JA but not JA-Ile is the cell-nonautonomous signal activating JA mediated systemic defenses to herbivory in Nicotiana attenuata (original) (raw)
Related papers
PLoS ONE, 2011
A plant's inducible defenses against herbivores as well as certain developmental processes are known to be controlled by the jasmonic acid (JA) pathway. We have previously shown that ectopically expressing Arabidopsis thaliana JA Omethyltransferase in Nicotiana attenuata (35S-jmt) strongly reduces the herbivory-elicited jasmonate bursts by acting as metabolic sink that redirects free JA towards methylation; here we examine the consequences of this metabolic sink on N. attenuata's secondary metabolism and performance in nature. In the glasshouse, 35S-jmt plants produced fewer seed capsules due to shorter floral styles, which could be restored to wild type (WT) levels after hand-pollination, and were more susceptible to Manduca sexta larvae attack. When transplanted into the Great Basin Desert in Utah, 35S-jmt plants grew as well as WT empty vector, but were highly attacked by native herbivores of different feeding guilds: leaf chewers, miners, and single cell feeders. This greater susceptibility was strongly associated with reduced emissions of volatile organic compounds (hexenylesters, monoterpenes and sesquiterpenes) and profound alterations in the production of direct defenses (trypsin proteinase inhibitors [TPI], nicotine, diterpene glycosides [DTGs] and phenylpropanoid-polyamine conjugates) as revealed by a combination of targeted and metabolomics analyses of field collected samples. Complementation experiments with JA-Ile, whose formation is outcompeted in 35S-jmt plants by the methylation reaction, restored the local TPI activation to WT levels and partially complemented nicotine and DTG levels in elicited but not systemic leaves. These findings demonstrate that MeJA, the major JA metabolite in 35S-jmt plants, is not an active signal in defense activation and highlights the value of creating JA sinks to disrupt JA signaling, without interrupting the complete octadecanoid pathway, in order to investigate the regulation of plants' defense metabolism in nature.
Jasmonates and its mimics differentially elicit systemic defence responses in Nicotiana attenuata
Journal of Experimental Botany, 2007
Coronalon (6-ethyl indanoyl isoleucine), a synthetic jasmonate mimic, is known to regulate levels of transcripts and secondary metabolites that are commonly elicited by methyl jasmonate (MeJA) in a variety of plants. The ability of coronalon and its derivative (In-L-Ile-Me) to elicit MeJA-activated transcriptional and defence responses [nicotine and trypsin proteinase inhibitors (TPIs)] was compared in treated and systemic untreated tissues of wild-type (WT) and NaLOX3silenced Nicotiana attenuata plants which are unable to activate either local or systemic defence responses. Coronalon and its derivative significantly regulated 71% and 86% of genes up-regulated by MeJA and 53% and 66% of the genes down-regulated by MeJA in the treated leaves, but only 3% and 7% of all regulated genes in untreated, but phylotactically connected, leaves of WT plants. Consistent with their ability to elicit transcriptional responses in treated tissues, coronalon and In-L-Ile-Me increased nicotine and TPIs when applied to the tissues in which these metabolites are produced, namely roots and leaves. However, treating roots elicited TPI activity in leaves in both WT and NaLOX3-silenced plants, suggesting that mimics can be transported apoplastically from roots to leaves in the xylem. This response was lower in NaLOX3silenced plants, suggesting that the ability of coronalon and In-L-Ile-Me to elicit TPI responses in leaves after root treatments requires intact jasmonic acid (JA) signalling. Treating leaves did not elicit detectable changes in endogenous JA levels but did decrease free salicylic acid contents. It is concluded that coronalon and In-L-Ile-Me elicit jasmonate responses in treated tissues and could be valuable tools for dissecting local and systemic jasmonate signalling networks in plants.
