Phototropism: Bending towards Enlightenment

Abstract

Research on phototropism has had far-reaching consequences in the field of plant biology, from helping to refute the ancient misconception of plant insensitivity to the environment to the discovery of the plant hormone auxin and the identification of the phototropin photoreceptors. In this essay, we trace the major trends and ideas that shaped past shoot phototropism research and briefly summarize the current state of the field. For centuries, poets, philosophers, artists, and scientists have noted and studied the phototropic movement of plants. In one of the earliest depictions of plant phototropism, Venus, the ancient goddess of love, transforms Clytie, a water nymph, into a plant because of her infatuation with Apollo, the sun god. Associated with her metamorphosis into a green plant, Clytie turns and follows the movement of Apollo (Ovid et al., 1998). This tale of unrequited love is based on the assumption, developed by the early classical philosophers, that plants exhibit completely passive responses to the environment. The earliest Greek philosophers, Anaxagoras (500–428 BCE) and Empedocles (495–435 BCE), believed that plants, like animals, are sensitive and capable of motion (Drossaart Lulofs and Poortman, 1989). Although Plato (427–347 BCE) also believed in plant sensitivity, he rejected the idea of plant movement (Shemp, 1947; Plato, 2000). Aristotle (384–322 BCE) argued that plants are totally passive and insensitive, and plant insensitivity served as a key criterion for distinguishing between plants and animals (McKeon, 1947; Drossaart Lulofs and Poortman, 1989). Following Aristotle's reasoning, Theophrastus (371–287 BCE) also considered plants as passive organisms. In his botanical writings, Theophrastus recorded the phototropic (and solar-tracking) tendencies of plants, but rather than implicating any activators in the plant, he attributed the phenomenon to the sun's activity in removing fluid from the illuminated side of the plant (Theophrastus, 1976). Because Aristotelian scientific philosophy placed greater value on logic alone and downplayed the need for experimental testing, Theophrastus' simple explanation of phototropism persisted until the 17th century when experimental botanists began to recognize plant sensitivity (Webster, 1966). During the middle ages, herbalists were more interested in the medicinal properties of plants than understanding plant biology. According to the doctrine of signatures, which associated the shape of a plant with its medicinal usage, phototropic plants may have been prescribed for the treatment of snake and serpent bites due to the serpentine shapes they display (von Erhardt-Siebold, 1937). From today's scientific standpoint, the most significant advancement of the medieval herbals was the establishment of a nomenclature that separated plants whose flower-opening is dependent on the sun (composite) from plants that display shoot and leaf phototropism (solago) (von Erhardt-Siebold, 1937). During the renaissance, some early scientists began studying “natural magic,” which was reliant on the elements and occult properties of material things. In contrast with the Aristotelian disdain of experimentation, these early scientists used experimental observation in addition to classical texts to guide their thinking. Giambattista della Porta (1535–1615), probably one of the most well-known practitioners of natural magic, experimented with movement responses of cucumber seedlings. Drawing on Theophrastus' description of phototropism and anthropomorphic treatment of the response by medieval sources, della Porta described plant phototropism as a “rejoicing” response to the sun (della Porta, 1569). Furthermore, in an attempt to explain seemingly similar natural phenomenon, he proposed that the same fundamental law of nature, which he called “sympathy,” governed the attraction of iron toward magnets, hens toward eggs, and the phototropic movement of plants toward the sun (della Porta, 1569). Although it is unclear if della Porta actually believed the concept of plant sensitivity, his explanation of phototropism as a rejoicing and sympathetic response helped open the debate on plant sensitivity. Francis Bacon (1561–1626), who helped shape the modern scientific method, was familiar with della Porta's writing about plant movement. Bacon recorded the tropistic movements of many different plants but held to the classical belief in plant insensitivity. As such, Bacon discarded della Porta's explanation of plant phototropism as a sympathetic or rejoicing response to the sun, and, like Theophrastus, he viewed phototropism as a simple mechanical consequence of wilting. He wrote, “the cause (of phototropism) is somewhat obscure…the part beateth by the sun waxeth more faint and flaccid in the stalk, and less able to support the flower” (Bacon et al., 1627). Intrigued by Bacon's discussion of plants, Thomas Browne (1605–1685) began studying plant physiology. As an alchemist, Browne was seeking a mystical