The interaction of the bioinsecticide PA1b (Pea Albumin 1 subunit b) with the insect V-ATPase triggers apoptosis

Abstract

PA1b (Pea Albumin 1, subunit b) peptide is an entomotoxin, extracted from Legume seeds, with a lethal activity towards several insect pests, such as mosquitoes, some aphids and cereal weevils. This toxin acts by binding to the subunits c and e of the plasma membrane H+-ATPase (V-ATPase) in the insect midgut. In this study, two cereal weevils, the sensitive Sitophilus oryzae strain WAA42, the resistance Sitophilus oryzae strain ISOR3 and the insensitive red flour beetle Tribolium castaneum, were used in biochemical and histological experiments to demonstrate that a PA1b/V-ATPase interaction triggers the apoptosis mechanism, resulting in insect death. Upon intoxication with PA1b, apoptotic bodies are formed in the cells of the insect midgut. In addition, caspase-3 enzyme activity occurs in the midgut of sensitive weevils after intoxication with active PA1b, but not in the midgut of resistant weevils. These biochemical data were confirmed by immuno-histochemical detection of the caspase-3 active form in the midgut of sensitive weevils. Immuno-labelling experiments also revealed that the caspase-3 active form and V-ATPase are close-localized in the insect midgut. The results concerning this unique peptidic V-ATPase inhibitor pave the way for the utilization of PA1b as a promising, more selective and eco-friendly insecticide.

The functions of caspase in whitefly Bemisia tabaci apoptosis in response to ultraviolet irradiation

“…Strica is necessary for histolysis of salivary glands during metamorphosis and plays redundant roles in oogenesis in the ovaries (Baum et al, ). Similar research has been conducted on various insect species, including Bombyx mori (Zhang et al, ; Yi et al, ; Wang et al, ), Apis mellifera (Wu et al, ), Aedes albopictus (Feng et al, ; Meng et al, ), Helicoverpa armigera (Yang et al, ), Spodoptera frugiperda (Huang et al, ), Nilaparvata lugens (Huang et al, ), Spodoptera littoralis (Liu et al, ) and Sitophilus oryzae (Eyraud et al, ). However, the function of the caspase gene in Bemisia tabaci is completely unknown.…”

“…For example, DREDD can promote the synthesis of antimicrobial peptides and participate in an organism's innate immune response (Elrod-Erickson et al, 2000). Dronc plays an important role in apoptotic cell death by inducing the effector caspase DrICE (Kumar and Doumanis, 2000;Hay and Guo, 2006;Fan and Bergmann, 2010). In D. melanogaster, DrICE is abundantly expressed in all stages and necessary for the development of pupal retina, embryonic nervous system and adult wings (Fraser and Evan, 1997;Muro et al, 2006;Xu et al, 2006).…”

Clitoria ternatea (butterfly pea) cyclotides: insights on functional diversity, regulation and biotechnological applications

“…PA1b also adopts a cystine-knot topology which makes it resistant to trypsin digestion and renders it thermostable at 120⁰C for 15 mins [54]. Like cyclotides, the PA1b peptide is reported to have insecticidal activities [54][55][56][57]. However, unlike cyclotides where their bioactivity is due to membrane disruption, the insecticidal activity of PA1b is primarily attributed to its ability to inhibit the vacuolar-ATPase (V-ATPase) in the plasma membrane [55,57].…”

“…Like cyclotides, the PA1b peptide is reported to have insecticidal activities [54][55][56][57]. However, unlike cyclotides where their bioactivity is due to membrane disruption, the insecticidal activity of PA1b is primarily attributed to its ability to inhibit the vacuolar-ATPase (V-ATPase) in the plasma membrane [55,57]. Membrane proton pumps are essential for maintaining cellular pH and homeostasis, thus inhibition results in cell death [55,58].…”

“…However, unlike cyclotides where their bioactivity is due to membrane disruption, the insecticidal activity of PA1b is primarily attributed to its ability to inhibit the vacuolar-ATPase (V-ATPase) in the plasma membrane [55,57]. Membrane proton pumps are essential for maintaining cellular pH and homeostasis, thus inhibition results in cell death [55,58]. Further studies have shown that PA1b binding to VATPase is observed in a number of insect orders (Blattodea, Coleoptera, Hemiptera, Hymenoptera, Isoptera, Lepidoptera, Orthoptera, and Thysanura) [57].…”