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Toward understanding the ecological functions of tropisms: interactions among and effects of light on tropisms
Toward understanding the ecological functions of tropisms: interactions among and effects of light on tropisms Commentary Moritoshi Iino Tropisms of higher plants have been investigated for well over a century. Only recently, however, we have begun to establish their mechanisms firmly, mainly thanks to the availability of mutants and genome sequence information. For example, the starch-statolith hypothesis is now best supported as the main mechanism by which plants perceive gravity direction. Phototropins have been identified as the photoreceptors for the major blue-light-sensitive phototropism. Investigations have been extended to elucidate the relationships among tropisms and the controlling roles played by environmental factors, such as light. We are now finding examples in which phototropic and hydrotropic responses are modified through the environmental control of counteracting gravitropism. We are also finding that seedlings generally become phototropically competent only after phytochrome is activated. Such results are providing insights into how plants use tropisms to achieve adaptive growth movements. Addresses Botanical Gardens, Graduate School of Science, Osaka City University, Kisaichi, Katano-shi, Osaka 576-0004, Japan Corresponding author: Iino, Moritoshi ([email protected])
Current Opinion in Plant Biology 2006, 9:89–93 Available online 9th December 2005 1369-5266/$ – see front matter # 2005 Elsevier Ltd. All rights reserved. DOI 10.1016/j.pbi.2005.11.012
Introduction Plants have evolved the ability to move their organs by making axial growth asymmetric. With this mechanism, higher plants undertake many forms of movement including tropisms, nastic movements, and nutations. Tropisms are movements that are induced in the direction related to the stimulus direction. Being closely related to the sessile lifestyle of plants, they are used to establish body architecture and to orient body parts to more suitable environments. Gravitropism and phototropism are the most common tropisms and also the best studied. Recent years have seen significant advancements in our knowledge of the basic mechanisms of tropisms. Mutants that are impaired in tropisms have played especially important roles. Many lines of evidence now support the starchwww.sciencedirect.com
statolith hypothesis as the major, if not the sole, mechanism by which plants perceive the direction of gravity [1]. How the physical stimulus that results from statolith sedimentation is transduced into a biochemical signal is now under intense investigation. The photoreceptor for phototropism had long remained obscure until Briggs and colleagues [2] uncovered the flavin-bound photoreceptor phototropin in Arabidopsis thaliana. It has been established that two phototropins, phot1 and phot2, serve as the major photoreceptors for the phototropisms of both shoots and roots in Arabidopsis [2]. Arabidopsis NONPHOTOTROPIC HYPOCOTYL3 (NPH3), which strictly limits hypocotyl phototropism, has been identified as a phototropin-interacting protein that is likely to function as a downstream signaling component [3]. Rice COLEOPTILE PHOTOTROPISM1 (CPT1), a NPH3 ortholog, has been shown to limit coleoptile phototropisms [4], indicating that similar phototropic signaling pathways operate in hypocotyls and coleoptiles [5]. The hypothesis known as the Cholodny– Went theory of tropisms explains tropic growth asymmetry in terms of the lateral translocation of auxin. This hypothesis has been subjected to various criticisms, but its applicability to shoot phototropism [4,6,7] and root gravitropism [8] is now strongly supported by physiological, cell biological, and genetic results. Different tropisms operate together in nature and it is anticipated that plants combine tropisms to undertake adaptive growth movements. Therefore, it is of interest to know whether there are any specific interaction mechanisms among tropisms. We might also ask whether environmental signals play any modifying or controlling roles in tropisms other than inducing them. A fuller understanding of the functions of tropisms clearly depends on investigations of these aspects. Furthermore, such investigations are expected to help expand our knowledge of the mechanisms of tropisms, which is still far from complete. This article summarizes results that are related to these ecological aspects. I discuss recent results critically and present some hypothetical views.
