Molecular cross-talk in a unique parasitoid manipulation strategy

Kaiser, Maayan; Arvidson, Ryan; Zarivach, Raz; Adams, Michael E.; Libersat, Frédéric

doi:10.1016/j.ibmb.2018.11.009

Cited by 12 publications

(14 citation statements)

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“…Venoms are generally a complex mixture with correspondingly complex effects on an animal's physiology, and the jewel wasp seems to be a prime example of this truism [Moore et al, 2006[Moore et al, , 2018Banks and Adams, 2012;Arvidson et al, 2016Arvidson et al, , 2019Kaiser et al, 2019]. Neverthe-DOI: 10.1159/000511548 less, for the case of the wasp's stings to the 2nd thoracic ganglion, it seems reasonable to hypothesize about a mechanism based on the well-known anatomy and neurophysiology of the roach locomotor system.…”

Section: Discussionmentioning

confidence: 99%

“…In fact, acetylcholine is a prominent component of some wasp venoms [e.g., Piek, 1986]. However, as far as the author knows, acetylcholine has not been identified in the jewel wasp's venom [Banks and Adams, 2012;Arvidson et al, 2016Arvidson et al, , 2019Moore et al, 2018;Kaiser et al, 2019]. And yet, milked venom for previous analysis is presumably taken from wasps prior to sting 1 and sting 2.…”

Section: Discussionmentioning

confidence: 99%

“…The epic battle between the jewel wasp and the American cockroach (Periplaneta americana) was first described in detail by the entomologist Francis Williams in 1942 [Williams, 1942], and since that time, the wasp has become one of the most famous and well-studied parasitoids. It has been the subject of many investigations [i.e., Williams, 1942;Piek et al, 1984;Veltman and Wilhelm, 1991;Richardson and Paul, 1993;Fouad at al., 1994;Weisel-Eichler et al, 1999;Gal et al, 2005;Banks and Adams, 2012;Moore et al, 2018;Arvidson et al, 2016Arvidson et al, , 2019Kaiser et al, 2019], and it holds a prominent place in the emerging field of neuroparasitology [Hughs and Libersat, 2018]. Moreover, the model system is covered in many biology classes and is often featured in popular science accounts because it captures the public's imagination.…”

Section: Introductionmentioning

confidence: 99%

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Getting the Most Out of Your Zombie: Abdominal Sensors and Neural Manipulations Help Jewel Wasps Find the Roach’s Weak Spot

Catania

2020

Brain Behav Evol

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The parasitoid emerald jewel wasp (<i>Ampulex compressa</i>) subdues the American cockroach (<i>Periplaneta americana</i>) with a sting to the 1st thoracic ganglion, followed by a sting to the roach’s brain, causing long-term pacification. The wasp then leads the cockroach to a hole where it lays an egg on the roach middle leg before barricading the entrance and departing. Although many aspects of the wasp’s initial attack have been investigated, few studies have detailed the egg-laying process and the subsequent fate of the larvae. Here I show that larval survival depends on precise egg positioning on the cockroach by the female wasp. Ablation of sensory hairs on the wasp’s abdomen resulted in mislaid eggs, which seldom survived. In addition, the cockroach femur may block the oviposition site. The wasp contended with this challenge with a newly discovered suite of stings, 3 directed into the 2nd thoracic ganglion which resulted in extension of the femur, thus exposing the oviposition site and removing a potential barrier to the wasp’s successful reproduction. When the femur was glued in place, the wasp stung the cockroach over 100 times, in an apparent fixed action pattern triggered by the obscured oviposition target. These findings highlight the importance of proper egg placement by the wasp, and reveal sensors and new neural manipulations that facilitate the process.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Getting the Most Out of Your Zombie: Abdominal Sensors and Neural Manipulations Help Jewel Wasps Find the Roach’s Weak Spot

Catania

2020

Brain Behav Evol

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“…Using affinity chromatography and Label Free Quantitative Mass Spectrometry (LFQMS), Kaiser et al (2019) found that the venom binds to synaptic proteins and that numerous proteins are differentially expressed in the CX of stung cockroaches. Many of differentially expressed proteins are involved in signal transduction pathways, such as the Rho GTPase pathway, which is implicated in synaptic plasticity.…”

