Do leaf hairs swing to a caterpillar beat?

BPJ_113_9.c1.inddIn 2014, when Heidi Appel and Rex Cocroft demonstrated the ability of Arabidopsis leaves to respond to the sound of Pieris caterpillars feeding, people reacted with either disbelief or a sense of playfulness. For this cover image for the November 7 issue of Biophysical Journal, we have picked up the fanciful idea that plants can appreciate music.

The cover image conjures up the ghosts of science fairs past: playing music to plants, a favorite high school student project for well over half a century. Whether or not responses were measured, some responses should in theory occur if plant and parameters are selected appropriately. Many plants are extremely sensitive to small mechanical stimuli, and with a well-chosen plant it should be necessary to only include the right frequencies and a (perhaps unreasonably) high volume. Nevertheless, although plants have not evolved to appreciate Chopin and the Beatles, some certainly may have evolved to listen in on chompin’ and the beetles.

The cover illustrates the possibility that trichomes (hairs) of the weed called Arabidopsis thaliana are acoustic sensors. The trichomes are well known to have many other functions–for example protecting against the overly bright sunshine of the cover image, creating a layer of surface moisture to lessen dehydration, and greeting herbivores with a shield of distasteful toxins. But their evolution may have also been driven by the mechanical inputs shown. For example, they are the first cell type that insects touch when settling on an Arabidopsis leaf. And, as illustrated in the archetypal simulations on the cover, they have the form of miniature mechanical antennae.

The cover reflects how the percussion section contributes as well. Our recent study of trichome mechanoresponses showed that touching or brushing led to diverse complex patterns of acidification and cytosolic Ca2+ oscillations in the stalk, branches, and subsidiary cells (Zhou et al., Plant, Cell & Environment, 40:611-621. 2017).   Morphological observations suggest that information propagates to the leaf as a whole, where it was already shown that caterpillar feeding elicits rapid production of deterrent toxins.

The idyllic scene on the cover of Biophysical Journal highlights how the mechanoresponsive trichome is an idyllic system for studying plant signaling. The guard cells of the stomata that control gas exchange have been considered the premier system for such study, and it may be significant that the trichomes derive from the same kind of stem cells.  Evidences such as presented in our study play up the importance of the historical transition from the belief that walls are dead, to the concept that they play active and vital regulatory roles of mechanical, electrical, and biochemical character, especially when jamming out like the walls on the cover.

For more on our work in this area, please visit these websites: www.cemb.org, and http://bebc.xjtu.edu.cn/English/

– Shaobao Liu, Jiaojiao Jiao, Tianjian Lu, Feng Xu, Barbara Pickard, Guy Genin

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