Dietary Stress From Plant Secondary Metabolites Contributes to Grasshopper (Oedaleus asiaticus) Migration or Plague by Regulating Insect Insulin-Like Signaling Pathway.

Shuang Li,Xiongbing Tu,Mark Richard Mcneill,Xunbing Huang,Jingchuan Ma,Zehua Zhang,Shenjin Lv,Wen Liu

doi:10.3389/fphys.2019.00531

Abstract

Diets essentially affect the ecological distribution of insects, and may contribute to or even accelerate pest plague outbreaks. The grasshopper, Oedaleus asiaticus B-Bienko (OA), is a persistent pest occurring in northern Asian grasslands. Migration and plague of this grasshopper is tightly related to two specific food plants, Stipa krylovii Roshev and Leymus chinensis (Trin.) Tzvel. However, how these diets regulate and contribute to plague is not clearly understood. Ecological studies have shown that L. chinensis is detrimental to OA growth due to the presence of high secondary metabolites, and that S. krylovii is beneficial because of the low levels of secondary metabolites. Moreover, in field habitats consisting mainly of these two grasses, OA density has negative correlation to high secondary metabolites and a positive correlation to nutrition content for high energy demand. These two grasses act as a ‘push-pull,’ thus enabling the grasshopper plague. Molecular analysis showed that gene expression and protein phosphorylation level of the IGF → FOXO cascade in the insulin-like signaling pathway (ILP) of OA negatively correlated to dietary secondary metabolites. High secondary metabolites in L. chinensis down-regulates the ILP pathway that generally is detrimental to insect survival and growth, and benefits insect detoxification with high energy cost. The changed ILP could explain the poor growth of grasshoppers and fewer distributions in the presence of L. chinensis. Plants can substantially affect grasshopper gene expression, protein function, growth, and ecological distribution. Down-regulation of grasshopper ILP due to diet stress caused by high secondary metabolites containing plants, such as L. chinensis, results in poor grasshopper growth and consequently drives grasshopper migration to preferable diet, such as S. krylovii, thus contributing to grasshopper plague outbreaks.

Highlights

Half of all insect species are herbivores (Gatehouse, 2002; Wu and Baldwin, 2010), that have co-evolved with plants for 350 million years (Kessler and Baldwin, 2002)
From routine surveys of plant and grasshoppers composition in Stipa (S. krylovii) and Leymus (Leymus chinensis) (Trin.) Tzvelev (Poales: Poaceae) grasslands (Han et al, 2008), we found that O. asiaticus was mainly confined to the former (Huang et al, 2016, 2017a)
Grasshoppers that fed on L. chinensis had reduced growth variables compared to those fed on S. krylovii, which indicated that L. chinensis was unsuitable for O. asiaticus compared to S. krylovii

Summary

Introduction

Half of all insect species are herbivores (Gatehouse, 2002; Wu and Baldwin, 2010), that have co-evolved with plants for 350 million years (Kessler and Baldwin, 2002). Plants have evolved various defense mechanisms against phytophagous insect (Padul et al, 2012) Such defenses can be broadly classified into two categories: constitutive defenses, including physiological barrier and nutritional hurdle; and inducible defenses, including secondary metabolites and protein inhibitors (PIs) (Zavala et al, 2004; Wu and Baldwin, 2010; Padul et al, 2012). Indirect defenses include volatile organic compounds produced when the plant is subject to herbivory that attract predators and parasitoids of the insect (Dicke and Loon, 2000; Despland and Simpson, 2005; Despres et al, 2007). Insect dietary stress predominantly originates from high levels of plant secondary metabolites (Behmer, 2009; Despres et al, 2007; Wetzel et al, 2016)

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