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Plants That Track The ~77~•------------------------------------NEWSANOVIEWS;----------------------~N~A~ru~~~vo=L=. n~~~M~R=IL~I~~ Botany To find even a promising idea it is necessary to go back 70 years to the work of Haberlandt14, who was far ahead of his time in so many fields of plant physiology. Plants that track the Sun Studying the relationships between the from Harry Smith structural anatomy of plant cells and their evident functions, he described the wide­ THE facility with which heliotropic leaves minimum absorption of radiant energy and spread occurrence of papillose epidermal and flowers turn to face the Sun has for so consequent reduction of the heat load on cells --surface cells which are raised more­ long been part of nature lore that it may the leaf with obvious benefits in times of or-less into the shape of a dome but in well seem surprising to the casual observer water stress 1•8 • which the inner walls are flat and parallel to that so little is known of the mechanisms of In contrast to the irreversible orientation the leaf surface. Such cells act as surface perception and response of foliar of the leaves of compass plants -- which is lenses and concentrate perpendicular light orientation. An even more puzzling fixed during leaf development by a mech­ into a central illuminated zone of the inner problem of photoperception is posed by anism that seems to involve photo­ wall, leaving the outer parts and the the so-called compass plants, whose leaves reception, since plants grown in the shade flanking walls comparatively dark. have a fixed orientation along the have randomly orientated leaves 1 -- the Haberlandt originally thought papillose meridian. Our ignorance is particularly leaf movement of heliotropic plants is epidermes concentrated light on to the frustrating in view of the satisfying under­ reversible. Unlike stem phototropism, it is photosynthetic mesophyll cells but later standing of the ecological significance of not the result of asymmetric growth; in came to regard them as 'the optical sense­ these phenomena which has developed in most cases the movements are caused by organs of foliage-leaves' 14 • By ingenious recent years, as shown in a recent paper of specialized pulvinal -- or 'hinge' -- cells experiments on surgically removed 1 Werk and Ehleringer • They analysed the situated at the bases of leaves and/ or epidermes he showed that bright spots behaviour of Lactuca serriola, a common leaflets, although some petioles appear to could indeed be visualized in positions weed whose cauline leaves have laminae have pulvinal characteristics along most or corresponding to the papillose cells, and he facing east-west. The ecological advantage part of their length. Changes in the ionic was even able to focus the image of a micro­ of this strategy seems to lie in the decreased relationships between the pulvinal cells and scope stand using the particularly bulging light interception at the middle of the day, their neighbours result in rapid spatial cells of Anthurium warocqueanum. By which reduces leaf surface temperature by as variations in turgor throughout the wetting one portion of a heliotropic leaf much as 5°C, a major factor in limiting pulvinus region, causing movement of the with a thin film of water, separating it from water loss. Photosynthetic rates are high, dependent lamina9 • The perception prob­ the remaining dry portion by a black paper however, in the morning and afternoon, lem, therefore, becomes one of under­ screen and exposing each to an oblique when water relations are more favourable. standing how the direction of the Sun's rays beam of light, Haberlandt showed that the The opposite strategy -- that of maxi­ incident upon the leaf is transduced into leaf always orientated itself preferentially mum interception of light- is favoured by internal signals which regulate the ionic in response to the stimulus received by the plants whose leaves track the Sun with their characteristics of specific pulvinal cells. dry region. This is exactly what would be laminae perpendicular to the direction of The general characteristics of diahelio­ predicted were the epidermal cells acting as solar radiation. The increase in the daily tropic movements are well-defined in a condensing lenses. Oblique illumination of rate of net photosynthesis due to such 'dia­ recent paper by Vogelmann and Bjorn on the epidermis results in a