Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory

Roots play a critical, but largely unappreciated, role in aboveground anti-herbivore plant defense (e.g. resistance and tolerance) and root-leaf connections may therefore result in unexpected coupling between above- and belowground consumers. Using the tobacco (Nicotiana tabacum) system we highlight...

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Bibliographic Details
Published in:Ecology letters 2008-08, Vol.11 (8), p.841-851
Main Authors: Kaplan, Ian, Halitschke, Rayko, Kessler, Andre, Rehill, Brian J, Sardanelli, Sandra, Denno, Robert F
Format: Article
Language:English
Subjects:
Animal and plant ecology
Animal, plant and microbial ecology
Animals
Autoecology
Biological and medical sciences
Carbon - metabolism
Feeding Behavior - physiology
Fundamental and applied biological sciences. Psychology
Indirect effects
Invertebrates
Moths - physiology
Nemathelminthia. Plathelmintha
Nematoda
Nematoda - physiology
Nicotiana - genetics
Nicotiana - physiology
Nicotine - biosynthesis
Nicotine - genetics
phytoparasitic nematode
plant parasitic nematodes
Plant Roots - physiology
Plant Shoots - physiology
plant-mediated interactions
Plants and fungi
resistance
root herbivory
sink strength
stable isotope
tolerance
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Summary:Roots play a critical, but largely unappreciated, role in aboveground anti-herbivore plant defense (e.g. resistance and tolerance) and root-leaf connections may therefore result in unexpected coupling between above- and belowground consumers. Using the tobacco (Nicotiana tabacum) system we highlight two examples of this phenomenon. First, the secondary metabolite nicotine is produced in roots, yet translocated aboveground for use as a foliar resistance trait. We demonstrate that nematode root herbivory interferes with foliar nicotine dynamics, resulting in positive effects on aboveground phytophagous insects. Notably, nematode-induced facilitation only occurred on nicotine-producing plants, and not on nicotine-deficient mutants. In the second case, we use stable isotope and invertase enzyme analyses to demonstrate that foliar herbivory elicits a putative tolerance response whereby aboveground nutritional reserves are allocated to roots, resulting in facilitation of phytoparasitic nematodes. Thus, plants integrate roots in resistance and tolerance mechanisms for leaf defense, and such root-leaf connections inherently link the dynamics of above- and belowground consumers.
ISSN:1461-023X
1461-0248
DOI:10.1111/j.1461-0248.2008.01200.x