Ecology of herbivore-induced leaf-to-root signaling in plants: Finding and testing the elusive messengers

Final Report Summary - SHOOT-ROOT-SIGNALING (Ecology of herbivore-induced leaf-to-root signaling in plants: Finding and testing the elusive messengers)

The capacity of plants to withstand insect attack is of crucial importance for their own fitness and for global food production. The induction of toxic compounds and an increase in regrowth capacity have been found to be a particularly important strategy in this context small molecular weight signals, so called phytohormones, regulate the metabolic changes after insect attack and are therefore widely recognized as key messengers in plant immunity. Interestingly, the reaction of plants to insect attack is not constrained to the leaves, but involves the root system as well: Plants synthesize a variety of secondary metabolites and even defensive proteins in their roots that are then transported aboveground. They furthermore increase their assimilate uptake and storage capacity belowground to optimize regrowth after defoliation. Also, short-term reductions of root growth may liberate the resources necessary to defend leaves. Given the fact that roots actively respond to leaf attack, signals have to travel from the site of attack to the roots to induce the observed responses. Until today, however, few herbivore induced leaf-to-root signal has been unambiguously identified. This project aimed at unraveling herbivore induced leaf-to-root messengers in the wild tobacco Nicotiana attenuata.

First a set of markers were identified that change in the roots of leaf-attacked N. attenuata plants. To identify markers, we conducted i) an untargeted metabolomics screen; ii) targeted HPLC/MS-MS measurements of known defensive metabolites, iii) enzyme assays to determine soluble sugars and starch and iv) mining of a microarray time course, covering a large body of root transcripts. Using this method, we identified a number of markers, from which we selected sugars, starch and nicotine as robust, reproducible and ecologically relevant markers to assess shoot-to root signaling. We then carried out a time-course experiment in which we measured the induction of possible signaling metabolites in the leaves and the roots following leaf-induction using UPLC-TOF metabolomics and HPLC/MS-MS phytohormone analysis. While no common features between the roots and the leaves could be identified, a strong and rapid induction of jasmonates (JA, JA-Ile) and the auxin indole-3-acetic acid were measured. We therefore hypothesized that these two compounds may be responsible for the changes in the markers we observed before. To understand the involvement of jasmonates as systemic signals, we carried out a series of experiments using jasmonate-deficient irAOC plants, micrografting and natural variation in jasmonate signaling. Using this approach, we could show that jasmonates directly determine the root-depletion of carbohydrate pools as well as the induction of secondary compounds. Furthermore, using pharmacological assays, we also accumulated evidence that the auxin IAA may modulate this response. Following the identification of IAA as a potential herbivore induced systemic signal, we initiated a number of experiments, including detailed induction kinetics with herbivore-derived elicitors and gene expression measurements. These findings resulted in a detailed map on the timing, distribution and specificity of the IAA burst in herbivore attacked N. attenuata plants.

To understand the consequences of carbohydrate depletion in the roots following leaf-attack, we removed the shoots of induced plants and then measured the regrowth response. It was found that leaf-herbivory reduces regrowth from the rootstock, but only in plant genotypes that show a depletion of carbohydrates, suggesting that leaf-herbivory reduces the plants regrowth capacity by depleting root carbohydrates. We also performed a field experiment, which confirmed that roots play an important role in herbivore-induced growth defense trade offs. We expect that the gained insights will be of considerable fundamental relevance for the research field. The conducted research highlights the important role of roots in plant tolerance, and may in the long run help to develop herbivore resistant plant varieties based not only on simple leaf-resistance screening, but the concious inclusion of root performance traits into the selection regimes.

Contact: Prof. Matthias Erb, Institute of Plant Sciences, University of Bern, Switzerland. matthias.erb@ips.unibe.ch;
Website: http://www.ice.mpg.de/ext/828.html

Final Report Summary - SHOOT-ROOT-SIGNALING (Ecology of herbivore-induced leaf-to-root signaling in plants: Finding and testing the elusive messengers)

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