Clinorotation Effect on Response of Cress Leaves to ... - Springer Link

Microgravity Sci. Technol. (2011) 23:227–233 DOI 10.1007/s12217-010-9208-7

ORIGINAL ARTICLE

Clinorotation Effect on Response of Cress Leaves to Red and Far-Red Light Danguole˙ Rakleviˇciene˙ · Regina Losinska · Danguole˙ Švegždiene˙

Received: 30 October 2009 / Accepted: 13 May 2010 / Published online: 23 June 2010 © Springer Science+Business Media B.V. 2010

Abstract Responses of cress (Lepidium sativum L.) seedling leaves to separate and simultaneous illumination with red (660 nm) and far-red (735 nm) light were studied under fast clinorotation (50 rpm) and usual gravity (1g) conditions. The monochromatic light emitting diodes (LEDs) have been used for illumination of seedlings from above. The growth and spatial orientation of leaves and the location of presumable gravisensors in petioles were analysed. Clinorotation in the dark promoted the radial expansion of leaf lamina and unfolding of leaves. It was shown that clinorotation in red light inhibited significantly the elongation of petioles as compared with that under the action of gravity force. Simultaneous red and far-red illumination promoted the growth of petioles under clinorotation, but did not affect the orientation of laminas, which remained the same as of the 1-g control ones. Red light, applied separately and simultaneously with farred light, guided the bending of laminas as well as the unfolding of leaf petioles in both usual and clinorotation conditions. Histological and cytological analyses of petioles revealed the presence of movable amyloplasts in endodermic cells in proximal region of petioles. Comparison of intracellular positioning of amyloplasts in petioles of leaves grown under clinorotation and the action of gravity allows a presumption that these plastids may be identified as gravisensors of garden cress leaves. The obtained data imply that clinorotation and exposition to monochromatic red light or simulta-

D. Rakleviˇciene˙ (B) · R. Losinska · D. Švegždiene˙ Department of Gravitational Physiology, Institute of Botany of Nature Research Centre, Žaliu˛ju˛ Ežeru˛ Str. 49, Vilnius 08406, Lithuania e-mail: [email protected]

neous illumination by red and far-red light affect the elongation of petioles of cress seedling leaves. Spectral components guide the unfolding of laminas in a gravityindependent manner. Keywords Gravity · Clinostat · Fast clinorotation · Red light · Far-red light · Leaf tropisms · Lepidium

Introduction Gravitational force is one of the most constant factors guiding the formation and development of organisms (Volkmann and Baluška 2006). Plants respond to the action direction and magnitude of gravity as well as to the direction, intensity and spectral components of light. These are two major stimuli strongly determining the directional growth of terrestrial plants (Hangarter 1997). Plants have adjusted to constant presence of gravity (1g) and simultaneously changing action of solar lighting on Earth and have acquired plasticity of growth and development (Trewavas 2005). Gravity-related growth responses have been revealed during space experiments with Lepidium seedlings in the dark (Merkys and Laurinavicius 1991; Laurinaviˇcius et al. 2001; Svegzdiene et al. 2005). Gravisensing of Lepidium roots and hypocotyls extensively investigated (Gaina et al. 2003; Švegždiene˙ et al. 2007). Phototropic responses of Lepidium involve bending towards or away from light with consequent deviation from the vector of gravity (Hart and Macdonald 1980, 1981). Interactions between photo- and gravitropic responses of roots, hypocotyls or shoots were thoroughly investigated during the last decade. Spectral components (Hangarter 1997; Corell and Kiss