Establishing body architecture in an upright stationary condition Upward growth of shoots and downward growth of roots determine the primary body architecture of plants. It is generally stated that these growth orientations are achieved by negative gravitropism of shoots and positive gravitropism of roots. However, the induction of asymmetric Current Opinion in Plant Biology 2006, 9:89–93
90 Commentary
growth (gravitropism) in displaced plants and the maintenance of symmetric growth in upright plants are not exactly congruent. In fact, under the condition in which circumnutation does not take place, seedling shoots can grow straight upward [9]. It has not yet been clearly explained how plants can achieve symmetric growth by detecting the direction of gravity. The lag time between gravitropic stimulation and response (15–30 min) appears to be too long to allow the fine control of growth direction to be explained by gravitropism. Plants can detect relatively small displacement but not to the extent that they can effectively detect a few degrees of displacement [10]. Straightening of a gravitropically bent organ involves the process known as autotropism or autostraightening [11,12]. Autostraightening is based on a unique mechanism that actively counteracts gravitropic curvature [10]. In fact, our recent results obtained with pea epicotyls indicated that asymmetric distribution of auxin correlates with gravitropic curvature but not with autostraightening [13]. It is hypothesized here that the mechanism that underlies autostraightening generally operates in upright plants and contributes to the maintenance of symmetric growth. Autostraightening has been thought to be a process that is induced as a consequence of gravitropic curvature, or of any induced curvature [12]. By contrast, the above hypothesis assumes that the mechanism of autostraightening is already functioning when gravitropism is induced and counteracts the induced gravitropism from the beginning. It has occasionally been observed that a displaced organ shows a rapid gravitropic curvature, but stops this curvature before the tip reaches the vertical position and retains the non-vertical orientation for a relatively long time (e.g. pea epicotyls [13,14]; Arabidopsis hypocotyls [15]; or oat coleoptiles [10]). Such observations might indicate that autostraightening counteracts and balances the gravitropic response that is induced at that orientation, while the basal region cannot obtain a completely upward orientation owing to counteracting autostraightening.
organs such as hypocotyls and coleoptiles establish a nearly stable phototropic curvature, which is often less than 908 from the vertical. This curvature apparently represents the equilibrium between phototropism and gravitropism, or photogravitropic equilibrium [18,19]. These organs are arcshaped in the initial stage of curvature development, but straighten in the upper part as they establish the photogravitropic equilibrium. This straightening is probably not achieved only by the balance between the two tropisms but with a contribution from autostraightening [6]. Takahashi and colleagues reported interesting results concerning the relationship between the hydrotropism and gravitropism of roots ([20] and references cited therein). They used starch-deficient mutants to demonstrate that hydrotropism is counteracted by gravitropism. They subsequently found that the amyloplasts of gravitysensing columella cells are degraded in hydrotropically responding roots of Arabidopsis and radish. Takahashi and colleagues concluded that roots develop greater hydrotropism by degrading amyloplasts and thereby reducing gravitropic activity. The same workers also found that non-directional water stress causes amyloplast degradation. This finding suggests that roots become more hydrotropically responsive by degrading amyloplasts, thus reducing gravitropic responsiveness under water-deficient conditions. Although not discussed by the Takahashi and colleagues, the experimental procedure used to induce hydrotropism makes it possible that the amyloplast degradation observed during hydrotropism was also caused by water deficiency. We may now ask if there are any mechanisms by which plants can change the balance between gravitropism and phototropism. As discussed below, plants use light signals to achieve this.
Photocontrol of gravitropism
Interactions between gravitropism and other tropisms
Early results indicated that red light (R) either inhibits or stimulates the gravitropic curvature of etiolated seedling shoots. Because R greatly influences straight growth of seedling shoots, these results, which were obtained by measuring the angle of curvature, do not clearly resolve the relationship between R and gravitropism. Our recent data, obtained with rice coleoptiles, indicated that R reduces the rate of gravitropic curvature but not to the extent that it inhibits straight growth. In fact, measurements of differential growth indicated that R rather enhances gravitropic responsiveness [21]. Gravitropism is necessary for plants that grow upward above ground. Therefore, it is reasonable to assume that gravitropic responsiveness is generally not inhibited by light.
When phototropic curvature is induced in upright plants, it is counteracted by gravitropism. This is clear from the observation that a substantially greater phototropic curvature occurs in mutants that are impaired in gravitropism [9,17]. Under continuous stimulation by unilateral light,
There are special cases in which gravitropism is specifically regulated by light. The primary root of maize, which grows horizontally (i.e. diagravitropically) in darkness, becomes positively gravitropic following phytochrome activation
Plants are capable of growing in a horizontal or oblique direction by detecting the direction of gravity [16]. These growth movements, called diagravitropism and plagiogravitropism, respectively, are also basic response elements that contribute to the establishment of plant body architecture. In spite of their importance, we know little about the mechanisms that allow these growth movements.
