Ecological Consequences Of Jasmonate-Induced Responses For Plants In Native Populations

July 09, 1998

Herbivore attack is widely known to reduce food quality and to increase chemical defenses and other traits responsible for herbivore resistance. Researchers at the Max Planck Institute for Chemical Ecology in Jena/Germany demonstrated that inducible defenses allow plants to forgo the costs of defense when not needed (PNAS, vol. 95, July 7, 1998).

All plants use chemical defenses to protect themselves from attack by herbivores and pathogens and a majority of these chemical defenses are inducibly deployed in some species, that is their production is dramatically increased after attack. Inducible defenses are inherently inferior to constitutively deployed defenses due to the time lag between the first attack and the activation of the defense, a delay which could leave a plant vulnerable for hours or even days as the defense is activated. Why then is this mode of defense deployment so common, having been demonstrated in over 110 plant-herbivore interactions? The commonly-held explanation is that chemical defenses are beneficial and increase a plant's fitness when it is under attack, but they are costly when not needed, utilizing resources that could be used instead for growth or reproduction, or by other means decrease the fitness of well-defended plants when grown in competition with less-defended plants in environments lacking herbivores. For example, plants that are chemically well-defended may have a lower reproductive success than undefended plants due to difficulties in attracting pollinators. In short, inducible defenses are thought to have evolved as a cost-savings measure, allowing plants to time the production of a chemical defense with the prevailing environmental conditions and forgo the costs of defense when they are not needed.

Despite the general acceptance that inducible responses are adaptive, two critical assumptions remain untested. Surprisingly, it has yet to be demonstrated that an inducible complexities of ecological interactions in nature frequently wreak havoc with the best defense strategies. For example, plant chemical defenses are frequently sequestered by specialist herbivores for their own defense, thereby turning a plant's defense against itself. Many inducible chemical responses, such as protease inhibitors which slow herbivore growth by reducing their digestive efficiency, may only function as defenses in nature when expressed in concert with other responses, such as the induced alarm calls of plants that increase the vulnerability of the herbivore to its own predators. Without the use of the third trophic level, an plant may lose more leaf area and have a lower fitness as a result of slowing the growth rates of their herbivores. These considerations underscore the importance of examining the benefits of induced defenses in natural populations.

A second, untested assumption is that the induced, well-defended phenotype has a lower fitness than the uniduced, poorly-defended phenotype in environments without herbivores. While genetical analysis of constitutively-deployed chemical defenses support the view that chemical defense can be costly, the phenotypic costs of an induced defense, that is, the fitness difference between the induced and uninduced members of the same genotype remains to be critically evaluated, due in large part to the experimental difficulties of activating defenses without wounding or controlling for the fitness consequences of tissue lost during induction. If induced defenses are costly due either to the resource demands of their production or to other ecological costs, then these costs can best be evaluated in the environments in which these responses presumably evolved.

Nicotiana attenuata synthesizes the toxic alkaloid, nicotine, in its roots and dramatically increases its rate of nicotine synthesis after leaf wounding and herbivory, which, in turn, results in a systemic increase in nicotine concentrations in both vegetative and reproductive tissues. In laboratory feeding trials, induced levels of nicotine protect plants against nicotine-tolerant herbivores, but these herbivores may suffer lower rates of parasitisms when feeding on plants with high nicotine concentrations, indicating that this induced defense may have both ecological benefits and costs. Moreover, 6% of an N. attenuata  plant's total nitrogen content is in this toxin alone in an induced plant, and this nitrogen is not available for other activities such as seed production, suggesting that inducing nicotine production may incur large resource-based costs. Hence, it is reasonable to suppose that the fitness consequences of producing this toxin will vary greatly depending on the plant's habitat.

The discovery of the endogenous wound signals which plants use to activate induced responses, have provided researchers with valuable tools to activate defenses independently of herbivore attack in plants growing in their native habitats. Jasmonic acid, a ubiquitous wound-hormone known to increase the synthesis of diverse defense-related metabolites, is strongly implicated as a long-distance endogenous wound-signal activating nicotine synthesis in the roots after leaf wounding and it is reasonable to propose that the treatments of roots with jasmonate will stimulate responses comparable to those elicited by leaf wounding.

N. attenuata has life history characteristics that make it particularly useful for a test of the cost-benefit model for induced defenses. It is an ephemeral member of the annual community in burned sagebrush, blackbrush and pinyon-juniper forests of the Great Basin desert and synchronizes its growth with the post-fire environment by producing dormant seeds that germinate in response to cellulose combustion product(s) found in wood smoke. Such synchronization allows this species to exploit the ephemeral but nutrient-rich, herbivore- and competition-poor environments that are commonly found after fires. This temporal window of growth opportunity is frequently quite short, for as post-fire succession proceeds, herbivores and competitors quickly recolonize the burned habitats and plants found after each successive growing season after a fire are smaller and attacked more frequently by herbivores than those of the preceding season. It can be the most abundant species during the first growing season after a fire but it rarely persists for more than three years after fires. Hence, by studying plants growing in different-aged burns, one can study plants with different attack probabilities.