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2002), photon flux density (Heathcote et al. 1995; Galland 2002 and action direction (Vitha et al. 2000; Rakleviciene et al. 2005) of light are factors influencing the directional growth and morphogenesis of plants. Light can either enhance or reduce graviresponses of the plant (Heathcote et al. 1995; Hangarter 1997; Corell and Kiss 2002). Blue and red spectral components of light modulate gravitropism of plant axial organs (Kiss et al. 1997; Corell and Kiss 2002; Lariguet and Fankhauser 2004, 2005; Rakleviˇciene˙ et al. 2007). In this context, investigations of the effects of red and far-red light under altered gravity deserve greater attention. Different organs exhibit diverse responses to light and gravity stimuli (Buizer 2007). As far as we are aware, current knowledge of the nature of the events related to the interaction between light and gravity signals in the control of leaf orientation is sparse (Inoue et al. 2008; Mano et al. 2006), because the mechanism of gravisensing of leaves has not been explored. Application of LEDs enables the investigation of the effects of monochromatic light under altered gravity. The actual expression of growth movement depends on the interaction of phototropic and gravitropic responses. These processes are disturbed in hypogravity conditions. One of the efficient approaches to separate gravitropism from photo effects may be the use of plant clinorotation (Soga et al. 2002; Vitha et al. 2000) or simulation of microgravity applying the random positioning machine (Kraft et al. 2000). Illumination of clinorotated plants is one of the modes to determine separate effects of monochromatic light and gravity on plant growth.

Fig. 1 Hardware for plant cultivation in altered gravity and light: metallic container and its cap with LEDs (a); centrifuge–clinostat complex (b) with orthogonal axes (b 1, b 2, b 3, b 4) allowing independent or simultaneous rotation around four horizontal axes (clinostat) and vertical axis (centrifuge); vertical control device (c). Four containers (a1, a2, a3, a4) are attached to four horizontal axes of the centrifuge-clinostat, other four (a5, a6, a7, a8)—to the device of vertical control

Microgravity Sci. Technol. (2011) 23:227–233

Taking into consideration the fact that the development of plants is regulated by the directional growth of organs, we presume that the impact of a certain light wavelength on the growth of leaf laminas and petioles as well as on their orientation might be more or less evident when the unidirectional action of gravity is eliminated by clinorotation. Therefore, the objective of this study was to determine the effects of red (660 nm) and supplemental red and far-red (735 nm) light on leaves under fast clinorotation (50 rpm). For this reason, measurement of growth parameters and orientation of leaves as well as cytological analysis of gravirespondent tissues of petiole were performed in order to determine the location of gravisensors in Lepidium leaves.

Materials and Methods In order to test the effects induced by clinorotation and illumination by red and far-red light, seedlings of cress (Lepidium sativum L.) were grown using an original hardware which consists of a centrifuge-clinostat complex (Fig. 1b), a device for vertical control (Fig. 1c) and 8 metallic containers for plant cultivation (Fig. 1a). An inside diameter of plant cultivation containers is 32 mm, therefore, the growing seedlings during clinorotation might by affected by a centrifugal force not exceeding 4.5·10−2 g. However, in darkness petiole moved away from the longitudinal axis of the container by approximately 0.5 – 1 mm (centrifugal force was


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1.4·10−3 – 2.8·10−3 g) and in light – by 2 – 3 mm (5.6·10−3 – 8.4·10−3 g). The centrifuge-clinostat complex is the device with two orthogonal axes allowing independent or simultaneous rotation around four horizontal axes (horizontal clinostat) and vertical (centrifuge) axis. The rotation rate of horizontal axes is controlled by the software commands. It equalled 50 rpm during our experiments. Light emitting diodes (LEDs, EPITEX INC, Japan) have been used for illumination of the seedlings from above. LEDs emitting monochromatic red (L660–01 V, R, 660 nm) and far-red (L735–05AU, FR, 735 nm) light were built in the caps of the plant cultivation containers (Fig. 1a). Photon flux density was measured with a photo-radiometer (HD2102.1, Delta OHM, Italy) and amounted to approximately 13 μmol m−2 s−1 for red and 1 μmol m−2 s−1 for far-red light. The experiments were performed at ambient temperature of 23o ± 1o C. After planting single Lepidium seeds on a solid medium with 1/2 Murashige and Skoog (1962) salts and 0.2% (w/v) gelrite (Sigma) at the centre of glass test tubes (diameter 2.8 cm, height 2.6 cm), they were inserted into metallic containers. For an anchorage of germinating seeds, the containers were kept for 1 day in vertical orientation without illumination. Later four cultivation containers with growing seedlings were placed on the horizontal axes of the centrifuge-clinostat for clinorotation, the other – in the device for vertical control. Detailed course of experimental operations is presented in Table 1. Light relays were used for the control of synchronic illumination and photoperiod in both clinostat and vertical control devices. Experiments were finished at the end of the third light period. At the end of the experiments, the over-ground parts of seedlings were photographed with a PENTAX *ist D digital camera. The seedlings possessed two leaves, which were scanned and the bigger of them was earmarked as the first leaf. Growth parameters and unfold-

