Effect of foliar application of Silicic acid on biological parameters of Lipaphis erysimi and activity of plant defensive enzymes in rapeseed

doi:10.21203/rs.3.rs-4389846/v1

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Effect of foliar application of Silicic acid on biological parameters of Lipaphis erysimi and activity of plant defensive enzymes in rapeseed

https://doi.org/10.21203/rs.3.rs-4389846/v1

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published 20 Sep, 2024

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Silicic acid (SA) is an important source of silicon (Si) that induces resistance in plants against insect pests. The present investigation aimed to investigate the impact of foliar spray of SA on the biological parameters of aphid, Lipaphis erysimi and the activity of defensive enzymes in rapeseed. The results demonstrated applying 0.4% SA significantly reduced the nymphal period, adult longevity and fecundity of L. erysimi compared to the control. In the 0.4% SA- treated rapeseed, the nymphal period, adult longevity and fecundity of L. erysimi were 7.00 days, 7.96 days and 23.52 nymphs/ female, respectively, while in the control, these were 7.92 days, 8.80 days and 26.04 nymphs/ female, respectively. The present investigation revealed that there were no significant changes in activity of defense related enzymes such as peroxidase (POD), polyphenol oxidase (PPO) and phenylalanine ammonia- lyase (PAL) in 0.4% SA- treated rapeseed without aphid infestation. However, a significant increase in the activity of these enzymes was observed in rapeseed amended with 0.4% SA that were subsequently infested with aphids. The application of SA significantly increased the Si content in rapeseed. Furthermore, the study established a significant negative correlation between Si content and biological parameters of L. erysimi.

Silicon

silicic acid

rapeseed

aphid

defensive enzymes

Rapeseed is the third most important oilseed crop in the world (Rai et al. 2016) playing a key role in agricultural economy. India is the third largest producer of rapeseed after Canada and China, contributing approximately 27% of the total oilseed production of the country with an annual production of 30.55 million tones and a productivity of 1188 kg per hectare (Kumar et al. 2022). Despite the high production potentiality and wider adaptability to varied agroclimatic conditions of the country, the yield of rapeseed-mustard in India has been fluctuating because of various biotic and abiotic stresses (Sharma et al. 2019). Amongst the biotic stresses, insects are one of the major constraints of rapeseed cultivation, causing considerable yield loss. Rapeseed is attacked by at least 30 insect species, among which, aphid, Lipaphis erysimi alone causes a yield loss up to 90% in India (Patel et al. 2019).

Although the application of insecticides is the most common and popular practice against L. erysimi, it has consequences such as insecticide resistance, secondary pest outbreak and adverse effects on non-target organisms (Ujjan and Shahzad 2012). In contrast, silicon (Si) is the second most abundant element after oxygen in the earth’s crust (Laine et al. 2019) that helps to enhance the resistance in crops against biotic stresses including arthropod pests (Islam et al. 2023). It has been proved that application of Si could be an ecofriendly alternative to the synthetic chemicals against chewing insect pests viz., Chilo infuscatelus, Scirpophaga incertulas, Cnaphalocrocis medinalis and Spodoptera frugiperda (Alvarenga et al. 2017; Han et al. 2015; Liang et al. 2015) and sucking pests viz., Nephotettix virescens, Nilaparvata lugens, including aphids Brevicoryne brassicae, Aphis craccivora and Rhophalosiphum maidis (Abdollahi et al. 2021; Islam et al. 2020; Moraes et al. 2005; Parthiban et al. 2019) that induces resistance through mediation and upregulation of inducive resistance mechanisms of plants (Alhousari and Greger 2018).

Silicic acid (SA) is a major available source of Si for the plants (Shwethakumari et al. 2021). It has been reported that the application of SA improves the yield and oil content of rapeseed (Karthik et al. 2024; Kuai et al. 2017). SA i.e. Si(OH)₄, is a bioavailable form of silicon (Shwethakumari et al. 2021), which get translocated through the xylem and condenses into polymerized silica gel on the shoots creating a physical barrier against insect feeding (Massey and Hartley 2009). It also acts indirectly through biochemical and physiological mechanisms (Islam et al. 2020). Previous study has indicated that foliar application of SA can reduce L. erysimi colonization (Karthik et al. 2023). However, there is a lack of research specifically examining the effect of SA foliar application on the biological parameters of L. erysimi. Therefore, this study aims to investigate the impact of SA foliar application on various biological parameters of L. erysimi in rapeseed.