Current Opinion in Plant Biology 2006, 9:89–93
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Ecological functions of tropisms Iino 91
[22]. The shoot of the lazy-2 tomato mutant shows normal negative gravitropism in darkness, but becomes positively gravitropic following phytochrome activation [23]. The gravitropic behavior of the nodes of Tradescantia flumiensis is greatly affected by light; in this case the response appears to be mediated mainly by photosynthesis [24]. The hypocotyl of Arabidopsis is another example in which gravitropism is specifically regulated by phytochrome. In darkness, Arabidopsis hypocotyls grow upward, but they become randomly oriented upon exposure to R. This light response involves both a phytochrome A (phyA)dependent very-low-fluence response, which can be induced effectively by far-red light (FR) as well as by blue light, and a phyB-dependent low-fluence response [25,26]. Gravitropism is apparently inhibited by phytochrome to the extent that the hypocotyl cannot maintain upward growth. Investigation with cryptochrome-deficient mutants suggested that cryptochrome 1 (cry1) and cry2 also participate in the light-induced inhibition of gravitropism [27]. Owing to the strong inhibition of gravitropism, the hypocotyl orientation under exposure to directional white or blue light is almost entirely determined by phototropism [28]. We might speculate that Arabidopsis has developed the ability to undergo a strong light-induced inhibition of gravitropism so as to express strong phototropism. Because of its rosette lifestyle, Arabidopsis does not need to sustain an upward orientation of hypocotyls and, therefore, can benefit from maximal expression of phototropism. Any effect of light on autostraightening will also result in a change in gravitropic response. This will be especially so if autostraightening generally operates during organ growth as hypothesized above. I will not extend discussion along this possibility, which is too speculative at the moment. However, it may be mentioned that white-lightor R-grown seedlings are generally straighter than darkgrown seedlings. A part of the difference might be due to the effect of light on autostraightening.
Photocontrol of phototropism The multiphasic fluence-response relationship for the blue-light-sensitive phototropism of seedling shoots is affected by phytochrome in a complex manner [6]. Among all the effects noted, that observed for timedependent phototropism deserves special attention. This phototropism is induced by extended phototropic stimulation in such a way that the curvature response depends more on the stimulation time than on the fluence rate in a major effective range of fluence rates [6]. Time-dependent phototropism is directly related to and represents the properties of the phototropism that is induced by continuous stimulation. The occurrence of time-dependent phototropism is strictly controlled by phytochrome, as shown for maize www.sciencedirect.com
coleoptiles [29], Arabidopsis hypocotyls [30,31], and tomato hypocotyls [32]. It is generally difficult to demonstrate this because the blue light used to induce phototropism can also initiate phytochrome signaling. In maize, the strict control by phytochrome was uncovered because the phytochrome response was based almost entirely on a low-fluence mode (i.e. the response cannot be induced as effectively by blue light) and also because of the lag time of phytochrome action. On the other hand, the strict phytochrome control in Arabidopsis and tomato was found using a phyA/phyB-deficient double mutant and a phyA-deficient mutant, respectively. These mutants began to express phototropism when blue light stimulation was extended beyond 1–2 h. It is possible that one or more of the other photoreceptors present in the mutants, including non-mutated phytochromes, are responsible for the delayed establishment of phototropic responsiveness. Stowe-Evans et al. [33] concluded that the R-induced enhancement of phototropic responsiveness in Arabidopsis is primarily a phyA-mediated FR-reversible low-fluence response. This conclusion is crucial because it contradicts the earlier genetic evidence that both phyA and phyB function in the response [30,31], and also because no other examples show that phyA functions in a R/FR reversible manner in dark-grown seedlings. Although phyA could function in a R/FR-reversible manner under the condition in which the bulk amount of light-labile phyA has disappeared [34], the data presented by Stowe-Evans et al. might not justify the above conclusion. In their study, the R/FR reversibility test was conducted only with wildtype seedlings. Although the effect of R was reversed almost entirely by FR to the control level, the control seedlings were necessarily irradiated with blue light (for phototropic stimulation), which could have induced the phyA-dependent very-low-fluence response. Lariguet and Fankhauser [28] suggested that the phytochrome-mediated enhancement of phototropism in the Arabidopsis hypocotyl is mainly caused by the phytochrome-mediated inhibition of gravitropism. There is no doubt that the strong inhibition of gravitropism found in this organ will result in an enhancement of phototropism (see above), but this does not exclude the possible involvement of the more direct mechanism discussed above. A crucial point is whether phytochrome-deficient Arabidopsis mutants show reduced or no phototropic curvature from the beginning. Because gravitropism interferes with phototropic curvature after a lag of about 30 min [6], these mutants will initially show a wildtype level of phototropic curvature if gravitropism inhibition is the primary cause of phototropism enhancement. The phytochrome-deficient mutants of Arabidopsis [30] and tomato [32] did not show any such curvature. Current Opinion in Plant Biology 2006, 9:89–93
92 Commentary
