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James H Tumlinson

Publications and source records attributed to James H Tumlinson.

17 recordsLinked to original sources

Compatible and incompatible Xanthomonas infections differentially affect herbivore-induced volatile emission by pepper plants.

Recent studies have alerted us to the potential for conflicts between pathogen- and herbivore-induced plant defenses. The lack of studies on the induced chemical changes that simultaneous insect and pathogen attacks have on the host plant has become apparent. In the present study, we found that pepper plant volatile profiles can be differentially induced by compatible and incompatible bacterial infection and beet armyworm (BAW) damage when applied alone or in combination upon the same host. We also found that plants under simultaneous compatible bacterial and BAW attack are able to produce volatiles in quantities greater than those produced by healthy plants in response to BAW feeding. In contrast, plants exposed to the incompatible pathogen challenge showed a total volatile release below the level of healthy plants exposed to BAW damage. This suppression of BAW-induced volatiles coincided with increased methyl salicylate production from incompatible bacteria-infected plants. Feeding choice experiments revealed that, when given a choice, BAW larvae fed significantly more on leaves of plants infected with the incompatible bacteria as soon as 2 d after inoculation, while a significant increase in insect feeding on the plants infected with the compatible bacterial strain was not seen until day 4 after inoculation. Additionally, survival for third instars to pupation was significantly higher when feeding on infected plants than on healthy plants, regardless of compatibility. These results are indicative of lowered herbivore defenses due to disease progression on the plants.

Animals↗

Systemic induction of volatile release in cotton: how specific is the signal to herbivory?

Plants attacked by herbivorous insects release chemical signals that attract natural enemies of the herbivores to the damaged plants. Feeding of Spodoptera exigua larvae on the lower leaves of cotton (Gossypium hirsutum L.) for multiple feeding periods of 9-12 h with a 12 h, interval in between when the caterpillars are removed overnight, will induce a systemic release of volatile compounds that is comparable to the volatiles released in response to continuous feeding damage on the lower leaves for several days. The systemic volatile release in response to herbivory can be mimicked by mechanically damaging the lower leaves and applying caterpillar oral secretion to the injured leaves over 4 days. Cotton plants that are only mechanically damaged systemically release significantly less beta-pinene, myrcene, (Z)-3-hexenyl acetate, (E)-beta-farnesene and (E,E)-alpha-farnesene after 4 days compared to plants damaged mechanically with application of caterpillar regurgitant. However, multiple 9-12 h mechanical damage alone induces a significantly higher systemic release of (Z)-3-hexenyl acetate, myrcene, (E)-beta-ocimene, and (E)-beta-farnesene after 4 days compared to undamaged control plants. This indicates that multiple mechanical damage alone cannot mimic completely the response induced by mechanically injuring the leaves and applying caterpillar regurgitant. A specific elicitor in the regurgitant of the caterpillar enhances the amount of several systemically released volatiles. Thus, the systemic release of volatile compounds by herbivore-damaged cotton plants appears to be regulated by at least two different mechanisms.

Animals↗

Biosynthesis of fatty acid amide elicitors of plant volatiles by insect herbivores.

Larvae of several species of Lepidoptera produce fatty acid amide elicitors that induce the plants on which they feed to synthesize and release volatile organic compounds. The volatiles released by the plants act as cues that aid in host location by natural enemies of the herbivorous larvae. The elicitors are synthesized in the larvae by enzymes embedded in the membranes of the crop and anterior midgut tissues. The fatty acid precursors of the elicitors are obtained from the plants on which the caterpillars feed, while the amino acid moieties appear to be obtained from pools within the insects. The fatty acid amide elicitors are rapidly hydrolyzed in the midgut and hindgut by enzymes in the gut lumen. The role of these fatty acid amides in caterpillar metabolism is not yet understood.

Amides↗

Lepidopteran herbivory and oral factors induce transcripts encoding novel terpene synthases in Medicago truncatula.

