JXB Advance Access originally published online on February 7, 2005
Journal of Experimental Botany 2005 56(413):851-856; doi:10.1093/jxb/eri071
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RESEARCH PAPER |
Phototropic response induced by wind loading in Maritime pine seedlings (Pinus pinaster Aït.)
Laboratoire de Rhéologie du Bois de Bordeaux, Mixed Unit: INRA/CNRS/Université Bordeaux I, Domaine de l'Hermitage, 69 Route d'Arcachon, F-33612 Cestas cedex, France
* Present address and to whom correspondence should be sent: Forestry Commission, NRS, Roslin, Midlothian EH25 9SY, UK. Fax: +33 5 56680713. E-mail: stephane.berthier{at}forestry.gsi.gov.uk
Received 16 June 2004; Accepted 2 November 2004
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Abstract |
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Both woody and herbaceous plant species are known to respond to wind loading, with consequences for growth and morphology. Wind has usually been classified as a mechanical stress which is detrimental to plant growth. Few experiments exist whereby plants and, in particular, woody species are exposed to wind, as opposed to mechanical perturbation by touching, flexing or shaking. Such experiments have always been short term and often carried out in wind tunnels in a controlled greenhouse environment. This study introduces an experiment to test the responses of Maritime pine (Pinus pinaster Aït.) seedlings to recurrent and short wind loading in the field, over two growing seasons. These experiments provide evidence that periodic short-term exposure to wind can induce phototropic responses in the early stage of pine seedlings' development. An interpretation is proposed in terms of efficiency to light tracking and hypotheses are discussed concerning the underlying physiological process.
Key words: Calcium, gravitropism, mechanical strain, phototropism, thigmomorphogenesis
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Introduction |
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In the natural world, wind is an environmental parameter as ubiquitous and fluctuating as light or temperature, but which has received comparatively little attention as a factor affecting plant growth. Plants subjected to steady winds usually have a stunted appearance, with an increase in stem diameter and/or reduced elongation (Jaffe, 1973
; Mitchell et al., 1975; Biddington, 1986; van Gardingen and Grace, 1991; Telewski, 1995). Trees tend to have a windswept form and the mechanical properties of wood may change, due to structural and geometrical modifications in the new xylem cells produced (Telewski, 1989). Root architecture and anchorage may also be affected (Stokes et al., 1995, 1997; Nicoll and Ray, 1996; Mickovski and Ennos, 2003; Tamasi et al., 2005). Such changes result in trees that are considered to be more resistant to the mechanical stress imposed by wind loading. The term ‘seismomorphogenesis’ describes the plant growth response to shaking and vibration (Mitchell et al., 1975; Biddington, 1986) whereas ‘thigmomorphogenesis’ designates the plant growth response to touch and rubbing (Jaffe, 1973) events like mechanical stimuli. Usually, all these loadings are simultaneously and repeatedly induced in a plant exposed to the wind. Such dynamics are not to be confused with static loading, whereby some supporting organs are displaced over a period of time and gravitropic responses induced (Kwon et al., 2001). Most experiments on plant reactions to wind exposure have been carried out in an artificial environment, and few studies have combined the effects of wind with a second environmental stress (Heiligmann and Schneider, 1974; Grace and Russell, 1982; Stokes et al., 1997). The minimum wind dose necessary to induce a growth response has not been defined, nor has the effect of repeated wind loading on plant growth (Telewski, 1995). In order to investigate the influence of recurring wind loading, for example daily breezes on tree growth, a device was designed to expose Maritime pine seedlings to a periodic short-term air flow in the field. The economic importance of timber species, particularly Maritime pine in the south-west of France, and the appreciable influence of mechanical loads on wood formation, justified the choice of woody material. Although the principal measurements were concerned with growth responses in terms of biomass allocation and root anchorage, an unexpected stem lean was observed 8 weeks after germination: seedlings were bent towards the sunlight only when exposed to recurrent wind loading. |
Materials and methods |
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Field site and plant material