With regard to the regulation of time-dependent phototropism by phytochrome, two additional points deserve a mention. First, phytochrome is likely to act on the process that underlies the time-dependent feature of phototropism [6]. Second, phytochrome activation begins to establish phototropic responsiveness after a lag of about 10 min [29]. It is likely that the phytochrome action involves the expression of one or more genes that are needed for timedependent phototropism. The fluence rate–response curves for the phototropism of continuously stimulated seedling shoots span a wide range of fluence rates [18,19,35]. In Arabidopsis, phot1 is sufficient to generate nearly the entire fluence rate– response curve [35]. These results suggest that the photoreceptor system for phototropism, at least the one based on phot1, involves a sensory adaptation mechanism. The major pulse-induced phototropism (the so-called first positive curvature) of grass coleoptiles is desensitized by phytochrome, and also in response to blue light [6]. As shown for maize coleoptiles, phytochrome-mediated desensitization progresses slowly over a period of 2 h, whereas blue-light-induced desensitization occurs immediately [36–38]. Although the causal relationship between pulse-induced phototropism and time-dependent phototropism remains to be elucidated [6], these results suggest that phytochrome and a blue-light-absorbing photoreceptor mediate adaptation with different kinetics (i.e. slow adaptation by phytochrome and rapid adaptation by a blue-light-absorbing photoreceptor). Whippo and Hangarter [39] used cryptochrome- and phototropin-deficient Arabidopsis hypocotyls to investigate the time courses of phototropic responses to continuous stimulation at different fluence rates. If any one of the mutated photoreceptors were involved in sensory adaptation, then it would be expected that its absence would result in a narrower fluence rate–response curve. The reported data do not indicate that the cryptochromes (cry1 and cry2) or phot2 mediate the sensory adaptation. Whether or not phot1 (i.e. the major photoreceptor of phototropism itself) is involved in the adaptation cannot be resolved by using the phot1-deficient mutant. Whippo and Hangarter [39] did find, however, that a high fluence rate of blue light causes a substantially delayed phototropic curvature, and that this curvature response is enhanced in the cry1 cry2 double mutant. This delayed curvature might be the result of slow adaptation. A possible explanation is that phytochrome mediates this adaptation and cryptochrome has a negative effect on this mediation. The phototropic fluence rate–response curve obtained by Galland [19] for oat coleoptiles spanned over a much wider range of fluence rates than that obtained by Neumann and Iino [18] for rice coleoptiles. The extension of Current Opinion in Plant Biology 2006, 9:89–93
the curve occurred toward lower fluence rates. Galland [40] also showed that the shape of the fluence rate– response curve changes with stimulation time. Many possible reasons can be suggested for the difference between the fluence rate–response curve of Galland and that of Neumann and Iino. Among them is the difference in growth conditions. For phototropic stimulation, Neumann and Iino used R-grown seedlings, whereas Galland used seedlings that had been grown under white light until phototropic stimulation. The blue-light component of white light might have made the seedlings more sensitive and adaptive to phototropic stimulus. Further investigation with blue-light-grown seedlings might provide useful information.
Conclusions Higher plants use tropisms to establish their body architecture and to achieve adaptive growth movements. Upward orientation of shoots and downward orientation of roots, which represent the basic body architecture, are established in response to gravity. It is suggested here that, in addition to gravitropism, the mechanism of autostraightening contributes to the maintenance of stable organ orientation under an upright stationary condition. The body architecture that is established in response to gravity is modified by other tropisms. When such a tropism is induced, it is counteracted by gravitropism that is initiated as a consequence of the induced curvature, and the balance between the two tropisms determines the organ orientation. In fact, it appears that plants specifically control this balance, as depicted by the following two examples, to achieve adaptive growth movements. First, the roots of Arabidopsis and radish show greater hydrotropism by degrading columella amyloplasts and thereby reducing gravitropic responsiveness. Water deficiency is a probable cause of amyloplast degradation. Second, the gravitropic responsiveness of Arabidopsis hypocotyls is greatly inhibited by the action of phytochrome and, as a consequence of this response, the growth direction under directional light stimulus is almost entirely determined by phototropism. This type of regulatory mechanism, which has not been found in other investigated plants, might be related to the rosette lifestyle of Arabidopsis. It has also become clearer that plants germinating and growing within the dark environment of the soil generally have little ability to express functional phototropism (i.e. time-dependent phototropism) and that phytochrome is used to establish phototropic responsiveness. Furthermore, it appears that phototropic signaling involves sensory adaptation mechanisms that are mediated by phytochrome and a blue-light-absorbing photoreceptor. Further investigations should clarify the response components that are involved in the photocontrol of tropisms. Such components are expected to include key players in tropic signal transduction. www.sciencedirect.com
Ecological functions of tropisms Iino 93
