Introduction
Onion (Allium cepa L.)
is a monocot vegetable that belongs to the Alliaceae
family. It is ranked second after tomato (Solanum lycopersicum L.) depending upon its
consumption (Brice et al. 1997).
Onion is the prime bulbous vegetable crop cultivated commercially in most parts
of the world (Hanci and Gökçe
2016; Havey and Ghavami
2018). China is the leading onion producer with 17.8 million tons while Turkey
holds 4th position in the world with a production of 2.0 million
tons and covering an area of 105,000 ha (FAOSTAT 2020). Onion is adapted to a
wide range of climatic conditions, but its growth is observed best at mild
climatic conditions without extreme climate (Mubarak and Hamdan
2018). It also requires sufficient moisture content in soil with a pH of
6.0–7.0 for good production (Ibrahim 2017). The crop is consumed as green and
mature forms (Astley 1990). Onions vary in taste from
sweet to mild flavoured and pungent for making an onion aroma as a condiment in
almost every cuisine (Crowther et al. 2005).
Stress is considered as an external environmental factor
that affects the growth and productivity of plants and causes an ultimate
reduction in plant’s yield (Ozturk et al. 2002). Abiotic stress covers a
diverse class ranging from unwanted fluctuations in temperature to drought
caused by limited water availability yearly, monthly, and even on daily basis.
Drought rises due to inadequate rainfall results in decreased water content in
the soil, and it is predicted to be increased by 2090 (Kogan
and Guo 2016). Water scarcity is a versatile problem
imposing a negative influence on plant physiological functions resulting in
retarded morphological growth due to the closure of stomata that disrupts
photosynthetic machinery causing reduced photosynthesis and transpiration (Farooq et al.
2009). Salinity, on the other hand, is more common in arid regions due to
excessive evaporation which causes accumulation of inorganic salts disrupting
the plant metabolism (Shahzad et al. 2017; Murtaza et al.
2017). Although saline soils have existed long before agriculture, poor quality
irrigation water had worsened this problem (Zhu 2001). High salt concentration
interferes with the absorption of water by plant roots; therefore, it also
aggravates drought stress effects on crops (Gökçe and
Chaudhry 2020).
Researchers have been struggling to circumvent abiotic
stress issue and unravelling defending mechanisms for crop tolerance for a long
time (Gokce et
al. 2020; Maggio et al. 2006),
especially by focusing on drought and salinity negatively influencing the
production and yield of staple food crops up to 70% (Mittler
2006). In addition, it is predicted that abiotic stress conditions will become
even worse in the coming future due to global climate change as reported by the
Intergovernmental Panel on Climate Change (IPCC 2014). Due to a shallow root
system penetrating only up to 60 cm, salinity and drought stress negatively
affects normal onion growth which ultimately reduces its bulb yield (Hanci and Cebeci 2015).
Therefore, onion production suffers from yield losses due to inadequate
availability of water resulting in moderate to severe drought stress conditions
and salinity problems across Turkey (Ardahanlioglu et al. 2003; Sönmez
et al. 2005; Kendirli
et al. 2005; Cemek
et al. 2007; Bilgili
et al. 2011). Although this is the
case, contrary to many reports on the investigation of responses of
agricultural crops to these two most important abiotic stresses, literature for
onion is extremely limited. Thus, this study aimed to observe the effects of
salinity and drought stresses on onion growth, root functioning and
fluctuations in physiological changes of selected short-day Turkish onion
cultivars. To the best of our knowledge, this is the first study comparing
morphological and physiological variables in several onion cultivars in
response to salinity and drought stress treatments. It was hypothesized that;
different onion cultivars would be screened as tolerant or susceptible to
salinity and drought stresses, which can be used for future breeding programs.
Materials and Methods
Experimental site
This study was conducted in semi-controlled greenhouse
conditions (no artificial lightening, temperature control with 20°C day/10°C night until bulbing, 25°C day/15°C night during stress treatment, ambient humidity with 40 to 70%
during the growing season) at Niğde Ömer Halisdemir University, Niğde, Turkey.
Plant material and
growth conditions
Seven short-day onion cultivars ‘Elit’
(round bulb shape with yellow-colored scale), ‘Hazar’ (top bulb shape with brownish-colored
scale), ‘Inci’ (top bulb shape with white-colored scale), ‘Naz’ (round bulb
shape with yellow-colored scale), ‘Perama’ (round bulb shape with pinkish-colored
scale), ‘Seyhan’ (globe bulb shape with straw yellow-colored scale) and ‘Sampiyon’
(round bulb shape with yellowish-brown colored scale)
were used. Pots (10 L) were filled with torf and
perlite in a 3:1 ratio. Twelve onion seeds were sown in each pot and necessary
management practices were taken to ensure proper growth. After germination, ten
plants per pot were maintained, and onion plants were divided into three groups
[i.e., control (C), salinity stress (SS) and drought stress (DS)]. The
first group consisted of control plants (C) without stress application, while
the second group of plants was under salinity stress (SS) and the third group
was subjected to drought stress (DS). The treatments were arranged according to
a completely randomized design under factorial arrangements with three
replications. Stress application was started at the onion bulbification
stage or leaf bases begin to thicken or expand stage (BBCH 41) (BBCH Monograph
2001). Plants were daily watered in the control group, whereas water was
suspended for 20 days for drought-stressed onion plants. For salinity stress
treatments, irrigation was performed in 3-day intervals with water containing
increasing amounts of NaCl, starting with 100 mM followed by 125 mM,
150 mM, 175 mM
and 200 mM (Hanci
and Cebeci 2015). In total, onion cultivars were
exposed to 750 mM of salinity stress in 20
days. The plants were subjected to salinity and drought stresses after which
drought stressed plants were well–watered, and salinity stressed plants were
washed with normal irrigation water to drain all the salts from the pot to get
rid of excess salt. Afterward, the rescued plants were allowed to grow for a
further two weeks until harvesting. When onion plants showed bending of neck
and started falling, they were harvested through uprooting for measuring bulb
yield traits.
