Induced Resistance to Sitobion Avenae by Bacillus Subtilis

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Induced resistance to Sitobion avenae by Bacillus subtilis, Zinc, and aphid feeding inTriticum aestivum L.  

 

Abstract

English grain aphid (EGA), Sitobion avenae (Fabricius), is an important worldwide phloem-feeding pest of wheat due to direct sucking damage and transmission of viruses. Here, we tested the effects of five treatments including; (1) wheat with a 6 days pest infestation period, (2) wheat grown in the collected field soil and then sprayed with Biomin zinc at 4-6 leaves stages, (3) wheat seed treated with Probio96 (Bacillus subtilis UTM96), and (4 and 5) combined treatments of Biomin zinc + Pre-infestation and B. subtilis  + Pre-infestation as well as a control on some secondary metabolites contents in wheat leaves, and fitness traits of aphidEGA. Results showed that there were significant differences among treatments concerning some secondary metabolites and fitness traits. The amount of total phenol content in wheat leaves significantly increased on B. subtilis + Pre-infestation (298.20 mg/ml) and Probio96 (292.17 mg/ml) than on other treatments. The net reproductive rate (R0) of EGA fed on plants treated with various treatments varied from 1.533 to 6.887 offspring individual-1, with the lowest and highest values on B. subtilis + Pre-infestation and control plants, respectively. The lowest and highest intrinsic rate of increase (r) of S. avenae were observed on B. subtilis + Pre-infestation and control plant (0.022 and 0.105 day-1,respectively). The lowest (0.024) and highest (0.058) nymphal growth index (NGI) of aphid were found on B. subtilis + Pre-infestation and control, respectively. Therefore, it was concluded that B. subtilis + Pre-infestation in wheat plants can induce systemic resistance to EGA, which can be used in the IPM of this aphid.

Keywords: Age-stage, two-sex life table, EGA, Plant-insect interactions.


Introduction

Wheat (Triticum aestivum L.; Poaceae) is an essential cereal grown in many parts of the world including Iran. This crop is constrained via both distractive sub-sucking insects and pathogens. One of the most important sub-sucking constraints of crop wheat is the damage inflicted via English grain aphid (EGA), Sitobion avenae (Fabricius) (Hemiptera: Aphididae), which is non-host-alternating species and a holocyclic aphid (Williams and Wratten 1987; Powell and Bale 2004). The feeding behavior of the nymph and adult of EGA not only cause direct damage via phloem-feeding but also can be increased transmit barley yellow dwarf virus (BYDV) that might result in significant crop losses (Oerke 1994; Thackray et al. 2009). Presently, the control of sub-sucking insects is mostly managed with synthetic insecticides; but, it causes the evolution of resistant populations through strong selective pressure (Bass et al., 2015). In the last decades, fertilizer- and insecticide- chemical applications were an agronomical method to increase yield, but their remains in crops have become a great concern of users in the current years (Savary et al. 2012). Some chemical fertilizers can have a positive influence on plant mineral nutrition, but it may result in the population of phytophagous pests enhanced through the nutritional quality of the host plants (Lu et al. 2007; Mardani-Talaee et al. 2016, 2017). Henceforward, the use of resistant cultivars (RC) and/or induction of resistance (IR) in the host plants are novel tactics for less emphasis on fertilizer- and insecticide- chemical in addition to an ecologically safe method for control sub-sucking and chewing insects (Herron et al. 2000; Shen et al. 2013).

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Induced systemic resistance (ISR) is a resistance mechanism in plants that can enhance the defense system via mechanical, biological, and chemical factors to plant pathogens and insect herbivores (Walters et al. 2013). The induction of plant defenses via insect feeding is also regulated through two key methods of action that consist of ISR and/or systemic acquired resistance (SAR) pathways (Traw and Bergelson 2003; Morkunas and Gabry´s 2011). During plant- phloem-feeding interactions, the most important defense systems to aphid are induced through phytohormones (for instance the salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and abscisic acid (ABA)) and molecular pathways (Hopkins et al. 2009; Morkunas and Gabry´s 2011; Pieterse et al. 2012; Giron et al. 2013). Synthetic JA is not directly toxic to herbivores (Kagale et al. 2004); although the SA signaling can induce defenses in some plant species via phloem-feeding insects (Poelman et al. 2008; Coppola et al. 2013).

