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. 2019 Jun 24;14(9):e1633887. doi: 10.1080/15592324.2019.1633887

Current opinions about herbivore-associated molecular patterns and plant intracellular signaling

Takuya Uemura 1, Gen-Ichiro Arimura 1,✉
PMCID: PMC6768233  PMID: 31230525

ABSTRACT

Elicitor-associated compounds included in oral secretions of herbivorous arthropods, defined as herbivore-associated molecular patterns (HAMPs), induce defense responses in plants. Recognition of HAMPs by the host plants triggers the activation of downstream intracellular and intercellular signaling, resulting in the production of defensive secondary metabolites and volatile emissions to defend against herbivore attack. Thus far, several chemical classes of HAMPs, e.g., fatty acid-amino acid conjugates, peptides, enzymes, and oligosaccharides, have been characterized from not only plant-chewing arthropod herbivores but also plant-sucking arthropod herbivores. Here, we introduce the latest insights about HAMPs and the HAMPs-induced defense signaling network in host plants.

KEYWORDS: Elicitor, herbivore-associated molecular patterns (HAMPs), pattern recognition receptors (PRRs)

Plants recognize herbivore damage by perceiving elicitor components included in herbivores’ oral secretions (OS) (Table 1). The best-characterized representative elicitor, volicitin [N-(17-hydoroxylinolenoyl)-L-Gln], one of the fatty acid-amino acid conjugates (FACs) in OS of Spodoptera exigua larvae, is able to induce the emission of a blend of volatiles in corn seedlings, like the emission induced by S. exigua OS, indicating that secreted volicitin plays a central role in eliciting the indirect defense of the host corn plants.1 Like volicitin, several types of FACs, secreted from not only lepidopteran but also non-lepidopteran species, may play a role in elicitation of host plants’ defense responses.2–4 In addition to FACs, other types of OS components have been characterized as HAMP-type elicitors that induce plant defense responses. These include disulfooxy fatty acids (caeliferins) from the American bird grasshopper Schistocerca americana,5 a disulfide-bridged peptide (inceptin) from OS of fall armyworm (Spodoptera frugiperda) that is derived originally from the chloroplastic ATP synthase γ-subunit protein of host cowpea plants,6 bruchins, which are long-chain ester compounds from the eggs of pea weevil (Bruchus pisorum) and cowpea weevil (Callosobruchus maculatus),7 and β-galactofuranose polysaccharide from OS of Spodoptera littoralis, of which the structure is still unknown.8 A porin-like protein that is secreted by intestinal bacteria in the gut of S. littoralis larvae has been shown to exhibit channel-forming activity in Arabidopsis host plants that acts in early defense-related cellular signaling.9 Elicitors may serve in host-specific manners, via jasmonate (JA) and/or other hormone signaling such as ethylene signaling, to specifically induce defense activities of the host plants,10 essentially through early signaling such as rapid perturbations of the plasma membrane potential (Vm) following intracellular Ca2+ influx and the production of reactive oxygen species (ROS).11

Table 1.

Features of the characterized HAMPs.

Herbivore species HAMPs Molecular structure Host References
Plant-chewing Lepidopteran caterpillars Volicitin spp. Fatty-acid amino acid conjugates Corn, eggplant, 1,2,4
Herbivores Drosophila melanogaster   Tomato, etc. 3
  Teleogryllus taiwanemma       3
  Schistocerca americana Caeliferins Sulfooxy fatty acids Corn 5
  Spodoptera frugiperda Inceptin Peptides Corn, cowpea 6
  Ostrinia nubilalis Glucose oxidases Enzymes Tomato 13
  Helicoverpa zea     Tobacco 14
  Pieris brassicae β-Glucosidase Enzymes Cabbage 12
  Spodoptera littoralis Porin-like proteins Protein Arabidopsis, soybean 9
  Spodoptera littoralis β-Galactofuranose polysaccharide Oligosaccharide Arabidopsis 8
  Bruchus pisorum Bruchins Ester Cowpea, pea 7
  Callosobruchus maculatus     7
Plant-sucking Tetranicus urticae Tetranin Protein Kidney beans, eggplant 16
Herivores Nilaparvata lugens Mucin-like salivary protein Protein Rice 15
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Moreover, there are enzyme types of elicitors: β-glucosidase in OS of Pieris brassicae was found to elicit the emission of volatiles from host cabbage plants.12 Another example is glucose oxidases, which catalyze the production of H2O2 (ROS) and serve as elicitor and effector for tomato and tobacco host plants, respectively.13,14

In contrast to an array of saliva/OS components of several plant-chewing herbivores as described above, only a few elicitors have been identified in plant-sucking arthropod herbivores. Notably, a mucin-like salivary protein (NIMLP), one of the glycoproteins that are specifically expressed in the salivary gland of the brown planthopper (Nilaparvata lugens), has been identified as an elicitor of the sucking type of herbivores.15 In the host plant rice, NlMLP induces cell death, defense gene upregulation, and callose deposition through intracellular Ca2+ influx, and MAP kinase and JA signaling activation.15 Likewise, putative salivary gland proteins of spider mites designated as tetranins (Tet1 and Tet2) have recently been characterized as elicitors of the two-spotted spider mite (Tetranychus urticae).16 Tetranins elicit intracellular Ca2+ influx, membrane depolarization, the activation of JA, salicylate and abscisic acid signaling, and increased transcript levels of defense genes in the bean leaves, resulting in reduced survivability of the mites on the host leaves as well as attraction of predatory mites (Phytoseiulus persimilis).

The pattern recognition receptors (PRRs) localized in plant cell surface membrane are the best-characterized elicitor perception molecules. For instance, rice leucine-rich repeat receptor-like kinase 1 (OsLRR-RLK1) has been shown to be positively involved in defense responses of rice against striped stem borer (Chilo suppressalis).17 Moreover, lectin receptor kinases (LecRKs) in rice and tobacco may also be positively and negatively involved in defense responses of the host plants during damage by N. lugens and Manduca sexta, respectively.18,19 However, their possible insect-derived ligands are still unknown.

The downstream, intracellular signaling, is generally largely committed to JA signaling mediated by the COI1-JAZ system for induced defense responses.20 Moreover, in Arabidopsis, it has recently been shown that the JAV1/JUL1 system serves for the promotion of defense actions against attack by lepidopteran larvae but not for plant development or growth.21 JAV1 was found to be phosphorylated in a Ca2+-dependent manner,22 leading to the decomposition of the JAV1-WRKY51-JAZ8 complex via JAV1 protein degradation by JUL1 (JAV1-ASSOCIATED UBIQUITIN LIGASE 1) and the 26S proteasome system.21 Given these facts, there is no doubt that the JA signaling network plays a central role in plant herbivory resistance, which consists of an array of signaling systems in which positive and negative factors work alternatively as appropriate to switch defense either on or off.

Funding Statement

This work was financially supported in part by MEXT Grants-in-Aid for Scientific Research on Innovative Areas [18H04630 and 18H04786].

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

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