Plants circling in outer space

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Oscillatory movements are ubiquitous in plants

Plants do not grow in a strict linear manner, rather they circumnutate. That is, they exhibit an oscillatory or helical growth pattern around an axis. Circumnutation is readily apparent in vines such as morning glory or grape (Fig. 1), but in fact it is nearly ubiquitous in plants. Circumnutation occurs in almost all plant organs throughout all stages of development (Johnsson, 1997; Larson, 2000). In the late 19th century, plant scientists noted that plant organs, including roots, shoots, stems, hypocotyls, branches, leaves and flower stalks, did not grow exactly in a linear direction. The mean growth direction may be maintained for long periods of time, but the organ's instantaneous growth direction usually rotates or oscillates slowly around a mean. Circumnutation is best visualized using time-lapse photography (Fig. 2), and numerous examples, including sunflower seedlings, Arabidopsis stems and morning glory stems, are illustrated in movies found at the Plants-in-Motion website (http://plantsinmotion.bio.indiana.edu/). The paper by Johnsson et al. (pp. 621–629) in this issue of New Phytologist uses microgravity as a tool to study this interesting phenomenon in plants.

Figure 1.

Circumnutation is most obvious in climbing vines, as shown in this illustration from Darwin (1875). In this flower stalk, circumnutation leads the flower tendril (B) to wrap around an object. A, peduncle; C, subpeduncle with flower buds; D, petiole.

Figure 2.

Circumnutation demonstrated in a time-lapse image of a single shoot of the vine Lonicera japonicaare (Larson, 2000). Sixteen photographs taken over a 2-h period were superimposed to illustrate the clockwise rotation in this vine.

‘... this paper suggests not only that endogenous nutations occur in stems as Darwin predicted, but also that gravitational accelerations amplify these circumnutations.’

Plant movement was the subject of two of Charles Darwin's books, The movements and habits of climbing plants (Darwin, 1875) and The power of movement in plants (Darwin & Darwin, 1880). Darwin hypothesized that circumnutation is the major developmental phenomenon in plants and that understanding this oscillatory movement was the key to understanding all aspects of plant movements, including gravitropism, phototropism, thigmotropism and nastic movements. He viewed all of these phenomena as an outgrowth of circumnutation.

In order to verify his observations, Charles Darwin performed his studies on many types of plants. In his book, he lists the 320 plant species he studied and concludes ‘every growing part of every plant is continually circumnutating, though often on a small scale’ (Darwin & Darwin, 1880). Darwin hypothesized that circumnutation was an endogenous mechanism found in all plants that they employ in order to explore their immediate environment.

Is circumnutation dependent upon gravity?

Supporting Darwin's endogenous hypothesis, Shabala (2006) summarized other possible functions of circumnutation, including synchronizing events between cells at different sites, functioning as a filter that helps separate signal from environmental noise and decreasing the response time when reacting to external stimuli. However, an alternate hypothesis is that circumnutation is dependent upon gravity and therefore is not a strictly endogenous feature of plants (Brown, 1993).

Several modern experiments support Darwin's ‘endogenous hypothesis’. For example, in a spaceflight experiment, 93% of sunflower (Helianthus annuus) seedlings exhibited circumnutation in microgravity compared with 100% of control seedlings on the ground (Brown et al., 1990). The circumnutation of the seedlings in microgravity had a reduced period and amplitude relative to the ground control plants. By contrast, a series of papers by the Takahashi group in Japan suggested that gravity was required for circumnutation to occur. In their first report, they suggested a link between circumnutation and gravity based on their finding that an agravitropic mutant of morning glory (Pharbitis nil) also was defective in circumnutation (Hatakeda et al., 2003). In a follow-up study, this group also showed that mutants of P. nil and Arabidopsis thaliana lacking the endodermal layer, which is involved in gravity sensing in shoots (Kiss, 2000), exhibited severely reduced circumnutations – thus linking this phenomenon directly to mechanisms of gravity perception (Kitazawa et al., 2005).

Space experiments provide a research opportunity for fundamental biology

How can the results between the Brown group and the Takahashi group be reconciled? Kitazawa et al. (2005) suggested that the sunflower seedlings in the experiments by Brown et al. (1990) sensed gravity before the space experiment started because some seedlings germinated prior to the launch of the spacecraft. Thus, an experiment in which all seeds were germinated in space (and seedlings developed completely in microgravity) would help to resolve these controversies. The paper by Johnsson et al. uses this very approach with Arabidopsis plants.

In these elegant spaceflight studies (Johnsson et al.), a laboratory incubator facility with a centrifuge, termed the European Modular Cultivation System (EMCS), was used on the International Space Station (Kiss et al., 2007). Centrifuges provide important controls for spaceflight studies but have not been available for most biological experiments performed in space to date (Perbal & Driss-Ecole, 2002). Arabidopsis plants developed from seeds in microgravity, and once inflorescence stems were formed, the centrifuge provided 0.8 g of acceleration, which is similar to the earth nominal control. After acceleration, the centrifuge was turned off so that the plants would again experience microgravity.

Johnsson et al. detected small nutational movements (with minute amplitude) of the side stems in microgravity before centrifugation. However, when the gravitational acceleration was provided to the level of 0.8 g, the amplitude of the circumnutations increased five to ten times. Light also had an effect on circumnutations in that the period was decreased from 85 min (dark) to 60 min (light). Thus, the results presented in this paper suggest not only that endogenous nutations occur in stems, as Darwin predicted, but also that gravitational accelerations amplify these circumnutations.

What is the overall significance of these results? Johnsson et al. seem to favor a model that incorporates both hypotheses – the endogenous model and the idea that circumnutation is related to, and dependent upon, gravity. This space study was able to show that small, endogenous circumnutations do occur in microgravity, but that the gravitational accelerations provided by the centrifuge clearly increased their magnitude. Johnsson et al. and others in the field have referred to this idea as the ‘combined model’, which has been outlined in Brown (1991) and in Johnsson (1997).

In summary, the unique microgravity environment was used to test the hypothesis that circumnutations are an internal, endogenous feature of plant organs. This is important because, in previous studies, researchers could not study circumnutations in plants without the ‘complicating’ effects of gravity. In a similar manner, the microgravity environment obtained in orbiting spacecraft has been used effectively to study phototropism without the interference of gravity or gravitropism (Heathcote et al., 1995; Kiss et al., 2007). Thus, the experiments of Johnsson et al. provide a fine example of using the microgravity environment aboard orbiting spacecraft as a unique research tool to study important problems in fundamental biology (Perbal & Driss-Ecole, 2002). We look forward to further contributions from the science programs of the European Space Agency and the National Aeronautics and Space Administration from the laboratories aboard the International Space Station.

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