Physiological
measurements
Physiological parameters were measured from all three
groups (C, SS and DS) from three different plants in three replicates from each
group. All the physiological measurements were taken during 09:00–13:00.
Gaseous exchange
traits
Gaseous exchange traits were measured at 0, 10th
and 20th day after stress application. Photosynthetic rate,
transpiration rate, and stomatal conductance
measurements from control (C) and stress application groups (SS and DS) were
conducted with the help of constant light intensity of photosynthesis device
(1500 μmol m–2 sec–1),
CO2 amount (400 μmol) and
airflow (500 μmol s–1) and
when photosynthesis gained steady state, the measurement was recorded using a
portable gas exchange system LiCor 6400 XT (Li-Cor Biosciences, USA).
Relative water
content (RWC)
Onion leaf segments of about 5 cm long (3rd
or 4th leaf) in three replications were collected from C, SS and DS
groups. The fresh weight of onion leaves was measured and the turgid weight of
the leaves was determined after keeping them in distilled water overnight. The
leaves were dried in a microwave at 500 W for 10 min followed by oven drying at
95°C for 2–3 h to ensure complete drying of the leaves before determining dry
weight. Relative water content (RWC) values of plants were calculated according
to the following equation:
Chlorophyll index
Leaf chlorophyll index was measured from control as well
as from salt and drought-stressed plants with SPAD 502 Chlorophyll-Meter (Soil
Plant Analysis Development; Minolta, Japan). Onion leaf (3rd or 4th
fresh leaf) was selected from each pot and measurements were carried out as the
average of three replications.
Leaf temperature
Leaf temperature was measured using Infrared Thermometer
(IRT) device (MASTECH BM380). The values were represented as the average of
three measurements from each pot.
Chlorophyll and
carotenoids contents
Leaf Chl a and b content and carotenoids were determined
by 0.5 g of fresh onion leaves (3rd or 4th fresh leaf)
homogenized in 80% of 10 mL acetone. The homogenized solution was kept at 4°C
overnight for complete extraction. The mixture was centrifuged at 10,000 rpm
for 5 min at 4°C. The absorption of the supernatant was measured by using a
UV–Vis spectrophotometer (UV–1800, Shimadzu) at 470 nm, 646 nm, and 663 nm.
Calculation of chl a, chl b, and carotenoids contents were determined by formula defined by Arnon (1949).
Morphological
measurements
All the
morphological measurements were taken from three plants from each pot. Leaf
length (cm) of the onion cultivars were measured with a measuring tape. The
number of leaves was averaged by counting three plants from each pot. The onion
bulbs were harvested from every pot at harvest time and the weight of bulb per
plant was determined. The bulb length (cm) and bulb diameter (cm) per plant
were determined from each pot in three replicates.
Root morphology
The roots were
collected from each pot and in three replicates for each group. The root
samples were washed with distilled water to remove dirt. The roots were placed
in 20 cm wide and 30 cm long acrylic tank with one-inch distilled water and
placed on EPSON scanner. The scanned images of roots were analyzed
by WinRHIZOTM 2013 (Régent
Instruments Inc., 2013) software for root morphological traits including
total root length (cm), the total surface area of the root (cm2),
average root diameter (mm), and root volume (cm3).
Statistical analysis
The data collected was analysed statistically using
Fisher’s Analysis of Variance (ANOVA) technique. The least significant
difference (LSD) test at P ≤ 0.05
was applied to compare the treatment mean values (Steel et al. 1997) using Statistical Package Statistix
8.1 (Tallahassee Florida, USA). Principal component analysis
(PCA) was performed for visualizing differences between the treatments among
cultivars by using XLSTAT-2014.