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22. Mandoli DF, Tepperman J, Huala E, Briggs WR: Photobiology of diagravitropic maize roots. Plant Physiol 1984, 75:359-363. 23. Behringer FJ, Lomax TL: Genetic analysis of the roles of phytochromes A and B1 in the reversed gravitropic response of the lz-2 tomato mutant. Plant Cell Environ 1999, 22:551-558. 24. Digby J, Firn RD: Light modulation of the gravitropic set-point angle (GSA). J Exp Bot 2002, 53:377-381. 25. Poppe C, Hangerter RP, Sharrock RA, Nagy F, Scha¨fer E: The light-induced reduction of the gravitropic growth-orientation of seedlings of Arabidopsis thaliana (L.) Heynh. is a photomorphogenetic response mediated synergistically by the far-red-absorbing forms of phytochromes A and B. Planta 1996, 199:511-514. 26. Robson PR, Smith H: Genetic and transgenic evidence that phytochromes A and B act to modulate the gravitropic orientation of Arabidopsis thaliana hypocotyls. Plant Physiol 1996, 110:211-216. 27. Ohgishi M, Saji K, Okada K, Sakai T: Functional analysis of each blue light receptor, cry1, cry2, phot1, and phot2, by using combinational multiple mutants in Arabidopsis. Proc Natl Acad Sci USA 2004, 101:2223-2228. 28. Lariguet P, Fankhauser C: Hypocotyl growth orientation in blue light is determined by phytochrome A inhibition of gravitropism and phototropin promotion of phototropism. Plant J 2004, 40:826-834. 29. Liu YJ, Iino M: Phytochrome is required for the occurrence of time-dependent phototropism in maize coleoptiles. Plant Cell Environ 1996, 19:1379-1388. 30. Hangarter RP: Gravity, light and plant form. Plant Cell Environ 1997, 20:796-800. 31. Janoudi A-k, Konjevic R, Whitelam G, Gordon W, Poff KL: Both phytochrome A and phytochrome B are required for the normal expression of phototropism in Arabidopsis thaliana seedlings. Physiol Plant 1997, 101:278-282. 32. Srinivas A, Behera RK, Kagawa T, Wada M, Sharma R: high pigment1 mutation negatively regulates phototropic signal transduction in tomato seedlings. Plant Physiol 2004, 134:790-800. 33. Stowe-Evans EL, Luesse DR, Liscum E: The enhancement of phototropin-induced phototropic curvature in Arabidopsis occurs via a photoreversible phytochrome A-dependent modulation of auxin responsiveness. Plant Physiol 2001, 126:826-834. 34. Long C, Iino M: Light-dependent osmoregulation in pea stem protoplasts. Photoreceptors, tissue specificity, ion relationships, and physiological implications. Plant Physiol 2001, 125:1854-1869. 35. Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K: Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 2001, 98:6969-6974. 36. Iino M: Kinetic modelling of phototropism in maize coleoptiles. Planta 1987, 171:110-126. 37. Iino M: Desensitization by red and blue light of phototropism in maize coleoptiles. Planta 1988, 176:183-188. 38. Liu YJ, Iino M: Effects of red light on the fluence-response relationship for pulse-induced phototropism of maize coleoptiles. Plant Cell Environ 1996, 19:609-614. 39. Whippo CW, Hangarter RP: Second positive phototropism results from coordinated co-action of the phototropins and cryptochromes. Plant Physiol 2003, 132:1499-1507. 40. Galland P: Photogravitropic equilibrium in Avena coleoptiles: fluence rate-response relationships and dependence on dark adaptation and clinostating. J Plant Res 2002, 115:131-140. Current Opinion in Plant Biology 2006, 9:89–93
Current Opinion in Plant Biology 2006, 9:89–93 Available online 9th December 2005 1369-5266/$ – see front matter # 2005 Elsevier Ltd. All rights reserved. DOI 10.1016/j.pbi.2005.11.012
Introduction Plants have evolved the ability to move their organs by making axial growth asymmetric. With this mechanism, higher plants undertake many forms of movement including tropisms, nastic movements, and nutations. Tropisms are movements that are induced in the direction related to the stimulus direction. Being closely related to the sessile lifestyle of plants, they are used to establish body architecture and to orient body parts to more suitable environments. Gravitropism and phototropism are the most common tropisms and also the best studied. Recent years have seen significant advancements in our knowledge of the basic mechanisms of tropisms. Mutants that are impaired in tropisms have played especially important roles. Many lines of evidence now support the starchwww.sciencedirect.com
statolith hypothesis as the major, if not the sole, mechanism by which plants perceive the direction of gravity [1]. How the physical stimulus that results from statolith sedimentation is transduced into a biochemical signal is now under intense investigation. The photoreceptor for phototropism had long remained obscure until Briggs and colleagues [2] uncovered the flavin-bound photoreceptor phototropin in Arabidopsis thaliana. It has been established that two phototropins, phot1 and phot2, serve as the major photoreceptors for the phototropisms of both shoots and roots in Arabidopsis [2]. Arabidopsis NONPHOTOTROPIC HYPOCOTYL3 (NPH3), which strictly limits hypocotyl phototropism, has been identified as a phototropin-interacting protein that is likely to function as a downstream signaling component [3]. Rice COLEOPTILE PHOTOTROPISM1 (CPT1), a NPH3 ortholog, has been shown to limit coleoptile phototropisms [4], indicating that similar phototropic signaling pathways operate in hypocotyls and coleoptiles [5]. The hypothesis known as the Cholodny– Went theory of tropisms explains tropic growth asymmetry in terms of the lateral translocation of auxin. This hypothesis has been subjected to various criticisms, but its applicability to shoot phototropism [4,6,7] and root gravitropism [8] is now strongly supported by physiological, cell biological, and genetic results. Different tropisms operate together in nature and it is anticipated that plants combine tropisms to undertake adaptive growth movements. Therefore, it is of interest to know whether there are any specific interaction mechanisms among tropisms. We might also ask whether environmental signals play any modifying or controlling roles in tropisms other than inducing them. A fuller understanding of the functions of tropisms clearly depends on investigations of these aspects. Furthermore, such investigations are expected to help expand our knowledge of the mechanisms of tropisms, which is still far from complete. This article summarizes results that are related to these ecological aspects. I discuss recent results critically and present some hypothetical views.
