JA but not JA‐Ile is the cell‐nonautonomous signal activating JA mediated systemic defenses to herbivory in Nicotiana attenuata

Abstract

The whole-plant activation of defense responses to wounding and herbivory requires systemic signaling in which jasmonates (JAs) play a pivotal role. To examine the nature of the slower cell-nonautonomous as compared to the rapid cell-autonomous signal in mediating systemic defenses in Nicotiana attenuata, reciprocal stem graftingexperiments were used with plants silenced for the JA biosynthetic gene ALLENE OXIDE CYCLASE (irAOC) or plants transformed to create JA sinks by ectopically expressing Arabidopsis JA-O-methyltransferase (ovJMT). JA-impaired irAOC plants were defective in the cell-nonautonomous signaling pathway but not in JA transport. Conversely, ovJMT plants abrogated the production of a graft-transmissible JA signal. Both genotypes displayed unaltered cell-autonomous signaling. Defense responses (17-hydroxygeranyllinalool diterpene glycosides, nicotine, and proteinase inhibitors) and metabolite profiles were differently induced in irAOC and ovJMT scions in response to graft-transmissible signals from elicited wild type stocks. The performance of Manduca sexta larvae on the scions of different graft combinations was consistent with the patterns of systemic defense metabolite elicitations. Taken together, we conclude that JA and possibly MeJA, but not JA-Ile, either directly functions as a long-distance transmissible signal or indirectly interacts with long distance signal(s) to activate systemic defense responses.

The Asian corn borer Ostrinia furnacalis feeding increases the direct and indirect defence of mid‐whorl stage commercial maize in the field

“…Plant defences are mediated by phytohormones, including jasmonic acid (JA), abscisic acid (ABA) and salicylic acid (SA) (Ankala et al, 2009;Howe and Jander, 2008;Kessler and Baldwin, 2002;Rehrig et al, 2014;Schweiger et al, 2014;Thaler et al, 2012;Tzin et al, 2015;Yan et al, 2012), and the accumulation of JA and SA plays an important role in regulating plant-induced resistance to insects (Kawazu et al, 2012;Kerchev et al, 2012;Nahar et al, 2011;Wang and Wu, 2013). JA-mediated signalling is generally activated by feeding insects (Stam et al, 2014), and directly and indirectly functions in the activation of both local and systemic defences in plants (Bozorov et al, 2017;Kaur et al, 2010). Insect attack generally causes release of several interacting phytohormones (Caarls et al, 2015;Erb et al, 2012;Pieterse et al, 2012;Vos 2009).…”

Shoot-to-root translocation of the jasmonate precursor 12-oxo-phytodienoic acid (OPDA) coordinates plant growth responses following tissue damage

“…Nonetheless, JA amounts were lower in wounded wt/aos rootstocks compared to wt or wt/wt controls. Previous reports analyzing endogenous oxylipin translocation excluded leaf--to--leaf JA and JA--Ile movement [3], or concluded that JA but not JA--Ile is moving acropetally to undamaged tissues [26,27]. However, OPDA was not analyzed in those experiments, and after re--evaluation of the published material, the data is also compatible with OPDA translocation.…”

“…As opr is unable to synthesize de novo JA and JA--Ile, the increase of those compounds in opr rootstocks after wt scion damage indicated that additional compounds downstream of OPDA translocate basipetally from wounded shoots. endogenous JA and JA--Ile were found to be mobile in tomato and wild tobacco [26,27]. The identification of NPF2.10/GTR1 as JA and JA--Ile transporter [43,44] and of AtABCG16/JAT1 mediating nuclear JA--Ile influx [45], further underline the importance of a regulated distribution of jasmonate species across cells and organs.…”

“…Exogenous treatments of labeled OPC--8, JA, or JA--Ile have implied translocation of all tested compounds from the sites of application to distal tissues in different plant species [21--25]. Grafting experiments in tomato (Solanum lycopersicum) and wild tobacco (Nicotiana attenuata) between wt and JA--deficient mutants have indicated acropetal (upwards) translocation of wound--induced oxylipins including JA and JA--Ile [26,27]. Studies in barrel medic (Medicago truncatula) further support acropetal translocation of JA species [28], although contrasting evidence has also been reported for tomato [29].…”

Plant–arthropod interactions: who is the winner?

“…In contrast, systemic responses from wounded Arabidopsis cotyledons to roots was shown to be independent of GLRs and electrical signaling, but more probably due to JA transport (Gasperini et al ., ). Similarly, JA but not JA‐Ile was identified as a long‐distance transmissible signal in N. attenuata response to M. sexta using stem‐to‐stem grafted plants (Bozorov et al ., ). In tomato, application of isotope‐labeled precursors in wounded leaves indicated that JA‐Ile may be a mobile signal (Matsuura et al ., ).…”