Section: The Cerebral Ganglia (Crg)mentioning

confidence: 99%

On the Role of the Head Ganglia in Posture and Walking in Insects

et al. 2020

Self Cite

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In insects, locomotion is the result of rhythm generating thoracic circuits and their modulation by sensory reflexes and by inputs from the two head ganglia, the cerebral and the gnathal ganglia (GNG), which act as higher order neuronal centers playing different functions in the initiation, goal-direction, and maintenance of movement. Current knowledge on the various roles of major neuropiles of the cerebral ganglia (CRG), such as mushroom bodies (MB) and the central complex (CX), in particular, are discussed as well as the role of the GNG. Thoracic and head ganglia circuitries are connected by ascending and descending neurons. While less is known about the ascending neurons, recent studies in large insects and Drosophila have begun to unravel the identity of descending neurons and their appropriate roles in posture and locomotion. Descending inputs from the head ganglia are most important in initiating and modulating thoracic central pattern generating circuitries to achieve goal directed locomotion. In addition, the review will also deal with some known monoaminergic descending neurons which affect the motor circuits involved in posture and locomotion. In conclusion, we will present a few issues that have, until today, been little explored. For example, how and which descending neurons are selected to engage a specific motor behavior and how feedback from thoracic circuitry modulate the head ganglia circuitries. The review will discuss results from large insects, mainly locusts, crickets, and stick insects but will mostly focus on cockroaches and the fruit fly, Drosophila.

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“…4 As a consequence of the rapid development of transcriptomics and proteomics in recent years, venom proteins from numerous parasitoids have been identified, and it is clear that their numbers and functions vary dramatically across species. 6 Venom proteins have been shown to control host behaviors, 7,8 host development, 9, 10 metabolism 11 and immune responses. [12][13][14][15] However, the functions of most identified venom proteins have not been investigated experimentally and very few have been shown to have cytotoxic activity.…”

Section: Introductionmentioning

confidence: 99%

Characterization of a cell death‐inducing endonuclease‐like venom protein from the parasitoid wasp Pteromalus puparum (Hymenoptera: Pteromalidae)

Wang

Yan

Xiao

et al. 2020

Pest Management Science

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BACKGROUND: Parasitoid wasps are valuable natural enemies for controlling pests. To ensure successful parasitism, these wasps inject venoms along with their eggs that are deposited either into or on their hosts. Parasitoid venoms regulate host behaviors, development, metabolism and immune responses. Pteromalus puparum is a pupal endoparasitoid that parasitizes a number of butterflies, including the worldwide pest cabbage butterfly, Pieris rapae. Venom from P. puparum has a variety of effects on host hemocytes, including alteration of absolute and relative hemocyte counts, and inhibition of hemocyte spreading and encapsulation. In particular, P. puparum venom causes hemocyte cell death in vivo and in vitro. RESULTS: Using assay-guided chromatography, a cell death-inducing venom fraction was identified and defined as P. puparum endonuclease-like venom protein (PpENVP). It belongs to the DNA/RNA nonspecific endonuclease family, which contains two conserved endonuclease activation sites. We analyzed its expression profiles and demonstrated that PpENVP inhibits gene expression in transfected cells relying on two activation sites. However, RNA interference of PpENVP did not significantly reduce P. puparum venom cytotoxicity, suggesting that PpENVP may not be the sole cytotoxic factor present. CONCLUSION: Our results provide novel insight into the function of the P. puparum venom cocktail and identify a promising insecticide candidate endonuclease that targets insect hemocytes.

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Molecular cross-talk in a unique parasitoid manipulation strategy

Cited by 12 publications

References 97 publications

Getting the Most Out of Your Zombie: Abdominal Sensors and Neural Manipulations Help Jewel Wasps Find the Roach’s Weak Spot

Getting the Most Out of Your Zombie: Abdominal Sensors and Neural Manipulations Help Jewel Wasps Find the Roach’s Weak Spot

On the Role of the Head Ganglia in Posture and Walking in Insects

Characterization of a cell death‐inducing endonuclease‐like venom protein from the parasitoid wasp Pteromalus puparum (Hymenoptera: Pteromalidae)

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