Peroxidase (POD), polyphenol oxidase (PPO) and phenylalanine ammonia-lyase (PAL) are some of the important biochemical enzyme systems that confer resistance against herbivore attack (Sha et al. 2015). Si has been shown to increase the activity of these plant defensive enzymes during insect infestation (Han et al. 2015), leading to enhanced plant defenses against herbivory. However, the specific activity of these enzymes during L. erysimi infestation in rapeseed treated with silicon or SA is not yet known. Thus, this study also explores the hypothesis that SA foliar application induces the activity of these plant defensive enzymes in rapeseed plants, aiding in the defense against L. erysimi infestation.

Experiment 1: Effect of foliar spray of silicic acid on biological parameters of L. erysimi

Raising of plants and Treatment details

The certified seeds of the popular and recommended rapeseed variety TS-38 were collected from the Assam Agricultural University-Zonal Research Station (AAU-ZRS), Shillongani, Assam and raised in the experimental pots following standard package of practices recommended for rapeseed and mustard. These pots were kept protected in wooden insect rearing cages and maintained properly. Two treatments viz., Foliar spray of 0.4% SA thrice i.e. 30,40 and 50 days after sowing (DAS) at 10 days interval (n = 25), and a control (n = 25) were performed. The Si source utilized in this study was concentrated soluble SA, acquired from ReXil Agro BV, Chennai, India. This formulation contains 2% Si in the form of soluble H₄SiO₄. It was applied at concentration of 4 ml L^− 1, corresponding to 0.4% solution.

Insect maintenance and observation

Before performing the experiment, the aphid (L. erysimi) population was collected from the available rapeseed fields and its culture was maintained in the laboratory for up to 2 generations. The clip cage experiment was performed to study the biological parameters of aphids (Haas et al. 2018). Five days after the final application of treatments, the newly laid adult apterous aphids from the laboratory culture were individually placed on the abaxial surface of the leaves of rapeseed plants maintained in the pots. The newly laid nymphs and adults were removed on the next day of release and only one nymph was kept for studying the nymphal and adult period of aphid. In another set of plants, only adult aphids were maintained, and all the newly laid nymphs were counted and removed daily to record fecundity.

Estimation of Silicon content

To quantify the Si content, the plant samples were collected after experimentation and dried properly. Then the samples were powdered, pre-digested and microwave digested with acid composition and the Si content was estimated using the molybdenum blue colorimetric method at 600 nm (Laxmanarayanan et al. 2022).

Experiment 2: Determination of the activity of plant defensive enzymes

To study the activity of plant defensive enzymes with application of SA and aphid infestation, rapeseed variety TS-38 that were maintained under pots in protected in wooden insect rearing cages. Four treatments viz., 0.4% SA alone, aphid alone, 0.4% SA + aphid and a control (no aphid infestation + no SA application) were applied and replicated quadruple. In SA treatments, three foliar sprays of SA were applied starting from 30 DAS up to 50 DAS at ten days interval. Five days after applying final foliar spray, twenty numbers of newly emerged laboratory cultured adult aphids were released on the potted plants, wherever aphid infestation treatments were applicable.

Plant defensive enzyme analysis

Preparation of enzyme extracts

The leaf sample (2 g each) at 24 h after releasing the aphids were collected from the plants and brought to the Physiology Laboratory, AAU, Jorhat for preparation of extract. The leaf samples were grounded using pestle mortar after adding liquid nitrogen, added 2 ml of phosphate buffer (pH 6.0), and centrifuged for 15 minutes at 15000 rpm with the help of refrigerator centrifuge separately for each of the tested enzymes viz., peroxidase (POD) and polyphenol oxidase (PPO). In the case of phenylalanine ammonia lyase (PAL), 3 ml of 100 mM borate buffer having the pH 8.7 was added to the 2 g leaf sample after grinding, spun at 10000 rpm, 4ºC for 25 mins in refrigerated centrifuge, and the supernatant was collected for analysis of PAL (Savani et al. 2020). The leaf samples of the rapeseed plants were collected at 24 h intervals up to 96 h after releasing the aphids and analyzed to figure out the change in activity of defensive enzymes.