Establishing body architecture in an upright stationary condition Upward growth of shoots and downward growth of roots determine the primary body architecture of plants. It is generally stated that these growth orientations are achieved by negative gravitropism of shoots and positive gravitropism of roots. However, the induction of asymmetric Current Opinion in Plant Biology 2006, 9:89–93
90 Commentary
growth (gravitropism) in displaced plants and the maintenance of symmetric growth in upright plants are not exactly congruent. In fact, under the condition in which circumnutation does not take place, seedling shoots can grow straight upward [9]. It has not yet been clearly explained how plants can achieve symmetric growth by detecting the direction of gravity. The lag time between gravitropic stimulation and response (15–30 min) appears to be too long to allow the fine control of growth direction to be explained by gravitropism. Plants can detect relatively small displacement but not to the extent that they can effectively detect a few degrees of displacement [10]. Straightening of a gravitropically bent organ involves the process known as autotropism or autostraightening [11,12]. Autostraightening is based on a unique mechanism that actively counteracts gravitropic curvature [10]. In fact, our recent results obtained with pea epicotyls indicated that asymmetric distribution of auxin correlates with gravitropic curvature but not with autostraightening [13]. It is hypothesized here that the mechanism that underlies autostraightening generally operates in upright plants and contributes to the maintenance of symmetric growth. Autostraightening has been thought to be a process that is induced as a consequence of gravitropic curvature, or of any induced curvature [12]. By contrast, the above hypothesis assumes that the mechanism of autostraightening is already functioning when gravitropism is induced and counteracts the induced gravitropism from the beginning. It has occasionally been observed that a displaced organ shows a rapid gravitropic curvature, but stops this curvature before the tip reaches the vertical position and retains the non-vertical orientation for a relatively long time (e.g. pea epicotyls [13,14]; Arabidopsis hypocotyls [15]; or oat coleoptiles [10]). Such observations might indicate that autostraightening counteracts and balances the gravitropic response that is induced at that orientation, while the basal region cannot obtain a completely upward orientation owing to counteracting autostraightening.
organs such as hypocotyls and coleoptiles establish a nearly stable phototropic curvature, which is often less than 908 from the vertical. This curvature apparently represents the equilibrium between phototropism and gravitropism, or photogravitropic equilibrium [18,19]. These organs are arcshaped in the initial stage of curvature development, but straighten in the upper part as they establish the photogravitropic equilibrium. This straightening is probably not achieved only by the balance between the two tropisms but with a contribution from autostraightening [6]. Takahashi and colleagues reported interesting results concerning the relationship between the hydrotropism and gravitropism of roots ([20] and references cited therein). They used starch-deficient mutants to demonstrate that hydrotropism is counteracted by gravitropism. They subsequently found that the amyloplasts of gravitysensing columella cells are degraded in hydrotropically responding roots of Arabidopsis and radish. Takahashi and colleagues concluded that roots develop greater hydrotropism by degrading amyloplasts and thereby reducing gravitropic activity. The same workers also found that non-directional water stress causes amyloplast degradation. This finding suggests that roots become more hydrotropically responsive by degrading amyloplasts, thus reducing gravitropic responsiveness under water-deficient conditions. Although not discussed by the Takahashi and colleagues, the experimental procedure used to induce hydrotropism makes it possible that the amyloplast degradation observed during hydrotropism was also caused by water deficiency. We may now ask if there are any mechanisms by which plants can change the balance between gravitropism and phototropism. As discussed below, plants use light signals to achieve this.
Photocontrol of gravitropism
Interactions between gravitropism and other tropisms
Early results indicated that red light (R) either inhibits or stimulates the gravitropic curvature of etiolated seedling shoots. Because R greatly influences straight growth of seedling shoots, these results, which were obtained by measuring the angle of curvature, do not clearly resolve the relationship between R and gravitropism. Our recent data, obtained with rice coleoptiles, indicated that R reduces the rate of gravitropic curvature but not to the extent that it inhibits straight growth. In fact, measurements of differential growth indicated that R rather enhances gravitropic responsiveness [21]. Gravitropism is necessary for plants that grow upward above ground. Therefore, it is reasonable to assume that gravitropic responsiveness is generally not inhibited by light.
