Jennifer S. Thaler

Evolution of jasmonate and salicylate signal crosstalk

The evolution of land plants approximately 470 million years ago created a new adaptive zone for natural enemies (attackers) of plants. In response to attack, plants evolved highly effective, inducible defense systems. Two plant hormones modulating inducible defenses are salicylic acid (SA) and jasmonic acid (JA). Current thinking is that SA induces resistance against biotrophic pathogens and some phloem feeding insects and JA induces resistance against necrotrophic pathogens, some phloem feeding insects and chewing herbivores. Signaling crosstalk between SA and JA commonly manifests as a reciprocal antagonism and may be adaptive, but this remains speculative. We examine evidence for and against adaptive explanations for antagonistic crosstalk, trace its phylogenetic origins and provide a hypothesis-testing framework for future research on the adaptive significance of SA-JA crosstalk.

Jasmonate-inducible plant defences cause increased parasitism of herbivores

In many plants, defence systems against herbivores are induced through the octadecanoid pathway,, which may also be involved in recruiting natural enemies of herbivores. This pathway can beinduced by treating plants with jasmonic acid or by natural herbivory, and increases resistance against herbivorous insects intomato plants, in part by causing production of toxic and antinutritive proteinase inhibitors and oxidative enzymes. Herbivore-infested tomato plants release increased amounts of volatiles and attract natural enemies of the herbivores, as do other plants. The octadecanoid pathway may regulate production of these volatiles, which attract host-seeking parasitic wasps,. However, plant resistance compounds can adversely affect parasitoids as well as herbivores. It is unclear whether the combination of increased retention and/or attractiveness of parasitic wasps to induced plants and the adverse effects of plant defence compounds on both caterpillars and parasitoids results in a net increase in parasitization of herbivores feeding on induced plants.Here I show that inducing plants with jasmonic acid increases parasitism of caterpillar pests in an agricultural field twofold. Thus, elicitors of plant resistance may become useful in agriculture.

Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field.

Wounding increases the levels and activities of several defense-related proteins in the foliage of the tomato plant,Lycopersicon esculentum Mill. Evidence indicates that two of these responses, the systemic increases in polyphenol oxidase and proteinase inhibitors, are regulated by an octadecanoid-based signalling pathway which includes the wound hormone, jasmonic acid. It is not known whether other responses to wounding are also regulated by this same signalling pathway. In this paper, we show that application of jasmonates (jasmonic acid or its volatile derivative, methyl jasmonate) in low concentrations to foliage of young tomato plants induced, in a dose-dependent manner, the same protein responses-polyphenol oxidase, proteinase inhibitors, lipoxygenase, and peroxidase-as doesHelicoverpa zea Boddie feeding. Application of jasmonic acid to a single leaflet of four-leaf tomato plants induced these four proteins in a spatial pattern nearly identical to that produced by localized feeding ofH. zea. Exogenous jasmonic acid also decreased suitability of foliage for the beet armyworm,Spodoptera exigua Hubner in the laboratory. Based on these results, we conducted an experiment to measure the effects of jasmonic acid spray under field conditions. We provide the first evidence that jasmonic acid spray on field plants induces production of chemical defenses above the levels found in unsprayed controls. Exogenous jasmonic acid sprayed on plants in agricultural plots increased levels of polyphenol oxidase and proteinase inhibitors. Because application of jasmonic acid induces these defensive compounds at low concentrations in a manner similar to natural wounding, it may prove to be a useful tool for stimulating plant resistance to insects in the field.

The Role of the Jasmonate Response in Plant Susceptibility to Diverse Pathogens with a Range of Lifestyles

Plants defend themselves against attack from insects and pathogens with various resistance strategies. The jasmonate and salicylate signaling pathways are two induced responses that protect plants against these attackers. Knowledge of the range of organisms that are affected by each response is important for understanding how plants coordinate their defenses against multiple attackers and the generality of effect of different resistance mechanisms. The jasmonate response is known to protect plants against a wide range of insect herbivores; in this study, we examined the role of the jasmonate response in susceptibility to eight pathogens with diverse lifestyles in the laboratory and field. Recent biochemical models suggest that the lifestyle of the pathogen (necrotroph versus biotroph) should predict whether the jasmonate response will be involved in resistance. We tested this by examining the susceptibility of wild-type (cv Castlemart with no known genes for resistance to the pathogens used) and jasmonate-deficient mutant tomato (Lycopersicon esculentum) plants (def1) and by employing rescue treatments of the mutant. Plant susceptibility to five of the eight pathogens we examined was reduced by the jasmonate response, including two bacteria (Pseudomonas syringae and Xanthomonas campestris), two fungi (Verticillium dahliae and Fusarium oxysporum f. sp. lycopersici), and an oomycete (Phytophthora infestans). Susceptibility to three fungi was unaffected (Cladosporium fulvum, Oidium neolycopersici, and Septoria lycopersici). Our results indicate that the jasmonate response reduces damage by a wide range of pathogens from different lifestyles, a result that contrasts with the emerging picture of diseases on Arabidopsis. Thus, the generality of jasmonate-based resistance of tomato challenges the view that ecologically distinct plant parasites are resisted via different mechanisms.

