The Ecological Consequences of herbivore- induced plant responses in wild Solanum species

Plants respond to herbivore damage with a bewildering array of transcriptional and metabolic changes some of which may function as direct or indirect defenses against insect attackers. The induced responses are thought to produce significant fitness costs that are traded-off with the increased resistance to herbivory. The fitness costs are categorized as physiological costs, resulting from a resource allocation from growth to defense, and ecological costs, resulting from compromised mutualistic interactions of the plant with other organisms, such as natural enemies of the herbivores or pollinators.

In this project we use an integrative approach to study the fitness consequences of altered pollinator attraction in response to leaf herbivory in wild tomato species. It follows preliminary experiments on native tomato (Solanum habrochaites, S. chmielewskii and S. peruvianum) and tobacco (Nicotiana attenuata) species, which demonstrated that herbivory and mechanical leaf damage (i) reduce pollinator attraction, (ii) induces volatile organic compound (VOC) emission (iii) induce a reduction in pistil growth and pollen competition in the newly developed flowers. The preliminary results generated four major hypothesis that will be tested with this proposal: (i) the induced changes in flower morphology and floral VOC emission result from plant hormonal and transcriptional responses to herbivore damage, (ii) the herbivore-induced changes cause a decreased quality of the pollinator reward; (iii) the quality changes are sensed by the pollinators by means of changed floral VOC emission; and (iv) the plants compensate for the reduced pollinator attraction by increasing the probability of inbreeding and reducing pollen competition through reduced pistil length and altered secondary metabolite content (advanced opportunity). To test these hypotheses a series of manipulative field and laboratory bioassays with different native Solanum species are proposed where morphological changes as well as transcriptional and metabolic plant responses to various damage treatments are measured and evaluated in respect to pollinator behavior and plant fitness traits.

This project is part of the ECO-SOL initiative, an international and integrative research network of scientists to share and enrich resources, visions and capacities relating to biodiversity, ecology, conservation, breeding and sustainable agriculture of Solanaceae in the centers of their biodiversity.

 


Solanum habrochaites in bloom ©Andre Kessler

 


VOC collection from leaves and flowers of Solanum
habrochaites
in the field ©Andre Kessler

 


Bumblebee "buzz"-pollinating a Solanum peruvianum
flower ©Andre Kessler

 
 
     

Solidago Project

With goldenrod (Solidago altissima) we have the opportunity to study the biochemical mechanisms of plant defenses and their ecological significance in a native system with a well understood arthropod community ecology and a very high insect biodiversity, including species of all feeding guilds covering a broad range of taxa. Employing this system, we will be able to understand the relative importance of constitutive and induced plant defenses in structuring the arthropod community and can reveal mechanistic explanations for the interaction patterns that have been identified, to a great extent, by Cornell researchers in the past. Moreover, with a diverse herbivore community such as the one of goldenrod, we can address many questions dealing with the specificity of plant responses to various herbivore species and host plant selection of the insects. The understanding of the coevlutionary processes between plants and the diversity of insects attacking them is one of the crucial pre-requisites for the creation of a sustainable insect pest control program.

S. altissima
dominates early succession communities in its native North American habitats and is an invasive neophyte in Asia and Europe. Knowledge about the secondary metabolites that mediate the plants’ resistance to various herbivores and their ecological consequences will help to understand both “invasiveness” and apparent biodiversity patterns. With this study we utilize a plant system that had long been used as an ecological model by Cornell scientists to accomplish the consolidation of two research fields, community ecology and chemical ecology and to “ask the plant” how to best control insect enemies.

   
     
Plant Vaccination

The native tobacco plant Nicotiana attenuata is one of the plant species that currently arise as model ecological expression systems and, which are propagated to understand the molecular and chemical mechanisms of plant-insect interactions. The species is native to disturbed habitats such as burns and washes in the Great Basin Desert of the southwestern USA. It germinates from long-lived seed banks in response to chemical cues in wood smoke. This fire-enhanced germination of N. attenuata results in a random (fire-dependent) distribution of plant populations within the landscape and forces the plant’s arthropod community to re-establish with every new plant population. Herbivore-induced plant defenses are thought to be an adaptation to such unpredictable herbivore pressure. Wild tobacco increases its production of secondary metabolites (e.g. nicotine, phenolics, diterpeneglycosides, volatile organic compounds (VOCs)) and defensive proteins (e.g. trypsin proteinase inhibitors (TPI)) after attack by herbivores as well as in response to mechanical damage or elicitation with methyl jasmonate. Although the responses to these different elicitors frequently differ qualitatively and quantitatively, they diminish the plant’s palatability to herbivores (direct defense) and/or increase the attractiveness to the natural enemies of the herbivores (indirect defense).

In field studies on N. attenuata we found that herbivory-induced changes of plant metabolism influence the composition of the arthropod community through cross-resistance effects. Specifically: The relatively mild damage of the mirid suckflies, Tupiocoris notatus, vaccinates tobacco against more damaging lepidopteran tomato hornworms, Manduca quinquemaculata. The vaccination is a result of the synergistic effect of induced direct (toxins) and indirect defenses (volatile organic compounds (VOCs), attracting natural enemies). Thereby tobacco seems to compensate for the suckfly-induced allocation of resources into defensive metabolite production because no negative plant fitness effect of the suckfly damage could be detected. We seek to identify the mechanisms underlying this very specific plant response. Therefore we are focusing on the identification of the chemical elicitors in the suckfly’s salivary excretions and their effects on the plant.

 


Wild Tobacco, Nicotiana attenuata in the
Great Basin Desert
© Andre Kessler


Tomato hornworm, Manduca quinquemaculata,
feeding on wild tobacco © Andre Kessler


Tupiocoris notatus (Heteroptera, Miridae) vaccinates
tobacco plants against more damaging hornworms © Andre Kessler