Terpenes are an important class of defense compounds that accumulate in plants after pathogen infection or arthropod injury. Sequences predicted to encode terpene synthases were selected from an expressed sequence tag (EST) database of Medicago truncatula. Four putative terpene synthase clones (MtTps1-MtTps4), originating from a chewing insect-damaged M. truncatula leaf cDNA library, were isolated. Transcript levels of each gene examined increased in response to artificial wounding, Spodoptera exigua herbivory, and treatment with volatile methyl jasmonate (meJA). Addition of S. exigua regurgitant to wound sites triggered transcript accumulation of MtTps1 and levels increased with higher concentrations of regurgitant. Furthermore, induction of MtTps1 occurred after application of N-linolenoyl-glutamate or N-linoleoyl-glutamate, factors found in lepidopteran regurgitant. Genomic DNA blots indicate that each of the putative proteins is encoded by a single-copy gene or a small gene family. Proteins encoded by MtTps3 and MtTps4 are imported into the soluble fraction of chloroplasts in in vitro assays, whereas proteins encoded by MtTps1 and MtTps2 are not imported into chloroplasts. Combined with sequence comparisons of multiple plant terpene synthases, the import data indicate that MtTps1 and MtTps2 likely encode sesquiterpene synthases and that MtTps3 and MtTps4 encode mono- or di-terpene synthases. In addition to serving as a valuable model legume species for genomic studies, M. truncatula should prove a valuable source of novel terpene-producing enzymes. Induction of wound-responsive genes by insect oral factors suggests that M. truncatula senses biotic damage through the presence of elicitors originating in the herbivore.

Alkyl and Aryl Transferases↗

Phytohormones mediate volatile emissions during the interaction of compatible and incompatible pathogens: the role of ethylene in Pseudomonas syringae infected tobacco.

Interactions between the phytohormones ethylene, salicylic acid (SA), and jasmonic acid (JA) are thought to regulate the specificity of induced plant defenses against microbial pathogens and herbivores. However, the nature of these interactions leading to induced plant volatile emissions during pathogen infection is unclear. We previously demonstrated that a complex volatile blend including (E)-beta-ocimene, methyl salicylate (MeSA), and numerous sesquiterpenes was released by tobacco plants, Nicotiana tabacum K326, infected with an avirulent/incompatible strain of Pseudomonas syringae pv. tomato (Pst DC3000). In contrast, a volatile blend, mainly consisting of MeSA and two unidentified sesquiterpenes, was released by plants infected with P. syringae pv. tabaci (Pstb) in a virulent/compatible interaction. In this study, we examined the interaction of multiple pathogen stresses, phytohormone signaling, and induced volatile emissions in tobacco. Combined pathogen infection involved the inoculation of one leaf with Pst DC 3000 and of a second leaf, from the same plant, with Pstb. Combined infection reduced emissions of ocimene and MeSA compared to plants infected with Pst DC 3000 alone, but with no significant changes in total sesquiterpene emissions. In the compatible interaction, Pstb elicited a large ethylene burst with a peak emission occurring 3 days after inoculation. In contrast, the incompatible interaction involving Pst DC3000 displayed no such ethylene induction. Pstb-induced ethylene production was not significantly altered by Pst DC3000 in the combined infection. We postulated that Pstb-induced ethylene production may play a regulatory role in altering the typical volatile emission in tobacco in response to Pst DC3000 infection. To clarify the role of ethylene, we dynamically applied ethylene to the headspace of tobacco plants following infection with Pst DC3000. Consistent with Pstb-induced ethylene, exogenous ethylene reduced both ocimene and MeSA emissions, and selectively altered the ratios and amounts of induced sesquiterpene emissions. Our findings suggest that ethylene can regulate the magnitude and blend of induced volatile emissions during pathogen infection.

Cyclopentanes↗

Airborne signals prime plants against insect herbivore attack.