ing as well as spatial orientation of laminas and petioles of the control and horizontally clinorotated (HC) leaves were analyzed on digital images using SigmaScan Pro5 (Jandel Scientific Software) and Motic Images Plus 2.0 ML on a PC platform. For the histological and cytological analyses, petioles were cut transversely in half and fixed in a mixture of 70% ethanol, formalin and acetic acid (18:1:1 v/v/v), retaining the original orientation of their apical and basal parts. Parts of petioles (approximately 3 mm) were embedded in paraffin, cut longitudinally (10 μm) and stained with periodic acidSchiff’s and saffranin. Later petiole sections were photographed by means of a Moticam2000 or PENTAX*ist D digital cameras attached to microscope photometer SMP 03 (Opton, Germany). Images were analyzed using the program Sigma Scan Pro 5 (Jandel Scientific Software). 2–3 median longitudinal sections of petioles of 4–5 plants were analyzed in each test variant. Measurements of clinorotated leaves grown without and with illumination were compared with the corresponding samples of the 1-g control. Sets of experiments were repeated three or five times. Values are represented as the mean and standard error. Statistical significance is set at p ≤ 0.05.

Results First, we estimated morphometric parameters of seedling growth related to gravity and light conditions (Fig. 2). Laminas of leaves clinorotated in darkness were by 22% wider but not longer than those of 1-g ones (Fig. 1b). Length of laminas at 1g and on HC was 4.4 ± 0.1 mm and 4.5 ± 0.2 mm. Light stimulated the elongation of both laminas and petioles of leaves. In comparison with the dark, illumination with red light or red and far-red light promoted the elongation of 1-g laminas approximately by 15.9% and

Table 1 Description of temporal conditions in the performed experiments Time, hours From–to

Usual gravity conditions (1 g) Darkness Light, 12 h/day

Horizontal clinorotation (HC) Darkness Light, 12 h/day

0–24 24–60 60–72 72–84 84–96 96–108 108–120

1a–8a 1a–4a – 1a–4a – 1a–4a –

– 5a–8a – 5a–8a

– – 1a–4a – 1a–4a – 1a–4a

5a–8a –

– – 5a–8a – 5a–8a – 5a–8a

Eight containers (1a–8a) with seedlings were used in each experiment. One set of experiments performed at 1g (1a –4a) and other under horizontal clinorotation (5a–8a)

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Fig. 2 The mean length (a) and width (b) of the petioles and middle laminas of the first leaf of Lepidium cultivated in red (R) light and in red supplemented with far-red light (R+FR). 1g-normal, HC—altered gravity conditions. *—the difference between 1g and HC variants is significant at p ≤ 0.05

