Arab J Sci Eng (2017) 42:2207–2215

DOI 10.1007/s13369-016-2378-x

RESEARCH ARTICLE - BIOLOGICAL SCIENCES

Smoke Priming Regulates Growth and the Expression of

Myeloblastosis and Zinc-Finger Genes in Rice under Salt Stress
Ijaz Malook1 · Gulmeena Shah1 · Mehmood Jan1 · Kamran Iqbal Shinwari1 ·
M. Mudasar Aslam2 · Shafiq ur Rehman2 · Muhammad Jamil1

Received: 10 November 2015 / Accepted: 14 December 2016 / Published online: 12 January 2017
© King Fahd University of Petroleum & Minerals 2017

Abstract Salinity negatively affects the rice growth and pro- the drastic effect. It was concluded that priming with smoke
ductivity around the globe including Pakistan. The current solution protects the plants from ionic toxicity, shows promis-
study describes about the application of new approach of ing effect on rice growth and can be used for enhancing crop
smoke solution priming, which was used to overcome the productivity under saline condition.
deteriorating effect of salinity by investigating its affects on
biochemical and molecular attributes of rice crop. Seeds of Keywords Rice · MYB · ZAT12 · Transcription factors ·
two rice varieties (Basmati-385 and Shaheen Basmati) were RT-PCR · Smoke priming
soaked in smoke solution for 24 h. Smoke-soaked seeds were
used to evaluate its effect on plant fresh and dry biomass,
elemental uptake and expression of myeloblastosis (MYB) 1 Introduction
and zinc-finger (ZAT12) genes against different levels of
NaCl (0, 50, 100 and 150 mM). Fresh and dry biomass A wide range of abiotic stresses are responsible for huge crop
of plant was decreased with increasing level of salt stress, losses and productivity by altering various physiological and
while plant raised from smoke-primed seeds had lowers the biochemical mechanisms. Among different types of abiotic
adverse effect of salt stress. Concentration of sodium ion and stresses, salinity is the major factor in Asia, especially in
Na+ /K+ ratio was increased, while potassium ion concen- Pakistan, that reduces both productivity and cost per annum
tration was decreased with increasing salt concentration in of rice [1,2]. Plants adopt various physiological, cellular and
the medium. The amount of sodium ion was noted higher in molecular variations to cope these stresses [3,4].
roots than shoots, while potassium was in low amount in roots Gene activation during abiotic stress condition can pro-
than shoot. Smoke solution reduced the harmful effect of salt tect plants from oxidative damage because of ionic toxicity,
stress by reducing the uptake of sodium ion and increasing osmotic stress and oxidative stress [5]. Various reports have
potassium ions both in roots and in shoots. The expression documented that gene expression is significantly altered by
of MYB and ZAT12 genes was checked by using RT-PCR salt stress in rice and other plants [6]. The expression of the
approach. Result shows that MYB and ZAT12 protein genes stress-inducible genes is mainly controlled by transcription
were expressed differently under various levels of salt stress, factors. MYB transcription factor is one of the key regularity
while priming with the smoke solution changed the expres- units involved in the regulation of stress-inducible genes with
sion profile of MYB and ZAT12 protein genes by alleviating a diverse role in the plant development and defense response
to abiotic stresses [7,8]. Similarly, zinc-finger protein ZAT12
B Muhammad Jamil gene family with a small group of genes also responds to vari-
dr.jamil@kust.edu.pk ety of abiotic and biotic stresses [9]. ZAT12 gene expression
1 was also noted against types of abiotic stresses such as heat,
Department of Biotechnology and Genetic Engineering,
Kohat University of Science and Technology, Kohat 26000, cold, drought, H2 O2 , heavy metal and UV [9–14].
Pakistan Priming, a pre-sowing treatment of seeds, is an effective
2 Department of Botany, Kohat University of Science and technique against the inhibitory response of different types of
Technology, Kohat 26000, Pakistan stresses and plays a vital role in the improvement of seed per-

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Table 1 List of RAc-1(Actin), OsMYB2, OsMYB6, ZAT12-1andZAT12-9 gene primers, which were used in the experiment
Genes Forward primer sequences Reverse primer sequences