Green leafy volatiles (GLV), six-carbon aldehydes, alcohols, and esters commonly emitted by plants in response to mechanical damage or herbivory, induced intact undamaged corn seedlings to rapidly produce jasmonic acid (JA) and emit sesquiterpenes. More importantly, corn seedlings previously exposed to GLV from neighboring plants produced significantly more JA and volatile sesquiterpenes when mechanically damaged and induced with caterpillar regurgitant than seedlings not exposed to GLV. The use of pure synthetic chemicals revealed that (Z)-3-hexenal, (Z)-3-hexen-1-ol, and (Z)-3-hexenyl acetate have nearly identical priming activity. Caterpillar-induced nocturnal volatiles, which are enriched in GLV, also exhibited a strong priming effect, inducing production of larger amounts of JA and release of greater quantities of volatile organic compounds after caterpillar regurgitant application. In contrast, GLV priming did not affect JA production induced by mechanical wounding alone. Thus, GLV specifically prime neighboring plants against impending herbivory by enhancing inducible chemical defense responses triggered during attack and may play a key role in plant-plant signaling and plant-insect interactions.

Animals↗

The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites.

Through complex networks of signaling interactions, phytohormones regulate growth, development, reproduction and responses to biotic and abiotic stress. Comprehensive metabolomic approaches, seeking to quantify changes in vast numbers of plant metabolites, may ultimately clarify these complex signaling interactions and consequently explain pleiotropic effects on plant metabolism. Synergistic and antagonistic phytohormone signaling interactions, referred to as crosstalk, are often considered at the level of transduction without proper consideration of synthesis or accumulation of phytohormones because of the limitation and difficulty in quantifying numerous signals. Significant progress has recently been made in the expansion of metabolic profiling and analysis of multiple phytohormones [Birkemeyer et al. (J. Chromatogr. A, 2003, 993, 89); Chiwocha et al. (Plant J., 2003, 35, 405); Müller et al. (Planta, 2002, 216, 44); Schmelz et al. (Proc. Natl Acad. Sci. USA, 2003, 100, 10552)]. We recently presented a novel metabolic profiling approach to the analysis of acidic phytohormones and other metabolites based on a simplistic preparation scheme and analysis by chemical ionization-gas chromatography/mass spectrometry. We now provide a detailed description of this vapor phase extraction technique and use pathogen infection of Arabidopsis with Pseudomonas syringae DC3000 to illustrate metabolic changes in salicylic acid, cinnamic acid, jasmonic acid, indole-3-acetic acid, abscisic acid, unsaturated C(18) fatty acids, 12-oxo-phytodienoic acid, and phytotoxin coronatine. Directions for further method expansion are provided and include issues of recovery, derivatization, range of accessible analytes, optimization, reproducibility and future directions.

Arabidopsis↗

Volatiles released from cotton plants in response to Helicoverpa zea feeding damage on cotton flower buds.

Feeding of Helicoverpa zea larvae on cotton ( Gossypium hirsutum L.) flower buds (squares) for 24 or 48 h induced the release of a number of terpenes [( E)-beta-ocimene, linalool, ( E)-beta-farnesene, ( E, E)-alpha-farnesene, ( E)-4,8-dimethyl-1,3,7-nonatriene, ( E, E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene], isomeric hexenyl butyrates, 2-methylbutyrates, indole and ( Z)-3-hexenyl acetate. These compounds are not released in significant amounts from undamaged squares and freshly damaged squares. The release of inducible compounds was not limited to the damaged squares themselves. The compounds were also released systemically from the upper undamaged leaves of the same plant after 72 h. However, the composition of the blend of systemically released volatiles differed from the blend released by damaged squares. The compounds that were systemically released from undamaged leaves in response to feeding on the squares were ( Z)-3-hexenyl acetate, ( E)-beta-ocimene, linalool, ( E)-4,8-dimethyl-1,3,7-nonatriene, ( E)-beta-farnesene, ( E, E)-alpha-farnesene, and indole. This study shows that insect damage inflicted to the reproductive parts of a plant causes a systemic emission of volatiles from its vegetative parts.

Animals↗

Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants.