Results
Gaseous exchange
parameters
Stomatal conductance was found to be consistently reduced
compared to control in response to salinity and drought stress irrespective of
onion cultivar. The cultivars acclimatized to stress conditions showed a
significant reduction (P ≤ 0.05)
in stomatal conductance activity when compared with
their respective controls. The cultivar ‘Perama’
excelled the other cultivars with the least decrease in stomatal
conductance after 10 days of salinity and drought stress. In contrast, cultivar
‘Hazar’ showed a decrease of 70 and 84% in stomatal conductance after 10 days of SS and DS,
respectively. The response of onion cultivars was also noted after 20 days of
stress imposition. The cultivars ‘Hazar’ and ‘Sampiyon’ showed a significant decrease up to 90 and 93% in
stomatal conductance after 20 days of salinity and
drought stress (Table 1). The photosynthetic rate was significantly (P ≤ 0.05) suppressed in all
cultivars (Table 1). The maximum photosynthetic rate was observed in cultivar ‘Perama’, whereas the minimum photosynthetic rate was
measured from cultivar ‘Hazar’ with a reduction of 42
and 43%, after 10 days of SS and DS, respectively. The cultivars ‘Perama’ and ‘Seyhan’ showed the
least decline in the Table 1: Effect of salinity and drought stress on
gaseous exchange traits of onion cultivars
Cultivars |
Photosynthesis rate (µmol m-2
s-1) |
Stomata conductance (mol m-2 s-1) |
Transpiration rate (mmol m-2 s-1) |
||||||
|
0 day |
10th day |
20th day |
0 day |
10th day |
20th day |
0 day |
10th day |
20th day |
Elit–C |
21.35 ± 2.70 |
22.65 ± 1.5* |
19.33 ± 0.65* |
0.16 ± 0.06 |
0.25 ± 0.07* |
0.12 ± 0.01* |
2.79 ± 0.26 |
2.60 ± 0.43* |
2.12 ± 0.32* |
Elit–SS |
22.31 ± 1.31 |
14.77 ± 1.92 |
11.20 ± 0.98 |
0.17 ± 0.12 |
0.09 ± 0.03** |
0.02 ± 0.01 |
2.88 ± 0.48 |
1.95 ± 0.30* |
0.43 ± 0.33** |
Elit–DS |
22.50 ± 1.99 |
15.58 ± 2.07 |
11.31 ± 0.67 |
0.16 ± 0.11 |
0.04 ± 0.01 |
0.01 ± 0.01 |
2.91 ± 0.40 |
1.76 ± 0.05 |
0.24 ± 0.32 |
Hazar–C |
20.24 ± 1.20 |
21.31 ± 1.82* |
21.02 ± 1.51* |
0.19 ± 0.05 |
0.25 ± 0.10* |
0.10 ± 0.02* |
2.69 ± 0.60* |
3.51 ± 0.37* |
2.65 ± 0.52* |
Hazar–SS |
20.58 ± 1.90 |
16.40 ± 1.86 |
12.16 ± 0.56 |
0.22 ± 0.07* |
0.07 ± 0.07** |
0.01 ± 0.01 |
2.50 ± 0.09 |
1.97 ± 0.41** |
0.62 ± 0.50 |
Hazar–DS |
20.51 ± 0.80 |
16.67 ± 0.65 |
11.96 ± 0.55 |
0.20 ± 0.08 |
0.04 ± 0.01 |
0.01 ± 0.01 |
2.31 ± 0.63 |
1.75 ± 0.35 |
0.56 ± 0.32 |
Inci–C |
22.67 ± 1.29 |
24.52 ± 2.96* |
24.29 ± 3.90* |
0.18 ± 0.03 |
0.24 ± 0.09* |
0.15 ± 0.01* |
3.20 ± 0.27* |
3.60 ± 0.73* |
2.80 ± 0.61* |
Inci–SS |
24.07 ± 3.51 |
15.30 ± 0.78 |
12.91 ± 0.45 |
0.21 ± 0.15 |
0.07 ± 0.01 |
0.03 ± 0.01 |
2.86 ± 0.44 |
1.48 ± 0.24 |
1.29 ± 0.69** |
Inci–DS |
24.61 ± 1.76 |
14.65 ± 2.81 |
12.07 ± 1.49 |
0.17 ± 0.05 |
0.05 ± 0.01 |
0.01 ± 0.01 |
3.22 ± 0.59* |
2.05 ± 0.50** |
0.62 ± 0.21 |
Naz–C |
23.31 ± 1.90 |
21.48 ± 2.22* |
19.76 ± 2.91* |
0.20 ± 0.07* |
0.21 ± 0.04* |
0.13 ± 0.01* |
3.20 ± 0.79* |
2.91 ± 0.15* |
1.99 ± 0.35* |
Naz–SS |
22.39 ± 2.88 |
12.31 ± 1.93 |
13.74 ± 0.99** |
0.18 ± 0.04 |
0.05 ± 0.01 |
0.02 ± 0.01 |
2.72 ± 0.24 |
1.45 ± 0.14 |
0.87 ± 0.22** |
Naz–DS |
22.60 ± 1.48 |
17.22 ± 2.26** |
11.05 ± 0.22 |
0.21 ± 0.04 |
0.04 ± 0.01 |
0.01 ± 0.01 |
3.27 ± 0.44** |
1.66 ± 0.43** |
0.44 ± 0.27 |
Perama–C |
21.04 ± 0.82 |
24.18 ± 2.02* |
20.12 ± 2.30* |
0.22 ± 0.08 |
0.18 ± 0.07* |
0.15 ± 0.01* |
3.03 ± 0.74 |
3.03 ± 0.74* |
3.13 ± 0.33* |
Perama–SS |
25.02 ± 0.64* |
19.06 ± 2.84 |
14.20 ± 0.44 |
0.20 ± 0.08 |
0.12 ± 0.05** |
0.02 ± 0.01 |
3.05 ± 0.29** |
2.60 ± 0.10 |
1.39 ± 0.47 |
Perama–DS |
22.44 ± 1.51 |
18.53 ± 1.23 |
13.18 ± 1.69 |
0.19 ± 0.08 |
0.08 ± 0.01 |
0.02 ± 0.01 |
2.81 ± 0.29 |
2.46 ± 0.43 |
1.49 ± 0.37 |
Seyhan–C |
21.93 ± 1.22 |
24.17 ± 1.72* |
19.76 ± 0.66* |
0.20 ± 0.01 |
0.21 ± 0.08* |
0.13 ± 0.02* |
3.11 ± 0.39* |
3.66 ± 0.33* |
3.03 ± 0.38* |
Seyhan–SS |
23.31 ± 2.14* |
17.20 ± 2.48 |
14.82 ± 0.34** |
0.22 ± 0.09 |
0.05 ± 0.01 |
0.03 ± 0.01 |
2.97 ± 0.24 |
1.56 ± 0.27 |
1.29 ± 0.46** |
Seyhan–DS |
20.87 ± 0.40 |
15.72 ± 2.36 |
12.64 ± 0.33 |
0.19 ± 0.07 |
0.05 ± 0.01 |
0.01 ± 0.01 |
3.01 ± 0.51 |