RAc-1(Actin) 5 - TGCTATCCCTCGTCTCGACCT-3 5 -CGCACTTCATGATGGAGTTGTAT-3

OsMYB-2 5 -CGTGCTTGGATTGGTACGAG-3 5 -TCAGGCTGTGGCACAGCCCG-3
OsMYB-6 5 -TCCAGCTTTCCAGTTCTTGG-3 5 -GAAGGTGTAATCCATGGCCG-3
ZAT12-1 5 -GATCGGCGACGTTAGTGAT-3 5 -AAGGAAACAATCCAACATGG-3
ZAT12-9 5 -GCTCGTCATTAAGAGCGAAA-3 5 -TACAAGAAGGTTAAGTAACT-3

formance in achieving better germination and better seedling (v/v) was selected for seed priming. The sterilized seeds were
[15]. Seed ability to germinate under stress condition can soaked in a priming solution for 24 h at room temperature.
be improved by the application of plant growth regulators After priming seeds were air-dried at ambient temperature of
and hormones with seed priming and other pre-sowing treat- 25 ◦ C.
ments [16]. Smoke is a highly composite chemical mixture
with plant active compounds such as butenolide designated 2.3 Germination, Seedling Growth and Salt Treatment
as karrikins that can provide a stimulant to plants in different
environment [17]. Smoke solution compound karrikin has For germination, 20 seeds were allowed to germinate in Petri
been reported to enhance seedling growth of various plant plates containing filter paper saturated with water at 30 ◦ C
species, signifying its importance as a seed priming agent for 10 days in triplicate. Ten seedlings per pots were then
[18,19]. It has been reported that smoke is largely effective grown in Hoaglands solution for 1 week [23]. Salt treatment
stimulant that promotes germination of nearly 1200 species in this solution was started after 1 week of transplantation.
in more than 80 genera around the world [17]. Plant-derived The NaCl treatment used was control, 50, 100 and 150 mM
smoke solution can create tolerance in the plant against dif- for 1 week. Plants were harvested after 24 days and divided
ferent type of stresses [18,20]. Various studies have been into shoots and roots. Then fresh weight of root and shoot
conducted to evaluate the effect of plant-derived smoke on of both varieties was determined. For dry weight, roots and
physiological and biochemical process of plant [18,19,21] shoots were dried at 80 ◦ C in an oven for 48 h.
but still less reports are available on its effect on molecular
mechanisms that occur in plant under salt stress condition.
2.4 Flame Emission Spectrophotometery
By considering all these observations, the present study was
conducted to find out the effect of salt stress and smoke prim-
Dry roots and shoots of 25 mg were well grinded and
ing on the plant biomass, elemental uptake and expression
digested with concentrated sulfuric acid and hydrogen perox-
profile of MYB and ZAT12 genes in rice.
ide (2:1 ratio v/v). After complete digestion, each sample was
diluted with deionized distilled water upto 25 ml. Electrolytes
(Na+ , K+ ) were analyzed by flame emission spectropho-
2 Material and Methods tometer by following method of Awan and Saleem [24] with
a little bit modification.
2.1 Seed Collection and Sterilization
2.5 RNA Isolation and Reverse Transcription
The seeds of two rice (Oryza sativa L.) varieties Basmati-
385 and Shaheen Basmati were obtained from the National
Total RNA was isolated from both stressed and control rice
Agriculture Research Center (NARC), Islamabad, Pakistan.
leaves by using TRIzol reagent (Invitrogen) with slight mod-
Hypochlorite solution 3.5% was used for surface sterilization
ification according to manufacturer’s protocol. First-strand
of the seeds.
cDNA was synthesized by using M-MLV reverse transcrip-
tase (Fermentas) using oligo (dT) primer. To check the
2.2 Preparation of Smoke Solution and Seed Treatment expression of OsMYB-2, OsMYB-6, OsZAT12-1, OsZAT12-
9, the reverse transcriptase-PCR technique was used. RT-
Smoke solution was produced by burning 333 g of Bauhinia PCR was performed with an applied Biosystems thermo-
variegate shade-dried leaves, and smoke was bubbled through cycler. Constitutively expressed Actin gene RAc1 was used
one liter of distilled water [20,22]. Various dilutions of smoke as a positive control. The target genes and their primers for
solution were prepared and analyzed to find out the most the RT-PCR are listed in Table 1.The PCR conditions were
effective dilutions. Among these smoke dilutions, 1:5000 as follows: pre-denaturation of 5 min at 95 ◦ C; 45 cycles of