Frontiers in Plant Science
The jasmonate hormones are essential regulators of plant defense against herbivores and include several dozen derivatives of the oxylipin jasmonic acid (JA). Among these, the conjugate jasmonoyl isoleucine (JA-Ile) has been shown to interact directly with the jasmonate co-receptor complex to regulate responses to jasmonate signaling. However, functional studies indicate that some aspects of jasmonate-mediated defense are not regulated by JA-Ile. Thus, it is not clear whether JA-Ile is best characterized as the master jasmonate regulator of defense, or if it regulates more specific aspects. We investigated possible functions of JA-Ile in anti-herbivore resistance of the wild tobacco Nicotiana attenuata, a model system for plant-herbivore interactions. We first analyzed the soluble and volatile secondary metabolomes of irJAR4xirJAR6, asLOX3, and WT plants, as well as an RNAi line targeting the jasmonate co-receptor CORONATINE INSENSITIVE 1 (irCOI1), following a standardized herbivory treatment. irJAR4xirJAR6 were the most similar to WT plants, having a ca. 60% overlap in differentially regulated metabolites with either asLOX3 or irCOI1. In contrast, while at least 25 volatiles differed between irCOI1 or asLOX3 and WT plants, there were few or no differences in herbivore-induced volatile emission between irJAR4xirJAR6 and WT plants, in glasshouse-or field-collected samples. We then measured the susceptibility of jasmonate-deficient vs. JA-Ile-deficient plants in nature, in comparison to wild-type (WT) controls, and found that JA-Ile-deficient plants (irJAR4xirJAR6) are much better defended even than a mildly jasmonate-deficient line (asLOX3). The differences among lines could be attributed to differences in damage from specific herbivores, which appeared to prefer either one or the other jasmonate-deficient phenotype. We further investigated the elicitation of one herbivore-induced volatile known to be jasmonate-regulated and to mediate resistance to herbivores: (E)-α-bergamotene. We found that JA was a more potent elicitor of (E)-α-bergamotene emission than was JA-Ile, and when treated with JA, irJAR4xirJAR6 plants Schuman et al. JA-Ile, Direct and Indirect Resistance emitted 20-to 40-fold as much (E)-α-bergamotene than WT. We conclude that JA-Ile regulates specific aspects of herbivore resistance in N. attenuata. This specificity may allow plants flexibility in their responses to herbivores and in managing trade-offs between resistance, vs. growth and reproduction, over the course of ontogeny.
PLANT PHYSIOLOGY, 2010
Jasmonic acid (JA) and ethylene (ET) are known to play important roles in mediating plant defense against herbivores, but how they affect development in herbivore-attacked plants is unknown. We used JA-deficient (silenced in LIPOXYGENASE3 [asLOX3]) and ET-insensitive (expressing a mutated dominant negative form of ETHYLENE RESPONSE1 [mETR1]) Nicotiana attenuata plants, and their genetic cross (mETR1asLOX3), to examine growth and development of these plants under simulated herbivory conditions. At the whole plant level, both hormones suppressed leaf expansion after the plants had been wounded and the wounds had been immediately treated with Manduca sexta oral secretions (OS). In addition, ectopic cell expansion was observed around both water-and OS-treated wounds in mETR1asLOX3 leaves but not in mETR1, asLOX3, or wild-type leaves. Pretreating asLOX3 leaves with the ET receptor antagonist 1-methylcyclopropane resulted in local cell expansion that closely mimicked the mETR1asLOX3 phenotype. We found higher auxin (indole-3-acetic acid) levels in the elicited leaves of mETR1asLOX3 plants, a trait that is putatively associated with enhanced cell expansion and leaf growth in this genotype. Transcript profiling of OS-elicited mETR1asLOX3 leaves revealed a preferential accumulation of transcripts known to function in cell wall remodeling, suggesting that both JA and ET act as negative regulators of these genes. We propose that in N. attenuata, JA-ET cross talk restrains local cell expansion and growth after herbivore attack, allowing more resources to be allocated to induced defenses against herbivores.
bioRxiv (Cold Spring Harbor Laboratory), 2021
The phytohormone jasmonoyl-L-isoleucine (JA-Ile) regulates many stress responses and developmental processes in plants. A co-receptor complex formed by the F-box protein Coronatine Insensitive 1 (COI1) and a Jasmonate (JA) ZIM-domain (JAZ) repressor perceives the hormone. JA-Ile antagonists are invaluable tools for exploring the role of JA-Ile in specific tissues and developmental stages, and for identifying regulatory processes of the signaling pathway. Using two complementary chemical screens, we identified three compounds that exhibit a robust inhibitory effect on both the hormonemediated COI-JAZ interaction and degradation of JAZ1 and JAZ9 in vivo. One molecule, J4, also restrains specific JAinduced physiological responses in different angiosperm plants, including JA-mediated gene expression, growth inhibition, chlorophyll degradation, and anthocyanin accumulation. Interaction experiments with purified proteins indicate that J4 directly interferes with the formation of the Arabidopsis (Arabidopsis thaliana) COI1-JAZ complex otherwise induced by JA. The antagonistic effect of J4 on COI1-JAZ also occurs in the liverwort Marchantia polymorpha, suggesting the mode of action is conserved in land plants. Besides JA signaling, J4 works as an antagonist of the closely related auxin signaling pathway, preventing Transport Inhibitor Response1/Aux-indole-3-acetic acid interaction and auxin responses in planta, including hormone-mediated degradation of an auxin repressor, gene expression, and gravitropic response. However, J4 does not affect other hormonal pathways. Altogether, our results show that this dual antagonist competes with JA-Ile and auxin, preventing the formation of phylogenetically related receptor complexes. J4 may be a useful tool to dissect both the JA-Ile and auxin pathways in particular tissues and developmental stages since it reversibly inhibits these pathways.