unification of the universe and was more open to the idea of plant sensitivity than Bacon (Webster, 1966). At the time, plants were thought to emit “bad air,” so Browne believed that plant movements allowed plants to avoid the bad air produced by neighboring plants. In what is probably the first crude scientific experiment on plant phototropism, Brown observed that mustard seedlings grown in front of a basement window would eventually reorient themselves toward the window after he rotated the pot (Browne, 1658). When Robert Sharrock (1630–1684) repeated Browne's experiment, he concluded that the response was stimulated by fresh air and caused by growth rather than a mechanical consequence of wilting (Sharrock, 1672). These early phototropism experiments are significant because they provided some of the first scientific examples of plant sensitivity. As the leading botanical taxonomist, John Ray (1628–1705) would have recognized the taxonomic implications that plant sensitivity would have on the classical distinction between plants and animals. To escape the problem this created, Ray considered phototropic movement of plants to be a mechanical effect of temperature on growth. Believing that the rapid etiolated growth of dark-grown seedlings was caused by warmer temperatures, Ray argued that phototropism is caused by a temperature gradient across the seedling with the side closest to the window being colder and slower-growing (Ray et al., 1686; Sachs et al., 1890). Although Ray's temperature hypothesis was later disregarded, his proposition that etiolated growth and phototropism are somehow connected remains a topic of investigation. Woodcut Depicting a Charles Bonnet Tropism Experiment from 1779. Two etiolated bean seedlings (a and b) oppositely placed in a vase (v) of water were tied downward (e). With the shutter (f) closed, each seedling reoriented upward toward the nearest wall (seedling a toward wall q and seedling b toward wall p). When the shutter was raised, both seedlings reoriented toward the opening (o). Reprinted from Bonnet (1779). The Romantic period of the late 18th and early 19th centuries was characterized by a philosophical backlash against the mechanistic view of life that had dominated the enlightenment, and the concept of an endogenous “vital force” served as a common explanation of plant phenomena (Sachs et al., 1890). As this outlook began losing popularity between 1820 and 1840, Henri Dutrochet (1776–1843) proposed that phototropism was an inductive response to light (Dutrochet, 1824, 1826, 1828, 1837). However, Dutrochet's contemporary, Augustin Pyramus de Candolle (1778–1841), thought that phototropism was simply a mechanical consequence of greater etiolated growth on the shaded side of the plant (de Candolle, 1832). This explanation of phototropism was challenged by Albert Bernard Frank (1839–1900), who was the first to propose that phototropism and gravitropism are inductive responses sharing a common underlying process (Frank, 1868). The inductive nature of the response was finally confirmed when Julius von Wiesner (1838–1919) showed that plants continue to bend toward a light source even after the light is turned off (von Wiesner, 1878). Charles Darwin (1809–1882) further explored the inductive nature and mechanistic connection between phototropism and gravitropism. He proposed that the back and forth circumnutation associated with plant growth could be directed by a stimulus such as light or gravity (Darwin, 1880). Although Darwin's circumnutation theory of tropism served to propose a common mechanism underlying gravitropism and phototropism, the most significant discovery from his studies of plant movements was his demonstration that the site of photoperception at the shoot tip and the location of curvature are separable. From his observations, Darwin was able to propose that a transmissible substance produced in the tip is responsible for inducing curvature in lower regions of the plant (Darwin, 1880). This insightful discovery eventually lead to the discovery of the first plant hormone, auxin. Darwin's ideas were initially dismissed by other plant physiologists (reviewed in Heslop-Harrison, 1980). Nevertheless, evidence in favor of Darwin's transmissible substance began to accumulate when Rothert (1894) also showed that light sensitivity is greatest near the tip of maize coleoptiles. Subsequent results of Fitting (1907), Boysen-Jensen (1911), and Paal (1918) provided more direct evidence that a transmissible substance produced in the tip participates in the response. This research culminated in a model put forth independently by Cholodny (1927) and Went (1926, 1928), which proposed that light-mediated lateral redistribution of a plant growth hormone to the shaded side of the seedling causes the differential growth associated with phototropic curvature. This growth substance was shortly identified from human urine by Kogl and Haagen-Smit (1931), who named the hormone auxin, derived from the Greek verb auxein, meaning “to grow.” Although the Cholodny-Went model