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Fig. 1 Effect of smoke priming on fresh root weight (a), dry root 50: 50 mM NaCl; 100: 100 mM NaCl; 150: 150 mM NaCl; 1:5000B:
weight (b), fresh shoot weight (c) and dry shoot weight (d) of Basmati- smoke solution; S50: smoke solution + 50 mM NaCl; S100: smoke
385 and Shaheen Basmati under various concentrations of salt stress. solution + 100 mM NaCl; S150: smoke solution + 150 mM NaCl

20 s at 95 ◦ C, 30 s at 60 ◦ C, 40 s at 72 ◦ C and a final exten- significance. All the data were expressed as mean±SD for
sion for 15 min at 72 ◦ C. The PCR products were separated on three replications.
1.5% agarose gel having ethidium bromide and photographed
under UV light.
3 Results
2.6 Statistical Analysis
3.1 Seedling Growth
The study was designed by using completely randomized
designs with factorial arrangement. The experiment was Seedling growth of shoot and root of both varieties was
replicated three times. ANOVA was carried out by using the decreased with increasing concentration of NaCl (Fig. 1), but
Student’s Statistix 9 software. Mean values were compared higher fresh and dry weights were observed in smoke-primed
by least significant difference (LSD) test at the 5 % level of seed plants as compared to hydro-primed seeds, suggesting

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Fig. 2 Effect of smoke priming on sodium contents in the roots and NaCl; 150: 150 mM NaCl; 1:5000B: smoke solution; S50: smoke solu-
shoots of Basmati-385 (a) and Shaheen Basmati (b) under various con- tion + 50 mM NaCl; S100: smoke solution + 100 mM NaCl; S150:
centrations of salt stress. DW: control; 50: 50 mM NaCl; 100: 100 mM smoke solution + 150 mM NaCl

that smoke alleviates the adverse effect of NaCl (Fig. 1). In concentration of salts in the medium. It was noted to be 44.2
Basmati-385, shoot and root fresh weight of hydro-primed mg/L in roots and 41.9 mg/L in shoot under 150 mM salt
seed plants was 0.32 and 0.58g, respectively, which reduced stress by comparing with control as 35.05 and 33.85 mg/L in
to 0.18 and 0.20 g at 150 mM NaCl. However, plant raised Basmati-385 (Fig. 2a). In Shaheen Basmati, sodium content
from smoke-treated seeds had higher fresh weight of shoot was found to be 50.5 mg/L in roots and 44.6 mg/L in shoot
(0.19 g) and root (0.32 g) at 150 mM salt. Similarly, plant under 150 mM salt concentration, while in control (DW)
raised from smoke-treated seeds had the higher dry weight medium, the amount was 45.15 mg/L in roots and 36.5 mg/L
of shoot (0.02 g) and root (0.018 g) as compared to control in shoot (Fig. 2b). Roots contained relatively higher sodium
(Fig. 1). In S. Basmati, high fresh weight of shoot (0.27 g) content (44.2 mg/L) than shoot (41.9 mg/L) under control
and root (0.29 g) was observed in plants raised from smoke- and all stressed conditions (Fig. 2). The potassium ion con-
primed seeds. Plant raised from smoke-primed seeds had tent in roots was low (17.3 mg/L) than shoot (23.5 mg/L) in
higher dry weights of shoot (0.028 g) and root (0.002 g) as Basmati-385 at high salt stress condition (Fig. 3a), while in
compared to hydro-primed seeds (0.027 and 0.001 g) (Fig. 1). Shaheen Basmati, potassium content was 17.15 mg/L in root
and 17.95 mg/L in shoot under 150 mM salt stress condition
3.2 Sodium and Potassium Concentration in Roots and (Fig. 3b).
Shoots In both varieties, smoke priming effects sodium and potas-
sium content positively by alleviating the drastic effect of
Sodium and potassium ion concentration was different in dif- salinity by reducing the overall sodium content from 41.55
ferent plant parts such as roots and shoots. Sodium content to 39.4 mg/L under 50 mM salt stress condition in roots, while
in root and shoot was significantly increased with increasing in shoot, smoke priming reduced the sodium ion content from

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Fig. 3 Effect of smoke priming on potassium contents in the roots mM NaCl; 150: 150 mM NaCl; 1:5000B: smoke solution; S50: smoke
and shoots of Basmati-385 (a) and Shaheen Basmati (b) under various solution + 50 mM NaCl; S100: smoke solution + 100 mM NaCl; S150:
concentrations of salt stress. DW: control; 50: 50 mM NaCl; 100: 100 smoke solution + 150 mM NaCl