Plants are in constant interaction with potentially beneficial microorganisms such as rhizobacteria (PGPR), which are the vital components of the soil and can expand plant growth in different biotic activities of the soil ecosystem for nutrient turn over (Pieterse et al. 2014; Verbon and Liberman 2016). Furthermore, PGPRs can improve ISR and/or SAR in crop plants to sub-sucking and chewing insects due to increasing JA- independent and JA- dependent genes (Bloemberg and Lugtenberg 2001; Valenzuela-Soto et al. 2010; Zamioudis et al. 2015; Verbon et al. 2017).

Recently, the study of ISR has become an active field of research due to negative influence on some phytophagous insects (Shelton 2004; Prado and Tjallingii 2007; Mahfuza and Gordo 2008; Huan– Huan et al. 2012; Mardani- Talaee et al. 2016). The purpose of this research was to evaluate the impact of mechanical (Pre-infestation), chemical (Biomin zinc), and biological (Probio96 [Bacillus subtilis UTM96]) treatments either individually or in combination on some secondary metabolites of the wheat leaves and the effects on the fitness of EGA under greenhouse conditions. This study can help to find some solutions for pest control management.

Materials and Methods

Plant and aphid cultures

In during 2018- 2019, the soil was collected from a fallow wheat field in Khorramabad plain (Lorestan province, Iran) (33°29׳16׳N, 48°21׳21׳E) and then soil analysis carry out that contained 6.00 mg/kg P, 0.160% K, 1.15% Ca; 0.087% N, 0.018% Na, 0.084% Mg, 0% Cu, 0% Zn, 0% Fe, 0% Mn, 0% C, pH= 7.55, and electrical conductivity (EC) = 0.891 deci Siemens/meter. The seeds of wheat cultivar Azar 2 were obtained from the Agricultural Research and Education Institute in Khorramabad, Iran. Afterword, the seed of wheat were developed in 2L pots (10 cm in diameter by 22 cm in height) that filled with a suitable mixture of soil (2 field soil and 1 sand, respectively) and protected via muslin (100 meshes) to prevent natural enemies attack. The pots were arranged in a completely randomized design within the greenhouse set at 25±5 °C, 60± 5% RH and 16:10 h (L:D) conditions. Once the plants reached to 4-6 leaf stage were used for the experiments.

The colony of EGA, S. avenae, was collected from a wheat field in Khorramabad in May 2018. It was transferred to the potted plants raised in the greenhouse under the above-mentioned conditions. To maintain an aphid colony, the individuals were weekly transferred from infested plants to new young plants. After rearing the EGA for numerous generations on the wheat plant, they were used in the experiments.

Experiments and treatments application

All following experiments including induction of resistance, some secondary metabolites, fitness traits, and growth index were carried out for all the treatments and control, which was replicated 50 times in a completely randomized design under greenhouse conditions including;

1. Aphid Per-infestation test; to determine the induced resistant by EGA apterous, adults (five aphids per plant) from the stock colony were transferred to central leaves of wheat plants. Aphids were removed from plants after being allowed to feed for 6 days. Then, the plants were kept aphid-free for 48 h. Afterward one adult aphid was transferred to each plant for the experiments.

2. Biomin zinc induced resistance; the chemical (Biomin zinc) was obtained from the Bazargan Kala Company in Tehran, Iran. Resistance was artificially induced on wheat via the foliar application of Biomin zinc spray (15%) with a concentration 0.1g per 1 lit of water at 4-6 expanded leaves stages. After 2 days, one adult aphid was transferred to each plant for the experiments.

3. Probio96 induced resistance; PGPR strain (bio-fertilizer of Probio96) for evaluation was obtained from the Biorun Company in Karaj, Iran. To determine the induced resistant via Probio96 (Bacillus subtilis strain UTM96), per seed of wheat was dipped into the concentration of l mL of B. subtilis before planting in plastic pots (8 cm in diameter by 7 cm in height) containing sterilized soil and sand. After that, the population of B. subtilis around 1×107 colony-forming units/mL was grown into each pot after planting. Then, in the 4-6 leaf stage, one adult aphid was transferred to each plant for the experiments.

