIFSA against the

minimum achene yield from FSCKF (water stress at FS;

no application of GB and SA), which was at par with

FSVGB and FSVSA. During 2007, maximum achene yield

was obtained in CKIFGB (normal irrigations; exogenous

application of GB at FS), which was at par with CKIFSA

against the minimum achene yield from FSCKI (water

stress at FS; no application of GB and SA) (Table 7).

Plant height

Water stress treatments had a significant effect on plant

height. Maximum plant height was recorded from well-

watered control (CKI) during both years; however, it was

at par with water stress at flowering (FS) during 2007,

whereas the minimum plant height was recorded from

water stress at vegetative (budding) stage (VS) during

both years (Table 5). Exogenous applications of GB and

SA did not affect the plant height appreciably (Table 6).

Furthermore, interactive effect of irrigation levels (I) and

exogenous applications of GB and SA (F), I · F, was not

significant during the years 2006 and 2007 (Table 7).

Biological yield

Maximum biological yield was produced when crop was

grown with normal irrigations (CKI). However, minimum

biological yield was harvested from water stress at VS,

which was at par with FS (water stress at FS) in 2007

(Table 5). In 2006, maximum biological yield was

produced by FGB (exogenous application of GB at FS)

that was similar with VGB against the minimum in con-

trol (CKF). Likewise, in 2007, maximum biological yield

was produced in FGB (exogenous application of GB at

FS) treatment against the minimum in control (CKF),

which was statistically at par with VSA and FSA (exoge-

nous application of SA at budding and FS respectively)


exogenous applications of GB and SA (F), I · F, on

biological yield was non-significant during both years

(Table 7).

Harvest index

Irrigation levels had a significant effect on harvest index

during 2006 and non-significant effect during 2007. In

2006, maximum harvest index was observed from

drought stress at VS, which was similar with normal

irrigation (no water stress) and the lowest harvest index

was recorded from water stress at flowering (FS)

(Table 5). Exogenous applications of GB and SA at differ-

ent growth stages and interactive effect of irrigation levels

(I) and exogenous applications of GB and SA (F), I · F,

had non-significant effect on harvest index during both

years (Tables 6 and 7).

Alleometry

Leaf area index progressively increased and reached the

maximum level at 75 DAS and then declined. At 60 DAS,

Leaf

are

a in

dex

0

1

2

3

4

5

30 45 60 75 90

CKI

VS

FS

0

1

2

3

4

5

30 45 60 75 90

CKI(b)(a)

VS

FS

Days after sowing

Fig. 1 Leaf area index as affected by drought

stress in sunflower during (a) 2006 and (b)

2007. CKI = control, VS = drought stress at

budding stage; FS = drought stress at

flowering stage.

Leaf

are

a in

dex

0

1

2

3

4

5

30 45 60 75 90

CKF

(a) (b)

VGB FGB VSA FSA

0

1

2

3

4

5

30 45 60 75 90

CKF VGB FGB VSA FSA

Days after sowing

Fig. 2 Leaf area index as affected by foliar

application of GB and SA in sunflower during

(a) 2006 and (b) 2007. CKF = control (no GB

and SA application); VGB = exogenous

application of GB at flowering stage;

FGB = exogenous application of GB at

flowering stage; VSA = exogenous application

of SA at flowering stage; FSA = exogenous

application of GB at flowering stage.

Hussain et al.


normal irrigation (CKI) and water stress at flowering (FS)

had a higher LAI compared with water stress at budding

stage (VS). At 75 and 90 DAS, CKI (no water stress) had

maximum LAI against the minimum LAI in case of water

stress at flowering (FS) during the years 2006 and 2007

(Fig. 1). At 60 DAS, foliar application of GB at vegetative

(budding) stage (VGB) and at 75 DAS, foliar application

of GB at FS (FGB) had high a LAI against the minimum

LAI from CKF (no application) for both years (Fig. 2).

Leaf area duration (LAD) progressively increased with

increase in growth period (Fig. 3). Drought stress severely

affected total LAD of the crop, whereas higher LAD was

noted when the crop faced no water stress (CKI) against

the minimum LAD that resulted when crop faced water

stress at FS during both years, which was at par with the

LAD from water stress at budding stage (VS) during 2006

(Fig. 3). Nonetheless, exogenous applications of GB and

SA improved the LAD. Maximum LAD was observed

from exogenous application of GB at flowering (FGB),

but it was at par with the LAD from foliar application of

GB at VS (VGB). During 2007, maximum LAD was

observed from exogenous application of GB at FS (F2)

against the minimum from no foliar application, which

was at par with the LAD from application of SA at FS

(F4) (Fig. 4).