Molecular Ecology, 2008
To determine the impact of genotypic variation in secondary metabolite production on antiherbivore resistance and plant fitness, we genetically silenced biosynthetic genes for nicotine, trypsin proteinase inhibitors (TPI), and jasmonate (JA) production in two accessions of Nicotiana attenuata: one from Utah (UT) which responds to herbivory with JA-induced nicotine and TPI production, and one from Arizona (AZ) which is TPI-deficient but also produces JA-induced nicotine. Transient silencing of JA biosynthesis increased Manduca sexta larval growth on wild type (WT) plants of both accessions, but not on TPI-deficient UT or nicotine-deficient AZ lines, demonstrating that JA-mediated resistance to M. sexta requires TPIs in the UT and nicotine in the naturally TPI-deficient AZ accession. When transplanted into a native UT population, AZ and UT plants, rendered equally able or unable to produce nicotine and TPIs by stable transformation, received significantly different levels of herbivory. Both accessions differed in their resistance depending on the type of herbivores: resistance to rare, voracious herbivores (Saltatoria and Mammalia) was greater in AZ than UT lines, and dependent on nicotine production, while resistance to small, abundant herbivores (Coleoptera and Thysanoptera) was greater in UT lines, and dependent on TPI production. AZ lines produced more flowers and seed capsules than UT lines independently of TPI production costs. This fitness advantage was lost when accessions did not produce nicotine. We conclude that these two accessions have developed different survival strategies and thus differ in the cost-benefit functions of their JA-mediated defences.
Plant molecular biology, 1999
Jasmonic acid (JA) is involved in regulating the expression of certain plant defense genes and response to various stresses. JA biosynthesis is hypothesized to occur both in chloroplasts and the cytoplasm. In order to test whether or not a cytosol-localized allene oxide synthase (AOS) can promote JA biosynthesis, transgenic tobacco plants containing a flax AOS cDNA without a chloroplast transit sequence under the control of a tetracycline-inducible promoter were generated. Induction of the flax AOS gene in transgenic plants with chlor-tetracycline (Tc) led to the expression of the flax AOS mRNA and protein, which resulted in high level of metabolism of 13(S)-hydroperoxyoctadecatrienoic acid (13(S)-HPOT) and formation of 12-oxo-phytodienoic acid (12-O-PDA). Subcellular fractionation demonstrated that the flax AOS protein and activity were associated with the cytosol. Overexpression of the flax AOS in induced transgenic plants did not increase JA levels in healthy, undamaged leaf tiss...
Insect Science, 2011
The jasmonic acid (JA) pathway is the main signal-transduction pathway induced by insect folivory. Mutant plants affected in the jasmonate pathway (18:0 and/or 16:0-oxylipin routes) were studied to assess the effects of JA and its oxylipin intermediates 12-oxophytodienoic acid (OPDA) and dinor-OPDA (dnOPDA) on interconnected signaltransduction pathways that underlie induced defenses in Arabidopsis. Our data show that the oxylipin jasmonates dnOPDA, OPDA and JA have different roles in defense signaling induced after feeding by the chewing-biting caterpillar Pieris rapae. Jasmonic acid, and not OPDA or dnOPDA, is the major signaling compound required for the induction of the defense-related genes LOX2 (Lipoxygenase 2), OPR3 (12-Oxophytodienoate reductase 3), ACX1 (Acyl-CoA oxidase 1) and PAL1 (Phenylalanine ammonia-lyase 1). Monitoring PAL1 transcript levels clearly showed that accumulation of JA upon P. rapae feeding results in the induction of the salicylic acid pathway. Furthermore, JA is the major signaling compound required for the P. rapae-induced expression of the defense-related gene HPL1 (Hydroperoxide lyase 1). The jasmonate dnOPDA influences the induction of the HPLbranch as well, yet its effect is antagonistic to the effect of JA. Our data show that these jasmonates may be used to fine-tune Arabidopsis' herbivore-induced responses in terms of the HPL-branch from the oxylipin pathway.