4. Biomin zinc + Pre-infestation treatment; to determine the effects of Biomin zinc plus Pre-infestation period (6 days) treatments, all plants were sprayed with Biomin zinc (15%) in 4-6 leaf stage. Then, the Pre-infestation period (6 days) was carried out under the above-mentioned conditions.

5. Probio 96 + Pre-infestation treatment; to determine the effects of Probio96 plus pre-infestation period (6 days) treatments, all seed of plants were treated with B. subtilis strain UTM96 solution. Then, the Pre-infestation period (6 days) was carried out under the above-mentioned conditions.

6. Control; wheat seeds are grown in the collected field soil were utilized. Then, the treated and control plants were used for bioassays or/and extractions.

Determination of some secondary metabolites consist of flavonoids, anthocyanin and total phenolic in wheat leaves, T. aestivum

The value of flavonoids and anthocyanin in wheat leaves was investigated based on the method of Kim et al. (2003) using 0.1g of wheat leaves as sample and homogenized in a porcelain mortar via pestle. In a nutshell, 3 mL of acidified ethanol was gradually added to the substances of porcelain mortar and grinded the plant samples. Then, the samples were centrifuged at 12,000 g for 15min. Afterword, the supernatants were passed through the Whatman filter paper (No.1), and the tubes were incubated for 5min in a hot water bath (80 °C) for measuring the flavonoids. Finally, 1 mL of the reaction mixture was poured into cells of spectrophotometer and absorbance were read at the wavelengths of 230, 300, and 330nm. Also, a similar procedure was used to measure the anthocyanin except for that homogenized amount of 0.2 g of wheat fresh samples in acidified Methanol solution (3 mL). Followed by centrifugation at 12000 g for 15 min was centrifuged and then supernatants were passed from Whatman filter paper (No. 1). The reaction mixture was incubated in lightness for 24 h at room temperature and afterward, absorbance was read at 550 nm.

According to the method of Slinkard and Singleton (1997), the amount of total phenolic components of the wheat plant was assayed via adding 10 mL of Methanol (80 %) in 1 gr of fresh samples of wheat leaves. The samples were passed through Whatman filter paper (No. 1) and the supernatants centrifuged at 1000 g for 5 min. Afterward, 100 µL of samples, with 15000 µL of Folin–Ciocalteau (1:10) and 1400 µL sodium carbonate (7%) were incubated for 5 min at 35℃. Finally, the absorbance read at 765 nm.

Determination of the fitness of EGA, S. avenae

For evaluating of EGA fitness, 50 apterous adult aphids were randomly transferred to wheat leaves for pre-treatment. Each adult aphid restricted in a clip cage (8 cm diameter, 35cm height with a hole covered by a fine mesh net for ventilation) on leaf surface with suitable ventilation in the greenhouse conditions. The adult aphids EGA were eliminated from the clip cages after 24 hours. Each plant received one newborn nymph that was confined to the first true leaf. The duration of nymph and adult stages was recorded at 24 hours intervals on wheat leaves. After the appearance of adults, the duration of successive developmental stages and mortality was recorded daily until the adult died (Zhao et al. 2015).

The data were processed based on the theory of the age-stage and two-sex life table developed via Chi and Liu (1985), Chi and Su (2006) and Chi (2018). The life expectancy (exj) is the length of time that an individual of age x and stage j is expected to live and it was calculated as:

exj=i=xy=jβS׳iy

Where S׳iy is the possibility that individuals of age x and stage j will survive to age i and stage y, and is calculated by assuming S׳= 1.

The age-stage specific survival rate (Sxj) was calculated by dividing nxj (the number of individuals surviving to age x and stage j)byn01 (the total number of individuals used as the beginning of the demography study)

Sxj=nxjn01

The age-stage specific fecundity (fxj) is the mean fecundity of individuals of age x and stage j that was calculated by dividing Exj (total nymphs laid) by nxj (individuals).

fxj=Exjnxj

The formula for the age-specific survival rate (lx) and the age-specific fecundity (mx) are:

lx=j=1kSxj

mx=j=1kSxjfxjj=1kSxj

Where;

k is the number of stages

mx, the daily number of nymphs produced per adult aphids

Sxj, the probability that a newborn nymph will survival to age x and stage j  

fxj, the daily number of nymphs produced per adult aphid at age x.

