Plant defense in the absence of jasmonic acid: The role of cyclopentenones

Abstract

The Arabidopsis opr3 mutant is defective in the isoform of 12-oxophytodienoate (OPDA) reductase required for jasmonic acid (JA) biosynthesis. Oxylipin signatures of wounded opr3 leaves revealed the absence of detectable 3R,7S-JA as well as altered levels of its cyclopentenone precursors OPDA and dinor OPDA. In contrast to JA-insensitive coi1 plants and to the fad3 fad7 fad8 mutant lacking the fatty acid precursors of JA synthesis, opr3 plants exhibited strong resistance to the dipteran Bradysia impatiens and the fungus Alternaria brassicicola. Analysis of transcript profiles in opr3 showed the wound induction of genes previously known to be JA-dependent, suggesting that cyclopentenones could fulfill some JA roles in vivo. Treating opr3 plants with exogenous OPDA powerfully up-regulated several genes and disclosed two distinct downstream signal pathways, one through COI1, the other via an electrophile effect of the cyclopentenones. We conclude that the jasmonate family cyclopentenone OPDA (most likely together with dinor OPDA) regulates gene expression in concert with JA to fine-tune the expression of defense genes. More generally, resistance to insect and fungal attack can be observed in the absence of JA.OPDA reductase ͉ opr3 ͉ Arabidopsis ͉ insect A major objective in plant biology is to develop an integrated understanding of how plants survive in their environment and reproduce. Although it has become clear in the last decade that jasmonic acid (JA) is a key regulator in the development, physiology, and defense of plants, the complexity of the signaling network in which JA evolves is just emerging (1). JA is involved in carbon partitioning (2), in mechanotransduction (3), and the ability of plants to synthesize and perceive JA is absolutely essential for the correct development and release of pollen in Arabidopsis (4-7). Highlighting the regulatory importance of JA, a JA-responsive transcription factor, ORCA3, first found in Catharanthus, provides an important link between primary and secondary metabolism (8). There is also strong evidence supporting a central role of JA in plant defense. Exogenous JA powerfully regulates the expression of many defense genes in plants, and its in vivo production and perception seem to be of vital importance in mounting successful defense against insect attackers (9-11). Together with ethylene, JA also plays a crucial role in defense against necrotrophic fungi (12-14) and in induced systemic resistance in response to nonpathogenic rhizobacteria (15). Broader roles of JA in plant stress responses are likely; it is known that the JA biosynthesis pathway is important in gene activation subsequent to UV damage in plants (16), and JA has been implicated in some responses to water stress (17).The biosynthesis of JA occurs through the octadecanoid pathway (18,19) and is initiated by the addition of molecular oxygen to linolenic acid (18:3) to form 13-hydroperoxylinolenic acid (13-HPOTrE). This fatty acid hydroperoxide is then dehydrated by allene oxide synthase (AOS) and cyclized by ...

Transcriptomics of induced defense responses to greenbug aphid feeding in near isogenic wheat lines

“…5). An increase in OPDA concentration in response to wounding has been documented before [60][61][62][63], while JA levels were not necessarily altered [64,65]. On the other hand, increased expression of OPR related JA biosynthesis genes in SB could be explained by our previous observations that greenbugs begin to feed on the S genotype soon after infestation [41], triggering basal defense responses.…”

The Role of Octadecanoids and Functional Mimics in Soybean Defense Responses

“…Re-cently, this concept received a remarkable extension. By exploiting the opr3 mutant of A. thaliana, the participation of biosynthetic precursors of JA in disease resistance was evaluated (Stintzi et al, 2001). Surprisingly, JA-deficient opr3 plants developed wildtype levels of COII-dependent resistance against an insect as well as a fungal pathogen, suggesting that defense pathways can be triggered by OPDA in the absence of JA (Stintzi et al, 2001).…”

“…By exploiting the opr3 mutant of A. thaliana, the participation of biosynthetic precursors of JA in disease resistance was evaluated (Stintzi et al, 2001). Surprisingly, JA-deficient opr3 plants developed wildtype levels of COII-dependent resistance against an insect as well as a fungal pathogen, suggesting that defense pathways can be triggered by OPDA in the absence of JA (Stintzi et al, 2001). Likewise, the resistance of A. thaliana to Phytophthora porri was reported to be independent of the presence of JA as signal transmitter, although the pathway itself was activated (Roetschi et al, 2001).…”

“…(Blechert et al, 1999), in the induction of volatile biosynthesis in lima bean (Phaseolus lunatus) (Koch et al, 1999), and in transcript profiles in Arabidopsis thaliana (Stintzi et al, 2001), respectively, suggested that JA and its biosynthetic precursor 12-oxo-phytodienoic acid (OPDA) very likely represent compounds differentially involved in signaling. In order to cover both possible signaling pathways, in the present study we comparatively investigated the impact of the naturally occurring JA, JAMe, OPDA, and coronatine, and of synthetic functional mimics of these compounds on inducible defense reactions in soybean cell cultures.…”

COS1: An Arabidopsis coronatine insensitive1 Suppressor Essential for Regulation of Jasmonate-Mediated Plant Defense and Senescence

“…They also play pivotal roles in reproduction (Feys et al, 1994;McConn and Browse, 1996;Xie et al, 1998) and regulate many other plant developmental processes . Without JA, Arabidopsis thaliana plants, such as the JA biosynthetic mutants fad (McConn and Browse, 1996), opr3/dd1 (Sanders et al, 2000;Stintzi and Browse, 2000;Stintzi et al, 2001), and aos (Park et al, 2002), are unable to generate viable pollen and therefore fail to complete their life cycle. Without JA signaling or JA adenylation, Arabidopsis plants, including jar1 (Staswick et al, , 1998, coronatine insensitive1 (coi1) (Feys et al, 1994), and jin (Berger et al, 1996), are unresponsive to JA-inhibitory root growth, unable to accumulate JA-inducible genes, and susceptible to pest attack and pathogen infection.…”