Wound-induced changes in root and shoot jasmonic acid pools correlate with induced nicotine synthesis in Nicotiana sylvestris spegazzini and comes (original) (raw)
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New Phytologist, 1997
SVMM.^HY In Nicotiana .n'hestris Spegazzini and Comes {Solanaceae), we examined the relationships among wounding, endogenous leaf jasmonic acid (JA) pools, and whole-plant (\VP) nicotine accumulation ovet a range of woundmg intensities and spatial distributions, in order to explore optimal defence (OD) theory-predictions. We quantitatively wounded one or four leaves and then quantified: (1) JA in damaged and undamaged leaves 90 min after wounding; (2) WP nicotine concentration after 5 d (the times when JA and nicotine attain the largest wound-induced concentrations). We find: (1) statistically significant, positive relationships on a !eaf-by-leaf basis among tbe number of leaf punctures, endogenous leaf JA, and WP nicotine accumulation; (2) tbat young, undamaged leaves have a bigber concentration of JA tban do older, undamaged leaves, and produce a greater amount of JA per puncture tban older leaves, but tbat all leaves bave tbe same JA content (ng JA per leaf); and (3) that a damaged leaf produces less JA when other leaves in tbe canopy are wounded than when it is the only wounded leaf in tbe canopy, but tbat when it is tbe only wounded ieaf, tbe pbylotactically adjacent, undamaged leaves do not mcrease their JA concentrations. Tbe observation tbat younger leaves produce more JA per puncture tban do older leaves is consistent with OD theory predictions. The observation that a small amount of damage localized to a single leaf is as effective as a larger amount of damage dispersed across the canopy in increasing leaf JA and WP nicotine accumulation shows the plant's ability to differentiate between dispersed and localized damage. Because the quantity of JA in a wounded leaf 90 min after wounding is a reliable indicator of the WP nicotine response to wounding, this trait provides insight into how plants integrate information about environmental insults and tailor tbeir defence responses.
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.
Planta, 1997
Both herbivory and mechanical damage result in increases in the concentration of the wound-signal molecule, jasmonic acid (JA), and the defense metabolite, nicotine, in native tobacco plants, Nicotiana sylvestris Speg. et Comes (Solanaceae). We found that higher concentrations of JA resulted from herbivory by Manduca sexta (L.) larvae than from the mechanical damage designed to mimic the herbivory. While both herbivory and mechanical damage increased JA concentrations in roots of wounded plants, herbivory did not induce either higher root JA or nicotine responses than mechanical damage. In a separate experiment in which mechanical damage was not designed to mimic herbivory, JA responses to herbivory were higher than those to mechanical damage, but the whole-plant (WP) nicotine responses were smaller. Furthermore, when regurgitants from M. sexta larvae were applied to standardized mechanical leaf wounds, leaf JA responses were dramatically ampli®ed. However, neither the root JA response nor the WP nicotine response was comparably ampli®ed by application of regurgitants. Our ®ndings demonstrate that the response of N. sylvestris to herbivory is dierent from its response to mechanical damage; moreover, oral secretions from larvae may be partly responsible for the dierence. During feeding, M. sexta larvae appear to modify the plant's normal defensive response to leaf wounding by reducing the systemic increase in root JA after leaf damage and the subsequent WP nicotine response.
