Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities

Abstract

Background: Plants are hotbeds for parasites such as arthropod herbivores, which acquire nutrients and energy from their hosts in order to grow and reproduce. Hence plants are selected to evolve resistance, which in turn selects for herbivores that can cope with this resistance. To preserve their fitness when attacked by herbivores, plants can employ complex strategies that include reallocation of resources and the production of defensive metabolites and structures. Plant defences can be either prefabricated or be produced only upon attack. Those that are ready-made are referred to as constitutive defences. Some constitutive defences are operational at any time while others require activation. Defences produced only when herbivores are present are referred to as induced defences. These can be established via de novo biosynthesis of defensive substances or via modifications of prefabricated substances and consequently these are active only when needed. Inducibility of defence may serve to save energy and to prevent self-intoxication but also implies that there is a delay in these defences becoming operational. Induced defences can be characterized by alterations in plant morphology and molecular chemistry and are associated with a decrease in herbivore performance. These alterations are set in motion by signals generated by herbivores. Finally, a subset of induced metabolites are released into the air as volatiles and function as a beacon for foraging natural enemies searching for prey, and this is referred to as induced indirect defence.

Scope: The objective of this review is to evaluate (1) which strategies plants have evolved to cope with herbivores and (2) which traits herbivores have evolved that enable them to counter these defences. The primary focus is on the induction and suppression of plant defences and the review outlines how the palette of traits that determine induction/suppression of, and resistance/susceptibility of herbivores to, plant defences can give rise to exploitative competition and facilitation within ecological communities "inhabiting" a plant.

Conclusions: Herbivores have evolved diverse strategies, which are not mutually exclusive, to decrease the negative effects of plant defences in order to maximize the conversion of plant material into offspring. Numerous adaptations have been found in herbivores, enabling them to dismantle or bypass defensive barriers, to avoid tissues with relatively high levels of defensive chemicals or to metabolize these chemicals once ingested. In addition, some herbivores interfere with the onset or completion of induced plant defences, resulting in the plant's resistance being partly or fully suppressed. The ability to suppress induced plant defences appears to occur across plant parasites from different kingdoms, including herbivorous arthropods, and there is remarkable diversity in suppression mechanisms. Suppression may strongly affect the structure of the food web, because the ability to suppress the activation of defences of a communal host may facilitate competitors, whereas the ability of a herbivore to cope with activated plant defences will not. Further characterization of the mechanisms and traits that give rise to suppression of plant defences will enable us to determine their role in shaping direct and indirect interactions in food webs and the extent to which these determine the coexistence and persistence of species.

Keywords: Herbivory; adaptation; community interactions; detoxification; facilitation; herbivore; induction; jasmonate; manipulation; plant defence; plant–animal interaction; resistance; salicylate; sequestration; suppression.

Fig. 1.

The herbivore digestive system. The insect digestive system has two openings, the mouth and the anus. The digestive tract has three sections: the foregut, the midgut (stomach) and the hindgut. Food is stored in the foregut and mixed with saliva to help digestion; sometimes this mixture is regurgitated, but most digestion takes place in the midgut. Nutrients are absorbed in the midgut and the hindgut. Nitrogen-containing waste from metabolic processes is excreted from the Malpighian tubules and the remaining waste from the anus. The midgut is lined with a semipermeable membrane, called the peritrophic membrane, which is composed of proteins and chitin and allows the passage of liquids while blocking the passage of solid food particles and microorganisms.

Fig. 2.

The plant defence response. Mechanical damage and exposure to oral secretions from herbivores lead to osmotic stress, cause ion fluxes and elicit signalling cascades leading to rapid accumulation of jasmonates (JAs). Jasmonoyl isoleucine diffuses into the nucleus, where it associates with a protein complex including its receptor encoded by the coi (coronatine insensitive) gene. Binding to this complex initiates degradation of transcriptional suppressor proteins, thereby stimulating defence gene expression. Jasmonate also stimulates increased accumulation of secondary metabolites (phytotoxins). Together, these changes make plant tissues less palatable. Upstream processes are shown in black, the defence substances produced by the plant in green.

Fig. 3.

Mode of action of plant defence proteins in the herbivore gut. Herbivores utilize plant material predominantly to obtain sugar and amino acids. They digest proteins into amino acids via proteases and starch/sucrose into free sugars via amylases/invertases. Plants produce special proteins that are co-ingested and interfere with digestive processes in the gut. Defensins inhibit α-amylase activity. Deaminases degrade amino acids. Proteinase inhibitors and peptidases inhibit the arthropod’s proteases. Peptidases, lectins and possibly some PR proteins damage the peritrophic membrane. Plant polyphenol oxidases in combination with plant phenolics are believed to generate quinones in the arthropod gut. These quinones may damage soluble and membrane proteins and DNA. Digestive processes of the herbivore are shown in red and counter-measures of the plant in green.

Fig. 4.

The herbivore resistance response. Plant secondary metabolites can have diverse target sites. Two general mechanisms allow arthropod herbivores to cope with plant secondary compounds: mechanisms that decrease exposure via detoxification, transport and/or sequestration (shown in this figure) but also mechanisms that decrease sensitivity (see main text). Detoxification (indicated as ‘Detox’ in this figure) usually occurs in three phases: in phase I, enzymes such as P450s and CCEs (carboxyl/cholinesterases) modify the metabolite; in phase II GSTs and UGTs conjugate it and in phase III the conjugated metabolites are transported out of the cell, typically by ABC transporter and SLC family proteins. The midgut, fat body and Malpighian tubes are the insect tissues where these detoxification phases occur (Harrop et al., 2014). Metabolites are excreted via faeces and urine. Some metabolites, or modified metabolites, are stored in the cuticle or in other organs and are used by the arthropod for its own protection. Plant substances are indicated in green and arthropod responses in red.