The field site was located in a forest nursery, 20 km south-west of Bordeaux in France, i.e. 45 km from the Atlantic Ocean (altitude 58 m, latitude 44°44' N, longitude 0°46' W) with an average yearly rainfall of 900 mm and a mean temperature of 13.5 °C. The experimental site was sheltered from winds by a 4 m high, 15-year-old Thuya sp. hedge at a distance of 10 m from the study plots. The prevailing winds were westerly, with a mean speed of 2.5±1.1 m s–1 at a height of 10 m, according to data collected between 1998–1999 at a weather station situated 3 km from the site (Berbigier et al., 2001
). The soil was a medium humid sandy podzol on a flat location, thoroughly ploughed and treated against parasitic fungi during May 1998, notably against the damping off disease (Pythium debaryanum). At the same time, 3000 Maritime pine seeds (Pinus pinaster Aït) were soaked for 48 h in cold water and kept on moist blotting paper for 3 weeks at 5 °C, in the dark. The seeds were sown on 15 June, directly in the field, in two blocks with 3–4 seeds per position. On 30 July, after the overall germination, one representative individual was randomly chosen per position, by cutting extra seedlings at the stem base with scissors. The first block was ‘wind-treated’ and its layout was circular with more than 250 individuals in three concentric rows (Fig. 1). The second block was a rectangular ‘control’ with four rows of 30 individuals, oriented at 45° from the north-south axis (Fig. 1). The rows in both blocks were 1 m apart and split into 12 groups with spacings of 20 cm, 25 cm, and 30 cm alternately. Different spacings were used as this study formed part of a larger project dealing with the effects of wind loading on tree growth at different densities. All plants were subjected to the same automatic daily irrigation regime, manual weeding, and antifungal treatment until the end of the growing season. In addition, a repetition of the experiment was performed in the following year, at the same site. Seeds were subjected to the same pregermination process as in 1998 and sown on 15 June 1999 in the same layouts, except for the circular block that consisted of only one row of 200 individuals, with regular spacing of 15 cm. Seeds were also subjected to the same treatments as in 1998 until the winter.
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Wind loading device
Seeds in the circular block were planted around a wind loading device (Fig. 1). At the centre of the block, a motor was installed to make a horizontal metallic arm 8 m long revolve permanently at a speed of 0.05 rpm (1 full revolution in 20 min), in an anti-clockwise direction. As an electrical fan was fixed to one end of the rotating arm, the seedlings were exposed to an intermittent wind loading, day and night since their germination. Every 20 min, the individuals in R1 (population size n=115, diameter=10 m) were exposed to a mean artificial wind speed of 3.21 m s–1 for 10 s, seedlings in R2 (n=87, diameter=12 m) to 2.57 m s–1 for 13.5 s, and in R3 (n=63, diameter =14 m) to 2.21 ms–1 for 16 s, with maximum instantaneous wind speeds reaching 8.7 m s–1, 6.0 m s–1 and 4.8 m s–1, respectively.
Characterization of growth conditions
The control and ‘wind-treated’ blocks were expected to provide the same growth conditions for seedlings as they were only 10 m apart in a forest nursery. To confirm this, the pH and quantity of N, P, K, Ca, and Mg in the top 10 cm of soil were recorded, in 24 samples taken randomly from the blocks. Neither significant differences nor restrictive values for Maritime pine seedling growth were noticed (P >0.05 with pH=6.0±0.3, N=0.80±0.14 g kg–1, P205=0.131±0.003 g kg–1, Ca=1.16±0.11 Cmol kg–1, Mg=0.09±0.02 Cmol kg–1, and K=0.03±0.01 Cmol kg–1). Anemometers (034A, Met One Instruments Inc., Oregon, USA) and thermometers (Unilog Ltd., Czech Republic) were installed in each block, above the seedlings, to register the local atmospheric properties. Sensors measuring soil humidity and temperature at a depth of 20 cm were added (ML2x, Delta-T Devices Ltd., Cambridge, GB). All instruments were connected to a datalogger (Minicube VX, EMS Brno, Czech Republic) programmed to record the specified data every 5 min throughout the growing season. The sensors were moved around inside the blocks to reveal possible within-block differences and microclimates. No durable significant difference, i.e. over 1 d, was revealed between or within blocks (P >0.05). In particular, natural winds at a height of 1.5 m within the overall experimental site were found to originate from an azimuth of 294±26°, with a mean speed of only 0.52±0.23 m s–1 during June-September. Photosynthetically Active Radiation (PAR) data were also available from a weather station located 3 km from the site (Berbigier et al., 2001). PAR was measured at a height of 38 m, i.e. 13 m above a forest canopy. No significant differences were found between the growing seasons of 1998 and 1999 (for both years the PAR ranged from roughly 500 mol m–2 d–1 in June, to 380 mol m–2 d–1 in September).
