Nanosilicon enhances maize resistance against oriental armyworm (Mythimna separata) by activating the biosynthesis of chemical defenses

https://doi.org/10.1016/j.scitotenv.2021.146378Get rights and content

Highlights

  • 50 mg/L Si nanodots and sodium silicate significantly inhibited the growth of maize armyworm.

  • Si nanodots have better foliar adhesion and bioavailability than conventional silicate fertilizer.

  • Si nanodots induced the upregulation of key genes involved in chlorogenic acid biosynthesis.

  • Nanosilicon is emerging as a promising new abiotic elicitor for plant production and chemical defenses.

Abstract

Silicon, in its nanoscale form, has shown plant-promoting and insecticidal properties. To date, however, we lack mechanistic evidence for how nanoscale silicon influences the regulation of plant chemical defenses against herbivore attacks. To address this gap, we compared the effect of Si nanodots (NDs) and sodium silicate, a conventional silicate fertilizer, on maize (Zea mays L.) chemical defenses against the oriental armyworm (Mythimna separata, Walker) caterpillars. We found that Si NDs and sodium silicate additions, at the dose of 50 mg/L, significantly inhibited the growth of caterpillars by 53.5% and 34.2%, respectively. This increased plant resistance was associated with a 44.2% increase in the production of chlorogenic acid, as well as the expression of PAL, C4H, 4CL, C3H and HCT, core genes involved in the biosynthesis of chlorogenic acid, by 1.7, 2.4, 1.9, 1.8 and 4.5 folds, respectively. Particularly, in the presence of M. separata, physiological changes in maize plants treated with 50 mg/L Si NDs, including changes in shoot biomass, leaf nutrients (e.g., K, P, Si), and chemical defense compounds (e.g., chlorogenic acid, total phenolics), were higher than those of plants added with equivalent concentrations of conventional silicate fertilizer. Taken together, our findings indicate that Si, in nanoscale form, could replace synthetic pesticides, and be implemented for a more effective and ecologically-sound management of insect pests in maize crop farming.

Introduction

In recent years, nanoparticles (NPs) have been widely applied in the fields of electroanalytical biosensors, nanomedicine and biofuels (McNamara and Tofail, 2017; Sekoai et al., 2019; Zhang and Wei, 2016). In addition, the use of NPs has gained considerable interest in agricultural settings, due to their beneficial, and potentially environmentally-friendly, effects on plant growth, plant resistance and food production (Athanassiou et al., 2018; Hofmann et al., 2020; White and Gardea-Torresdey, 2018). Indeed, an assessment of 78 studies indicates that the efficacy of nano-agrochemicals (e.g., nanopesticides, nanofertilizers) were significantly higher than their conventional analogues by 20–30% (Kah et al., 2018), and as a consequence, various nano-enabled strategies were proposed to improve crop protection agasint pests (Kah et al., 2019). Metal-based NPs, more specifically, have also been shown to exhibit insecticidal properties, and have thus been advocated to be used as bioactive pesticide agents (White and Gardea-Torresdey, 2018). For instance, larval and pupal weights of two lepidopteran pests, Spodoptera litura and Achaea janata, significantly decreased when they were fed with castor leaves treated with 500–4000 mg/L polyvinyl pyrrolidone coated-Ag NP suspensions (Yasur and Rani, 2015). Similarly, a rearing environment containing 20 mg/L nickel NPs for cowpea beetles (Callasobruchus maculates) adults resulted in 96.29% mortality rate (Elango et al., 2016). Despite of the high efficacy that NPs provide to pest control, the spreading of high doses of metal-based NPs (e.g., Ag NPs, Cu(OH)2 NPs) into the environment, can also result in heavy-metal phytotoxicity, and ultimately could cause risk of environmental contamination (Li et al., 2019). Therefore, the research for the use of NPs as an alternative to synthetic pesticides should be steered toward finding the appropriate NPs identity and dosage that, while being efficient against the target pests, should also minimize environmental pollution.

The metalloid silicon (Si) is the second most abundant element in the Earth's crust, as it forms the basis of silicious rocks. For plants, the bioavailable form of Si is the orthosilicic acid Si(OH)4 (Tubaña and Heckman, 2015). Si(OH)4 has been amply shown to promote plant growth, and increase plant resistance against biotic and abiotic stresses (Etesami and Jeong, 2018; Johnson et al., 2021; Waterman et al., 2020). Accordingly, together with the advantage of being generally inert, Si can be safely integrated into agricultural practices without harmful impacts on crop food, humans and environment health (Boraei et al., 2014). In addition, Si NPs (e.g., nanosilica) can more easily penetrate plant leaves and more efficiently affect their morphology and physiology than conventional silicate fertilizers (Rastogi et al., 2019). Therefore, agricultural scientists are questioning whether Si NPs can be used instead of silicate fertilized for enhancing plant growth and resistance against biotic stressors, such as insect herbivory (Mathur and Roy, 2020; Prasad et al., 2017). For instance, 5 mg/L fluorescent SiO2 NPs exposure under hydroponic conditions has been shown to promote rice plant resistance against the phloem-piercing pest planthopper Nilaparvata lugens by increasing lignin content by 30.13%, as well as the formation of silica cells in the stem (Cheng et al., 2021). Spraying nanosilica on leaves at doses of 300 and 350 mg/L resulted in 69% and 98% mortality of the African cotton leafworm Spodoptera littoralis, respectively (El-Bendary and El-Helaly, 2013). Spraying maize leaf with 0.4% SiO2 NPs also decreased the feeding rate of Mythimna separata caterpillars by 44%, and extended its larval stage period from 26 days to 31 days (Mousa et al., 2014). However, how exactly Si NPs increase the resistance of crop plants to insect pests is not yet well understood.

