The gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) stimulates different chemical and phytohormone responses in two Eucalyptus varieties that vary in susceptibility to galling

Abstract

Gall-inducing insects produce various types of galls on plants, but little is known about the gall-induction mechanism of these galling insects. The gall wasp Leptocybe invasa Fisher & LaSalle (Hymenoptera: Eulophidae) forms galls of different sizes on several Eucalyptus species. To clarify the physiological responses of Eucalyptus to L. invasa infestation, we measured the dynamics of nitrogen (N), carbon (C), total phenolics, total tannins and four types of phytohormones (zeatin [Z] + zeatin riboside [ZR], gibberellins [GA], indole-3-acetic acid [IAA] and abscisic acid [ABA]) in galled and ungalled leaf tissues of two Eucalyptus horticultural varieties (DH201-2 [Eucalyptus grandis × Eucalyptus camaldulensis] and EA [Eucalyptus exserta]) with different susceptibility to galling throughout the larval developmental stages. Nitrogen, total phenolics, tannins and four kinds of phytohormones strongly accumulated in tissues galled by L. invasa (especially during early larval feeding stages). While N, Z + ZR and GA levels were higher, tannins and ABA levels were lower in the galled tissues on the highly susceptible variety. Nitrogen, total phenolics, GA, Z + ZR and IAA levels in the galled tissues gradually decreased during gall development, but ABA and tannins conversely increased in the galled tissues of the less susceptible variety. Our results suggest that the effects of gall-inducing insects on plants depend not only on the susceptibility of the plant infested but also on the developmental stage of galled tissues. Gall formation process is thus synergistically influenced by both gall-inducing insect and plant genotypes.

The mechanism of plant gall induction by insects: revealing clues, facts, and consequences in a cross-kingdom complex interaction

“…Other authors have also reported differences in the concentrations of certain secondary compounds as well as certain types of phytohormones in plant gall tissue (Kraus & Spiteller, 1997;Pinkwart, Diettrich, & Luckner, 1998). Kot et al (2017), Li et al (2017) and Hall et al (2017) demonstrated that galls induced by cynipid species and the wasp Leptocybe invasa (Hymenoptera: Eulophidae), respectively, contain high levels of phenolic compounds compared with control tissues. Moreover, increased production of waxes in the gall induced by the insect Baccharopelma spp.…”

“…Research conducted on galls of different species of plants have revealed that the composition and concentration of chemical substances in these structures can differ from those of other plant tissues and organs Saltzmann et al, 2008;Giron & Huguet, 2011;Huang et al, 2015;Oates et al, 2015;Hall, Carrol, & Kitching, 2017;Kot, Jakubczyk, Karaś, & Złotek, 2017). Tissues near the outside of the gall frequently accumulate high levels of tannins and other chemical compounds related to the process of defense of the gall and, in consequence, of the insect (Ananthakrishnan, 1998;Li et al, 2017;Chen et al, 2018;Nogueira et al, 2018). A study by Vereecke et al (1997) revealed that the chemical composition of ethanol and aqueous extracts of galls produced in the leaves of Nicotiana tabacum differs drastically from that of non-infected plant tissue extracts.…”

“…Several authors have reported high concentrations of certain nutritive substances in gall tissues; some of those substances include sugars, proteins, phosphates, lipids, and nitrogen compounds Giron & Huguet, 2011;Huang et al, 2015;Li et al, 2017). In contrast, some researchers have described that galls can present low levels of certain chemical compounds related to the processes of plant defense, such as some phenolic compounds (Price et al, 1986;Agudelo et al, 2018).…”

“…Taking into consideration studies such as the those carried out by Nyman & Julkunen (2000), , , Giron & Huguet (2011), Huang et al (2015), Oates et al (2015), Li et al (2017), Kot et al (2017), Chen et al (2018), and Agudelo et al (2018), comparing the chemical composition of galls with that of normal plant tissue, the conclusion would be that gall-inducing insects could control some the chemical properties of these structures.…”

Eavesdropping on gall–plant interactions: the importance of the signaling function of induced volatiles

“…33,50 Thus, the different developmental gall stages and plant genotypes show that the gall-plant interaction is a synergistic process. 73,74 Additionally, the phenological association between plant and galling organism life cycles represents a new frontier of chemical ecology, which determines how the VOCs released during the host plant phenological stages interact with the galling insects, natural enemies or host plant interactors such as pollinators.…”