The formula of the population parameters such as the gross reproductive rate (GRR) and the net reproductive rate (R0) are as follows:

GRR=X=αβmx

R0=x=0lxmx

The intrinsic rate of increase (r) can be estimated with the iterative bisection method via Euler- Lotka equation with age indexed from zero (Goodman 1982) and the finite rate of increase (λ) were calculated as;

x=0er(x+1)lxmx=1

λ=er

The mean generation time (T) is the time required for a population to increase to R0 fold at stable age-stage distribution and was calculated as:

T=LnR0r

The formula for the nymphal growth index (NGI) is based on the equation Setamou et al. (1999); 

NGI=lxT

Where;

lx; the survival rate of the nymphal stage

T; the period of each nymphal stage

Data analysis

In the first step, data of secondary metabolites were tested via Kolmogorov-Smirnov for normality. Then, data were analyzed by one-way analysis of variance (ANOVA) followed via comparison of the means with TurkeyHSD test, with a significant level at p< 0.05 using statistical software MINITAB 16.0. Also, data of life table were analyzed according to an age-stage, two-sex life table Chi (1988) and Chi and Liu (1985) and mean comparisons were done through the paired bootstrap test based on CI of differences using statistical software TWO-SEX-MSChart (Chi 2018). The method of bootstrap used 100,000 repetitions per treatment (Akca et al. 2015; Reddy and Chi 2015).

Results

The effect of treatments on the amounts of some secondary metabolites

Some secondary metabolites in un-infested leaves of wheat were significantly affected by the treatments (Table 1). The amount of flavonoids contents increased significantly in Probio96 (2.030, 1.848 and 1.962 mg/ml, respectively) in comparison to other treatments when the absorbance was read at 270, 300 (and 330nm, respectively. The lowest and highest contents of anthocyanin were recorded in Pre-infestation (1.409 mg/ml) and Biomin zinc + Pre-infestation (2.439 mg/ml) treatments, respectively; while there was no significant difference among maximum and minimum contents of anthocyanin compared to control. Total contents of phenol in the leaves varied significantly amongst different various treatments although the highest value was observed on Probio96 + Pre-infestation (298.20 mg/ml) and Probio96 (292.17 mg/ml), respectively; as well as the lowest value was observed in Biomin zinc + Pre-infestation (183.63 mg/ml). However, significant difference was found on treatments to control (Table 1).

Treatment effects on developmental time and fecundity of EGA, S. avenae

Results demonstrated that there were significant differences among treatments concerning the aphids nymphal development time (Table 2). The shortest nymphal development time of EGA was found on Biomin zinc (14.69 days) compared to the other treatments. The shortest adult longevity (6.78 days) was recorded in the EGA fed on Probio96 + Pre-infestation and the longest ones on control (14.77 days) and Probio96 (14.33 days), respectively. Significant differences were observed among different treatments in the reproductive period and adult pre-reproductive period (AROP) of EGA. The shortest reproductive period was recorded on Probio96 + Pre-infestation and Biomin zinc + Pre-infestation treatments (2.883 and 3.653 days, respectively) and the longest one was observed in control and Biomin zinc (5.778 and 5.293 days, respectively). The shortest and longest AROP of aphid were recorded on Probio96 + Pre-infestation (1.00 days) and Probio96 (1.53 days), respectively. Also, there were no significant differences among different treatments in the total pre-reproductive period (TROP) of EGA. The lowest and highest nymphal growth index (NGI) for the pre-adult stages were recorded 0.024 and 0.058 on Probio96+ Pre- infestation and control, respectively (Table 2).

