Perception, signaling and molecular basis of oviposition-mediated plant responses

Abstract

Eggs deposited on plants by herbivorous insects represent a threat as they develop into feeding larvae. Plants are not a passive substrate and have evolved sophisticated mechanisms to detect eggs and induce direct and indirect defenses. Recent years have seen exciting development in molecular aspects of egg-induced responses. Some egg-associated elicitors have been identified, and signaling pathways and egg-induced expression profiles are being uncovered. Depending on the mode of oviposition, both the jasmonic acid and salicylic acid pathways seem to play a role in the induction of defense responses. An emerging concept is that eggs are recognized like microbial pathogens and innate immune responses are triggered. In addition, some eggs contain elicitors that induce highly specific defenses in plants. Examples of egg-induced suppression of defense or, on the contrary, egg-induced resistance highlight the complexity of plant-egg interactions in an on-going arms race between herbivores and their hosts. A major challenge is to identify plant receptors for egg-associated elicitors, to assess the specificity of these elicitors and to identify molecular components that underlie various responses to oviposition.

Fig. 1

Structures of known egg-associated elicitors. Bruchins are found in oviposition fluids of pea weevils. They are C₂₂–C₂₄ long-chain α,ω-diols, esterified at one or both ends with 3-hydroxypropanoic acid and induce neoplasm formation when applied to pea pods. Benzyl cyanide is a male-derived anti-aphrodisiac molecule found in accessory gland secretions coating eggs of Pieris brassicae. It induces the arrest of the egg parasitoid Trichogramma brassicae on Brassicaceae plants. Indole is another anti-aphrodisiac molecule found in Pieris rapae eggs that also arrests T. brassicae

Fig. 2

Variability of egg-induced necrosis in Arabidopsis. Oviposition by Pieris brassicae causes cell death on Arabidopsis thaliana Col-0 leaves but no strong necrosis can be observed, in contrast to Brassica oleracea var gemmifera. However, some Arabidopsis accessions display a much stronger HR-like necrosis after treatment with P. brassicae egg extract. a P. brassicae eggs on Arabidopsis thaliana Col-0; b visualization of cell death by trypan blue staining in Col-0 leaves 72 h after oviposition; c B. oleracea var gemmifera leaf 72 h after oviposition, some eggs were removed to show necrosis; d Col-0 leaf treated for 72 h with P. brassicae egg extract; e Ra-0; f Bor-4; g Lz-0. Arrows indicate the site of egg extract deposition

Fig. 3

Summary of the current knowledge on egg perception, signaling and defense gene expression. Typical responses of plants to oviposition are shown. a In plants from the Brassicaceae family, eggs deposited on the leaf surface release elicitors that are either contained in the egg (lipid elicitor) or found in secretions coating the eggs (benzyl cyanide, BC). In Arabidopsis, after binding to the putative LecRK-I.8 receptor, a lipid elicitor triggers the SA pathway that in combination with ROS activates the expression of defense genes, including PR1, and an HR-like necrosis. Egg-induced SA accumulation suppresses JA-dependent defenses against larvae from a generalist herbivore. In addition, BC triggers the expression of cell wall metabolism and transport genes that results in leaf surface chemical changes (gray) arresting egg parasitoids. In Brassica nigra and Arabidopsis, oviposition leads to induced resistance against larvae from a specialist herbivore. b In tomato, oviposition triggers H₂O₂ accumulation and expression of the JA-dependent PIN2. Eggs prime plants for enhanced JA accumulation and defense gene expression in response to further herbivory. c In pine and elm trees, a combination of wounding and proteinaceous elicitors present in secretions coating the eggs induce the emission of plant volatiles and the activation of stress and defense genes through the JA pathway. These terpenoids are synthesized by terpene synthase genes (TPS) and attract egg parasitoids. In addition, oviposition by pine sawfly Diprion pini decreases further larval performance and adult fecundity. d In pea, bruchins found in oviposition fluids of the bruchid weevil induce neoplasm formation (gray), activate gene expression and stimulate the accumulation of the defense compound pisatin. The induction of an OPDA-reductase gene (OPR) suggests that the JA pathway is involved in these responses