Mealybug salivary microbes inhibit induced plant defenses

Abstract

BACKGROUNDPhenacoccus solenopsis is a polyphagous invasive mealybug that caused serious damage to crops worldwide. Phloem‐sucking hemipterans are known to carry symbiotic microbes in their saliva. However, the role of salivary bacteria of P. solenopsis in modulating plant defenses remains limited. Exploring the impact of salivary bacteria on plant defense responses will contribute to the development of new targets for efficient control of invasive mealybugs.RESULTSSalivary bacteria of the invasive mealybug P. solenopsis can suppress herbivore‐induced plant defenses and thus enhance mealybug fitness. Mealybugs treated with an antibiotic showed decreased weight gain, fecundity and survival. Untreated mealybugs suppressed jasmonic acid (JA)‐regulated defenses but activated salicylic acid (SA)‐regulated defenses in cotton plants. In contrast, antibiotic‐treated mealybugs triggered JA‐responsive gene expression and JA accumulation, and showed shortened phloem ingestion. Reinoculating antibiotic‐treated mealybugs with Enterobacteriaceae or Stenotrophomonas cultivated from mealybug saliva promoted phloem ingestion and fecundity, and restored the ability of mealybugs to suppress plant defenses. Fluorescence in situ hybridization visualization revealed that Enterobacteriaceae and Stenotrophomonas colonize salivary glands and are secreted into the mesophyll cells and phloem vessels. Exogenous application of the bacterial isolates to plant leaves inhibited JA‐responsive gene expression and activated SA‐responsive gene expression.CONCLUSIONOur findings imply that symbiotic bacteria in the saliva of the mealybug play an important role in manipulating herbivore‐induced plant defenses, enabling this important pest to evade induced plant defenses and promoting its performance and destructive effects on crops. © 2023 Society of Chemical Industry.

Semiochemicals Produced by Microbes in Mealybug Honeydew Attract Fire Ants

“…We recently found that Bacillus, Staphylococcus, Microbacterium, and Pseudomonas were colonized in P. solenopsis saliva . It is highly likely that these honeydew bacteria are derived from the salivary gland and gut of P.…”

“…The universal primers 27F/ 1492R (27F: 5′-AGAGTTTGATCCTGGCTCAG-3′ and 1492R: 5′-GGTTACCTTGTTACGACTT-3′) were used to amplify 16S rRNA. The detailed procedure of 16S rRNA amplicon sequencing and the primers used have been described in our previous study 23 Attractiveness of Honeydew Bacteria to Fire Ants. To determine which isolated bacteria elicit the behavioral preference of fire ants, the behavioral response of fire ants to each identified bacterium was evaluated.…”

“…The universal primers 27F/ 1492R (27F: 5′-AGAGTTTGATCCTGGCTCAG-3′ and 1492R: 5′-GGTTACCTTGTTACGACTT-3′) were used to amplify 16S rRNA. The detailed procedure of 16S rRNA amplicon sequencing and the primers used have been described in our previous study 23 and are presented in Text S5.…”

“…We recently found that Bacillus, Staphylococcus, Microbacterium, and Pseudomonas were colonized in P. solenopsis saliva. 23 It is highly likely that these honeydew bacteria are derived from the salivary gland and gut of P. solenopsis. A previous study reported the isolation of two cultivable bacteria, S. sciuri and Acinetobacter calcoaceticus, from A. pisum honeydew.…”

Influence of Microbes in Mediating Sorghum Resistance to Sugarcane Aphids

“…The S. symbiotica in pea aphids upregulated the effector in the salivary glands and suppressed the plant defences, which facilitated the colonization of aphids on host plants [39]. Similarly, symbiotic bacteria present in the mealybug (Phenacoccus solenopsis) saliva modulated phytohormone levels, thereby enhancing mealybug colonization on host plants [40]. Whether SCA endosymbionts utilize a similar or different mechanism(s) to manipulate host defences is yet to be determined.…”