1.64 ± 0.05 |
0.82 ± 0.17 |
Sampiyon–C |
21.78 ± 1.53 |
25.74 ± 2.92* |
23.35 ± 2.40* |
0.18 ± 0.05 |
0.26 ± 0.05* |
0.15 ± 0.01* |
3.44 ± 0.03 |
3.43 ± 0.96* |
3.53 ± 0.34* |
Sampiyon–SS |
22.55 ± 2.91 |
17.57 ± 1.89 |
14.53 ± 2.80** |
0.21 ± 0.04 |
0.07 ± 0.01 |
0.01 ± 0.01 |
3.59 ± 0.29* |
2.15 ± 0.19** |
0.71 ± 0.27** |
Sampiyon–DS |
23.55 ± 1.99* |
17.95 ± 0.11 |
12.18 ± 1.89 |
0.22 ± 0.05* |
0.05 ± 0.01 |
0.01 ± 0.01 |
3.21 ± 0.40 |
1.84 ± 0.35 |
0.26 ± 0.18 |
Values represent mean
value ± standard deviation. C control plants, SS salt stressed plants and DS
drought stressed plants. (*) shows significant
difference with stressed group plants (P ≤
0.05). (**) shows significant difference among stressed
counterparts (drought or salinity stress) (P
≤ 0.05)
photosynthetic rate at 20th day
of stress treatments while all other cultivars showed a lower photosynthetic
rate under both stress conditions with a reduction of 39–50%. Results revealed
that SS and DS resulted in a reduction in the transpiration rate of all the
cultivars. The cultivar ‘Perama’ showed the least
decline in transpiration rate by 56 and 52% with the exposure of 20 days of SS
and DS, respectively. The cultivar ‘Elit’ showed a
reduction by 80% under SS, a 93% decrease was observed in cultivar ‘Sampiyon’ under DS (Table 1).
Fig. 1: Effect on
relative water contents of different onion cultivars subjected to salinity and
drought stress conditions. Asterisk (*) represents significant difference (P ≤ 0.05). Two vertical asterisks (**) shows significant difference among stressed
counterpart (salt or drought stress) (P ≤ 0.05)
Fig. 2: Leaf
temperature of different onion cultivars subjected to salinity and drought
stress conditions. Asterisk (*) represents significant difference (P ≤ 0.05). Two vertical asterisks (**) shows significant difference among stressed
counterpart (salt or drought stress) (P ≤ 0.05)
Fig. 3: Chlorophyll index of different onion cultivars subjected to salinity and
drought stress conditions. Asterisk (*) represents significant difference (P ≤ 0.05). Two
vertical asterisks (**) shows significant difference among stressed counterpart
(salt or drought stress) (P ≤
0.05)
Physiological
parameters
Relative water contents of onion cultivars significantly
reduced in all onion cultivars exposed to salinity and drought stress compared
to their respective controls (Fig. 1). Control onion cultivars did not show any
significant change. The RWC contents were measured on 20th day and
the cultivar ‘Inci’ had the highest RWC (83%) in the
case of SS while cultivar ‘Perama’ had the highest
RWC (81%) in case of DS even with no significant (P ≤ 0.05) difference from the control. The lowest RWC was
assessed from cultivar ‘Naz’ (68%) in the case of SS,
whereas cultivar ‘Sampiyon’ had the lowest RWC (57%)
under DS. A change in leaf temperature was observed before terminating stress
treatment (Fig. 2). The leaf temperature of the cultivar ‘Inci’
was lowest under SS (23.6°C) and
DS (24.9°C) on 20th
day, respectively, with no significant (P
≤ 0.05) difference from control plants. However, the cultivar ‘Elit’ had the highest rise in leaf temperature under SS
(28.6°C) and the cultivar ‘Sampiyon’ under DS (29.1°C). Chlorophyll index was also quantified which indicated
deterioration in all onion cultivars with prolonged stress. The cultivar ‘Hazar’ showed a decrease of 17% in response to SS and a 23%
reduction in cultivar ‘Sampiyon’ was recorded under
DS when compared with their respective control plants (Fig. 3). The chlorophyll
(a, b, and total) contents indicated that stress impositions damaged
the photosynthetic pigments (Fig. 4). Salt in irrigation water damaged
chlorophyll a and b content in cultivar ‘Hazar’ with a rate of 28 and 34%, respectively. However, cultivar ‘Sampiyon’
had maximum damage to chlorophyll a
and b content under DS with a
reduction of 38 and 42%, respectively. Carotenoid contents were also decreased
with both stress conditions, whilst the lowest value was observed in the
cultivar ‘Hazar’ with a decrease of 40% under SS and
51% in ‘Sampiyon’ under DS (Fig. 4).