Trade-Offs in Plant Defense Against Pathogens and Herbivores: A Field Demonstration of Chemical Elicitors of Induced Resistance

Two signaling pathways, one involving salicylic acid and another involving jasmonic acid, participate in the expression of plant resistance to pathogens and insect herbivores. In this study, we report that stimulation of systemic acquired resistance in field-grown tomato plants with the salicylate mimic, benzothiadiazole: (1) attenuates the jasmonate-induced expression of the antiherbivore defense-related enzyme polyphenol oxidase, and (2) compromises host-plant resistance to larvae of the beet armyworm, Spodoptera exigua. Conversely, treatment of plants with jasmonic acid at concentrations that induce resistance to insects reduces pathogenesis-related protein gene expression induced by benzothiadiazole, and partially reverses the protective effect of benzothiadiazole against bacterial speck disease caused by Pseudomonas syringae pv. tomato. We conclude that effective utilization of induced plant resistance to the multiple pests typically encountered in agriculture will require understanding potential signaling conflicts in plant defense responses.

Jasmonate-mediated induced plant resistance affects a community of herbivores

1. The negative effect of induced plant resistance on the preference and performance of herbivores is a well‐documented ecological phenomenon that is thought to be important for both plants and herbivores. This study links the well‐developed mechanistic understanding of the biochemistry of induced plant resistance in the tomato system with an examination of how these mechanisms affect the community of herbivores in the field.

INTERACTIONS BETWEEN ABSCISIC-ACID-MEDIATED RESPONSES AND PLANT RESISTANCE TO PATHOGENS AND INSECTS

One goal of phytohormonal ecology is to study the interactions between biotic and abiotic stress at hierarchical levels of biological organization. From an ecological perspective, exposure to one stress may alter the plants probability of being exposed to another stress. From a mechanistic perspective, hormonal and biochemical signaling in- teractions between responses to each stress may influence the severity or ability to adaptively respond to the subsequent stress. In this article, we consider the relationship between plant water and salt stress and attack by pathogens and herbivores. Empirical data suggest that water stress and the probability of attack by pathogens and herbivores are correlated between habitats. Biochemical interactions between plant responses to water and salt stress and insect and pathogen attack are also interrelated. Initial biochemical models indicated that abscisic acid (ABA), an important hormone in responses to water and salt stress, had a synergistic positive role with jasmonate-induced defenses against herbivores and an an- tagonistic role with salicylate-based resistance to some pathogens. Based on this back- ground, we developed predictions about how water and salt stress would alter plant resis- tance to insects and pathogens and tested the predictions using tomato plants as a model system. We used polyphenol oxidase activity as a marker of the jasmonate response and pathogenesis-related protein P4 as a marker of the salicylate response. First, we examined levels of chemical defense in wild-type and ABA-deficient plants and the ability of these plants to resist insect and pathogen attack. In the second experiment, we exposed plants to short-term salinity stress and tested their subsequent resistance to a chewing insect Spodoptera exigua and the bacterial speck pathogen Pseudomonas syringae pv. tomato. We have two key findings. First, ABA-deficient plants had higher levels of salicylate-mediated responses and were more resistant to bacterial speck disease, consistent with the proposed role of salicylate in defense against pathogens. This suggests linkage between water avail- ability to the plant and salicylate action in pathogenesis through ABA signaling. ABA- deficient plants had reduced resistance to the insect Spodoptera exigua, suggesting a positive correlation between responses to water stress and herbivory. The lack of difference in chemical expression of the jasmonate (JA) response (polyphenol oxidase activity) between wild-type and ABA-deficient plants did not support the proposed mechanism of synergism with the jasmonate response. Second, salt stress reduced the chemical induction (e.g., pathogenesis-related protein P4) of the salicylate response, but this did not affect resistance to the pathogen. Salt stress did not alter resistance to the herbivore Trichoplusia ni, but did alter the negative signal interaction between the jasmonate and salicylate responses. Under control conditions, the jasmonate and salicylate responses are antagonistic to one another, with induction of one response reducing the inducibility of the other. Under salt stress conditions, the negative effect of salicylate on the jasmonate response was reduced. Thus, complex interactions occur between ABA, JA, and SA, hormones that are important regulators of abiotic and biotic stress responses. Phytohormonal ecology is attempting to link ecological and hormonal interactions to develop a predictive framework for how and why plants coordinate responses to the environment.