relative darkening heliotropic' movements is considered to be Lupinus succulentus 10 • Typically, when of the central region of the inner wall and a of particular advantage in seedling estab­ they irradiated a leaf with a beam of white relative brightening of part of the flanking lishment and for ephemeral or annual vege­ light directed obliquely at the upper regions -- sufficient, perhaps, to estabish tation constrained to complete its life cycle surface, leaf movement began 30-60 min the intracellular gradient which may be the quickly before the onset of long periods of later, and reached a maximum rate of prelude to the movement of the leaf. Little drought or thermal stress 2·3. Ehleringer about 15° per hour. Importantly, modern evidence on the epidermal ana­ and Forseth4 recognized solar tracking in irradiating the lower (abaxial) surface of tomy of solar-tracking leaves appears to plants of 16 families growing in the arid the leaf caused no response. Using exist, although the prevalence of papillose regions of the southwestern United States, Lavatera cretica, Koller had previously epidermes in petals has been highlighted by including both C3 and C4 species. In terms shown experimental rates of movement of Kay eta/. 1 ~ who see their importance more of total daily photosynthetic photon more than 90° per hour, far greater than in terms of light reflection than light fluence, they estimated diaheliotropic the minimum required to track the Sun 11 • It perception. Perhaps a return to the ideas leaves to be 38 per cent more effective in is also interesting that a beam directed from and methods of Haberlandt would prove light interception than were fixed horizon­ the base to the tip of the leaf causes it to illuminating, in more ways than one. D tal leaves, and an amazing 167 per cent rotate upwards, whilst the opposite orien­ more effective than non-tracking vertical tation of the beam causes downward rota­ I. Werk , K.S. & Ehleringer, J. Pl. Cell Environ. 7, 81 (19&4). 4 2. Mooney, H.A. & Ehleringer, J.R. Pl. Cell Environ. I, leaves of random azimuth • Relating these tion; in both cases, the adaxial epidermis 307 (1978). values of potential photosynthesis to actual comes to lie perpendicular to the beam 12 • 3. Shell, G.S.G. & Lang, A.R.G. Agric. Metereol. 16, 161 (1976). productivity indicates that diaheliotropism The perception of vectorial stimuli by 4. Ehleringer, J.R. & Forseth, I. Science 110, 1094 (1980). increases carbon assimilation by at least plants is a particularly perplexing problem. S. Kevan, P.G. Science 119, 723 (197~). 30-40 per cent, principally by enhancing Haupt and Feinleib have put forward two 6. Kjellberg, B. eta/. Oecologia 54. 10 (1982). 7. Begg, J.E. &Torsall. B.W. Bull. R. Soc. N.Z. ll, 271(1974). photosynthetic rates in the morning and possible scenarios: either each sensor cell 8. Shackel. K.A . & Hall, A.E. Aust. J. Pl. Physio/. 6, 2M (1979). evening, when solar elevation is low and perceives the direction of the stimulus and 9. Wainwright, C.N. Am. J. Bot. W, 1032 (1977). 10. Vogelmann, T.C. & Bjorn, L.O. Physio/ogia Pl. 59, plant-water relations are favourable. An the resultant intracellular gradients are ~33 (1983). intriguing example of the ecological integrated within the organ during trans­ II. Koller, D. Yb. Carnegie lnstn Wash. 1910-1!111, 72 (1981). 12. Schwartz, A. & Koller, D. Pl. Physiol. 61,924 (1978). advantage of heliotropism occurs with duction, or different sensor cells are stimu­ 13 . Haupt, W. & Feinleib, M.E. Encycl. Pl. Physio/. N.S. certain flowers in which solar tracking lated differently because of the directional 7, I (1979). elevates the temperature within the floral nature of the stimulus and the intercellular 14. Haberlandt, G. Physiological Plant Anatomy 4th Edn, 613 (1914). parts, producing 'solar furnaces' which aid gradient is transduced to the orientation 1~. Kay , Q.O.N., Daoud, H.S. & Stirton, C.H. Bot. J. Linn. both pollination and seed development~- 6 • response 13 • For heliotropism it is not yet Soc. 83, ~7 (1981). The complement to diaheliotropism is possible to distinguish between these two paraheliotropism, in which leaf laminae possibilities and a satisfactory hypothesis Harry Smith is Professor of Botany at the are held parallel to the Sun's rays, ensuring for vectorial photoperception does not exist. University of Leicester, Leicester LEI 7RH. © 1984 Nature Publishing Group.
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