Morphological
parameters
All the morphological
changes showed a reduction in vegetative growth at prevailing stress conditions
(Fig. 5). It was noticed that there were fewer number of leaves per plant in
response to both stresses. The maximum number of leaves per plant was noted in
cultivar ‘Perama’ and ‘Seyhan’
under SS and DS, respectively. The minimum number of leaves was counted from
cultivar ‘Naz’ with a decrease of 40 and 53% under SS
and DS when compared to its control. The decrease in leaf diameter was also
observed in stressed plants. Under DS, cultivars ‘Naz’
and ‘Sampiyon’ showed a 40% decrease and under SS,
cultivars ‘Inci’ and ‘Naz’
showed a 30% decrease; while a higher leaf diameter was observed in cultivar ‘Perama’ followed by cultivar ‘Seyhan’.
The cultivars ‘Hazar’ and ‘Elit’
exhibited stunted leaf length under SS and DS conditions with a decrease of 32
and 28%, respectively (Fig. 5a).
Yield related
parameters
Bulb characteristics are important economic traits to
evaluate bulb yield (Fig. 6). Onion bulb length and bulb diameter were affected
significantly (P ≤ 0.05) under
stress conditions. The reduction in bulb diameter was more compared to the
decrease in bulb length. The cultivar ‘Perama’ showed
the highest bulb weight under SS (50.6 g) and DS (44.2 g) conditions,
respectively. The lowest bulb weight was observed from cultivar ‘Hazar’ with a reduction of 51% under SS and 53% in cultivar
‘Sampiyon’ under DS (Fig. 6d).
Root morphological
parameters
Fig. 4: Effect on photosynthetic
pigments of different onion cultivars subjected to salinity and drought stress
conditions. (a) Chlorophyll a content (µg mL-1)
(b) Chlorophyll b content (µg mL-1) (c)
Total chlorophyll content (µg mL-1)
(d) Carotenoid content (µg mL-1).
Asterisk (*) represents significant difference (P ≤ 0.05). Two vertical asterisks (**) shows significant
difference among stressed counterpart (salt or drought stress) (P ≤ 0.05)
Fig. 5: Vegetative
growth of different onion cultivars subjected to salinity and drought stress
conditions (a) Number of leaves per plant (b)
Length of leaves per plant (c) Diameter of leaf per plant. Asterisk (*)
represents significant difference (P
≤ 0.05). Two vertical
asterisks (**) shows significant difference among stressed counterpart (salt or
drought stress) (P ≤ 0.05)
Fig. 6: Yield
parameters of different onion cultivars subjected to salinity and drought
stress conditions. (a) Diameter of bulb per plant (b)
length of bulb per plant (c) total weight of bulb per plant.
Asterisk (*) represents significant difference (P ≤ 0.05). Two
vertical asterisks (**) shows significant difference among stressed counterpart
(salt or drought stress) (P ≤
0.05)
Fig. 7: Effect on root
morphology of different onion cultivars subjected to salinity and drought
stress conditions. (a) Total root length (cm), (b) root surface
area (cm2), (c) root diameter (mm), (d) root volume
(cm3). Asterisk (*) represents significant difference (P ≤ 0.05). Two
vertical asterisks (**) shows significant difference among stressed counterpart
(salt or drought stress) (P ≤
0.05)
Roots response towards SS resulted in retarded growth as
compared to DS group, which showed an increase in root characteristics.
Salinity stress suppressed the total root length by 14% in cultivar ‘Sampiyon’ contrarily least reduction by 4% in ‘Inci’, while under DS the cultivar ‘Sampiyon’
exhibited 17% increase in root length followed by 13% in cultivar ‘Inci’ (Fig. 7a). The root surface area also decreased under
SS, whereas the same variable depicted an increasing trend under DS. The
cultivars ‘Sampiyon’ and ‘Elit’
showed a decline of 12% in root surface area in response to SS, while the
cultivars ‘Hazar’ and ‘Sampiyon’
resulted an increase of 16 and 13%, respectively in
root surface area under DS (Fig. 7b). The average root diameter showed a 15%,
reduction with the imposition of SS in the cultivars ‘Elit’
and ‘Naz’. On the other side, the cultivar ‘Seyhan’ showed 3% increase in root diameter. The cultivar ‘Perama’ showed 16% increase in root diameter under DS (Fig.
7c). The root volume was decreased by 31% in cultivar ‘Inci’
followed by 23% in cultivars ‘Elit’ and ‘Hazar’ under SS. A reverse trend was observed with an
increase in root volume by 35% in the cultivar ‘Inci’
under DS (Fig. 7d).