Determination of POD activity

To 0.01 ml of enzyme extract, 3.0 ml of 0.05 M pyrogallol was added. Then 0.5 ml of 3% H₂O₂ was added, and the optical density (OD) was measured at 436 nm between 30 s and 150 s. A reaction mixture consists of 3.0 ml of 0.05 M pyrogallol and 0.5 ml of 3% H₂O₂ was served as a blank. The unit activity/ g fresh weight per minute was used to express the POD activity (Savani et al. 2020).

Determination of PPO activity

One hundred micro liter of enzyme extract was taken on a test tube, to which 2.4 ml of phosphate buffer was added and later 0.5 ml of pyrogallol was added. Then the OD was measured at 495 nm once in every 10 minutes and the PPO activity was quantified. Only 3 ml of phosphate buffer was taken as a blank (Mahadevan and Sridhar 1982).

Determination PAL activity

The reaction mixture comprises 0.2 ml of enzyme extract, 1 ml of 0.1mM phenylalanine and 2.5 ml of 100 mM borate buffer (pH 8.7) was kept in a water bath at 32ºC for 30 minutes. Then the enzyme reaction was stopped by adding 0.5 ml of 1M trichloro acetic acid. The OD value was measured at 290 nm and the PAL activity was expressed as the synthesis of µmol trans-cinnamic acid / min / mg of protein. The reaction mixture without enzyme extract was taken as blank. Trans-cinnamic acid standard was prepared with different concentrations used to estimate PAL activity (Burrell and Rees 1984).

Statistical analysis

The data on biological parameters of L. erysimi and Si content was analyzed with the ‘independent Student t test’ (Ross and Willson 2017) while the plant defensive enzyme activity of the rapeseed plant was subjected to analysis of variance (ANOVA) with a completely randomized block design (CRD). In the present study the level of significance (α) was fixed as 5%. Hence all conclusions were made at 95% confidence level. The normality of the data was examined by Shapiro Wilk’s test (Shapiro and Wilk 1965) and the homogeneity of variance assumption was examined using Bertlett’s Test (Chao and Glaser 1978). Pearson’s correlation analysis (Gomez and Gomez 1984) was also performed to find out the relation between silicon content and biological parameters of L.erysimi. All the statistical analyses were done by using the R Software (R core Team 2022) with the R packages “agricolae” (Mendiburu and Yaseen 2020).

Biological parameters of L. erysimi

The nymphal period of L. erysimi varied significantly between control and 0.4% SA and the average nymphal period in the 0.4% SA amended rapeseed was the lower (7.00 days) as against 7.92 days in the control (Fig. 1). Similarly, the adult longevity of L. erysimi in 0.4% SA was the lowest (7.96 days) against 8.80 days in the control (Fig. 2). The fecundity of L. erysimi also significantly decreased in 0.4% SA amended plants (23.52 nymphs/ female) when compared to control (26.04 nymphs/ female) (Fig. 3).

Silicon content

The percentage of silicon content in rapeseed (Fig. 4) treated with 0.4% SA was the highest (0.31%) against 0.16% in the control.

Correlation between Si content of rapeseed and biological parameters of L. erysimi

The Si content of rapeseed had a significant and negative correlation between nymphal period (r= -0.61), adult longevity (r=-0.46) and fecundity (r=-0.64) of L. erysimi (Fig. 5).