has remained the dominant explanation of phototropism, other models have challenged its validity. Historically, the model advocated by A.H. Blaauw has been one of the most common alternatives to the Cholodony-Went theory. Similar to Candolle, Blaauw proposed that phototropism is a secondary consequence of differential growth inhibition associated with photomorphogenesis (Blaauw, 1919). While arguing against the Blaauw theory as the sole basis for phototropism, Boysen-Jensen et al. (1936) and Went and Thimann (1937) held out the possibility that both models might function during the phototropic response of dicotyledonous plants. Evidence for this complementary Blaauw/Cholodony-Went model was based on the work of Overbeek, who demonstrated that although unilateral light stimulates the movement of auxin to the shaded side of the hypocotyl, up to half the differential growth associated with phototropism can be attributed to light-mediated growth inhibition (Overbeek, 1932, 1933). More detailed measurements of growth during the 1980s supported this view by indicating that growth inhibition on the illuminated side is accompanied by growth promotion on the shaded side of seedlings (Iino and Briggs, 1984; Macleod et al., 1985; Rich et al., 1985; Baskin, 1986). However, Cosgrove (1985) demonstrated that light-mediated growth inhibition occurs much sooner than the onset of phototropic curvature, a finding that would not be predicted by the Blaauw model. Additional evidence against the Blaauw model came from a study by Liscum et al. (1992), which demonstrated that growth inhibition and phototropism are separable. Another major challenge to the Cholodny-Went model came from an experiment indicating that carotenoids (proposed phototropism photoreceptors) participate in photoinactivation of auxin (Kogl and Schuringa, 1944). This observation led to the hypothesis that phototropism is caused by differential carotenoid-mediated auxin inactivation (reviewed in Shank, 1950). Evidence against the auxin inactivation model came when Briggs et al. (1957) failed to see any in vivo change in total auxin concentration following treatment with light. Instead, their results showed that a barrier inserted between the illuminated and dark sides of the coleoptile prevents the development of an auxin gradient under unilateral illumination. Further support of the Cholodony-Went model came when Briggs (1963a) reported a correlation between an auxin gradient and the magnitude of phototropic response and when Pickard and Thimann (1964) showed that unilateral blue light causes greater radiolabeled auxin accumulation on the shaded flank of coleoptiles. Although these key studies demonstrated that a differential auxin gradient is associated with phototropism, they could not resolve how this gradient develops. According to the classical Cholodny-Went model, lateral auxin transport gives rise to phototropism. However, experiments by Shen-Miller and Gordon (Shen-Miller and Gordon, 1966; Shen-Miller et al., 1969) indicated that light inhibits polar auxin transport, which led them to propose that phototropism is caused by light-mediated inhibition of polar auxin transport on the illuminated flank of a seedling. Related to this model, Naqvi (1972) proposed that light-induced of on the illuminated flank of the seedling causes polar auxin To the idea that polar auxin transport gives rise to phototropism, et al. radiolabeled auxin that had been to coleoptiles. Although they were not able to completely a for light-mediated inhibition of polar auxin transport, their results further demonstrated that unilateral blue light lateral auxin At the same time, and reported that the of phototropism by light or not with an in lateral auxin transport and proposed that the magnitude of the phototropic response is by auxin sensitivity. these studies supported the of auxin in phototropism, but the mechanism of how auxin transport and cause phototropism remained more about how in auxin transport phototropism are from research as a model that in which an auxin in lateral auxin transport, can phototropism et al., the between blue light and is by et al. that blue light not effect the of as it for an auxin thought to be for polar auxin of to a in phototropism, as in a a less to the of and an phototropic response et al., With less to the of it was proposed that by polar auxin transport, phototropism may be by the of auxin for lateral transport et al., However, some polar auxin transport to be for the of phototropism as which have polar auxin transport, display phototropic and more research is to how in both lateral and polar auxin transport phototropism. In it be to how the of auxin transport are in the of the differential growth responses that lead to curvature. 