Phytohormones regulate the protective responses of plants against both biotic and abiotic stresses by means of synergistic or antagonistic actions referred to as signaling crosstalk. A bottleneck in crosstalk research is the quantification of numerous interacting phytohormones and regulators. The chemical analysis of salicylic acid, jasmonic acid, indole-3-acetic acid, and abscisic acid is typically achieved by using separate and complex methodologies. Moreover, pathogen-produced phytohormone mimics, such as the phytotoxin coronatine (COR), have not been directly quantified in plant tissues. We address these problems by using a simple preparation and a GC-MS-based metabolic profiling approach. Plant tissue is extracted in aqueous 1-propanol and mixed with dichloromethane. Carboxylic acids present in the organic layer are methylated by using trimethylsilyldiazomethane; analytes are volatilized under heat, collected on a polymeric absorbent, and eluted with solvent into a sample vial. Analytes are separated by using gas chromatography and quantified by using chemical-ionization mass spectrometry that produces predominantly [M+H]+ parent ions. We use this technique to examine levels of COR, phytohormones, and volatile organic compounds in model systems, including Arabidopsis thaliana during infection with Pseudomonas syringae pv. tomato DC3000, corn (Zea mays) under herbivory by corn earworm (Helicoverpa zea), tobacco (Nicotiana tabacum) after mechanical damage, and tomato (Lycopersicon esculentum) during drought stress. Numerous complex changes induced by pathogen infection, including the accumulation of COR, salicylic acid, jasmonic acid, indole-3-acetic acid, and abscisic acid illustrate the potential and simplicity of this approach in quantifying signaling crosstalk interactions that occur at the level of synthesis and accumulation.

Abscisic Acid↗

Rapid biosynthesis of N-linolenoyl-L-glutamine, an elicitor of plant volatiles, by membrane-associated enzyme(s) in Manduca sexta.

In response to elicitors in the oral secretions of caterpillars, plants produce and release volatile chemicals that attract predators and parasitoids of the caterpillar while it feeds. The most prevalent elicitors are fatty acid amides consisting of 18-carbon polyunsaturated fatty acids coupled with l-glutamine. We demonstrate rapid CoA- and ATP-independent in vitro biosynthesis of the fatty acid amide elicitor, N-linolenoyl-l-glutamine, by microsomal fractions of several alimentary tissues in Manduca sexta. N-linolenoyl-l-glutamine is a structural analog of several other elicitors including volicitin, the first fatty acid amide elicitor identified in caterpillars. The enzyme(s) that catalyzed biosynthesis of N-linolenoyl-l-glutamine was localized within the integral membrane protein fraction extracted from microsomes by Triton X-114 detergent phase partitioning and had maximum activity at alkaline pH. We found no evidence suggesting microbial or tissue-independent biosynthesis of N-linolenoyl-l-glutamine in M. sexta. The in vitro biosynthesis of N-linolenoyl-l-glutamine by membrane-associated enzyme(s) in M. sexta represents direct evidence of fatty acid amide synthesis by caterpillar tissues.

Animals↗

Differential volatile emissions and salicylic acid levels from tobacco plants in response to different strains of Pseudomonas syringae.

