Mélanie Body

A specialist root herbivore exploits defensive metabolites to locate nutritious tissues

The most valuable organs of plants are often particularly rich in essential elements, but also very well defended. This creates a dilemma for herbivores that need to maximise energy intake while minimising intoxication. We investigated how the specialist root herbivore Diabrotica virgifera solves this conundrum when feeding on wild and cultivated maize plants. We found that crown roots of maize seedlings were vital for plant development and, in accordance, were rich in nutritious primary metabolites and contained higher amounts of the insecticidal 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and the phenolic compound chlorogenic acid. The generalist herbivores Diabrotica balteata and Spodoptera littoralis were deterred from feeding on crown roots, whereas the specialist D. virgifera preferred and grew best on these tissues. Using a 1,4-benzoxazin-3-one-deficient maize mutant, we found that D. virgifera is resistant to DIMBOA and other 1,4-benzoxazin-3-ones and that it even hijacks these compounds to optimally forage for nutritious roots.

Insect-induced effects on plants and possible effectors used by galling and leaf-mining insects to manipulate their host-plant

Gall-inducing insects are iconic examples in the manipulation and reprogramming of plant development, inducing spectacular morphological and physiological changes of host-plant tissues within which the insect feeds and grows. Despite decades of research, effectors involved in gall induction and basic mechanisms of gall formation remain unknown. Recent research suggests that some aspects of the plant manipulation shown by gall-inducers may be shared with other insect herbivorous life histories. Here, we illustrate similarities and contrasts by reviewing current knowledge of metabolic and morphological effects induced on plants by gall-inducing and leaf-mining insects, and ask whether leaf-miners can also be considered to be plant reprogrammers. We review key plant functions targeted by various plant reprogrammers, including plant-manipulating insects and nematodes, and functionally characterize insect herbivore-derived effectors to provide a broader understanding of possible mechanisms used in host-plant manipulation. Consequences of plant reprogramming in terms of ecology, coevolution and diversification of plant-manipulating insects are also discussed.

Leaf-Miners Co-opt Microorganisms to Enhance their Nutritional Environment

Organisms make the best of their mother’s oviposition choices and utilize specific feeding options that meet energetic requirements and cope with environmental constraints. This is particularly true for leaf-miner insects that develop enclosed in the two epidermis layers of a single leaf for their entire larval life. Cytokinins (CKs) play a central role in plant physiology – including regulation of senescence and nutrient translocation – and, as such, can be the specific target of plant exploiters that manipulate plant primary metabolism. ‘Green-islands’ are striking examples of a CK-induced phenotype where green areas are induced by plant pathogens/insects in otherwise yellow senescent leaves. Here, we document how the leaf-miner caterpillar Phyllonorycter blancardella, working through an endosymbiotic bacteria, modifies phytohormonal profiles, not only on senescing (photosynthetically inactive) but also on normal (photosynthetically active) leaf tissues of its host plant (Malus domestica). This leaf physiological manipulation allows the insect to maintain sugar-rich green tissues and to create an enhanced nutritional microenvironment in an otherwise degenerating context. It also allows them to maintain a nutritional homeostasis even under distinct leaf environments. Our study also highlights that only larvae harboring bacterial symbionts contain significant amounts of CKs that are most likely not plant-derived. This suggests that insects are able to provide CKs to the plant through their symbiotic association, thus extending further the role of insect bacterial symbionts in plant-insect interactions.

Hypermetamorphosis in a leaf-miner allows insects to cope with a confined nutritional space

Hypermetamorphosis has been described in several Lepidoptera leaf-miner species (mostly Gracillariidae, Epipyropidae, and Phyllocnistidae) and can be defined as a strong modification of the larval morphology associated with a switch in its feeding mode. Evolution of this larval feeding strategy presumably influences nutritional resources that can be exploited and has strong consequences for plant morphology. The following study focuses on Phyllonorycter blancardella (Lepidoptera: Gracillariidae), a leaf-miner developing on Malus domestica. We characterize the morphology of larval mouthparts and the resulting morphological impact on leaf tissues. Our results show that first instars do not strongly affect the leaf anatomy and leave most plant cells intact, while later instars significantly disrupt leaf tissues. Additionally, young larvae are “fluid-feeders” and feed on plant cell fluids resulting from the progression of the larvae through the lower layer of the leaf spongy parenchyma. They occupy a feeding niche clearly distinct from later instars that are “tissue-feeders”. Hypermetamorphosis in P. blancardella most likely allows insects to cope with a confined nutritional space by partitioning the limited feeding resources, and may help leaf-miners to optimize their nutrition.

Effects of fertilisation on amino acid mobilisation by a plant‐manipulating insect

1. Phytophagous insects frequently manipulate their host‐plant to improve their immediate environment. This generally implies substantial modifications of host metabolism, and sometimes an alteration of nitrogen allocation within the host‐plant. However, the outcome of plant manipulation on amino acid or protein content can be modulated by environmental factors and host‐plant traits.

