Chapter 2 Nutation in Plants

This chapter aims to explore and describe the physiological aspects of oscillating growth patterns in rapidly elongating plant organs, such as roots, hypocotyls, shoots, branches and flower stalks. After a brief description of the phenomena, the theories and models proposed to explain circumnutation are reported, focusing largely on the internal oscillator model and the gravitropic overshoot model. The former is derived from the intuition of Charles Darwin, the first to suggest that circumnutatory movements are mediated by an endogenous oscillator, i.e. the driving and regulating apparatus responsible for circumnutation is internal. By contrast, the latter theory proposes a gravity-dependent model to account for circumnutations, essentially consistent with the Cholodny-Went theory, thus interpreting oscillations as being a continuous series of over-compensatory responses of the plant to the changing orientation of its gravisensory apparatus relative to the Earth’s gravity vector. A revised two-oscillator model is also reported, which is based on a combination of the above-mentioned two models. In this combined model, circumnutational movement involves a gravitropic reaction acting as an externally driven feedback oscillator, together with an endogenous or intrinsic oscillator which sends a rhythmic signal to the feedback system. The role of hormones will be finally discussed, with particular attention to the effect of ethylene in controlling nutation. 2.1 Overview of Nutations: Definition and Kinematic More than a century ago, plant physiologists were already aware that rapidly elongating plant organs—roots, hypocotyls, shoots, branches, flower stalks—rarely grow in only one direction. Mean growth direction may be maintained for long S. Mugnai E. Azzarello E. Masi C. Pandolfi S. Mancuso (&) LINV–International Lab for Plant Neurobiology, Dipartimento di Scienze delle Produzioni Agroalimentari e dell’Ambiente, University of Florence, viale delle idee 30, 50019 Sesto Fiorentino, FI, Italy e-mail: stefano.mancuso@unifi.it © Springer International Publishing Switzerland 2015 S. Mancuso and S. Shabala (eds.), Rhythms in Plants, DOI 10.1007/978-3-319-20517-5_2 19 intervals, but the organ’s instantaneous growth direction usually oscillates slowly around that mean. From a distal viewpoint, the plant organ tip, or an elongating cylindrical plant organ, describes an ellipse, a circleor pendulum-like movements about the plumb line, which can alternate between a clockwise and counterclockwise direction. The axes of the ellipse can vary: at one extreme, the ellipse approximates a line and, at the other, a circle. As the organ grows, its tip advances and (in three dimensions) traces an irregular helix (Migliaccio et al. 2009). This oscillating growth pattern was well known to nineteenth-century plant scientists as ‘revolving nutation’ until the Darwins (father and son, Darwin and Darwin 1880) introduced the term ‘circumnutation’, used to this day (Fig. 2.1). Thus, circumnutational oscillations are manifestations of the radially asymmetric growth rate typical of elongating plant organs (Fig. 2.2). These do not include tropic processes occurring in response to a directional cue, such as gravity or light, or nastic movements, which occur in response to external factors but are independent of the position, i.e. the closing of leaves at night. These various forms of movements usually occur together; for example, it has been shown that gravity amplifies the circumnutatory response in Arabidopsis thaliana (Johnsson et al. 2009). Darwin’s (1875) close observation of the behaviour of ‘climbing plants’, which tendrils appeared to ‘search’ for some upright support, led him to widen his investigation to a large variety of species in which, however, he found no exception to his generalization that circumnutations must be a universal kind of plant movement (Darwin and Darwin 1880). Indeed, today we know that the widespread occurrence of circumnutations is even greater than Darwin had ever suspected. It not only occurs in dicots and monocots (Brown 1993) but also is well established for gymnosperms, fungi (Basidiomycetes), bryophytes (Ceratodon purpureus, Kern et al. 2005) and algae (Spirogyra, Kim et al. 2005). Even some colonial forms of bacteria (Acetobacter xylinum) exhibit oscillating growth patterns which kinematically resemble higher plant circumnutations (Hoiczyk 2000). Although circumnutatory movements are of obvious use to twining plants seeking mechanical support, in other cases the movements appear to have no useful purpose. The amplitude, period and shape of circumnutation depend on the plant Fig. 2.1 Some sketches illustrating Darwin’s close observation of the behaviour of ‘climbing plants’ (extracted from Darwin 1875) 20 S. Mugnai et al.