Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars

Pechan, Tibor; Cohen, Allen Carson; Williams, W. Paul; Luthe, Dawn S.

doi:10.1073/pnas.202224899

Cited by 262 publications

(170 citation statements)

References 26 publications

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“…We recently documented post-ingestion effects of such trichomes on caterpillars, reporting the gut peritrophic matrix was punctured and ripped by trichomes passing through the gut. Given the importance of the peritrophic matrix to nutrient uptake and protection against pathogens [18], it is not surprising that larvae also grew more slowly when feeding on plants with more trichomes [19] or on artificial diet containing trichomes compared to control diet [3]. …”

Section: Discussionmentioning

confidence: 99%

Leaf trichomes affect caterpillar feeding in an instar-specific manner

Kariyat

Hardison

Ryan

et al. 2018

Communicative & Integrative Biology

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Leaf trichomes play well-established roles in defense against insect herbivores, both as a physical barrier that impedes herbivore movement and by mediating chemical defenses. However, little work has examined how different trichome types influence herbivory by herbivores at different stages of development. We examined whether caterpillar instar and trichome type (glandular or non-glandular) affected the ability of the specialist herbivore caterpillar Manduca sexta to initiate feeding on 11 Solanaceous species exhibiting variation in the density and type of leaf trichomes. Our results suggest that non-glandular trichomes are far more effective than glandular trichomes in deterring the initiation of feeding by first- and second-instar caterpillars. Meanwhile, neither glandular nor non-glandular trichomes significantly affected the ability of third-instar caterpillars to commence feeding. These findings suggest that while non-glandular trichomes deter feeding initiation by early instar caterpillars, the contribution of both trichomes on later instars may depend on effects after feeding initiation.

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Section: Discussionmentioning

confidence: 99%

Leaf trichomes affect caterpillar feeding in an instar-specific manner

Kariyat

Hardison

Ryan

et al. 2018

Communicative & Integrative Biology

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“…This damage may have been caused by the swelling and fragmenting cells. However, a direct effect of cyclotides on the peritrophic membrane cannot be discounted because it is a known target for some insecticidal molecules (23,24).…”

Section: Discussionmentioning

confidence: 99%

Plant cyclotides disrupt epithelial cells in the midgut of lepidopteran larvae

Barbeta¹,

Marshall

Gillon³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

208

202

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Several members of the Rubiaceae and Violaceae plant families produce a series of cyclotides or macrocyclic peptides of 28 -37 aa with an embedded cystine knot. The cyclic peptide backbone together with the knotted and strongly braced structure confers exceptional chemical and biological stability that has attracted attention for potential pharmaceutical applications. Cyclotides display a diverse range of biological activities, such as uterotonic action, anti-HIV activity, and neurotensin antagonism. In plants, their primary role is probably protection from insect attack. Ingestion of the cyclotide kalata B1 severely retards the growth of larvae from the Lepidopteran species Helicoverpa armigera. We examined the gut of these larvae after consumption of kalata B1 by light, scanning, and transmission electron microscopy. We established that kalata B1 induces disruption of the microvilli, blebbing, swelling, and ultimately rupture of the cells of the gut epithelium. The histology of this response is similar to the response of H. armigera larvae to the Bacillus thuringiensis delta-endotoxin, which is widely used to control these insect pests of crops such as cotton. circular peptides ͉ insecticidal ͉ kalata B1 ͉ Lepidoptera ͉ microscopy C yclotides are a series of cyclic minipeptides of 28-37 aa that are expressed at high levels in the leaves, stems, and roots of several plant species (1, 2). They have an unusual topology based on a cyclic peptide backbone together with a cystine knot in which two disulfide bonds are threaded by a third disulfide bond (2, 3). This structure forces hydrophobic amino acids onto the surface of the molecule, creating a hydrophobic face on the otherwise hydrophilic surface. The cyclotides are thus soluble in both organic and aqueous solvents and are very stable at extremes of pH and temperature (4). The absence of free N and C termini, together with the tightly packed cystine knot, also renders the cyclotides resistant to the activity of proteases (4). The cyclotides are the largest family of circular proteins, although others have been described in bacteria, plants, and animals (5).Cyclotides were first isolated from the African plant Oldenlandia affinis. Two peptides, kalata B1 and B2, were recognized as the active components in a traditional medicine used to accelerate childbirth (6). Additional members of the cyclotide family were subsequently identified in screening studies directed toward discovery of bioactive molecules such as neurotensin antagonists (7), inhibitors of HIV replication (8), and hemolytic agents (9). More than 100 cyclotides have since been isolated from various members of the Rubiaceae, Violaceae, and Cucurbitaceae plant families (10, 11). A single plant may have at least 12 cyclotide genes and produce dozens of different cyclotides (12)(13)(14). Although an earlier study reported antimicrobial activity (15), it appears that their predominant activity in plants is insecticidal (13, 16). Jennings et al. (13) demonstrated that Helicoverpa punctigera failed to devel...

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“…Most of the available data deal with insecticidal plant proteins such as lectins, ribosome-inactivating proteins, enzyme inhibitors, arcelins, chitinases, ureases and modified storage proteins (Carlini & Grossi-de-Sá 2002). On the other hand, Pechan et al (2002) have described a correlation between the impaired growth of caterpillars and a cysteine proteinase present in some Maize (Zea mays L.) lines that are resistant to feeding by a number of lepidopteran species. The insect's peritrophic matrix was severely damaged when caterpillars fed on these resistant maize plants or transgenic sweet corn containing the gene encoding the cysteine proteinase.…”

Section: Discussionmentioning

confidence: 99%