Pathogen-induced plant responses include changes in both volatile and non-volatile secondary metabolites. To characterize the role of bacterial pathogenesis in plant volatile emissions, tobacco plants, Nicotiana tabacum L. K326, were inoculated with virulent, avirulent, and mutant strains of Pseudomonas syringae. Volatile compounds released by pathogen-inoculated tobacco plants were collected, identified, and quantified. Tobacco plants infected with the avirulent strains P. syringae pv. maculicola ES4326 (Psm ES4326) or pv. tomato DC3000 (Pst DC3000), emitted quantitatively different, but qualitatively similar volatile blends of (E)-beta-ocimene, linalool, methyl salicylate (MeSA), indole, caryophyllene, beta-elemene, alpha-farnesene, and two unidentified sesquiterpenes. Plants treated with the hrcC mutant of Pst DC3000 (hrcC, deficient in the type-III secretion system) released low levels of many of the same volatile compounds as in Psm ES4326- or Pst DC3000-infected plants, with the exception of MeSA, which occurred only in trace amounts. Interaction of the virulent pathogen P. syringae pv. tabaci (Pstb), with tobacco plants resulted in a different volatile blend, consisting of MeSA and two unidentified sesquiterpenes. Overall, maximum volatile emissions occurred within 36 h post-inoculation in all the treatments except for the Pstb infection that produced peak volatile emissions about 60 h post-inoculation. (E)-beta-Ocimene was released in a diurnal pattern with the greatest emissions during the day and reduced emissions at night. Both avirulent strains, Psm ES4326 and Pst DC3000, induced accumulation of free salicylic acid (SA) within 6 h after inoculation and conjugated SA within 60 h and 36 h respectively. In contrast, SA inductions by the virulent strain Pstb occurred much later and conjugated SA increased slowly for a longer period of time, while the hrcC mutant strain did not trigger free and conjugated SA accumulations in amounts significantly different from control plants. Jasmonic acid, known to induce plant volatile emissions, was not produced in significantly higher levels in inoculated plants compared to the control plants in any treatments, indicating that induced volatile emissions from tobacco plants in response to P. syringae are not linked to changes in jasmonic acid.

Cyclopentanes↗

Simultaneous quantification of jasmonic acid and salicylic acid in plants by vapor-phase extraction and gas chromatography-chemical ionization-mass spectrometry.

Jasmonic acid and salicylic acid represent important signaling compounds in plant defensive responses against other organisms. Here, we present a new method for the easy, sensitive, and reproducible quantification of both compounds by vapor-phase extraction and gas chromatography-positive ion chemical ionization-mass spectrometry. The method is based on a one-step extraction, phase partitioning, methylation with HCl/methanol, and collection of methylated and, thus, volatilized compounds on Super Q filters, thereby omitting further purification steps. Eluted samples are analyzed and quantified by GC/MS with chemical ionization. Standard curves were linear over a range of 5-1000 ng for jasmonic acid and salicylic acid. The correlation coefficients were greater than 0.999 and the recovery rates estimated between 70 and 90% for salicylic acid and 90 and 100% for jasmonic acid. The limit of detection was about 500 fg by using single ion detection mode. Both, cis- and trans-isomers for jasmonic acid can be detected. A comparison with established methods indicates the new method to be highly efficient, allowing reliable quantification of both compounds from small amounts of plant material (5-400mg fresh weight).

Alamethicin↗

Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize.

Insect herbivore-induced plant volatile emission and the subsequent attraction of natural enemies is facilitated by fatty acid-amino acid conjugate (FAC) elicitors, such as volicitin [N-(17-hydroxylinolenoyl)-L-glutamine], present in caterpillar oral secretions. Insect-induced jasmonic acid (JA) and ethylene (E) are believed to mediate the magnitude of this variable response. In maize (Zea mays) seedlings, we examined the interaction of volicitin, JA, and E on the induction of volatile emission at different levels of nitrogen (N) availability that are known to influence E sensitivity. N availability and volicitin-induced sesquiterpene emission are inversely related as maximal responses were elicited in N-deficient plants. Plants with low N availability demonstrated similar volatile responses to volicitin (1 nmol plant(-1)) and JA (100 nmol plant(-1)). In contrast, plants with medium N availability released much lower amounts of volicitin-induced sesquiterpenes compared with JA, suggesting an alteration in volicitin-induced JA levels. As predicted, low N plants exhibited greater sustained increases in wound- and volicitin-induced JA levels compared with medium N plants. N availability also altered volicitin-E interactions. In low N plants, E synergized volicitin-induced sesquiterpene and indole emission 4- to 12-fold, with significant interactions first detected at 10 nL L(-1) E. Medium N plants demonstrated greatly reduced volicitin-E interactions. Volicitin-induced sesquiterpene emission was increased by E and was decreased by pretreatment the E perception inhibitor 1-methylcyclopropene without alteration in volicitin-induced JA levels. N availability influences plant responses to insect-derived elicitors through changes in E sensitivity and E-independent JA kinetics.

