Fall Armyworm-Associated Gut Bacteria Modulate Plant Defense Responses

Abstract

Mechanical damage caused by insect feeding along with components present in insect saliva and oral secretions are known to induce jasmonic acid-mediated defense responses in plants. This study investigated the effects of bacteria from oral secretions of the fall armyworm Spodoptera frugiperda on herbivore-induced defenses in tomato and maize plants. Using culture-dependent methods, we identified seven different bacterial isolates belonging to the family Enterobacteriacea from the oral secretions of field-collected caterpillars. Two isolates, Pantoea ananatis and Enterobacteriaceae-1, downregulated the activity of the plant defensive proteins polyphenol oxidase and trypsin proteinase inhibitors (trypsin PI) but upregulated peroxidase (POX) activity in tomato. A Raoultella sp. and a Klebsiella sp. downregulated POX but upregulated trypsin PI in this plant species. Conversely, all of these bacterial isolates upregulated the expression of the herbivore-induced maize proteinase inhibitor (mpi) gene in maize. Plant treatment with P. ananatis and Enterobacteriaceae-1 enhanced caterpillar growth on tomato but diminished their growth on maize plants. Our results highlight the importance of herbivore-associated microbes and their ability to mediate insect plant interactions differently in host plants fed on by the same herbivore.

Diversity of fall armyworm, Spodoptera frugiperda and their gut bacterial community in Kenya

“…Only three samples, two adult males from Kitale (Kitale-m2 and Kitale-m3) and one larvae from Ngeria (Ngeria-l2) were dominated by Firmicutes. Four genera of bacteria, Pseudomonas, Delftia, Enterococcus and Serratia that were recorded in this study have 15 previously been isolated from S. frugiperda (De Almeida et al 2017; Acevedo et al 2017). Surprisingly, Staphylococcus, Microbacterium, Arthrobacter and Leclercia that were previously isolated from S. frugiperda in Brazil (De Almeida et al 2017) were not found in any of the samples we profiled in Kenya.…”

“…Symbiotic bacteria play a key role in the biology of insects. We characterized the gut bacterial communities in S. frugiperda larvae and adult samples collected from several locations in Kenya, finding some important differences and similarities across samples and in relation to other studies on this species (Acevedo et al 2017; De Almeida et al 2017). Understanding the gut microbial symbionts of this pest species may facilitate the development of novel, cost-effective control strategies.…”

“…In Spodoptera exigua , the dominant bacterial clades are Proteobacteria and Firmicutes, with the predominant genus in larvae being Enterococcus . In S. frugiperda , previous studies have isolated several bacterial strains using culture-dependent methods (De Almeida et al 2017; Acevedo et al 2017). In this study, we used 16S rDNA sequence profiling to characterize the diversity of bacteria associated with populations of S. frugiperda in Kenya and assessed the prevalence of the corn and rice strains in these populations using Mitochondrial COI gene sequences.…”

Intraspecific differences in plant defense induction by fall armyworm strains

“…Leaf tissue (60–90 mg) frozen in liquid nitrogen was homogenized in a GenoGrinder 2000 (OPS Diagnostics, Lebanon, NJ, USA) and total RNA extracted using a modified Trizol protocol previously described (Acevedo et al ., ). Complementary DNA (cDNA) was synthesized from 1 μg of RNA using the High Capacity cDNA Reverse Transcription kit (Applied Biosystems) using Oligo‐dT following the manufacturer's protocol.…”

“…It is well known that oral secretions from caterpillars induce defenses in plants; however, caterpillars do not always secrete regurgitant during feeding (Peiffer & Felton, ). Therefore, we first quantified the amount of regurgitant secreted by the FAW strains on their host plants following a previously described procedure (Peiffer & Felton, ; Acevedo et al ., ), and then tested the plant defense response to the application of those regurgitant quantities. Regurgitant was collected from the oral cavity of plant‐fed caterpillars (by gently tapping their heads) and immediately placed on ice.…”