The circadian timing system in Nicotiana attenuata : a functional connection between the circadian clock and hormone signaling in plant-insect interactions

In the eighteenth century, scientists realized that the daily movements of plant leaves were driven by an endogenous rhythm that resonate with the external light-dark cycle. It is now well established that the timekeeper mechanism that drives these rhythms, the so-called circadian clock, regulates much of a plant metabolism, physiology and behaviors, and dictates how plants interact with their biotic and abiotic environment. This work describes the role of the circadian clock in shaping mutualistic and antagonistic interactions between plants and insects. Specifically, this work elaborates in the connection between the clock and two hormone signaling pathways in the regulation of reproductive and defensive traits that determine how Nicotiana attenuata plants interact with pollinators and herbivores. Phenotypic characterization of lines genetically modified in their endogenous rhythm by silencing the expression of different clock genes revealed far-reaching roles of the circadian system in the regulation of plant-insect interactions in this wild tobacco species. Disruption of normal clock activity changed the timing of flower opening/closing, the nightly emission of the floral volatile benzyl acetone (BA), diurnal changes in flower orientation, and the accumulation of the jasmonate-related compound nicotine in leaves of N. attenuata. Silencing the expression of the clock component ZEITLUPE (ZTL) altered the auxin-mediated growth movements of flowers, reducing outcrossing rates mediated by the plants main pollinator, Manduca sexta moths; whereas in leaves, abrogation of ZTL expression caused the reduction of nicotine accumulation, which rendered plants more susceptible to the attack of the generalist herbivore, Spodoptera littoralis. I furthermore present evidences of a novel and direct link between the circadian clock and the auxin and jasmonate signaling pathways that shape how N. attenuata plants interact with their biotic environment.

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