Aboveground Whitefly Infestation-Mediated Reshaping of the Root Microbiota

Abstract

Plants respond to various types of herbivore and pathogen attack using well-developed defensive machinery designed for self-protection. Infestation from phloem-sucking insects such as whitefly and aphid on plant leaves was previously shown to influence both the saprophytic and pathogenic bacterial community in the plant rhizosphere. However, the modulation of the root microbial community by plants following insect infestation has been largely unexplored. Only limited studies of culture-dependent bacterial diversity caused by whitefly and aphid have been conducted. In this study, to obtain a complete picture of the belowground microbiome community, we performed high-speed and high-throughput next-generation sequencing. We sampled the rhizosphere soils of pepper seedlings at 0, 1, and 2 weeks after whitefly infestation versus the water control. We amplified a partial 16S ribosomal RNA gene (V1–V3 region) by polymerase chain reaction with specific primers. Our analysis revealed that whitefly infestation reshaped the overall microbiota structure compared to that of the control rhizosphere, even after 1 week of infestation. Examination of the relative abundance distributions of microbes demonstrated that whitefly infestation shifted the proteobacterial groups at week 2. Intriguingly, the population of Pseudomonadales of the class Gammaproteobacteria significantly increased after 2 weeks of whitefly infestation, and the fluorescent Pseudomonas spp. recruited to the rhizosphere were confirmed to exhibit insect-killing capacity. Additionally, three taxa, including Caulobacteraceae, Enterobacteriaceae, and Flavobacteriaceae, and three genera, including Achromobacter, Janthinobacterium, and Stenotrophomonas, were the most abundant bacterial groups in the whitefly infested plant rhizosphere. Our results indicate that whitefly infestation leads to the recruitment of specific groups of rhizosphere bacteria by the plant, which confer beneficial traits to the host plant. This study provides a new framework for investigating how aboveground insect feeding modulates the belowground microbiome.

Surviving in a Hostile World: Plant Strategies to Resist Pests and Diseases

“…Plants control their rhizosphere microbiome through root exudates (34,107,119), which change the chemical composition of the rhizosphere to attract and support beneficial microbes, such as plant growth-promoting rhizobacteria (PGPR) and mycorrhizal fungi (Figure 5) (59,129). Pests and diseases are known to alter root exudation composition, which can result in changes in soil-and root-associated microbiomes (11,46,68). Although the exact mechanisms driving these stress-induced changes remain unclear, key defense signaling chemicals, including SA, JA, and benzoxaxinoids, have been shown to influence microbial communities in the rhizosphere (26,58,73).…”

Inheritance of seed and rhizosphere microbial communities through plant–soil feedback and soil memory

“…The production of root exudates increases in response to herbivore and pathogen attack of aboveground (systemic) plant parts, suggesting that plants utilize an aggressive strategy to recruit beneficial soil microbes for the protection of distal plant parts (Tkacz et al, 2015;Kong et al, 2016;Berendsen et al, 2018). Collectively, saprophytic microbes recruited by plant pathogens and herbivore-infected plants may promote plant innate immunity.…”

“…Plants respond to various biotic and abiotic stresses using well-developed defence mechanisms. Under stress conditions, plants also benefit from interactions with quickresponding soil microbes (Berendsen et al, 2012;Kong et al, 2016;Pineda et al, 2017;Santos-Medillin et al, 2017). Survival of plants in the natural environment depends on their interaction with a complex and dynamic community of microbes.…”

“…and Stenotrophomonas spp. in the microbial community in the rhizosphere increases after whitefly feeding (Kong et al, 2016). In Arabidopsis thaliana, the abundance of Stenotrophomonas spp., Xanthomonas spp., and Mycobacterium spp.…”

Foliar herbivory by caterpillars and aphids differentially affects phytohormonal signalling in roots and plant defence to a root herbivore

“…Defence responses occur not only locally, but throughout the plant. Although most studies on systemic responses focus on above ground tissues, in response to induction in either another leaf or in the roots (Papadopoulou & van Dam, ; Soler et al, ), there is an increasing body of literature showing that roots respond to leaf herbivory as well (Gulati, Baldwin, & Gaquerel, ; Huang, Siemann, Xiao, Yang, & Ding, ; Kim, Song, & Ryu, ; Kong, Kim, Song, Lee, & Ryu, ; Machado et al, ; Machado, Arce, McClure, Baldwin, & Erb, ; Soler, Erb, & Kaplan, ).…”