Treatment effects on population growth parameters of EGA, S. avenae

Life table traits of EGA, S. avenae, also were significantly affected by different treatments (Table 3). The lowest value of gross reproductive rate (GRR) was observed in EGA fed on Probio96 + Pre-infestation and Biomin zinc + Pre-infestation (5.85 and 5.71 offspring, respectively) while the highest value was recorded on Biomin zinc (14.44 offspring). The net reproductive rate (R0) of EGA fed on plants treated with different treatments varied from 1.533 to 6.887 offspring individual-1, with the lowest and the highest values on Probio96 + Pre-infestation and control, respectively. The lowest intrinsic rate of increase (r) and finite rate of increase (λ) of EGA were observed on Probio96 + Pre-infestation (0.022 and 1.022 day-1, respectively) and the highest values on control (0.105 and 1.110 day-1, respectively. Also, there were no significant differences among various treatments in mean generation time (T) of EGA. The lowest daily fecundity (F) of EGA was recorded on Probio96 + Pre-infestation and Biomin zinc + Pre-infestation (3.83 and 4.07 offspring, respectively) and the highest one was found for control (7.77 offspring) (Table 3).

Treatment effects on life table parameters of EGA, S. avenae

Age-stage life expectancies (exj) of EGA, S. avenae, reared on various treatments are given in Figure 1. The exj of EGA at the first day was 28.18, 21.59, 20.31, 19.23, 17.26, and 16.44 days on control, Biomin zinc, Biomin zinc + Pre-infestation, Pre-infestation, Probio96, and Probio96 + Pre-infestation treated plants, respectively. The exj at the first day of the adult stage was also 22.93, 20.21, 19.82, 14.14, 12.34, and 6.26 days for control, Probio96, Biomin zinc, Pre-infestation, Biomin zinc + Pre-infestation and Probio96 + Pre-infestation, respectively. Hence, the lowest and highest exj belonged to the Probio96 + Pre-infestation and control-treated plants, respectively.

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The age-stage specific survival rates (Sxj) of EGA reared on different treatments are shown in Figure 2. The highest Sxj for adult stages (0.77) was recorded on control but the lowest value was found on Pre-infestation (0.31) and Probio96 + Pre-infestation (0.31) treatments, respectively.

Figure 3 shows the age-specific survival rates (lx) of EGA reared on different treatments. A single curve of the female age-stage specific fecundity (fx2) has been shown because only female adults produce offspring. The number of nymphs laid per day were recorded as control (1.25 nymph at 10nd day); Biomin zinc (1.33 nymph at 11nd day); Probio96 (1.50 nymph at 39nd day); Biomin zinc + Pre-infestation (1.66 nymph at 11nd day); Pre-infestation (2.00 nymph at 10 and 12nd days) and Probio96 + Pre-infestation (2.00 nymph at 9nd day) (Figure 3). The mx(the age-specific fecundity of the total population) value of EGA was 1.33 on Biomin zinc (at day 35); 1.00 on Pre-infestation (at days 28, 30 and 33); 1.00 on Probio96 + Pre-infestation (at day 28); 0.83 on control (at day 33); 0.83 on Probio96 (at day 29) and 0.40 on Biomin zinc + Pre-infestation (at days 20 and 25) nymph per female per day (Figure 3). Thus, the highest and lowest mx were observed on Biomin zinc and Biomin zinc + Pre-infestation, respectively.

The age-specific net maternity (lxmx) value of EGA was 0.50 on control (at day 22); 0.43 on Biomin zinc (at day 16); 0.28 on Probio96 (at day 18); 0.27on Pre-infestation (at day 20); 0.22 on Biomin zinc + Pre-infestation (at day 17) and 0.15 on Probio96 + Pre-infestation (at days 15, 18 and 22, respectively) nymphs on the nth day (Figure 4). Thus, the highest and lowest fecundity were observed on control and Probio96 + Pre-infestation, respectively (Figure 4).

Discussion

Currently, healthy and safe food free of poisonous remains is demanded by consumers. To avoid dangerous chemicals against insect pests, induce resistance (IR) can be used to reduce the pest population and resulting damage. Several researches have proved that IR via various factors in many plant species has negative effects on the fitness of insect pests (Mahfuza and Gordo 2008; Mithöfer and Boland 2012;Pieterse et al. 2014; Zamioudis et al. 2015; Mardani- Talaee et al. 2016; Verbon et al. 2017). According to the results achieved in this research, various artificial inductions led to significant effects on growth index (GI) and life table traits of EGA and on some secondary metabolites in the wheat leaves, which confirm the potential effects of plant quality in induced resistance to EGA, S. avenae.