Animals↗

Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory.

Jasmonic acid (JA) has long been hypothesized to be an important regulator of insect-induced volatile emission; however, current models are based primarily on circumstantial evidence derived from pharmacological studies. Using beet armyworm caterpillars (BAW: Spodoptera exigua) and intact corn seedlings, we examine this hypothesis by measuring both the time-course of insect-induced JA levels and the relationships between endogenous JA levels, ethylene, indole and sesquiterpenes. In separate Morning and Evening time-course trials, BAW feeding stimulated increases in JA levels within the first 4-6 h and resulted in maximal increases in JA, indole, sesquiterpenes and ethylene 8-16 h later. During BAW herbivory, increases in JA either paralleled or preceded the increases in indole, sesquiterpenes and ethylene in the Morning and Evening trials, respectively. By varying the intensity of the BAW herbivory, we demonstrate that strong positive relationships exist between the resulting variation in insect-induced JA levels and volatile emissions such as indole and the sesquiterpenes. To address potential signaling interactions between herbivore-induced JA and ethylene, plants were pretreated with 1-methylcyclopropene (1-MCP), an inhibitor of ethylene perception. 1-MCP pretreatment resulted in reduced production of ethylene and volatile emission following BAW herbivory but did not alter the insect-induced accumulation of JA. Our results strongly support a role for JA in the regulation of insect-induced volatile emission but also suggest that ethylene perception regulates the magnitude of volatile emission during herbivory.

Animals↗

In vivo volatile emissions from peanut plants induced by simultaneous fungal infection and insect damage.

Peanut plants, Arachis hypogaea, infected with white mold. Sclerotium rolfsii, emit a blend of organic compounds that differs both quantitatively and qualitatively from the blend emitted from plants damaged by beet armyworm (BAW; Spodoptera exigua) larvae or from uninfected, undamaged plants. Attackby BAW induced release of lipoxygenase products (hexenols, hexenals, and hexenyl esters), terpenoids, and indole. The plant-derived compound methyl salicylate and the fungal-derived compound 3-octanone were found only in headspace samples from white mold infected plants. White mold-infected plants exposed to BAW damage released all the volatiles emitted by healthy plants fed on by BAW in addition to those emitted in response to white mold infection alone. When BAW larvae were given a choice of feeding on leaves from healthy or white mold-infected plants, they consumed larger quantities of the leaves from infected plants. Exposure to commercially available (Z)-3 hexenyl acetate, linalool, and methyl salicylate, compounds emitted by white mold-infected plants, significantly reduced the growth of the white mold in solid-media cultures. Thus, emission of these compounds by infected plants may constitute a direct defense against this pathogen.

Animals↗

Induced plant signaling and its implications for environmental sensing.

The sophisticated chemical responses of plants to environmental stimuli have profound implications for the development of remote sensing systems. Recent advances in the investigation of these responses have demonstrated that plants can be developed as reliable reporters of numerous environmental stimuli including soil and water conditions, light levels, temperature, mechanical damage, insect feeding, exposure to pathogens--including those that affect animals and humans--and exposure to airborne chemicals. Researchers are just beginning to understand the full range of plant phenotypic responses to these and other stimuli. These responses often have measurable physiological and molecular components that are readily observed. Other responses (e.g., internal biochemical changes) are less readily assayed, although sensing devices are being developed. Plant volatile emission "signatures" are particularly promising modes of plant reporting that can provide highly specific information regarding a diverse range of environmental variables on short time scales, but new approaches are needed for sensing these responses remotely. Modern molecular techniques promise to allow us to refine plant sensing and reporting, greatly enhancing the potential utility of plants as "sentinels." Continued basic research aimed at characterizing the physiological, biochemical, and molecular responses of plants to environmental stimuli (including airborne chemicals, insects and pathogenic microbes) are essential to achieving that promise.

Environmental Monitoring↗