POD activity

At all-time points, the treatments with 0.4% SA alone and the control did not cause any change in POD activity (Fig. 6). But right after aphid infestation, both the treatments i.e. aphid alone and 0.4% SA + aphid release triggered the POD activity in the leaves of rapeseed. At 24 h after infestation, the activity of POD was significantly higher in treatment with 0.4% SA spray + aphid infestation (1.504 (∆) Abs/min/g) as compared to aphid infestation alone (1.302 (∆) Abs/min/g). Compared to 24 h after aphid infestation, at both 48 and 72 h after aphid infestation, the POD activity was significantly higher in treatment with 0.4% SA + aphid as compared to aphid alone. At 96 h after aphid infestation, the enzyme activity gets reduced, recording the POD activity of 0.996 (∆) Abs/min/g in 0.4% SA + aphid which was significantly higher than aphid alone treatment.

PPO activity

The control and the treatment with SA alone did not change the activity of PPO at all time points. At 24 h after aphid infestation, the highest PPO activity was recorded in treatment with 0.4% SA spray + aphid release (0.049 (∆) Abs/min/g), which was statistically at par with the treatment of aphid infestation alone (0.045 (∆) Abs/min/g). The PPO activity was increased at 48 h after infestation in both aphid alone and 0.4% SA + aphid treatments. However, the PPO activity was significantly higher in 0.4% SA + aphid treatment as compared to the aphid alone treatment. The PPO activity remains stable around 0.048 (∆) Abs/min/g after 48h in aphid alone treatment. The PPO activity (0.053 (∆) Abs/min/g) was decreased at 72 h after aphid infestation in 0.4% SA + aphid condition. After 72h of infestation, the PPO activity in 0.4% SA + aphid condition becomes stable and it is similar to aphid alone treatment. The highest PPO activity of 0.058 (∆) Abs/min/g was recorded at 48h after aphid infestation under 0.4% SA + aphid treatment condition (Fig. 7).

PAL activity

The PAL activity was significantly increased in the treatment with 0.4% SA + aphid treatment as compared aphid infestation alone. At 24 h after aphid infestation, the PAL activity was recorded as 0.449 µ mol of trans-cinnamic acid/ min/ g in treatment with 0.4% SA + aphid as compared to 0.386 µ mol of trans-cinnamic acid/ min/ g in aphid alone (Fig. 8). The PAL activity was found slightly enhanced at 48 h after infestation. The highest PAL activity was recorded at 72 h after infestation by L. erysimi recording 0.601 µ mol of trans-cinnamic acid/ min/ g in treatment with 0.4% SA + aphid, while 0.518 µ mol of trans-cinnamic acid/ min/ g in aphid alone. Unlike POD and PPO, the PAL activity at 96 h after infestation was slightly higher than that of 24 h of infestation.

In the present experiment, it was found that SA application significantly reduced the biological fitness of L. erysimi, negatively affecting the nymphal period, adult longevity and fecundity. Prior research on the effect of Si application on aphid biology is minuscule. For example, Si application negatively affected the biology of Sitobion avenae in wheat (Dias et al. 2014), Myzus persicae in Zinnia elegens (Ranger et al. 2009) and Aphis gossypii in cotton (Tawfeek and Eldesouky 2022). Application of Si affects insects by enhancing the physical and chemical defensive responses of plants (Reynolds et al. 2016). Si acts as a feeding deterrent, disrupting insect feeding behaviour (Liang et al. 2015). For example, Si application reduces the probing time of Schizaphis graminum in wheat, leading to more frequent stylet withdrawals (Goussain et al. 2005). This, in turn reduces nutrient absorption and affects growth and reproduction of insect. From the current investigation, it is suggested that the reduced biological fitness in L. erysimi in SA amended rapeseed may be due to increased plant defensive responses and reduced nutrient absorption. The Si content in rapeseed significantly increased with the application of SA, as supported by previous studies (Karthik et al. 2023; Kuai et al. 2017), which aligns with the findings of the present investigation.