18.5%, respectively. Clinorotation of seedlings in red light did not significantly affect the length and width of light-grown laminas as compared with leaves at 1g. In red light, clinorotated petioles were by 19.5% shorter than petioles in light under usual gravity conditions. Supplement of red light with far-red light promoted the elongation of petioles of clinorotated leaves more significantly than of the 1-g ones (Fig. 2a). Before the analysis of the influence of applied light on the unfolding of 1-g and HC leaf laminas, the effect of clinorotation in darkness was measured (Figs. 3 and 4). Figure 3a shows the measurement mode of laminas bending in respect to petioles. Angles were measured from the abaxial (lower) side of lamina. In the dark, the adaxial (upper) surfaces of laminas of the 1-g and clinorotated leaves were closed. Stronger horizontal orientation (approximately 190◦ – 220◦ ) of 1-g laminas was observed; however, clinorotation directed the laminas towards the vertical position, and angles of the first and second leaf laminas amounted to 180◦ (Fig. 3b).

Fig. 3 Measurement mode of an angle between the leaf petiole and lamina (a) and mean angle in degrees (b) under 1g and HC conditions in the dark or illuminated with red (R) light and simultaneously red with far-red (R+FR) light

a

In red light, laminas were directed between horizontal and vertical positions independently of gravity conditions; their average angle reaching approximately 160◦ . The most obvious impact on maintaining the horizontal position and on unfolding of leaf laminas was observed after illumination with red and far-red light. The position of 1-g and clinorotated laminas was quite similar in red light or red with far-red light. This fact showed that the applied illumination influenced the unfolding of laminas of the first two leaves independently of gravity conditions. Clinorotation in the dark reduced the angles between petioles of the first pair of leaves from 13.9◦ at 1g to 7.4◦ on the clinostat (i.e. approximately by 47%). However, light eliminated differences between the opening of leaf petioles in normal and altered gravity conditions. Summarized representation of the data on the position and elongation of 1-g and clinorotated in the dark and light leaves of Lepidium are shown schematically in Fig. 4.

b


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Fig. 4 Representation of the orientation of 1g (1g) and clinorotated (HC) leaves in the dark and under illumination. 1L and 2L are marked as first and second leaf, respectively. Vertical arrow indicates the direction of the gravity vector

Clinorotation in the dark caused the rise of leaves, which might be connected with the bending of the hypocotyl hook. Simultaneously applied red and farred light stimulated the unfolding of laminas more significantly than red light alone. Clinorotation in light promoted the elongation of petioles; however, light guided the opening of leaves independently of the gravity conditions. Finally, we tested if petiole cells in first Lepidium leaves possess sedimenting amyloplasts. Location of amyloplasts is one of the key factors in gravity percep-

Fig. 5 Micrographs of petiole longitudinal sections of Lepidium leaves grown at 1g in the dark (a) and in combined red with far-red light conditions at 1g (b) and under clinorotation (c). Bars 10 μm, En layer of endodermis cells, Am amyloplasts

tion in root cap and in stem endodermis. In order to determine the presence of amyloplasts’ sedimentation in Lepidium petioles, the endodermis tissue and cells were tested on petiole longitudinal sections (Fig. 5). Amyloplasts, which sediment according to the direction of gravity vector, were observed in endodermic cells of the proximal region of 1-g Lepidium petioles after growth in the dark and in R with FR light (Fig. 5a, b). After clinorotation, they were not sedimented, but dispersed throughout the cells of endodermis (Fig. 5c).

