Colorado potato beetle exploits frass‐associated bacteria to suppress defense responses in potato plants

Abstract

BACKGROUND: Colorado potato beetle (CPB; Leptinotarsa decemlineata) is a destructive quarantine pest that develops broad physiological adaptations to potato plants. During feeding, CPB deposits a copious amount of wet frass onto the surface of leaves and stems that remains in place for long periods. Insect behaviors such as feeding, crawling and oviposition are able to mediate plant defenses. However, the specific role of CPB defecation-associated cues in manipulating plant defenses remains unclear.RESULTS: CPB larval frass significantly suppressed potato polyphenol oxidase activity and enhanced larval growth on treated potato plants. The incorporation of antibiotics into larval frass triggered higher jasmonic acid (JA)-regulated defense responses in potato plants compared with antibiotic-free frass. Four bacterial symbionts belonging to the genera Acinetobacter, Citrobacter, Enterobacter and Pantoea were isolated from larval frass and suppressed plant defenses. After reinoculation of these bacteria into axenic larvae, Acinetobacter and Citrobacter were found to be highly abundant in the frass, whereas Enterobacter and Pantoea were less abundant probably due to the negative effect of potato steroidal glycoalkaloids (SGA) such as ⊍-solanine. Furthermore, direct application of Acinetobacter and Citrobacter to wounded potato plants significantly inhibited the expression of genes associated with the JA-mediated defense signaling pathway and SGA biosynthesis. CONCLUSION: Our findings demonstrate that CPB exploits frass-associated bacteria as a deceptive strategy of plant defense suppression, adding an interesting dimension to our understanding of how CPB successfully specializes on potato plants.

Rice Defense Responses Orchestrated by Oral Bacteria of the Rice Striped Stem Borer, Chilo suppressalis

“…Among these isolates, Enterobacter and Acinetobacter were found to suppress JA-responsive defense when directly applied to rice plants. Our previous studies showed that Enterobacter and Acinetobacter isolated from the OS of Leptinotarsa juncta and the frass of Leptinotarsa decemlineata suppressed polyphenol oxidase activity in tomato plants and potato plants, respectively (Wang et al 2016 ; Gao et al 2022 ). In addition, changes in gene expression of maize inoculated with Enterobacter isolated from caterpillars were similar with maize gene profile change after insect feeding (Li et al 2022 ).…”

Challenges and opportunities in managing pests of potato

“…Ten of the research papers in this issue are on CPB; these papers provide evidence that RNA interference (RNAi), Bt toxin, and semiochemicals have attributes to become important tools in controlling CPB populations in potato IPM. [1][2][3][4][5][6][7][8][9][10] Zebra chip disease (ZC), associated with the plant pathogenic bacterium 'Candidatus Liberibacter solanacearum' (psyllaurous) (CLso), is another major threat to global potato production. This special issue contains a review article that provides a brief history of ZC and potato psyllid, a summary of currently available tools to manage ZC, and a comprehensive review of breeding efforts for ZC and potato psyllid management within the greater context of IPM strategies.…”

“…Novel and effective means of controlling CPB populations are constantly required to protect potato crops and prevent yield loss. Ten of the research papers in this issue are on CPB; these papers provide evidence that RNA interference (RNAi), Bt toxin, and semiochemicals have attributes to become important tools in controlling CPB populations in potato IPM 1–10 …”