37.7 to 31.25 mg/L under 50 mM NaCl stress condition in 3.3 Stress-Specific Gene Expression Profile
Basmati-385. In Shaheen Basmati smoke priming alleviates
the salt effect by lowering sodium content from 46.5 to 36.15 The expression profile of OsMYB-2, OsMYB-6, OsZAT12-1
mg/L in root, while in shoot, sodium reduced from 42.2 to and OsZAT12-9 genes was analyzed in rice plants exposed
31.8 mg/L (Fig. 2.) On the other side, salt stress decreases the to different concentration of salt stresses by using RT-PCR.
amount of potassium ion showing negative correlation with The results showed that these genes express differently under
salinity, but smoke priming significantly raised the amount different doses of stresses, control and smoke priming. For
of potassium ion in the salt stress medium in both varieties OsMYB-2 gene expression was moderate in 50 and 100 mM
(Fig. 3). and 5000B + 100 mM salt stress but it was weakly expressed
Na+ /K+ ratio increases with increasing salt in the in 5000B + 150 mM smoke-primed plant samples in Basmati-
medium in roots and shoot in both varieties. In Basmati-385, 385 (Fig. 5a). While in Shaheen Basmati, OsMYB-2 was
the ratio was 1.98 in roots and 1.41 in shoot in control, while strongly induced at 50, 100 mM salt stress and 5000B +
at 150 mM salt stress conditions, these ratios were 2.94 and 100 mM and 5000B + 150 mM smoke-primed plant samples,
2.48, respectively, while priming with smoke solution alle- low expression was observed in control, smoke, 150 mM and
viate the drastic effect of salinity in both roots and shoot and 5000B + 50 mM (Fig. 4b). In case of OsMYB-6 gene, high
Na+ /K+ ratio was noted 2.94 in roots and 2.48 in shoot at expression was noted at 50, 100 and 150 mM and 5000B +
150 mM (Fig. 4a). A similar situation was observed in case 50 mM, while weakly expressed in control and smoke-treated
of Shaheen Basmati, where high Na+ /K+ ratio was noted at plants (Fig. 5a). Similar results were also observed for Sha-
150 mM salt stress condition as compared to control, while in heen Basmati (Fig. 5b).
smoke-primed seedlings, these values were reduced to 1.93 In Basmati-385, OsZAT12-1 was significantly induced at
in roots and 1.45 in shoot under 150 mM smoke-alleviating 50 mM and low expression was noticed at 100 mM, 5000B +
solution (Fig. 4b). 50 mM and 5000B + 100 mM (Fig. 5b). In Shaheen Basmati,

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Fig. 4 Effect of smoke priming on Na+ /K+ ratio in the roots and shoots 150: 150 mM NaCl; 1:5000B: smoke solution; S50: smoke solution +
of Basmati-385 (a) and Shaheen Basmati (b) under various concentra- 50 mM NaCl; S100: smoke solution + 100 mM NaCl; S150: smoke
tions of salt stress. DW: control; 50: 50 mM NaCl; 100: 100 mM NaCl; solution + 150 mM NaCl