Principal component analysis
The interrelationship among
selected onion cultivars along with the tested variables under SS and DS
conditions were analysed by biplot principal
component analysis (PCA) as shown in Fig 8. It revealed that the first two
components explained 60.78% variance (contributed by PC1 38.78%, and PC2
22.00%) under SS conditions. DS conditions showed a total variation of 71.36%
(contributed by PC1 53.12%, and PC2 18.24%) among the onion cultivars for the
measured traits. PCA biplot grouped the onion
cultivars based on their response to the tested morphological and physiological
variables/traits. In SS, the cultivars ‘Perama’, ‘Seyhan’ and ‘Inci’ depicted positive PC1 values. The cultivar ‘Perama’
showed best performance for chlorophyll index, total chlorophyll contents,
photosynthesis, length of leaf and length of bulb. The cultivar ‘Seyhan’,
was best performing for the traits such as root surface area, average root
diameter, diameter of bulb, carotenoid content, stomatal
conductance, and transpiration rate. The cultivar ‘Inci’,
was best in total root length and RWC under SS. The cultivars ‘Perama’ and ‘Seyhan’,
were referred to as tolerant based on their response to the tested variables,
whereas the cultivars ‘Hazar’, ‘Elit’
and ‘Sampiyon’ were salt sensitive. The cultivar ‘Inci’ showed average response (Fig. 8). In DS condition,
the cultivar ‘Seyhan’ showed maximum chlorophyll
index, root diameter, and length of bulb, while the cultivar ‘Perama’ indicated the maximum diameter of leaf, number of
leaves, RWC, photosynthesis, transpiration rate and weight of bulb. The
cultivars ‘Elit’ ‘Hazar’
and ‘Sampiyon’, were drought
sensitive according to the observed traits (Fig. 8).
Fig. 8: PCA biplot for morpho-physiological
variables of seven onion cultivars grown under salinity stress (a) and drought stress (b) conditions. PCA biplot
is a combination of score plot of onion cultivars (represented in blue text)
and loading plot of variables (represented by red vectors; black text). SS:
salinity stress, DS: drought stress, NL: number of leaves, DL: diameter of leaf, LL:
length of leaf, DB: diameter of bulb, LB: length of bulb, WB: weight of bulb,
TRL: total root length, ARD: average root diameter, RV: root volume, RSA: root
surface area, RWC: relative water content, LT: leaf temperature, CI:
chlorophyll index, CHLA: chlorophyll a, CHLB: chlorophyll b, TCHL: total
chlorophyll, CT: carotenoid content, Pn:
Photosynthesis, Gs: stomatal
conductance, E: transpiration rate
Fig. 9: Schematic diagram showing general effect of drought and
salinity stress on onion. Drought and salinity stress negativley impacted
relative water contents of onion dirupting photosynthesis. Salinity stress
hindered uptake of water by onion roots along with weaker root development.
Both stresses resulted in decreased vegetative growth and resultantly lower
bulb yield
Discussion
The results of
current study highlighted the tolerance potential of short-day onion cultivars
to SS and DS. Both stresses adversely affected the gaseous exchange
characteristics (photosynthesis, stomatal conductance
and transpiration rate) of the all the cultivars, however, some cultivars
performed better in comparison to others (Table 1). All the cultivars showed
least disruption in gaseous exchange traits during the initial 10 days out of
the 20 days of SS and DS, which indicated that onion is less prone to short
exposure of stress period. Contrarily, after exposure to 20 days of stress
conditions, the cultivars ‘Elit’, ‘Hazar’ and ‘Sampiyon’ showed
maximum decline in photosynthetic rate due to decreased stomatal
activity. The reduction in transpiration rate in these cultivars was also more
as compared to the remaining cultivars. Decreased gaseous exchange in these
cultivars might have resulted due to the decline in leaf internal CO2
concentration which is a consequence of stomatal
closure and is evident by the decreased transpiration rate (Vesala
et al. 2017). Sensitivity of these cultivars might also be attributed to
the damaged photosynthetic apparatus caused by the generation of reactive
oxygen species (ROS), which are accumulated under the circumstances of reduced
CO2 influx and excess/continued light exposure (Farooq
et al. 2014). The reduction of cellular water caused by the contact of
roots with the stressful environment subsequently reduces the transport of
assimilates, that eventually affects the photosynthetic rate (Chaves et al. 2009). PCA analysis also endorsed the
sensitivity of the cultivars ‘Elit’, ‘Hazar’, and ‘Sampiyon’ under both
SS and DS conditions (Fig. 8). The least influence on gaseous exchange traits
in cultivars ‘Perama’ and ‘Seyhan’
was due to their high-water contents. It includes changes in the cellular
osmotic behaviour evident by high relative water contents in the cell under
stress conditions (Hussain et al. 2018). The
synthesis of osmo-protectants combined with high
chlorophyll pigments and enhanced photosynthesis could be a major decisive
factor for the stress tolerance response of these cultivars (Farooq et al. 2015). Our study grouped the cultivars
‘Perama’ and ‘Seyhan’ as
‘tolerant’ based on their better adaptive response to both the stresses. The
PCA analysis revealed that these cultivars were the best performing for the
gaseous exchange traits to both SS and DS. Demirel et
al. (2020) investigated the effect of drought stress on gaseous exchange
characteristics of potato cultivars and suggested that higher photosynthetic
rate was a key attribute exhibited by tolerant cultivars. A similar trend was
observed in our study.