Induced plant responses and information content about risk of herbivory

Plant defenses are plastic when a single genotype can produce different phenotypes depending upon the environment. Plastic responses might be favored by selection only if plants can respond appropriately to reliable information in their environments. Recent findings indicate that when information is accurate, plants can benefit by changing their defenses appropriately but, when information is inaccurate they produce inappropriate defenses and have lower fitness. Plants can potentially use a variety of cues to adjust their defensive phenotypes appropriately. The relationship between the information about risk of herbivory and plant defense can be evaluated by determining if the information available to plants is reliable enough to support the evolution of plastic-induced defenses.

Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites

Plants are often attacked by many herbivorous insects and pathogens at the same time. Two important suites of responses to attack are mediated by plant hormones, jasmonate and salicylate, which independently provide resistance to herbivorous insects and pathogens, respectively. Several lines of evidence suggest that there is negative cross-talk between the jasmonate and salicylate response pathways. This biochemical link between general plant defense strategies means that deploying defenses against one attacker can positively or negatively affect other attackers. In this study, we tested for cross-talk in the jasmonate and salicylate signaling pathways in a wild tomato and examined the effects of cross-talk on an array of herbivores of cultivated tomato plants. In the wild cultivar, induction of defenses signaled by salicylate reduced biochemical expression of the jasmonate pathway but did not influence performance of S. exigua caterpillars. This indicates that the signal interaction is not a result of agricultural selection. In cultivated tomato, biochemical attenuation of the activity of a defense protein (polyphenol oxidase) in dual-elicited plants resulted in increased of performance of cabbage looper caterpillars, but not thrips, spider mites, hornworm caterpillars or the bacteria Pseudomonas syringae pv. tomato. In addition, we tested the effects of jasmonate-induced resistance on the ability of thrips to vector tomato spotted wilt virus. Although thrips fed less on induced plants, this did not affect the level of disease. Thus, the negative interaction between jasmonate and salicylate signaling had biological consequences for two lepidopteran larvae but not for several other herbivores tested or on the spread of a disease.

Antagonism Between Jasmonate- and Salicylate-Mediated Induced Plant Resistance: Effects of Concentration and Timing of Elicitation on Defense-Related Proteins, Herbivore, and Pathogen Performance in Tomato

The jasmonate (JA) and salicylate (SA) signaling pathways in plants provide resistance to herbivorous insects and pathogens. It is known that these pathways interact, sometimes resulting in antagonism between the pathways. We tested how the timing and concentration of elicitation of each pathway influenced the interaction between the jasmonate and salicylate pathways measured in terms of five biochemical responses and biological resistance to caterpillars and bacteria. The salicylate pathway had a stronger effect on the jasmonate pathway than did the reverse. The negative signal interaction was generated by two distinct paths in the plant. A negative interaction in the biochemical expression of the two pathways was most consistent in the simultaneous elicitation experiments compared to when the elicitors were temporally separated by two days. Herbivore bioassays with Spodoptera exigua also consistently reflected an interaction between the two pathways in the simultaneous elicitation experiments. The negative signal interaction reducing biological resistance to the herbivore was also demonstrated in some temporally separated treatment combinations where attenuation of the biochemical response was not evident. Concentration of the elicitors had an effect on the pathway interaction with consistent biochemical and biological antagonism in the high concentration experiments and inconsistent antagonism in the low concentration experiments. The bacterial pathogen, Pseudomonas syringae pv. tomato (Pst), consistently showed reduced lesion development on plants with SA responses activated and, in some experiments, on JA-elicited plants. Resistance to Pst was not reduced or enhanced in dual-elicited plants. Thus, signal interaction is most consistent when elicitors are applied at the same time or when applied at high doses. Signal interaction affected the herbivore S. exigua, but not the pathogen Pst.