Crop growth rate was also progressively increased with

time because of increased dry matter accumulation and

reached the maximum level at 75 DAS and then started

declining (Fig. 5). Regarding water stress, at 60 DAS,

normal irrigations (CKI) and water stress at FS had

higher CGR than water stress at vegetative (budding)

stage (VS) during the years 2006 and 2007; however, at

75 and 90 DAS, maximum CGR was observed in normal

irrigations (CKI) against the minimum in FS (water stress

at FS). Similarly, at 60 DAS, foliar application of GB

(VGB) and SA at VS (VSA) had a high CGR than control

CKF (no application), FGB and FSA; and at 75 DAS,

foliar application of GB at FS (FGB) had a high CGR

Leaf

are

a du

ratio

n (d

ays)

0

30

60

90

120

150

180

(a) (b)

0

30

60

90

120

150

180

45 60 75 90

CKI VS FS

45 60 75 90

CKI VS FS

Days after sowing

Fig. 3 Leaf area duration as affected by

drought stress in sunflower during (a) 2006

and (b) 2007. CKI = control; VS = drought

stress at budding stage; FS = drought stress

at flowering stage.

Leaf

are

a du

ratio

n (d

ays)

45 60 75 90

CKF VGB FGB VSA FSA

0

30

60

90

120

150

180

0

30

60

90

120

150

180

(a) (b)

45 60 75 90

CKF VGB FGB VSA FSA

Days after sowing

Fig. 4 Leaf area duration as affected by foliar

application of GB and SA in sunflower during

(a) 2006 and (b) 2007. CKF = control (no GB

and SA application); VGB = exogenous

application of GB at flowering stage;

FGB = exogenous application of GB at

flowering stage; VSA = exogenous application

of SA at flowering stage; FSA = exogenous

application of GB at flowering stage.

Cro

p gr

owth

rat

e(g

m–2

day

–1)

0

5

10

15

20

25

45 60 75 90

CKI

(a) (b)

VSFS

0

5

10

15

20

25

45 60 75 90

CKIVS

FS

Days after sowing

Fig. 5 Crop growth rate as affected by

drought stress in sunflower during (a) 2006

and (b) 2007. CKI = control, VS = drought

stress at budding stage; FS = drought stress

at flowering stage.



against the minimum CGR resulted in CKF (no applica-

tion), VGB and VSA for the years 2006 and 2007 (Fig. 6).

Water stress, exogenous applications of GB and SA and

their interactions had non-significant effect on NAR

(Tables 5, 6 and 7).

Achene protein contents

Maximum achene protein contents were produced when

crop faced water stress at flowering (FS) and minimum

achene protein contents were observed with no water

stress at any growth stage (CKI) during both years

(Table 5). In 2006, maximum achene protein contents

were observed without any foliar application, but it was

at par with FGB and FSA. However, minimum achene

protein contents resulted from the foliar application of

GB at budding stage (VGB), which was similar with all

other treatments except control (no application). Likewise

during 2007, maximum achene protein contents were

noted without any foliar application (CKF) and

minimum from foliar application of SA at FS (FSA),

which was statistically at par with FGB and VSA


exogenous applications of GB and SA (F), I · F, regard-

ing achene protein contents (%) was significant during

2007 and non-significant in 2006 (Table 7). In 2007,

maximum protein contents resulted when crop faced

water stress and no foliar application of GB and SA was

done (FSCKF) against the minimum in CKIVSA (no

water stress and foliar application of SA at budding

stage), but it was at par with CKIFGB.

Discussion

The present investigation suggests that exogenous applica-

tion of GB may help reduce adverse effects of drought in

sunflower. During this study, LRWC were decreased

considerably with water stress, effects of stress were more

pronounced when imposed at flowering during both years

(Table 1). This may be related to higher water require-

ments at flowering (Atteya 2003), but limited availability

disturbed the water relations (Farooq et al. 2009). Never-

theless, foliar application of GB and SA at vegetative and

FS noticeably reversed the effect during 2006 and not in

2007. This temporal difference may be attributed to high

temperature at post-anthesis stage during later year

(Table 1). Improvement in RWC by foliar applications of

GB and SA might be the result of osmotic adjustment

because of improved accumulation of compatible solutes

like proline and GB under stress conditions. Exogenous

application of osmolytes has been found to aid in the

maintenance of tissue water status, principally because of

osmotic adjustment (Farooq et al. 2008a,2009).

Drought stress negatively impaired the crop water rela-

tions because of declined moisture during stress condi-

tions. Active lowering of osmotic potential is generally

considered as an adaptation to maintain turgor under

water limited conditions (Ludlow and Muchow 1990),

which are accomplished by the accumulation of solutes

during osmotic adjustment (Morgan 1984). The results of

this study indicated fall in leaf osmotic potential in

response to water stress, which was more pronounced

when water stress was imposed at FS during both years.

Maintenance of leaf turgor potential by exogenous appli-

cation of GB might be the direct result of having high leaf

water potential and more negative leaf osmotic potential.