Relative water
content is an important physiological attribute to estimate the internal water
status under stress conditions. The cultivars ‘Elit’,
‘Hazar’ and ‘Sampiyon’
showed decreased RWC under given stresses (Fig. 1). As, RWC is considered as an
indicator of stress tolerance (Dien et al. 2019), our results suggested that
the cultivars ‘Elit’, ‘Hazar’
and ‘Sampiyon’ were susceptible to applied stress. It
is evident from the PCA results that these cultivars showed poor performance
and existed in the negative quadrate (Fig. 8). Our results and previous studies
indicated that SS and DS affects negatively RWC which also leads to oxidative
stress in plants (Egert and Tevini
2002; Astaneh et
al. 2018). The cultivar ‘Inci’, showed more RWC
only under SS condition, whereas ‘Perama’ and ‘Seyhan’ were the best performers under DS. Interestingly,
these cultivars could have exhibited higher osmotic regulation through accumulation of osmolytes to alleviate SS and DS (Moharramnejad et al. 2019).
Leaf temperature was
elevated under both the stressed conditions with a higher increase under DS
(Fig. 2). The higher leaf temperature was noticed in the cultivars ‘Elit’, ‘Hazar’ ‘Naz’ and ‘Sampiyon’ under both
the stresses, which is attributed to lower RWC and disruption in gaseous
exchange traits. Isoda (2010) reported that
water-stressed plants showed lower transpiration rates resulting in higher leaf
temperature. The reason is that there is a close relationship between stomatal closure and increased leaf temperature (Liu et al. 2011). The cultivar ‘Inci’ exhibited comparatively lower leaf temperature under
SS, due to its capability to preserve higher levels of RWC. The cultivar ‘Seyhan’ prevented the tissue damage by regulating metabolic
processes such as increased stomatal opening,
transpiration rate, and enhanced photosynthesis that resulted in lowering of
leaf temperature. Other factors that might have contributed to better
adaptation response of this cultivar under both stresses is linked to the manipulation
of antioxidant system to scavenge oxidative stress caused by SS and DS (Farooq et al. 2019).
In this study,
exposition of onion plants to SS and DS damaged the photosynthetic pigments of
all the cultivars. The maximum impairment in chlorophyll contents was depicted
by the cultivars ‘Elit’, and ‘Hazar’
in response to SS and in ‘Sampiyon’ under DS (Fig.
4). This might be due to the damage caused by ROS in these cultivars. It
resultantly destroyed the chloroplast structure of the cultivars. Moreover, decrease
in chlorophyll of stressed plants is a general symptom of oxidative stress
which is attributed to inhibition in synthesis of chlorophyll (Santos 2004).
The findings of damaged chlorophyll contents are also supported by earlier
study of Romdhane et al. (2020). Total
chlorophyll content was higher in the cultivar ‘Perama’
that was credited to the minimal effect on the light harvesting complexes
present on the thylakoid membrane, as evident from enhanced photosynthesis
compared to others. Carotenoid is an antioxidant with the potential for
detoxifying the harmful effects of ROS in plants. Current study reported the
negative impact of SS and DS with damaged carotenoid contents causing photoinhibition. In cultivars ‘Elit’
and ‘Sampiyon’, a significant reduction of carotenoid
contents indicated susceptibility to SS and DS, whereas the cultivar ‘Hazar’ performed poorly under SS. These cultivars showed
decline in RWC and total chlorophyll content. Contrarily, the cultivars ‘Inci’ and ‘Seyhan’ were the
richest in carotenoid content and this was possible by retaining higher RWC
under SS. This finding was also supported by previous reports in onion (Hanci and Cebeci 2014,; Hanci and Cebeci
2015; Hanci et
al. 2015; Semida 2016).
Salinity and drought
stresses negatively influenced the above-ground biomass of onion (Fig. 5). The
cultivar ‘Naz’ showed minimum number of leaves under
both the stresses whereas the cultivars ‘Elit’, ‘Inci’ and ‘Sampiyon’ demonstrated
decreased number of leaves under DS. The stressed condition inhibited the
growth of the cultivars with alteration in cell size division and resulted in
decreased production of leaf and promoted senescence (Ghodke
et al. 2018). Leaf length was
decreased in the cultivars ‘Hazar’ and ‘Elit’ whereas the cultivars ‘Perama’
and ‘Seyhan’ showed the least reduction in leaf
length. The differences in vegetative growth among the cultivars found in this
study can be attributed to disruption in physiological characteristics. The
sensitive cultivars might have experienced a decrease in turgor pressure
limiting the expansion of leaf (Fahad et al.
2017). Metwally (2011) also demonstrated the negative
effects of stress on growth of onion.