high expression was noted at 50, 100 and 150 mM, while no [1,2,25]. It has been reported that seeds primed with buteno-
or low expression was found in control and in plant raised lide had a faster emergence of the radical, which resulted in
from smoke-treated seeds (Fig. 5b). In case of OsZAT12- significantly higher seedling growth [19].
9, high expression was noted at 50, 100 and 150 mM and Na+ is the main source of ion-specific damage for the
5000B + 100, while slight expression was seen in control, majority of the crops under saline environment. The capa-
5000B + 50 and 5000B + 150 in Basmati-385 (Fig. 5b). In bility to sustain a low Na+ concentration or a high K+ in
Shaheen Basmati, high expression was noted at 50, 100 and roots at the seedling stage is considered an important sign of
150 mM and 5000B + 150 mM, while weak expression was salt tolerance in rice [27,28]. Our results indicated a signif-
seen at smoke, 5000B + 50 and 5000B + 100 mM (Fig. 5b). icant increase in sodium ion and decrease in potassium ion
concentration in Basmati-385 and Shaheen Basmati under
various concentrations of salt stress (Figs. 2, 3). The Na+ was
4 Discussion increased more in roots than in shoots under NaCl conditions.
The mechanisms of Na+ and K+ absorption in rice were rec-
It has been well evident that smoke enhanced germination ognized to be independent under stress as the most important
and seedling growth [18,19,25]. In this study, we had also pathways of Na+ and K+ uptake take place in parallel and
observed that plant raised from smoke-treated seeds had not in direct competition [29]. Our results are similar to other
higher fresh and dry weight of root and shoot (Fig. 1). reports [30–35], indicated that salinity increases sodium ion
This may be due to the fact that plant raised from seeds concentration and prevents potassium ion to enter the cell
treated with smoke had less uptake of sodium as compared and so sodium potassium ratio increases. Sodium and potas-
to control plant. We know that Na+ is the toxic compound sium (Na+ /K+ ) ratio is an important parameter regarding
caused osmotic stress and ionic imbalance, which alters the salinity evaluation in crops, determined the tolerance abil-
function of cell membranes by inhibiting the functions of ity of the crop to saline environment. Our results indicated
many enzymes [26] and reduces rice growth and productivity that Na+ /K+ ratio increases with increasing salinity in the

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Fig. 5 RT-PCR analysis ofOsMYB-2, OsMYB-6, OsZAT12-1 and DW: control; 50: 50 mM NaCl; 100: 100 mM NaCl; 150: 150 mM
OsZAT12-9 gene expression in rice leaves in response to smoke and dif- NaCl; 1:5000B: smoke solution; S50: smoke solution + 50 mM NaCl;
ferent concentration of salt stress. The detection was performed based S100: smoke solution + 100 mM NaCl; S150: smoke solution + 150
on three independent samples and actin I was used as internal control. mM NaCl

medium both in roots and in shoot, but the increase was higher MYB transcription factor is an important regulators of
in roots as compared to shoot (Fig. 4). Our results were in line gene expression which involve in the regulation of various
with other study [36], and they observed that salinity caused physiological and biochemical processes by initiating the
high Na+ /K+ ratio in roots than shoot. According to Zhu, target genes [40] and widely present in plants, animals and
[37,38] low ratio of Na+ /K+ in plant cells is necessary for fungi [41]. MYB transcription factor has also been known to
normal cellular activity and function, so by increasing salin- regulate salt and dehydration responsive genes [42,43]. Our
ity in growth medium, Na+ /K+ ratio increases causing ionic results indicate high expression of MYB-2 and MYB-6 genes
toxicity and nutritional disorders. However, smoke priming in the salt-treated plants in both varieties as Basmati-385 and
alleviates the drastic effect of salinity by lowering the uptake Shaheen Basmati (Fig. 5). Our results were in close agree-
of sodium ion concentration and increasing accumulation of ment with other report [44] that salt and dehydration stresses
K + in plant raised from smoke-treated seeds as compared increase the up regulation of MYB genes in rice because
with plants raised from hydro- primed seeds (Figs. 2, 3). This MYB genes were known to involve in signaling pathway
may be due to the fact that smoke may activate the enzymes when the plant was in stress condition [45]. In this study it
which are responsible for change the membrane permeabil- was observed that ZAT12 genes were induced by salt stress
ity, due to which the transport of Na+ may be reduced in (Fig. 4) in both varieties, which is similar to studies [8,46].
plant, which ultimately enhance K+ content [39]. Similarly, They concluded that different types of stresses as salt, heat,
Jamil et al.[20] reported that smoke might have some role in cold and oxidative stresses induced the expression of ZAT12
reducing the uptake of Na+ , which help the plant in the accu- genes in plants. According to Davletova et al. [9], the expres-
mulation of K+ and other useful compounds. Jain and Van sion of ZAT12 genes is regulated by heat-shock factor (HSF
Staden [25] observed that smoke-primed seeds had a higher 21) which give early response to H2 O2 which accumulate in
amount of nuclei than hydro-primed seeds in tomato, which plants under various types of stresses. Plant raised from seeds
helped in higher growth values under stress conditions such treated with smoke solution had no/less expression of MYB
as salinity. and ZAT12 genes in both Shaheen Basmati and Basmati-385

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as compared to salt stress plants (Fig. 5). Absence of gene 5. Bartels, D.S.R.: Drought and salt tolerance in plants. Crit. Rev.
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