Journal of Chemical Ecology, 2004
Nicotiana attenuata plants growing in close proximity to damaged sagebrush (Artemisia tridentata ssp. tridentata) suffer less herbivory than plants near undamaged sagebrush. Sagebrush constitutively releases methyl jasmonate (MeJA), a compound that when applied directly to N. attenuata, elicits herbivore resistance and the direct defense traits [protease inhibitors (PIs), nicotine]. Damage increases the release of volatile MeJA, primarily in the cis epimer, suggesting that cis-MeJA may mediate this apparent interplant signaling. We characterized sagebrush's MeJA plume before and after damage in nature and in the laboratory, and compared the activity of trans-and cis-MeJA in inducing PIs, nicotine, and Manduca sexta resistance in N. attenuata. We used both lanolin applications and aqueous sprays that mimic natural exposures, and we determined the amount of volatilized MeJA required to elicit a nicotine response in open-grown plants. Wounding rapidly and transiently increased cis-MeJA emissions from damaged parts (but not systemically), and the released plume did not rapidly dissipate in nature. cis-MeJA was not consistently more active than trans-MeJA, and the order of exposure (trans-then cis-) did not influence activity. We conclude that volatile MeJA, either trans-or cis-, when applied at
Plant, Cell & Environment, 2009
Manduca sexta larvae to wounds in leaves. Feeding of M. sexta or OS elicitation is known to result in jasmonic acid (JA) and ethylene bursts, and activates a suite of defence responses. Because both plant hormones are known to strongly reduce root growth, their activation might account for the observed reduction of root growth following herbivory. To test this hypothesis, we measured primary root growth with digital image sequence processing at high temporal resolution in antisense-lipoxygenase 3 (asLOX3) and inverted repeat-coronatin-insensitive 1 (irCOI1) seedlings which are impaired in JA biosynthesis and perception, respectively, and wild-type (WT) seedlings. Higher root growth rates in irCOI1 compared with WT were observed after OS elicitation. The dynamics of wound-induced root growth reduction coincide with the dynamics of root growth reduction induced by external application of methyl JA. In an experiment with 1-methylcyclopropen (1-MCP), a potent ethylene receptor blocker, no wounding-specific difference between growth of 1-MCP-treated plants and non-treated plants was observed, suggesting that wound-induced endogenous JA and not ethylene mediates the wounding-specific reduction in root growth. Yet, inhibiting the ethylene response by applying 1-MCP led to markedly increased root growth compared with that of control plants, indicating that ethylene normally suppresses plant growth in N. attenuata seedlings.
Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata
Oecologia, 2000
After herbivore attack, plants launch a suite of direct and indirect defense responses that must be coordinated if plants are to realize a fitness benefit from these responses. Here we characterize the volatile emissions in the native tobacco plant, Nicotiana attenuata Torr. ex Wats., that are elicited by tobacco hornworm (Manduca sexta L.) attack and are known to function as attractants for parasitoids. To provide the first ecophysiological comparison of examples of both types of defense in the same species, we characterize the elicitation and signaling mechanisms, the resources required, and the potential costs and benefits of the volatile release and compare these traits with those of the well-described induced direct defense in this species, nicotine production. The release of (E)-β-ocimene, cis-α-bergamotene and linalool is dramatically induced within 24 h by application of methyl jasmonate (MeJA), caterpillar feeding, and the treatment of mechanical wounds with larval oral secretions (OS), but not by mechanical damage alone. Plants from different geographic locations produce volatile blends that differ in composition. The most consistently released component from all genotypes, cis-α-bergamotene, is positively related to the amount of MeJA and the level of wounding if OS are applied to the wounds. The volatile release is strongly light dependent, dropping to undetectable quantities during dark periods, even when temperatures are elevated to match those of the light period. Inhibitors of wound-induced jasmonate accumulation (salicylates and auxins), which are known to inhibit wound-induced nicotine production, do not inhibit the release of volatiles. By individually inducing different leaf positions with OS and, on other plants, excising them after induction, we demonstrate that the emission is largely a systemic, whole-plant response, which is maximally triggered when the second fully expanded leaf is induced. We conclude that while both are wholeplant, systemic responses that utilize recently acquired resources for their production and are activated by the jasmonate cascade, the elicitation of the volatile release exhibits greater tissue sensitivity and utilizes additional signaling components than does nicotine production. In contrast to the large investment of fitness-limiting resources required for induced nicotine production or the resources used in benzyl acetone release from flowers for pollinator attraction, the resource requirements for the volatile release are minor. Hence the argument that the volatile release incurs comparatively large physiological costs cannot be supported in this system.
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.
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.
Journal of integrative plant biology, 2017
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 grafting-experiments 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 gr...