Stress at bulbification stage significantly reduced the yield traits
in all cultivars tested in response to the SS and DS (Fig. 6), as expected
based on the previous reports (Pelter et al. 2004; Zayton
2007; Metwally 2011). The highest bulb weight of the
cultivar ‘Perama’ is attributed to the tolerance in
response to stress conditions. Bulb characteristics are known to show a
reduction in response to stress among the cultivars due to the difference in
soil water intake and evapotranspiration flux (Pelter
et al. 2004; Lipiec
et al. 2013). In the present study,
cultivars ‘Elit’ ‘Hazar’
and ‘Sampiyon’, having lower photosynthetic activity,
higher leaf temperature and lower chlorophyll contents compared to other
cultivars, showed the lowest bulb weight in response to SS and DS, which can be
explained as the reduction in morphological and physiological characteristics
of susceptible cultivars resulting into smaller cell size (Tisne
et al. 2010).
Salinity and drought
stress altered the root morphological characteristics of the cultivars under
study. To the best of our knowledge, this is the first study that focuses on
the effects of SS and DS on the root morphology of onion. Under DS, all the
onion cultivars used in this study showed elongated root development. However,
in case of the SS, opposite results were obtained (Fig. 7). The decreased root
length in the cultivar ‘Sampiyon’ under SS is due to
higher osmotic pressure in the vicinity of roots which prevented uptake of
water and resulted in shorter roots (Sadat-Noori et
al. 2008). The results obtained regarding inhibited root length with
exposure to SS are in accordance with Basu et al.
(2017). The increase in root length of the cultivar ‘Inci’
indicated the plasticity of root. It might be due to better cell division and
expansion of root apical meristem. Thus, it suggests that salinity stress
altered root growth with the enhanced and reduced cell division and cell
expansion (West et al. 2004). The growth increment in root could be due
to its ability to alleviate osmotic stress by maintaining osmotic potential.
The absorbed ions by the root might be quickly separated into vacuoles without
its higher accumulation, therefore increasing turgor of the cell and stimulated
cell elongation (Mukami et al. 2020).
Increased root length of cultivar ‘Sampiyon’ under
the DS is probably due to its sensitivity to moisture deficiency. It is known
to force plant roots to extract water from deeper soil pockets (Fang et al. 2017). The decreased root
diameter was observed with the application of SS in all cultivars, whereas DS
resulted in increased root diameter. The reduction in root diameter of the
cultivars ‘Elit’ and ‘Naz’, is due to ionic toxicity and osmotic pressure
(Fricke et al. 2006). The root surface area and root volume decreased in
response to SS while it increased under DS. The cultivars ‘Elit’
‘Sampiyon’, and ‘Hazar’
showed a decline in root surface area and root volume, respectively. The
reduction under SS was due to inhibited root growth due to osmotic stress and
hampers root meristem size (Jiang et al.
2016). In contrast, a reverse trend was noticed in the cultivars ‘Hazar’, ‘Sampiyon’ and ‘Elit’ resulted in increase in root surface area and root
volume under DS. It might be due to moisture deficiency that triggers synthesis
of abscisic acid for the closure of stomata (Hussain et al. 2016). These cultivars also showed
poor performance i.e., lower RWC, damage to photosynthesis and
photosynthetic pigments regarding which triggers oxidative stress. These
disruptions in physiological processes exert pressure with enlarged root
surface area and root volume to extract water. Our findings are
consistent with previous studies that reported a similar influence of stress on
root architecture of garlic, potato, tomato, eggplant, and pea (Akinci et al. 2004;
Al-Safadi and Faoury 2004; Karni et al.
2010; Khenifi et al. 2011; Pereira et al. 2020). In view of the
examined parameters during the stress duration and yield traits, an
illustrative diagram is described in Fig. 9.
Conclusion
This study was
conducted to evaluate the performance of seven onion cultivars under salinity
and drought stresses. Our results revealed a differential response of onion
cultivars. It was concluded that cultivars 'Seyhan'
and 'Perama' showed higher tolerance compared to
other cultivars under both stresses with minimal decline in morphological and
physiological traits evaluated. Cultivars 'Elit', 'Hazar' and 'Sampiyon', on the
other hand, exhibited susceptibility compared to other cultivars studied. The resilient cultivars 'Seyhan' and 'Perama' can be used in future breeding studies to increase
abiotic stress tolerance of onion against salinity and drought stresses.
Furthermore, these will be the most attractive onion cultivars for stress related
studies at the molecular level.
Acknowledgments
We acknowledge the Scientific Research Projects Unit
(BAP) of Niğde Ömer Halisdemir University,
Niğde, Turkey for providing funds for this study under the Project
No. TGT 2019/05–BAGEP. This study was the part of Ph.D.
thesis work of Usman Khalid Chaudhry.
He also acknowledges the Ayhan Şahenk
Foundation for providing fellowship during his doctoral study. The authors
would like to appreciate İbrahim Köken for his
partial contribution.
Author Contributions
Usman Khalid Chaudhry, Zahide Neslihan Öztürk Gökçe and Ali
Fuat Gökçe conceptualized the idea and designed the study. Usman Khalid
Chaudhry performed the experiment, collected the data, analyzed the data and
wrote the initial draft. Zahide Neslihan Öztürk Gökçe and Ali Fuat Gökçe edited
and reviewed the draft of paper. All the Authors, read and approved the final
draft.
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