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Because the phototropism the of carotenoids and and concentration is greatest in the phototropism sensitivity is carotenoids were considered to be the responsible for phototropism (reviewed in Shank, 1950). This hypothesis until and proposed the of a or during phototropism. The hypothesis was based on that have a and that can auxin in 1950). For the scientists would continue to debate the of the phototropism for or against a or of research proposed that the blue light would be studies of light-induced and and et al., Another of research used to to the of the blue light et al. and and showed that maize with to display a phototropic response. However, carotenoids also to a as because with the also a phototropic response and In and Briggs the of a in the of light for phototropism because treatment with the transport the sensitivity to unilateral blue light. 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Although these studies a in phototropism, they could not the of activity in the promotion of phototropism. studies indicated that can more than a secondary in phototropism under some For et al. proposed that may be for phototropism in some because they observed a phototropic response of maize to unilateral light. also blue light and or light from could the phototropic response of et al. also concluded that phototropism is by in with an blue light to as a secondary However, light is much less at inducing phototropism (von Wiesner, so the are not thought to be the in phototropism. studies confirmed a significant for the not in the light of phototropism et al., et al., et al., but also in the of a light and other studies that the blue light can the development of phototropic curvature et al., et al., and the and function in and somewhat during other light-mediated they may be phototropism in a similar display a phototropic response under light and responses and is that the of a associated with by the and participates in the promotion of phototropism because display a phototropic response to light and The of phototropism research the was with the mechanistic of the response. However, the to which a plant or plant part to unilateral light can In some different phototropic responses are a of a shoot more differential growth than a shoot to the same of curvature. In other in phototropism are more connected to the associated with in sensitivity and to light. of phototropism can in different under to light or of light. The observation that etiolated seedlings to unilateral light have a response than seedlings to light was first observed by von Wiesner As von Wiesner was phototropism is a passive mechanical consequence of light or an inductive response. According to the hypothesis that phototropism is a passive mechanical phenomenon, light was to cause a response. When this of the mechanical phototropism model, von Wiesner observed that the light past a actually the phototropic response of etiolated seedlings. However, von Wiesner also believed that the of phototropism was to the of photomorphogenesis and concluded that the of phototropic sensitivity and with light-mediated growth inhibition (von Wiesner, 1878). During the and von but a explanation of the phenomenon was not In a of and studied the effect of light on the phototropic response of etiolated From the results of these it that are at to the of phototropism. light was to cause a rapid in phototropic as display a rapid response and This may be due to of the phototropin or to the of phototropism because is not for a response in the of et al., 2000). after the rapid the and were to a phototropic response and The and probably function somewhat in this process by the of auxin and transport and Although elements associated with photomorphogenesis participate in the of phototropism in etiolated the between development and phototropism is In contrast with etiolated observed that seedlings are more to light than to light. Similar was observed in and and However, how this in phototropic sensitivity occurs is Additional during the first of the century also demonstrated that phototropic to of light is not as as might be light of or Blaauw that the magnitude of the response can be to light and reported that the described by Blaauw is under of light When further the light and stimulated a response even of light a phototropic response Following the of as a model for plant research during the and a of detailed studies how light and the first and phototropic responses of etiolated and et al., and et al., These studies demonstrated that light in phototropism is with both and on the development of curvature and et al. have proposed that the response associated with phototropism is to the and magnitude of phototropin However, this model testing, and more research is to the underlying basis for the of phototropism. The of phototropism is and current understanding of the response has its in ancient Greek philosophy and from the early studies of the research with has mechanistic understanding of phototropism. can view the response as a simple or response. Instead, phototropism be viewed as a response of and that the establishment of differential growth its much phototropism research remains to be we can of the underlying and the of its for her and are supported by from the the of and the Briggs