Integration of danger peptide signals with herbivore‐associated molecular pattern signaling amplifies anti‐herbivore defense responses in rice

Abstract

Plant defense against herbivores is modulated by herbivore-associated molecular patterns (HAMPs) from oral secretions (OS) and/or saliva of insects. Furthermore, feeding wounds initiate plant self-damage responses modulated by danger-associated molecular patterns (DAMPs) such as immune defense-promoting plant elicitor peptides (Peps). While temporal and spatial co-existence of both patterns during herbivory implies a possibility of their close interaction, the molecular mechanisms remain undetermined. Here we report that exogenous application of rice (Oryza sativa) peptides (OsPeps) can elicit multiple defense responses in rice cell cultures. Specific activation of OsPROPEP3 gene transcripts in rice leaves by wounding and OS treatments further suggests a possible involvement of the OsPep3 peptide in rice-herbivore interactions. Correspondingly, we found that simultaneous application of OsPep3 and Mythimna loreyi OS significantly amplifies an array of defense responses in rice cells, including mitogen-activated protein kinase activation, and generation of defense-related hormones and metabolites. The induction of OsPROPEP3/4 by OsPep3 points to a positive auto-feedback loop in OsPep signaling which may contribute to additional enhancement of defense signal(s). Finally, the overexpression of the OsPep receptor OsPEPR1 increases the sensitivity of rice plants not only to the cognate OsPeps but also to OS signals. Our findings collectively suggest that HAMP-DAMP signal integration provides a critical step in the amplification of defense signaling in plants.

Differential activities of maize plant elicitor peptides as mediators of immune signaling and herbivore resistance

“…Plant elicitor peptides have been demonstrated to be conserved regulators of defense responses across diverse plant species and are multigene families in most species (Huffaker et al, 2006(Huffaker et al, , 2011a(Huffaker et al, , 2013Lori et al, 2015;Lee et al, 2018;Shinya et al, 2018). However, the functional relevance of Peps as multigene families has remained largely undefined.…”

“…Since the initial discovery that systemin is a regulator of solanaceous anti-herbivore defenses a large number of peptide families have been found to amplify plant immune responses (McGurl et al, 1992;Yamaguchi and Huffaker, 2011;Ma et al, 2014;Yu et al, 2017b;Segonzac and Monaghan, 2019). While many of these peptides have only been identified in particular species, plant elicitor peptides (Peps) have emerged as widespread conserved signals across plant species, activating broadly protective immunity against microbial pathogens, parasitic nematodes and arthropod herbivores (Huffaker et al, 2011a(Huffaker et al, , 2013Trivilin et al, 2014;Lee et al, 2018;Ruiz et al, 2018b;Shinya et al, 2018;Zhang and Gleason, 2020).…”

“…Although homology searches predicted PROPEP precursors, the putative active Pep sequences are widely variable, with only Gly17 being perfectly conserved, along with a His or Asn residue at the carboxyl terminus and an enrichment of Ser and Gly residues in the carboxyl half of the peptide (Huffaker et al, 2006(Huffaker et al, , 2013Lori et al, 2015). Despite this sequence variability, predicted PROPEPs/Peps have been demonstrated as functionally orthologous to Arabidopsis, regulating defense responses in fabaceous, rosaceous, solanaceous and poaceous plants (Huffaker et al, 2011a(Huffaker et al, , 2013Trivilin et al, 2014;Lee et al, 2018;Ruiz et al, 2018a;Shinya et al, 2018;Zhang and Gleason, 2020).…”

Breaking Bad News: Dynamic Molecular Mechanisms of Wound Response in Plants

“…Furthermore, in all cases of HAMP application, the leaves are mechanically damaged; hence the presence of DAMPs is unavoidable and the specific effects of DAMPs and HAMPs are difficult to be distinguished (Huffaker et al, 2013). Albeit a more artificial system, application of elicitors to suspension cell culture circumvents the unintended consequences of wounding and to disconnect the application of elicitors from the wound response (Shinya et al, 2018). Simultaneous application of Oryza sativa Pep3 and oral secretions from Mythimna loreyi has an additive effect on the production of ROS and MAPK activity and a synergistic effect on defense metabolite accumulation in comparison to separate application.…”

“…Simultaneous application of Oryza sativa Pep3 and oral secretions from Mythimna loreyi has an additive effect on the production of ROS and MAPK activity and a synergistic effect on defense metabolite accumulation in comparison to separate application. This suggests that while DAMPs and HAMPs alone can trigger a defense response, perceiving both is critical for the strength of the induced plant defenses (Shinya et al, 2018).…”