Amino acid composition of the bushcricket spermatophore and the function of courtship feeding: variable composition suggests a dynamic role of the nuptial gift

Nuptial gifts are packages of non-gametic material transferred by males to females at mating. These gifts are common in bushcrickets, where males produce a complex spermatophore consisting in a sperm-containing ampulla and an edible sperm-free spermatophylax. Two non-mutually exclusive hypotheses have been suggested to explain the function of the spermatophylax: the paternal investment hypothesis proposes that it represents a male nutritional investment in offspring; the mating effort hypothesis proposes that the spermatophylax maximizes the males sperm transfer. Because gift production may represent significant energy expenditure, males are expected to adjust their investment relative to the perceived quality of the female. In this study, we first examined the free amino acid composition and protein-bound amino acid composition of the nuptial gift in the bushcricket, Ephippiger diurnus (Orthoptera: Tettigoniidae). Second, we investigated whether this composition was altered according to female age and body weight. Our study represents the first investigation of both free and protein-bound amino acid fractions of a bushcricket spermatophylax. We found that composition of the nuptial gift varied both qualitatively and quantitatively with respect to traits of the receiving female: older females received larger amounts of protein-bound amino acids (both essential and non-essential), less water and less free glycine. This result suggests that gift composition is highly labile in E. diurnus, and we propose that gift allocation might represent a form of cryptic male mate choice, allowing males to maximize their chances of paternity according to the risk of sperm competition that is associated with mate quality.

Morphometric analysis of young petiole galls on the narrow-leaf cottonwood, Populus angustifolia, by the sugarbeet root aphid, Pemphigus betae

An insect-induced gall is a highly specialized structure resulting from atypical development of plant tissue induced by a reaction to the presence and activity of an insect. The insect induces a differentiation of tissues with features and functions of an ectopic organ, providing nutrition and protection to the galling insect from natural enemies and environmental stresses. In this anatomical and cytological study, we characterized how the gall-inducing aphid Pemphigus betae reshapes the leaf morphology of the narrow-leaf cottonwood Populus angustifolia to form a leaf fold gall. Young galls displayed a bend on one side of the midvein toward the center of the leaf and back to create a fold on the abaxial side of the leaf. This fold was formed abaxially by periclinal and anticlinal divisions, effectively eliminating intercellular spaces from the spongy parenchyma. Galls at this stage exhibited both cell hypertrophy and tissue hyperplasia. Cells on the adaxial surface were more numerous and smaller than cells near the abaxial surface were, creating the large fold that surrounds the insect. Mesophyll cells exhibited some features typical of nutritive cells induced by other galling insects, including conspicuous nucleolus, reduced and fragmented vacuole, smaller and degraded chloroplasts, and dense cytoplasm compared to ungalled tissue. Even though aphids feed on the contents of phloem and do not directly consume the gall tissue, they induce changes in the plant vascular system, which lead to nutrient accumulation to support the growing aphid numbers in mature galls.

Increasing metabolic rate despite declining body weight in an adult parasitoid wasp

Metabolic rate is a positive function of body weight, a rule valid for most organisms and the basis of several theories of metabolic ecology. For adult insects, however, the diversity of relationships between body mass and respiration remains unexplained. The aim of this study is to relate the respiratory metabolism of a parasitoid with body weight and foraging activity. We compared the metabolic rate of groups of starving and host-fed females of the parasitoid Eupelmus vuilleti recorded with respirometry for 7days, corresponding to the mean lifetime of starving females and over half of the lifetime of foraging females. The dynamics of carbohydrate, lipid and protein in the body of foraging females were quantified with biochemical techniques. Body mass and all body nutrients declined sharply from the first day onwards. By contrast, the CO2 produced and the O2 consumed increased steadily. Starving females showed the opposite trend, identifying foraging as the reason for the respiration increase of feeding females. Two complementary physiological processes explain the unexpected relationship between increasing metabolic rate and declining body weight. First, host hemolymph is a highly unbalanced food, and the excess nutrients (protein and carbohydrate) need to be voided, partially through excretion and partially through respiration. Second, a foraging young female produces eggs at an increasing rate during the first half of its lifetime, a process that also increases respiration. We posit that the time-varying metabolic rate contributions of the feeding and reproductive processes supplements the contribution of the structural mass and lead to the observed trend. We extend our explanations to other insect groups and discuss the potential for unification using Dynamic Energy Budget theory.

Dynamics and origin of cytokinins involved in plant manipulation by a leaf-mining insect

Several herbivorous insects and plant‐associated microorganisms control the phytohormonal balance, thus enabling them to successfully exploit the plant by inhibiting plant defenses and withdrawing plant resources for their own benefit. The leaf‐mining moth Phyllonorycter blancardella modifies the cytokinin (CK) profile of mined leaf‐tissues, and the insect symbiotic bacteria Wolbachia is involved in the plant manipulation to the benefit of the insect host. To gain a deeper understanding into the possible origin and dynamics of CKs, we conducted an extensive characterization of CKs in larvae and in infected apple leaves. Our results show the enhanced CK levels in mines, both on green and yellow leaves, allowing insects to control their nutritional supply under fluctuating environmental conditions. The spatial distribution of CKs within the mined leaves shows that hormone manipulation is strictly limited to the mine suggesting the absence of CK translocation from distant leaf areas toward the insect feeding site. Mass spectrometry analyses reveal that major CK types accumulating in mines and larvae are similar to what is observed for most gall‐inducers, suggesting that strategies underlying the plant manipulation may be shared between herbivorous insects with distinct life histories. Results further show that CKs are detected in the highest levels in larvae, reinforcing our hypothesis that CKs accumulating in the mines originate from the insect itself. Presence of bacteria‐specific methylthio‐CKs is consistent with previous results suggesting that insect bacterial symbionts contribute to the observed phenotype. Our study provides key findings toward the understanding of molecular mechanisms underlying this intricate plant–insect–microbe interaction.