Elevated O₃ and TYLCV Infection Reduce the Suitability of Tomato as a Host for the Whitefly Bemisia tabaci.

Hongying Cui,Youjun Zhang,Feng Ge,Fajun Chen,Yucheng Sun

doi:10.3390/ijms17121964

Abstract

The effects of elevated atmospheric ozone (O3) levels on herbivorous insects have been well studied, but little is known about the combined effects of elevated O3 and virus infection on herbivorous insect performance. Using open-top chambers in the field, we determined the effects of elevated O3 and Tomato yellow leaf curl virus (TYLCV) infection on wild-type (Wt) tomato and 35S tomato (jasmonic acid (JA) defense-enhanced genotype) in association with whitefly, Bemisia tabaci Gennadius biotype B. Elevated O3 and TYLCV infection, alone and in combination, significantly reduced the contents of soluble sugars and free amino acids, increased the contents of total phenolics and condensed tannins, and increased salicylic acid (SA) content and the expression of SA-related genes in leaves. The JA signaling pathway was upregulated by elevated O3, but downregulated by TYLCV infection and O3 + TYLCV infection. Regardless of plant genotype, elevated O3, TYLCV infection, or O3 + TYLCV infection significantly decreased B. tabaci fecundity and abundance. These results suggest that elevated O3 and TYLCV infection, alone and in combination, reduce the nutrients available for B. tabaci, increase SA content and SA-related gene expression, and increase secondary metabolites, resulting in decreases in fecundity and abundance of B. tabaci in both tomato genotypes.

Highlights

The concentration of global atmospheric ozone (O3) has increased from 10 parts per billion in the 1900s to the current value of 40 ppb, at an annual rate of 1%–2% [1,2]
We found that Tomato yellow leaf curl virus (TYLCV) infection significantly increased secondary metabolites, salicylic acid (SA) content, and SA-related gene expression, but decreased jasmonic acid (JA) content and JA-related gene expression in Wt tomato plants
Secondary metabolite content, SA content, and the expression of SA-related genes were higher in 35S::prosystemin transgenic tomato plants (35S) plants than in Wt plants in the elevated O3 treatment, but were lower in 35S plants than in Wt plants in the TYLCV infection and O3 + TYLCV infection treatments. This resulted in lower B. tabaci fecundity and abundance on 35S plants than on Wt plant with the elevated O3 treatment, but higher fecundity and abundance on 35S plants than on Wt plants with the TYLCV infection and O3 + TYLCV infection treatments. These results indicate that the JA-overexpression tomato mutant 35S has higher resistance to B. tabaci than Wt plants under elevated O3, and that resistance to B. tabaci is decreased by TYLCV infection of 35S plants

Summary

Introduction

The concentration of global atmospheric ozone (O3) has increased from 10 parts per billion (ppb) in the 1900s to the current value of 40 ppb, at an annual rate of 1%–2% [1,2]. Elevated O3 causes leaf damage, inhibits photosynthesis, and reduces the growth of many plant species [4,5]. O3 enters the plant through stomata and is converted into reactive oxygen species (ROS), triggering a series of metabolic reactions [6,7]. Excess ROS can disrupt plant metabolism by causing irreversible damage to cell membranes, proteins, and carbohydrates [8]. Elevated O3 may change levels of primary metabolites and their allocation, leading to decreased nutrient content and increased levels of secondary metabolites in plant tissues [9,10]. Changes in the physical and chemical qualities of plant tissues are expected to affect herbivorous insects [11,12,13]. Reduced plant quality is thought to be directly related to the virus susceptibility of plants grown in high-O3 environments [7,14]

Methods

Results

Discussion

Conclusion