Trichomes mediate plant–herbivore interactions in two Cucurbitaceae species through pre- and post-ingestive ways

Abstract

Plant structural defenses such as trichomes exert a significant selection pressure on insect herbivores. However, whether variation in structural defense traits affects common herbivores in related plant species is less understood. Here, we examined the role of trichomes in plant–herbivore interactions in two commonly cultivated members in Cucurbitaceae: bottle gourd ( Lagenaria siceraria ) and cucumber ( Cucumis sativa ). In common garden experiments when the two species were grown together, we observed that they differed in their attractiveness to four major herbivore species ( Trichoplusia ni , Acalymma vittatum , Diaphania indica , and Anasa tristis ) and, consequently, their feeding behavior. We found that L. siceraria consistently harbored less herbivores, and the two lepidopteran herbivores ( T. ni and D. indica ) were found to take significantly longer time to commence feeding on them, a primary mode of pre-ingestive defense function of trichomes. To tease apart structural and chemical modes of defenses, we first used scanning electron microscopy to identify, quantify, and measure trichome traits including their morphology and density. We found that C. sativa has significantly lower number of trichomes compared to L. siceraria , regardless of trichome type and leaf surface. We then used artificial diet enriched with trichomes as caterpillar food and found that trichomes from these two species differentially affected growth and development of T. ni showing cascading effects of trichomes. Taken together, we show that trichomes, independent of chemical defenses, are an effective pre- and post-ingestive defense strategy against herbivores with negative consequences for their feeding, growth, and development. Supplementary Information The online version contains supplementary material available at 10.1007/s10340-023-01611-x.

The push–pull intercrop Desmodium does not repel, but intercepts and kills pests

“…Incidentally, the presence of small uncinate trichomes on leaves could also have affected the movement of first instar larvae and thereby support the observed preference pattern observed earlier ( Figure 4 ) and survival rate ( Figure 5 ). Stellar non-glandular trichomes were shown to decrease feeding of Manduca secta larvae on several Solanaceae species ( Kariyat et al, 2018 ), and uniserate non-glandular trichomes of bottle gourd ( Lagenaria siceraria ) affect the feeding and survival of Trichoplusia ni ( Kaur and Kariyat, 2023 ). How the size, shape and density of these surface structures affect lepidopteran behavior in a species- and stage-specific manner needs to be addressed in future studies.…”

“…First, Desmodium entices larval feeding, but truncates development. Second, trichomes on Desmodium hinder movement, damage the cuticle and even entirely immobilize larvae on the plant, increasing developmental time, exposure to natural enemies and overall mortality ( Kaur and Kariyat, 2023 ; Kariyat et al, 2017 ; Kaur and Kariyat, 2020 ). Third, ingestion of trichomes damages the intestinal lining and affects digestion, development and survival in closely related species ( Kaur and Kariyat, 2020 ; Acevedo et al, 2021 ).…”

“…With the mechanism at hand, the strategy can also be further tailored to the needs of local smallholder farmers e.g. replacing Desmodium with food crops with similar properties ( Kariyat et al, 2018 ; Kaur and Kariyat, 2023 ; Ballhorn et al, 2013 ; Gilbert, 1971 ; Xing et al, 2017 ; Acevedo et al, 2021 ; Johnson, 1953 ; QulRing et al, 1992 ), as well as rationally translating the concept to other cropping systems.…”

Belowground insect herbivory induces systemic volatile emissions that strengthen neighbouring plant resistance aboveground

“…Additionally, trichomes are inducible following insect herbivory (Kaur & Kariyat, 2020) and can reduce herbivore feeding rates or injure attacking herbivores (Andama et al, 2020). However, recent evidence showed that adult squash bugs preferred a cucurbit species with more trichomes (Kaur & Kariyat, 2023), suggesting trichomes were not a major deterrent, at least for the adult insects. It also remains unknown whether enhanced resistance following exposure to systemic HIPVs is due to defence induction or priming.…”

The chromosome-scale genome and the genetic resistance machinery against insect herbivores of the Mexican toloache,Datura stramonium

“…TRICHOME BIREFRINGENCE is responsible for trichome production in plants, which are often considered as the first line of defense against insect herbivores and pathogens ( Levin 1973 ; Mauricio 2005 ; Bischoff et al 2010 ; Tian et al 2012 ; Kaur and Kariyat 2023 ). Trichomes can impede the movement of insect herbivores, reducing leaf consumption, and even causing damage to herbivore gut linings ( Weinhold and Baldwin 2011 ; Kariyat et al 2017 ; Kaur and Kariyat 2023 ). In D. stramonium , previous research has shown that trichomes contribute to resistance against folivores like L. daturaphila and Epitrix parvula .…”