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Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense.

ABSTRACT: Insect-induced defenses occur in nearly all plants and are regulated by conserved signaling pathways. As the first described plant peptide signal, systemin regulates antiherbivore defenses in the Solanaceae, but in other plant families, peptides with analogous activity have remained elusive. In the current study, we demonstrate that a member of the maize (Zea mays) plant elicitor peptide (Pep) family, ZmPep3, regulates responses against herbivores. Consistent with being a signal, expression of the ZmPROPEP3 precursor gene is rapidly induced by Spodoptera exigua oral secretions. At concentrations starting at 5 pmol per leaf, ZmPep3 stimulates production of jasmonic acid, ethylene, and increased expression of genes encoding proteins associated with herbivory defense. These include proteinase inhibitors and biosynthetic enzymes for production of volatile terpenes and benzoxazinoids. In accordance with gene expression data, plants treated with ZmPep3 emit volatiles similar to those from plants subjected to herbivory. ZmPep3-treated plants also exhibit induced accumulation of the benzoxazinoid phytoalexin 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside. Direct and indirect defenses induced by ZmPep3 contribute to resistance against S. exigua through significant reduction of larval growth and attraction of Cotesia marginiventris parasitoids. ZmPep3 activity is specific to Poaceous species; however, peptides derived from PROPEP orthologs identified in Solanaceous and Fabaceous plants also induce herbivory-associated volatiles in their respective species. These studies demonstrate that Peps are conserved signals across diverse plant families regulating antiherbivore defenses and are likely to be the missing functional homologs of systemin outside of the Solanaceae.

SUBMITTER: Huffaker A

PROVIDER: S-EPMC3619339 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense.

Huffaker Alisa A Pearce Gregory G Veyrat Nathalie N Erb Matthias M Turlings Ted C J TC Sartor Ryan R Shen Zhouxin Z Briggs Steven P SP Vaughan Martha M MM Alborn Hans T HT Teal Peter E A PE Schmelz Eric A EA

Proceedings of the National Academy of Sciences of the United States of America 20130318 14

Insect-induced defenses occur in nearly all plants and are regulated by conserved signaling pathways. As the first described plant peptide signal, systemin regulates antiherbivore defenses in the Solanaceae, but in other plant families, peptides with analogous activity have remained elusive. In the current study, we demonstrate that a member of the maize (Zea mays) plant elicitor peptide (Pep) family, ZmPep3, regulates responses against herbivores. Consistent with being a signal, expression of t ...[more]

PMID: 23509266

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Project description:BACKGROUND:Plant elicitor peptides (Peps) are endogenous molecules that induce and amplify the first line of inducible plant defense, known as pattern-triggered immunity, contributing to protect plants against attack by bacteria, fungi and herbivores. Pep topic application and transgenic expression have been found to enhance disease resistance in a small number of model plant-pathogen systems. The action of Peps relies on perception by specific receptors, so displaying a family-specific activity. Recently, the presence and activity of Peps within the Rosaceae has been demonstrated. Here we characterized the population of Pep sequences within the economically important plant family of Rosaceae, with special emphasis on the Amygdaleae and Pyreae tribes, which include the most relevant edible species such as apple, pear and peach, and numerous ornamental and wild species (e.g. photinia, firethorn and hawthorn). RESULTS:The systematic experimental search for Pep and the corresponding precursor PROPEP sequences within 36 Amygdaleae and Pyreae species, and 100 cultivars had a highly homogeneous pattern, with two tribe-specific Pep types per plant, i.e. Pep1 and Pep2 (Amygdaleae) or Pep3 and Pep4 (Pyreae). Pep2 and Pep3 are highly conserved, reaching identity percentages similar to those of genes used in plant phylogenetic analyses, while Pep1 and Pep4 are somewhat more variable, with similar values to the corresponding PROPEPs. In contrast to Pep3 and Pep4, Pep1 and Pep2 sequences of different species paralleled their phylogenetic relationships, and putative ancestor sequences were identified. The large amount of sequences allowed refining of a C-terminal consensus sequence that would support the protective activity of Pep1-4 in a Prunus spp. and Xanthomonas arboricola pv. pruni system. Moreover, tribe-specific consensus sequences were deduced at the center and C-terminal regions of Peps, which might explain the higher protection efficiencies described upon topic treatments with Peps from the same tribe. CONCLUSIONS:The present study substantially enhances the knowledge on Peps within the Amygdaleae and Pyreae species. It can be the basis to design and fine-tune new control tools against important plant pathogens affecting Prunus, Pyrus and Malus species.

Project description:Plants can defend themselves against herbivores through activation of defensive pathways and attraction of third-trophic-level predators and parasites. Trophic cascades that mediate interactions in the phytobiome are part of a larger dynamic including the pathogens of the plant itself, which are known to greatly influence plant defenses. As such, we investigated the impact of a phloem-limited bacterial pathogen, Candidatus Liberibacter asiaticus (CLas), in cultivated citrus rootstock on a well-studied belowground tritrophic interaction involving the attraction of an entomopathogenic nematode (EPN), Steinernema diaprepesi, to their root-feeding insect hosts, Diaprepes abbreviatus larvae. Using belowground olfactometers, we show how CLas infection interferes with this belowground interaction by similarly inducing the release of a C12 terpene, pregeijerene, and disconnecting the association of the terpene with insect presence. D. abbreviatus larvae that were not feeding but in the presence of a CLas-infected plant were more likely to be infected by EPN than those near uninfected plants. Furthermore, nonfeeding larvae associated with CLas-infected plants were just as likely to be infected by EPN as those near noninfected plants with D. abbreviatus larval damage. Larvae of two weevil species, D. abbreviatus and Pachnaeus litus, were also more attracted to plants with infection than to uninfected plants. D. abbreviatus larvae were most active when exposed to pregeijerene at a concentration of 0.1 μg/μl. We attribute this attraction to CLas-infected plants to the same signal previously thought to be a herbivore-induced plant volatile specifically induced by root-feeding insects, pregeijerene, by assessing volatiles collected from the roots of infected plants and uninfected plants with and without feeding D. abbreviatus. Synthesis. Phytopathogens can influence the structuring of soil communities extending to the third trophic level. Field populations of EPN may be less effective at host-finding using pregeijerene as a cue in citrus grove agroecosystems with high presence of CLas infection.

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Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense.

Publications

Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense.

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