Measurements of stem lean
Stem height of seedlings was measured at the beginning and at the end of each growing season, until December 2000. As it was difficult to characterize three-dimensional geometry easily and to handle the seedlings safely due to their small size (6.0±1.6 cm on 15 September 1999), stem lean was estimated by pushing a thin, 15 cm long cane into the soil parallel to the stem. The angle of each individual cane to the vertical was measured using a small plumb-line fixed to a protractor, and the azimuth of lean was obtained with a compass (for inclined canes only). Stem lean was measured on 17 September 1998, 26 February 1999, and 7 May 1999 for the seedlings planted in 1998, and on 16 September 1999 for the second experiment. In order to quantify possible differences in stem lean within the ‘wind-treated’ block according to sun exposure, the block was divided into quadrants (Fig. 1). As angles are not linear but periodic elements, averages and differences in stem lean between or within seedlings were determined using basic circular statistics (Rao and SenGupta, 2001).
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Results |
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Stem lean in the ‘wind-treated’ block after 8 weeks of growth
In September, during both the first and second experiments, the stems of the ‘wind-treated’ seedlings were found to be inclined, which is common in plants subjected to wind loading (Biddington, 1986
; van Gardingen and Grace, 1991; Telewski, 1995). As expected, the degree of stem lean decreased with the distance from the fan, i.e. between circular rows (Fig. 1; Table 1). However, the direction of lean was not necessarily along the axis of wind, as illustrated by the western and eastern quadrants of the block (Fig. 1). In the eastern quadrant, the average stem orientation was 90+36°, i.e. 36° deviated from the average wind axis (the east) towards the south (Table 1). In the western quadrant, the average stem orientation was 270–25°, i.e. 25° deviated from the average wind axis (the west) towards the south (Table 1). The southern and northern quadrants were the most and the least inclined, respectively. Conversely, the control block did not exhibit any significant leaning with 80% of vertical individuals (Table 1). The patterns of stem lean were, therefore, very different between the two blocks. A comparison test for periodic data (Rao and SenGupta, 2001) clearly shows that the direction of stems was significantly different (P <0.001) between the control and treated blocks in both leaning intensity and azimuth dispersion. During the second experiment, similar results were obtained, using circular statistics (P <0.05). The ‘wind-treated’ block exhibited a polar pattern of stem lean deviated from the wind axis to the vicinity of the south (Table 1), whilst 81% of the control block consisted of straight individuals.
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Wind effect on stem lean during and after dormancy
A slight increase in stem lean, approximately 5%, was measured in the ‘wind-treated’ block in February 1999, but this change was not significant (P >0.2). In May 1999, strong and vertical shoot growth had begun. As a consequence, stems were straightening up and the gradient of lean observed in the ‘wind-treated’ block diminished by 40%: the leaning angle was only 7.8° (6.9–8.6°) in a direction of 209° (194–225°), whereas the control block leaned at 0.6° (0.6–1.1°) towards 164° (150–176°). Mean angles are given with the associated 95% confidence interval limits in parenthesis, calculated by a re-sampling method (Rao and SenGupta, 2001
). Most of the residual stem lean was due to basal curvature, in particular, in the southern quadrant of the circular block. The stem deviation observed in the ‘wind-treated’ block towards a direction between the south and the axis of wind therefore appears to occur only at an early stage of Maritime pine development i.e. the period prior to first dormancy. |
Discussion |
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Stem orientation undoubtedly resulted from several mechanisms, including passive bending along the axis of wind, gravitropism and possibly phototropism. In the control block, gravitropism effects on growth dominated, and almost all seedlings stayed upright. In the ‘wind-treated’ block, stem orientation occurred as a result of gravitropism, together with bending along the axis of artificial wind, but a significant deviation towards the south also took place. Competition or shading could not have affected aerial growth, as seedlings were separated from each other by at least twice their own height. The dominant natural winds do not come from the north, and therefore could have not inclined plants towards the south. Stem deviation towards the south in all the quadrants of the ‘wind-treated’ block, therefore, appears to be due to heliotropism, i.e. a phototropism towards the mean direction of the sunlight. Surprisingly, a periodic exposure to wind loading has revealed the effects of this phototropism on the growth of Maritime pine seedlings.