Evidence indicates that Si-mediated plant resistance against herbivores is dependent on the following two major processes (Luyckx et al., 2017). First, accumulation of Si in plants enhances the tissues' physical strength and abrasiveness, and thus helps reducing plant palatability and digestibility for herbivores (Massey and Hartley, 2009). Second, Si addition has been shown to alter biochemical and molecular processes related to the activation of plant chemical defenses (Singh et al., 2020; Ye et al., 2013). Particularly, a growing body of evidence shows that NPs can induce plant defenses via the activation of genes related to early responses to stress (El-Shetehy et al., 2020; Garcia-Sanchez et al., 2015; Lopez et al., 2020). Thereby, Si NPs have distinctive physiological characteristics that allow them to enter the plants, and alter plant molecular and metabolic activities. However, the advantage of nanosilicon application over the application of the corresponding bulk material for pest control, as well the regulatory effect of Si NPs on plant chemical defenses still needs to be explored.

In the present study, we aimed to compare the pest control efficacy of Si NDs and sodium silicate, which is a commonly used conventional silicate fertilizer and could provide insect herbivore resistance as well. Moreover, we aimed to investigate the molecular mechanisms for how Si NDs mediate chemical defense activation in plants. To address our aims, we measured maize (Zea mays) resistance against the oriental armyworm, Mythimna separata (Lepidoptera: Noctuidae), a polyphagous pest of numerous food crops, including rice, wheat and maize (Younas et al., 2018). Mythimna separata is widely distributed in Asia, Oceania, and Africa, in which it continues to pose severe threat to maize production particularly (Duan et al., 2017; Kim et al., 2018). In order to reduce damage caused by M. separata, high doses of synthetic pesticides (e.g., pyrethroid and organophosphorus insecticides) are traditionally applied, leading to negative impacts on non-target organisms, human and environmental health (Haddi et al., 2020; Rani et al., 2020). Moreover, the ever increasing and extensive application of pesticides has induced resistance in several M. separata populations (Sun et al., 2017). Accordingly, alternative solutions need to be explored for controlling insect pests, like M. separata, and thus reduce environmental harm and our current dependence on synthetic agrochemicals for food production (Athanassiou et al., 2018; Stenberg, 2017).

Specifically, we addressed the three following questions: i) Is the effect of Si NDs on maize resistance dose-dependent? ii) Are Si NDs more efficient than traditional chemical silicon fertilizer for increasing maize resistance against M. separata? And iii) are Si NDs efficient abiotic elicitors for increasing plant resistance, specifically by promoting the up-regulation of key genes involved in the biosynthesis of chemical defenses in plants? By addressing these questions, our study builds toward combining Si-based nanotechnology as a novel axis of the integrated pest management strategy for a more ecologically-sound and sustainable maize crop farming.

Section snippets

Nanosilicon and conventional silicon fertilizer

The Si NDs were synthesized by one-step method (Na et al., 2019). Briefly, 2.3 g of sodium ascorbate (AS) was dissolved with 8.0 mL ultrapure water, and then 2.0 mL of 3-(2-Aminoethylamino) propyldimethoxymethylsilane (DAMO) was mixed with the above AS solution in 80 °C water bath. After 8 h of stirring, the overplus reactants were removed with a dialysis bag (1 kDa, molecular weight cutoff) for about 5 h. The morphology of the obtained Si NDs was determined using transmission electron

Si-mediated effects on maize plant growth under herbivore stress

Plant growth in terms of shoot and root biomass was significantly influenced by Si treatment and herbivore stress, but was not by their interactions (Table S4). We observed variable effects of different Si forms and doses on plant growth in the absence or presence of herbivory (Fig. 1). More specifically, the ND50, SS50 and SS150 treatment significantly increased maize shoot biomass by 30.4%, 34.4% and 22.3% in the absence of M. separata, respectively (Fig. 1a). When maize plant grew under the

Conclusions

In this study, we demonstrated that foliar spray of nanosilicon, particularly at the dose of 50 mg/L, induced higher plant resistance to M. separata than the traditional chemical silicon fertilizer. Such effect was correlated to the induction of several key genes involved in chlorogenic acid biosynthesis, which ultimately resulted in the induction of chlorogenic acid, and as well as all phenolics, in maize leaves. Correspondingly, under herbivore stress, 50 mg/L Si nanodots enhanced shoot

CRediT authorship contribution statement

Zhenyu Wang: Conceptualization, Writing - original draft, Funding acquisition. Wenqing Zhu: Investigation, Methodology, Data analysis. Feiran Chen: Writing - review & editing, Funding acquisition. Le Yue: Investigation, Validation. Ying Ding: Material synthesis. Hao Xu: Resources. Sergio Rasmann: Writing - review & editing. Zhenggao Xiao: Conceptualization, Experimental design, Writing - review & editing, Funding acquisition.

Declaration of competing interest

All authors declared no conflict of interest.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (41820104009, 41807381, 41907304), Jiangsu Planned Projects for Postdoctoral Research Funds (2018K168C) and the Natural Science Foundation of Jiangsu Province (BK20190618). We thank Miss Yan Feng and Yangyang Ma for their kind help in laboratory analyses.

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