Plants are frequently challenged via various herbivorous insects in their natural environments. They have to develop diverse defense responses to protect themselves against various insects (including aphids). So, decreasing and/or increasing fitness of phloem-feeding insects depends on the defense traits (for instances repellents, deterrents, anti-nutrients and -digestive compounds) of their host plants (Mithöfer and Boland 2012; Lu et al. 2014; Nikooei et al. 2015). Our results point out that the nymphal development time of EGA fed on T. aestivum-treated Biomin zinc reduced and their reproductive period time and AROP increased compared to the other treatments. Hence, the suitability of Biomin zinc for EGA can due to increase quantities of nutrients or reduce levels of defenses-related chemical compounds (such as flavonoids, anthocyanin, total phenol and etc.), which are synthesized via JA/ ET and SA pathways in response to various environmental stresses for instance insects and pathogens attacks (Bourgaund et al. 2010; Campos et al. 2014), and preclude the fitness of sub sucking insects (Mardani- Talaee et al. 2016).

The growth index (GI) represents the effects of nourishment quality on both survival rate and developmental time of herbivore insects (Setamou et al. 1999). The value of aphid NGI decreased on treatment versus control. Wheat- mediated B. subtilis + Pre-infestation reduces NGI and increase mortality rate of phloem feeding aphid EGA, S. avenae that can induce gene expression of transcription factors for activing flavonoids biosynthesis (Ali and McNear2014). Flavonoids are found in many plants as anti-feeding or/and pigments against herbivorous insects (Schoonhoven et al. 2005). The colonization of wheat roots via B. subtilis UTM96, can increase the amount of flavonoids contents in wheat leaves versus control and induce ISR to aphid EGA that including production of hypersensitive response (HR)-type reactions, apoplastic peroxidase activity, callose deposition, and reactive oxygen species (Lugtenberg and Kamilova 2009; Valenzuela-Soto et al. 2010; Niu et al. 2011; Pieterse et al. 2012; Rahman et al. 2015). Thus, increased flavonoid content in treatment with PGPRsand feeding aphid decreased the NGI of the EGA due to enhance plant defense mechanisms of host plants that shown ISR activity against aphid (Pineda et al. 2010; de Oliveira Araujo 2015).

The foliar spraying of the wheat plants via Biomin zinc increased GRR values of EGA, S. avenae, compared to other treatments. Zinc is a vital micronutrient for the function of various enzymes that is required for healthy growth and reproduction of plants, and plays an important role in synthesis of protein, lipids and carbohydrates, cell division, maintaining integrity of the membrane structure and nucleic acid metabolism in plants (Zlatimira and Doncheva 2002; Spiegel-Roy and Goldschmidt 2008). So, foliar application Zinc to the wheat plant may increase the nutritional quality of plants for EGA and result in its increased GRR and mx values.

B. subtilis + Pre-infestation- wheat interactions decreased R0, r, λ, exj, Sxj and lxmx values of EGA, S. avenae, that are generally due to the longer development time, higher morality of pre-adult stages, low fecundity, and a later peak in reproduction versus control. The amount of R0 illustrates the ratio of population growth in each generation over the earlier generation that associates the physiological capability of a creature to its reproductive ability (Carey 1993, 2001; Liu et al. 2004). Also, r is a basic parameter to prognosticate the population growth rate of an insect, which it will be an appropriate parameter to calculate the performance of a herbivore insect on various plants (Southwood and Henderson 2000). The total phenolic in leaves of wheat via B. subtilis + Pre-infestation commence IR and reduces the r of EGA that can dependent on molecular pathways. A direct role of phenolic compounds is IR against EGA aphid. However, evidence about the role of phenolic compounds in a plant is limited in conifer and unconvincing to herbivores (Mumm and Hilker 2006.( Phenolic compounds are the major class of secondary metabolites in plant defense to herbivorous insects (Tsai et al. 2006; Bernards and Bastrup-Spohr 2008; War et al. 2011). Treatment with B. subtilis + Pre-infestation and B. subtilis can enhanced amounts of total phenolic, which immediately procreate poisonous and/or HR in plants (Singh et al. 2015; Kiprovski et al. 2016). Numerous studies showed that colonization of plant roots via PGPRs induces ISR enhanced the amount of phenolic compounds, hydrogen peroxide (H2O2) production, cell death, and callose deposition with EGA infestation in plant that reduces consumption rates, and feeding performance of chewing- and phloem-feeding insects (De Vleesschauwer et al. 2008; Sharma et al. 2009; Rani and Jyothsna 2010; Mazid et al. 2011; Ali and McNear 2014). So, insect feeding also induced oxidative stress that is the main component of plant defense to sub-sucking feeding insects (Bi and Felton 1995; Lei et al. 2014). In general, the higher amounts of phenolic, H2O2 and other oxidative products of ROS in wheat leaves can directly damage the midgut of EGA and have considerable negative effects on amount of R0 and r parameters of EGA, S. avenae

