Abstract
The family Pentatomidae (Hemiptera: Heteroptera) includes several invasive stink bug species capable to attack a large number of wild and cultivated plants, causing several damages to different crops. Pentatomids rely on obligate symbiotic associations with bacteria of the family Enterobacteriaceae, mainly of the genus Pantoea. A distinctive trait of these associations is the transmission route: during oviposition, females smear egg masses with symbiont-containing secretions, which are ingested by newly hatched nymphs, allowing the symbiont to pass through their digestive tract and establish in the crypts of the posterior midgut. Preventing newborns from orally acquiring symbionts seriously affects their fitness and survival. This symbiont inheritance process can be manipulated to develop innovative pest control measures by sterilization of egg masses prior to nymph hatching. This review summarizes the recent knowledge advances concerning the gut primary symbionts of pentatomids, with a specific focus on the most troubling pest species for agriculture. Current understanding of host colonization dynamics in pentatomids is presented, as well as the phenotypic effects determined in different insect species by the alteration of vertical transmission. Details on the current knowledge on the whole bacterial communities accompanying primary symbionts are analyzed. The recent research exploiting the perturbation of symbiont acquisition by pentatomid nymphs is discussed, by considering published work on laboratory and field trials with several active substances. These translational strategies are presently regarded as promising for limiting the populations of many important pentatomid pests in a sustainable way.
Highlights
Obligate symbioses with bacteria are widespread in many insect orders, and have particular evolutionary significance in species with nutritionally restricted diets
Morphological studies of the midgut of adult stink bugs highlighted a differentiation between males and females, with females displaying enlarged posterior midgut and bacteria occurring in the main tract outside of crypts, to allow egg smearing of symbiotic cells during oviposition (Hayashi et al, 2015)
P. carbekii genome analysis, besides showing the genetic potential for nutrient provisioning to the host, indicated that this bacterium shares some genomic traits with intracellular primary symbionts of insects, such as a reduced genome size (0.7–0.9 Mb) and a low G+C content (Kenyon et al, 2015)
Summary
Obligate symbioses with bacteria are widespread in many insect orders, and have particular evolutionary significance in species with nutritionally restricted diets. In Pentatomidae, bacteria of the family Enterobacteriaceae are often related to the genus Pantoea (Duron and Noël, 2016) These symbionts are obligate mutualists, provide their hosts with missing nutrients in their diets (Kenyon et al, 2015; OteroBravo et al, 2018), and inhabit crypts of the terminal portion of midgut, named region V4 (Fukatsu and Hosokawa, 2002; Prado et al, 2006; Karamipour et al, 2016). The persistence of symbionts in the extrachorion matrix—outside the insect tissues—is supported by genomes that, even though reduced with respect to their free-living counterparts, are larger than those of intracellular primary symbionts commonly found in other Hemiptera Their genomes retain genes encoding essential factors for autonomous life, such as those for the cell wall synthesis (Bergmann et al, 2014). Under an operational framework of sustainable pest control strategies, the environmental phase of the life cycle of these bacteria can be exploited to interfere with the symbiont acquisition process by the newborns that may impair their development (Taylor et al, 2017; Gonella et al, 2019; Kashkouli et al, 2019b)
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