Artificial wind exposure must have either inhibited the effects of gravity on shoot growth, or enhanced the effects of light. As far as we know (plant gravitropism reviewed in Blancaflor and Masson, 2003), wind exposure cannot inhibit the gravitropism of shoots. Connections are more likely to occur between the sensory pathways implicated in plant response to wind and light, somewhere upstream of the phototropic response. For example, two differentials of auxin concentrations, with respect to wind direction and sunlight, may occur around the stem (Hart, 1989; Friml et al., 2002) and combine together, leading to the polar pattern of seedlings lean observed; however, as lean was negligible in control plants, the differential of auxin oriented with respect to sunlight must have been induced by artificial wind, rather than light. As previously defined (Grolig et al., 2000), this interaction would be a tonic action of recurrent exposure to wind on phototropism.
Throughout recent decades, a common step has been identified between the transductions of a wide variety of signals (Plieth and Trewavas, 2002; Sanders et al., 2002), including wind (Knight et al., 1992) and light (Quail, 2002), i.e. a rapid and transient elevation of the free cytosolic ion calcium [Ca2+]cyt concentration. This transient elevation has consequences for gene expression and downstream physiological processes, including auxin regulation (Blancaflor and Masson, 2003). As wind stimulation involves several kinds of mechanical loads and simultaneous thermal/chemical stimuli (van Gardingen and Grace, 1991; Telewski, 1995), some of the resulting [Ca2+]cyt peaks could then activate a pathway normally operating in phototropism, for example periodic transients mechanically induced within the photoreceptors, or an extra pathway having a tonic effect on phototransduction. To boost the phototropic response of seedlings would be of essential interest in the case of permanently leaning individuals, especially if in competition with herbaceous species. Such an increase in phototropism will always therefore coexist with an initial stem lean. Therefore, two different patterns of initial stem lean probably occurred within the two blocks of the experiment. In the control block, a passive bending due to similar events like human or animal activity, may have inclined a small number of seedlings in random directions. The resulting phototropic reaction is scarcely observable as it is superimposed with an unknown initial stem lean. In the wind-treated block, however, another generalized and more homogeneous passive bending into the airflow may have occurred, due to, for example, the low bending resistance of the stem during the first days of growth. The resulting phototropic reaction is thus observable, not only at the block scale, but a row effect can also be seen whereby stem lean decreases from R1 to R3 (Table 1).
Furthermore, it was shown that recurrent wind loading ceased to have any significant effect on shoot orientation after the end of the first growing period. Some characteristics of the first months of growth appear, therefore, to govern the tonic effect of wind on seedling heliotropism. Acclimation or desensitization may occur, especially with such a periodic type of signalling (Trewavas, 1999; Plieth and Trewavas, 2002), but intrinsic development is more likely to explain such a physiological switch. In particular, the huge primary growth which occurs in Maritime pine seedlings after the first dormancy period ends the competition for light with most herbaceous species and hence any detrimental consequences.
Finally, these results illustrate the need to define more accurately the different growth and development pathways which exist in plant tissues, and how converging pathways may influence the plant's integrated response to an environmental signal. The importance of wind exposure in the seedling response to light has been highlighted and illustrated for the first time, although this has been suggested previously in the literature (Stokes et al., 1995). A repetition of this experiment, whereby seedlings in both blocks are intentionally inclined without any preferential direction, would help identify the exact component of wind loading, i.e. the role of both durable bending and periodic displacement of the stem in the boosting of phototropism during the early stages of seedling growth. Movement may have an effect on a plant's metabolic pathway, and may be one reason why plants grown in centrifuges and clinostats do not always exhibit the same responses as those grown in microgravity (Sievers and Hejnowicz, 1992; Plieth and Trewavas, 2002). Another key point that needs more investigation is the particular effect of repetition in plant response to environmental stimuli, especially mechanical loading and wind exposure. The device described here is practical and well adapted for this purpose in the case of plants exposed to wind, as its size or period of revolution can easily be modified. In an analogous study on the adaptive response of bone tissue to mechanical stimuli, Turner (1998) showed that the repetitive nature of the stimulation determines the nature of the response more efficiently than the dose itself. Further dose–response experiments also need to be carried out on different species with regards to light, gravity, and mechanical stimulation separately, in order to determine the relative importance of each parameter, at all stages of plant growth. Finally, any study including a molecular description of such experiments will greatly help elucidate the intricate intracellular signalling networks through which sensory information is transduced (Quail, 2002; Pruitt et al., 2003).
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Acknowledgements |
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This work was supported by funding from SERFOB (Région Aquitaine) and the Université Bordeaux I. Thanks are due to P Taris and JL Daban-Haurou who installed the wind device. We also would like to thank L Dupuy for comments on data analysis as well as T Fourcaud, EJ Poole, SB Mickovski, and A Achim for their helpful review of the text.
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