When phototropic curvature is induced in upright plants, it is counteracted by gravitropism. This is clear from the observation that a substantially greater phototropic curvature occurs in mutants that are impaired in gravitropism [9,17]. Under continuous stimulation by unilateral light,
There are special cases in which gravitropism is specifically regulated by light. The primary root of maize, which grows horizontally (i.e. diagravitropically) in darkness, becomes positively gravitropic following phytochrome activation
Plants are capable of growing in a horizontal or oblique direction by detecting the direction of gravity [16]. These growth movements, called diagravitropism and plagiogravitropism, respectively, are also basic response elements that contribute to the establishment of plant body architecture. In spite of their importance, we know little about the mechanisms that allow these growth movements.
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Ecological functions of tropisms Iino 91
[22]. The shoot of the lazy-2 tomato mutant shows normal negative gravitropism in darkness, but becomes positively gravitropic following phytochrome activation [23]. The gravitropic behavior of the nodes of Tradescantia flumiensis is greatly affected by light; in this case the response appears to be mediated mainly by photosynthesis [24]. The hypocotyl of Arabidopsis is another example in which gravitropism is specifically regulated by phytochrome. In darkness, Arabidopsis hypocotyls grow upward, but they become randomly oriented upon exposure to R. This light response involves both a phytochrome A (phyA)dependent very-low-fluence response, which can be induced effectively by far-red light (FR) as well as by blue light, and a phyB-dependent low-fluence response [25,26]. Gravitropism is apparently inhibited by phytochrome to the extent that the hypocotyl cannot maintain upward growth. Investigation with cryptochrome-deficient mutants suggested that cryptochrome 1 (cry1) and cry2 also participate in the light-induced inhibition of gravitropism [27]. Owing to the strong inhibition of gravitropism, the hypocotyl orientation under exposure to directional white or blue light is almost entirely determined by phototropism [28]. We might speculate that Arabidopsis has developed the ability to undergo a strong light-induced inhibition of gravitropism so as to express strong phototropism. Because of its rosette lifestyle, Arabidopsis does not need to sustain an upward orientation of hypocotyls and, therefore, can benefit from maximal expression of phototropism. Any effect of light on autostraightening will also result in a change in gravitropic response. This will be especially so if autostraightening generally operates during organ growth as hypothesized above. I will not extend discussion along this possibility, which is too speculative at the moment. However, it may be mentioned that white-lightor R-grown seedlings are generally straighter than darkgrown seedlings. A part of the difference might be due to the effect of light on autostraightening.
Photocontrol of phototropism The multiphasic fluence-response relationship for the blue-light-sensitive phototropism of seedling shoots is affected by phytochrome in a complex manner [6]. Among all the effects noted, that observed for timedependent phototropism deserves special attention. This phototropism is induced by extended phototropic stimulation in such a way that the curvature response depends more on the stimulation time than on the fluence rate in a major effective range of fluence rates [6]. Time-dependent phototropism is directly related to and represents the properties of the phototropism that is induced by continuous stimulation. The occurrence of time-dependent phototropism is strictly controlled by phytochrome, as shown for maize www.sciencedirect.com
coleoptiles [29], Arabidopsis hypocotyls [30,31], and tomato hypocotyls [32]. It is generally difficult to demonstrate this because the blue light used to induce phototropism can also initiate phytochrome signaling. In maize, the strict control by phytochrome was uncovered because the phytochrome response was based almost entirely on a low-fluence mode (i.e. the response cannot be induced as effectively by blue light) and also because of the lag time of phytochrome action. On the other hand, the strict phytochrome control in Arabidopsis and tomato was found using a phyA/phyB-deficient double mutant and a phyA-deficient mutant, respectively. These mutants began to express phototropism when blue light stimulation was extended beyond 1–2 h. It is possible that one or more of the other photoreceptors present in the mutants, including non-mutated phytochromes, are responsible for the delayed establishment of phototropic responsiveness. Stowe-Evans et al. [33] concluded that the R-induced enhancement of phototropic responsiveness in Arabidopsis is primarily a phyA-mediated FR-reversible low-fluence response. This conclusion is crucial because it contradicts the earlier genetic evidence that both phyA and phyB function in the response [30,31], and also because no other examples show that phyA functions in a R/FR reversible manner in dark-grown seedlings. Although phyA could function in a R/FR-reversible manner under the condition in which the bulk amount of light-labile phyA has disappeared [34], the data presented by Stowe-Evans et al. might not justify the above conclusion. In their study, the R/FR reversibility test was conducted only with wildtype seedlings. Although the effect of R was reversed almost entirely by FR to the control level, the control seedlings were necessarily irradiated with blue light (for