The survival rates (Sxj) illustrate the beneficial potency of the age-stage, two-sex life table, which reveals substantially more information on the life table including the overlaps between stages due to incorporation of the variable developmental rates among individuals into the age-stage, two-sex life table. The peak Sxj for adult stages was recorded on control compared to Pre-infestation and B. subtilis + Pre-infestation treatments, respectively. Lack of awareness of the variable developmental rate among the individuals of a population and the use of the adult age inevitably will generate errors in the life table traits estimation (Yu et al. 2005) and the overlapping in the stage-specific survival curves could not be properly shown (Chi 1988). Thus, differences among the fitness of EGA could be attributed to chemical properties and/or physical characteristics of various treatments.

Anthocyanin is the soluble compounds in plant cells that can repel destructive pests and attract beneficial natural enemies (Chan and Harper 1976). In the present research, the level of anthocyanin contents in the un-infested leaves increased significantly on Biomin zinc + Pre-infestation vs. Pre-infestation treatment. Thus, increased anthocyanin in Biomin zinc + Pre-infestation treatment can both, directly and indirectly, affect the feeding performance of herbivorous insects.

In a nutshell, plant resistance can be improved by a variety of biotic and abiotic inducers that can be a valuable method in sustainable pest management. Our study demonstrated that B. subtilis + Pre-infestation as the effective host vis-à-vis other treatments to induce resistance of wheat toward EGA, S. avenae. It seems that B. subtilis + Pre-infestation can significantly decrease the population of EGA under greenhouse conditions, and hence, it is useful for ecological management of EGA in combination with other tactics. However, it should be performed in future studies.

 

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Table 1.The mean (±SE) amount of secondary metabolites in un-infested leaves of wheat on different treatments under greenhouse conditions [25± 5 °C, 65± 5% RH, and 16: 8 h (L:D)].

Table 2.The mean (±SE) developmental time of life stages of EGA, Sitobion avenae, reared on different treatments under greenhouse conditions [25± 5 °C, 65± 5% RH, and 16: 8 h (L:D)].

Table 3.The mean (± SE) life table parameters of EGA, Sitobion avenae, reared on different treatments under greenhouse conditions [25±5 °C, 65± 5% RH, and 16: 8 h (L:D)].

Figure 1. The age-stage life expectancies (exj) of EGA, S. avenae, reared on different treatments under greenhouse conditions [25± 5 °C, 65± 5% RH, and 16: 8 h (L:D)].

Figure 2. The age-stage specific survival rates (Sxj) of EGA, S. avenae, fed on different treatments under greenhouse conditions [25± 5 °C, 65± 5% RH, and 16: 8 h (L:D)].

Figure 3. The age- specific survival rate (lx), age-stage specific fecundity (fx) and age-specific fecundity (mx) of EGA, S. avenae, fed on different treatments under greenhouse conditions [25± 5 °C, 65± 5% RH, and 16: 8 h (L:D)].

Figure 4. The age-specific net maternity (lx mx) of EGA, S. avenae, fed on different treatments under greenhouse conditions [25± 5 °C, 65± 5% RH, and 16: 8 h (L:D)].

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