To test the cost-benefit model, 745 matched pairs of naturally occurring plants in 4 natural populations in SW Utah were established: 2 in 1-year-old burns (IA and IB) where herbivory is typically low (350 plant pairs) and 2 in 2-year-old burns (IIA and IIB) where herbivory is typically much higher (345 pairs). A fifth population of 50 pairs was created in a nearby field-plantation where plants were protected from herbivores with fencing and pyrethrin insecticide applications. The amount of jasmonate required to add to the roots of plants in order to elicit an induced nicotine response was determined and one member of each pair was treated during early rosette-stage growth (May-June). The effects of jasmonate induction on nicotine production, herbivory and lifetime viable seed production was determined.The root-produced toxin, nicotine, increases after herbivore attack in the native, post-fire annual, Nicotiana attenuata, and is internally activated by the wound-hormone, jasmonic acid. The roots of plants were treated with the methyl ester of this hormone (methyl jasmonate; 500μg suspended in 10 ml water, while control members of the pair were treated with 10 ml water) to elicit a response in one member of each of 745 matched pairs of plants growing in native populations in southwestern Utah (USA) with different probabilities of attack from herbivores (primarily rabbits and the larvae of the tobacco specialist, Manduca sexta).The lifetime production of viable seed was measured from all plants to determine the fitness consequences of jasmonate induction.

The results strongly support the cost-benefit model for inducible defenses. Jasmonate treatment significantly increased nicotine concentrations in the leaves of treated plants  22-54%   above those of their control, water-treated counterparts. In populations where plants were being heavily attacked (populations IIA, B),  nicotine concentrations of leaves from control plants were comparable to those of unattacked jasmonate-induced plants from the other populations, but the effect of jasmonate treatment was retained; clearly, the jasmonate treatment had not saturated the plants' nicotine response. How do these changes affect plant fitness as estimated by their lifetime viable seed production? The answer depends critically on the plant's environment, particularly, the likelihood of herbivore attack.

For plants in environments with high herbivory (the 2-year-old burns, populations IIA, B), the benefit of jasmonate-treatments could be readily seen. For example, in population IIA,  10 days after the treatment, 33% of the control plants had lost more than 40% of their leaf area to herbivores, as compared to 1% for Jasmonate-treated plants. However, this protective effect of jasmonate treatment did not translate into a fitness benefit for the plants in this population in which 81% of plants did not survive to produce any viable seed. No pairs survived to produce seed in the second 2-year-old burn (IIB).

For plants growing completely protected from herbivores (i.e., in the plantation) jasmonate-treatment significantly reduced lifetime viable seed production by 26% (9.9 capsules plant- 1 or 1552 viable seeds).  A similar cost was observed between induced and uninduced members of pairs growing in population IB which had largely escaped herbivory and lost less than 5% of their leaf area to herbivores by the end of the growing season.  In this population, jasmonate-treatment reduced the lifetime capsule production by 18% (26 capsules plant- 1). This reduction is similar to the reduction associated with removing half of a plant's leaf area at the rosette-stage of growth: 27% reduction equivalent to 23 fewer capsules plant- 1 or 2021 viable seeds. Hence when plants are protected or escape from herbivore attack, plants treated with jasmonate produced significantly fewer viable seeds at the time of senescence. This cost, however, becomes a net fitness benefit for plants growing in populations that have a higher probability of herbivore attack.

For plants in environments with modest herbivory (population IA), 241 pairs (80%) survived to produce seed, and of these surviving pairs, 358 individual plants (74%) lost 20% or more of their leaf area to herbivores by the first week of July. The number of mature capsules produced at the end of the growing season differed significantly within pairs, and the magnitude and sign of these differences depended on whether or not the plants had been attacked by herbivores. Overall, jasmonate-treated plants matured on average 11% more viable seed (6 capsules or a 349-viable-seed-plant- 1 benefit of jasmonate-treatment). Of these 241 surviving pairs, both members of 160 pairs lost 20% or more of their leaf area to herbivores; in this subset of attacked plant pairs, Jasmonate-treated plants matured 8 capsules and 537 viable seeds more than their control counterparts. In 13 pairs, only the jasmonate-treated member of the pair was similarly attacked, and in these, viable seed production did not differ significantly. In 25 pairs, only the control member of the pair was attacked, and in these pairs, the jasmonate-treated plants matured on average 35 more capsules and 2848 viable seeds more than controls (a 58-60% benefit). To summarize, in populations with an intermediate level of attack, jasmonate-induced plants had a higher fitness than control plants. Interestingly, the cost of jasmonate-induction was also detectable in the 43 pairs in which both members escaped herbivore attack; jasmonate-treated plants produced on average 20% less viable seed than did controls (13 fewer capsules and 1476-viable-seed-plant- 1 cost of jasmonate-treatment).

This study provides strong support for the contention that jasmonate-induced responses are examples of adaptive phenotypic plasticity. By timing their germination and growth with the post-fire environment, N. attenuata plants exploit a small phenological window of low herbivore pressure and high resource availability. However, within this window of opportunity, the probability of herbivore attack is highly variable and inducible defenses allow plants to cope with this variability by altering their defensive phenotype adaptively.  The resistance traits elicted by jasmonates are costly in terms of seed production, but these costs are offset by their benefit when the probability of fitness reductions due to herbivore attack is high. The advances in understanding the signal transduction pathways that mediate the defense responses of plants provide ecologists with the opportunity to rigorously test the costs and benefits of defenses under natural conditions and provide important insights into the design of ecologically-benign agricultural practices.



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