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Discussion Spatial orientation of plant organs in response to environmental stimuli is the most important factor for the optimal capture of light energy as well as for undergoing adaptive changes in the development of the whole plant (Merkys et al. 1981, 1984; Gàlvez and Pearcy 2003). Light and gravity induced signalling pathways interact (Corell and Kiss 2002; Lariguet and Fankhauser 2005) and make it difficult to distinguish whether light, gravity or a combined action of these two stimuli modify elongation and spatial orientation of different organs of the plant. Therefore, we applied a clinostat in order to create hypogravity conditions and separate the stimuli of gravity and light. In previous studies, the interaction between lightbased and gravity-related responses was revealed in roots and stem-like organs of plants (Fukaki and Tasaka 1999; Tasaka et al. 1999; Corell and Kiss 2002; Lariguet and Fankhauser 2004, 2005). It was determined that light modulates the gravitropic response, and the effect can be either positive or negative, depending on the species and organ. Red and far-red light caused a curvature in roots and hypocotyls of Arabidopsis through phytochromes (Corell and Kiss 2002). Contrarily, in Chenopodium album leaves, neither red nor far-red light was effective in the induction of the curvature, suggesting that phytochromes may not be responsible for the induction of the petiole curvature (Fujita et al. 2008). As far as we know, different studies on graviresponse of leaves performed with Arabidopsis thaliana (L.) Heynh. (Hangarter 1997; Millenaar et al. 2005; Stutte et al. 2005, 2006; Mano et al. 2006), rice (Oryza sativa L.), barley (Hordeum vulgare L.), sweet potato (Ipomoea batatas L.) (Abe et al. 1998; Kitaya et al. 2001; Hua et al. 2007) showed ambiguous results. We determined that clinorotation in darkness had promoted radial expansion of leaf lamina and slightly stimulated opening of petioles of Lepidium leaves (Figs. 2, 3). The position of leaves in darkness could be regulated by hypocotyl gravisensors located in apical endodermis of the petiole and by opening of the hypocotyl hook. The applied light conditions stimulated elongation of laminas and petioles. The positive effect of far-red light exceeded the rate of leaf growth induced by red light. Correspondingly, Tegelberg et al. (2004) and Fujita et al. (2008) also observed that the exposure to far-red light, as compared with the red light, leads to a faster elongation growth of silver birch (Betula pendula Roth.) and goosefoot (Chenopodium album L.) seedlings as well as leaf petioles.


According to our data concerning the behaviour of the first two leaves of Lepidium in red and farred light under clinorotation, the applied illumination stimulated elongation and directed spatial orientation of leaves (Figs. 2, 3). Clinorotation in red light inhibited elongation of petioles as compared with their elongation under the action of gravity force. Results on the position of garden cress leaves indicate that unfolding of leaves is unaffected by clinorotation in red and far-red light from above (Figs. 3, 4). The illumination caused unfolding of leaves; however, surfaces of laminas were located more horizontally after simultaneous red and far-red illumination. The applied light either restored or suppressed disorientation of leaves caused by a change of a unidirectional gravitropic stimulus in the dark. These results are consistent with the observation that light suppresses gravity-dependent leaf movement (Millenaar et al. 2005; Mano et al. 2006). The data obtained on rosette leaves of Arabidopsis showed that the direction of gravity under continuous white light did not affect their orientation (Mano et al. 2006). Thus, light-dependent control and gravity-independent manner of the unfolding of laminas were determined in the first pair of Lepidium leaves. Current understanding of gravity perception in the over-ground organs of plants has been mainly established in researches carried out with Arabidopsis. They suggest that gravity perception is initiated by sedimentation of amyloplasts in endodermic cells of the hypocotyl apical zone (Kiss et al. 1997) and the basal part of the petiole (Mano et al. 2006). In our researches, we recorded sedimenting amyloplasts in endodermic tissue cells located in the proximal region of Lepidium petioles (Fig. 5). The location of amyloplasts in leaf petioles of Lepidium was the same as in Arabidopsis petioles (Mano et al. 2006). These findings confirm the role of amyloplasts in gravity perception by leaf petioles. It is worthwhile to perform further experiments to estimate spatiotemporal changes of the location of amyloplasts in leaf petioles under altered gravity conditions in the dark as well as light in order to acquire better understanding of the relationship between leaf movement and gravity effects. ¯ Acknowledgements We are grateful to Prof. Dr. Habil. Arturas Žukauskas and other colleagues from the Institute of Material Science and Applied Research of Vilnius University for their original conceptions and contribution to the introduction of LEDs in the centrifuge-clinostat complex in accordance with the project “Solid-state lighting technology for the control of photophysiological processes in plants” supported by the Lithuanian State Science and Studies Foundation.


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