Plant defense related enzymes play a key role in eliciting biochemical resistance against biotic stress (Belete, 2018). Plants produce reactive oxygen species (ROS) during the herbivore attack conferring resistance, but excessive ROS production causes cytotoxic effects to plants (He et al. 2011). Excess ROS is produced during aphid infestation and the enzyme POD activity is important to protect the plants from adverse effects (He et al. 2011). POD is an important antioxidant enzyme that prevents these cytotoxic effects and cell damage by involving in degradation of H₂O₂ system (Sudhakar et al. 2001). In the present study, the POD activity in rapeseed was significantly enhanced with the application of SA under L. erysimi infestation. Earlier studies also confirmed that the application of calcium silicate significantly enhanced the POD activity in wheat against aphids Schizaphis graminum (Gomes et al. 2005). The enhancement of the POD activity was also noticed in the potassium silicate amended citrus trees against black fly, Aleurocanthus woglumi infestation (Vieira et al. 2014). These findings clearly show the role of Si in inducing the POD activity thereby protecting crops during excess production of ROS due to insect infestation.

The enzyme PPO plays a crucial role in protecting plants from insect pests attack by involving in phenol oxidation and lignin formation (Li and Steffens 2002). The present research indicates that PPO activity increases following infestation by L. erysimi, with significantly higher levels observed in rapeseed plants amended with SA. Si enhances PPO activity during herbivore attack, as demonstrated by the significant increase in PPO activity in cotton infested with Aphis gossypii, after potassium silicate application (Tawfeek and Eldesouky 2022). The present findings align with the previous studies. For example, Yang et al. (2017) reported that the Si amendment through sodium silicate induced the PPO activity, as a defensive response of rice against infestation by Nilaparvata lugens. Similarly foliar application of SA significantly increased the PPO activity in wheat after pink borer infestation (Jeer et al. 2022).

An important plant defensive enzyme, PAL facilitates the production of secondary metabolites, phenolics, phytoalexins and lignins (Lin et al. 2022). Han et al. (2016) found that Si addition alone did not change the PAL activity in rice but increases more in Si amended plants upon infestation of Cnaphalocrocis medinalis. The present investigation found a similar pattern in the PAL activity in rapeseed upon infestation of L. erysimi. Previous research has also reported increased PAL activity in Si treated rice plants upon infestation of N. lugens (Lin et al. 2022). Furthermore, a recent report demonstrated increased PAL activity in Si applied wheat plants, affecting the life cycle of aphid, Sitobion avenae (Qi et al. 2024). The results of present investigation are in line with these findings, showing that foliar application of SA significantly enhances PAL activity in rapeseed against L. erysimi, thereby affecting its biological parameters and reduce the biological fitness.

The current investigation confirms that the addition of Si in rapeseed decreases the growth and reproduction of L. erysimi. Furthermore, Si induces the activity of plant defensive enzymes against L. erysimi infestation in rapeseed. However, to better understand the underlying mechanisms, future research should focus on molecular studies to identify related genes and elucidate the upregulation mechanisms that suggest silicon’s role in inducing plant defensive enzymes against L. erysimi attack in rapeseed.

Acknowledgement

The authors express their gratitude to the Department of Entomology, Assam Agricultural University, Jorhat for providing the necessary facilities to conduct this experiment.

Funding statement

The authors declare that no fund received to conduct the experiments

Author contributions

Karthik R, Mukul Kumar Deka and Prakash, N. B: Planned the experiment

Prakash, N. B: Supplied silicic acid for experiments

Karthik R and Mukul Kumar Deka: Conducted the experiments

Karthik R, Mukul Kumar Deka and Surajit Kalita: Wrote the manuscript

Ajith S: Data Analysis

Compliance with Ethical Standards

The authors declare the investigation follows ethical standards.

Conflict of Interest

The authors declare no conflict of interest.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Data availability and Materials

The data generated for this study are included in the Supplementary file.

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Effect of foliar application of Silicic acid on biological parameters of Lipaphis erysimi and activity of plant defensive enzymes in rapeseed

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Journal Publication

Version 1

Abstract

Figures

Introduction

Materials and Methods

Raising of plants and Treatment details

Insect maintenance and observation

Estimation of Silicon content

Experiment 2: Determination of the activity of plant defensive enzymes

Plant defensive enzyme analysis

Preparation of enzyme extracts

Determination of POD activity

Determination of PPO activity

Determination PAL activity

Statistical analysis

Results

Silicon content

POD activity

PPO activity

PAL activity

Discussion

Conclusion

Declarations

References

Supplementary Files

Status:

Journal Publication

Version 1