Active lowering of leaf osmotic potential by exogenous

application of GB might be the result of higher accumula-

tion of compatible solutes like proline and GB etc., which

then enhance the osmoregulation ability of crop under

water-stress conditions (Farooq et al. 2008b,2009). Osmo-

tic adjustment allows the cell to decrease osmotic poten-

tial and, as a consequence, increases the gradient for

water influx and maintenance of turgor. Improved tissue

water status may be achieved through osmotic adjustment

and/or changes in cell wall elasticity. This is essential for

maintaining physiological activity for extended periods of

drought (Kramer and Boyer 1995). Drought stress also

reduced the plant height, which seems to be the result of

disturbed plant water relations in particular turgor poten-

tial (Table 2; Arnon 1972). Increase in achene yield seems

to be the direct result of improved head diameter,

Cro

p gr

owth

rat

e(g

m–2

day

–1)

0

5

10

15

20

25

(a) (b)

45 60 75 90

CKFVGBFGBVSAFSA

0

5

10

15

20

25

45 60 75 90

CKFVGBFGBVSAFSA

Days after sowing

Fig. 6 Leaf area duration as affected by foliar

application of GB and SA drought stress in

sunflower during (a) 2006 and (b) 2007.

CKF = Control (no GB and SA application);

VGB = exogenous application of GB at

flowering stage; FGB = exogenous application

of GB at flowering stage; VSA = exogenous

application of SA at flowering stage;

FSA = exogenous application of GB at

flowering stage.

Hussain et al.


number of achenes per had and 1000-achene weight (data

not given). It may be the result of maintenance of photo-

synthetic activity owing to GB application. By means of

osmotic adjustment, the organelles and cytoplasmic activ-

ities take place at about a normal pace and help plants to

perform better in terms of growth, photosynthesis and

assimilate partitioning to grain filling (Ludlow and

Muchow 1990, Subbarao et al. 2000). As a mechanism,

osmotic adjustment has been suggested as an important

trait in postponing the dehydration stress in water scarce

environments (Morgan 1990). Externally applied GB can

rapidly penetrate through leaves and be transported to

other organs, where it would contribute to improved

stress tolerance (Makela et al. 1998).

Reduction in biological yield by water stress might be

because of decreased LAI, LAD and CGR as indicated by

the data (Figs 1–6) resulting in reduced photo-assimila-

tion. It is a common adverse effect of water stress on

crop plants in the reduction of fresh and dry biomass

production (Ashraf and O’Leary 1996) and reduced bio-

mass production resulting from water stress had been

observed in almost all genotypes of sunflower (Tahir and

Mehdi 2001). Manivannan et al. (2007) also reported

reduction in fresh and dry weight in sunflower by

imposing water stress. Exogenous application of GB at

FS improved the biological yield by improving LAI, LAD

and CGR (Figs 1–3). This improvement may be attrib-

uted to maintenance of photosynthetic activity by GB

application.

Harvest index indicates the proportionate translocation

of assimilates into economic yield. Water stress

treatments had a significant effect on harvest index. The

lowest harvest index in case of water stress at FS might be

because water shortage at FS increases the chances of

pollen sterility, abortion, pollen germination and fertiliza-

tion in-compatibility, which directly reduce the number

of achenes per head and achene yield. Exogenous applica-

tions of GB and SA also did not considerably affect the

harvest index. The possible explanation might be that the

treatments producing higher achene yield also resulted in

higher biomass production, biological yield. So, harvest

index remained statistically similar because it is a ratio

between economic yield and biological yield.

Water stress at both the stages (vegetative and FS) ham-

pered the crop growth, but it was considerably improved

by the exogenous applications of GB and SA, particularly

by the exogenous application of GB at FS. Water stress

reduced the LAI, LAD and CGR, which may be attributed

to impaired water relations (Table 1). Sadras et al. (1993)

also reported a decrease in leaf expansion rate because of

decreased water potential under water stress in sunflower.

Likewise, total leaf area was decreased considerably in

sorghum by water stress (Yadav et al. 2005).

Reduced LAI resulted in reduced LAD as LAD is

directly calculated from LAI. Similarly improved CGR

under stress conditions might be the result of mainte-

nance of photosynthetic activity because of GB and SA

application. Earlier, Agboma et al. (1997) found that

exogenous GB application protects the photosynthetic

machinery in maize, wheat and sorghum thereby increas-

ing the final yield. Similarly, Makela et al. (1999) reported

that foliar application of GB increased net photosynthesis

and decreased photorespiration in turnip rape plants

under drought and salt stress. Exogenous application of

GB and SA increased the crop growth. It might be due

maintenance of LAI (assimilatory surface) due to high

turgor and sustained photosynthetic ability of the crop by

protecting the photosynthetic machinery from ROS

produced during drought stress and by increasing RuBP

content under drought condition. One of the interesting

findings of the study was that achene protein was reduced

as a result of GB application and increasing water

application, which might be due to dilution because yield

was increased.

In conclusion, water stress negatively affected the plant

water relations and growth of the crop including achene

yield, but exogenous GB and SA application particularly

GB appreciably improved these attributes under water

stress. However, exogenous GB application at the FS was

more effective than other treatments. NAR was not

considerably affected by water stress as well as application

of GB and SA. WUE was increased by missing irrigation

at budding stage, but considerably decreased by missing

irrigation at FS than control. The protein contents were

appreciably increased by increasing water stress at different

growth stages, but were reduced by exogenous GB and SA

application. The effects of water stress and foliar applica-

tion of GB were more pronounced when applied at FS than

at the budding stage. Moreover, exogenous GB application

was advantageous only under stress conditions.

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