phototropic stimulation), which could have induced the phyA-dependent very-low-fluence response. Lariguet and Fankhauser [28] suggested that the phytochrome-mediated enhancement of phototropism in the Arabidopsis hypocotyl is mainly caused by the phytochrome-mediated inhibition of gravitropism. There is no doubt that the strong inhibition of gravitropism found in this organ will result in an enhancement of phototropism (see above), but this does not exclude the possible involvement of the more direct mechanism discussed above. A crucial point is whether phytochrome-deficient Arabidopsis mutants show reduced or no phototropic curvature from the beginning. Because gravitropism interferes with phototropic curvature after a lag of about 30 min [6], these mutants will initially show a wildtype level of phototropic curvature if gravitropism inhibition is the primary cause of phototropism enhancement. The phytochrome-deficient mutants of Arabidopsis [30] and tomato [32] did not show any such curvature. Current Opinion in Plant Biology 2006, 9:89–93
92 Commentary
With regard to the regulation of time-dependent phototropism by phytochrome, two additional points deserve a mention. First, phytochrome is likely to act on the process that underlies the time-dependent feature of phototropism [6]. Second, phytochrome activation begins to establish phototropic responsiveness after a lag of about 10 min [29]. It is likely that the phytochrome action involves the expression of one or more genes that are needed for timedependent phototropism. The fluence rate–response curves for the phototropism of continuously stimulated seedling shoots span a wide range of fluence rates [18,19,35]. In Arabidopsis, phot1 is sufficient to generate nearly the entire fluence rate– response curve [35]. These results suggest that the photoreceptor system for phototropism, at least the one based on phot1, involves a sensory adaptation mechanism. The major pulse-induced phototropism (the so-called first positive curvature) of grass coleoptiles is desensitized by phytochrome, and also in response to blue light [6]. As shown for maize coleoptiles, phytochrome-mediated desensitization progresses slowly over a period of 2 h, whereas blue-light-induced desensitization occurs immediately [36–38]. Although the causal relationship between pulse-induced phototropism and time-dependent phototropism remains to be elucidated [6], these results suggest that phytochrome and a blue-light-absorbing photoreceptor mediate adaptation with different kinetics (i.e. slow adaptation by phytochrome and rapid adaptation by a blue-light-absorbing photoreceptor). Whippo and Hangarter [39] used cryptochrome- and phototropin-deficient Arabidopsis hypocotyls to investigate the time courses of phototropic responses to continuous stimulation at different fluence rates. If any one of the mutated photoreceptors were involved in sensory adaptation, then it would be expected that its absence would result in a narrower fluence rate–response curve. The reported data do not indicate that the cryptochromes (cry1 and cry2) or phot2 mediate the sensory adaptation. Whether or not phot1 (i.e. the major photoreceptor of phototropism itself) is involved in the adaptation cannot be resolved by using the phot1-deficient mutant. Whippo and Hangarter [39] did find, however, that a high fluence rate of blue light causes a substantially delayed phototropic curvature, and that this curvature response is enhanced in the cry1 cry2 double mutant. This delayed curvature might be the result of slow adaptation. A possible explanation is that phytochrome mediates this adaptation and cryptochrome has a negative effect on this mediation. The phototropic fluence rate–response curve obtained by Galland [19] for oat coleoptiles spanned over a much wider range of fluence rates than that obtained by Neumann and Iino [18] for rice coleoptiles. The extension of Current Opinion in Plant Biology 2006, 9:89–93
the curve occurred toward lower fluence rates. Galland [40] also showed that the shape of the fluence rate– response curve changes with stimulation time. Many possible reasons can be suggested for the difference between the fluence rate–response curve of Galland and that of Neumann and Iino. Among them is the difference in growth conditions. For phototropic stimulation, Neumann and Iino used R-grown seedlings, whereas Galland used seedlings that had been grown under white light until phototropic stimulation. The blue-light component of white light might have made the seedlings more sensitive and adaptive to phototropic stimulus. Further investigation with blue-light-grown seedlings might provide useful information.
Conclusions Higher plants use tropisms to establish their body architecture and to achieve adaptive growth movements. Upward orientation of shoots and downward orientation of roots, which represent the basic body architecture, are established in response to gravity. It is suggested here that, in addition to gravitropism, the mechanism of autostraightening contributes to the maintenance of stable organ orientation under an upright stationary condition. The body architecture that is established in response to gravity is modified by other tropisms. When such a tropism is induced, it is counteracted by gravitropism that is initiated as a consequence of the induced curvature, and the balance between the two tropisms determines the organ orientation. In fact, it appears that plants specifically control this balance, as depicted by the following two examples, to achieve adaptive growth movements. First, the roots of Arabidopsis and radish show greater hydrotropism by degrading columella amyloplasts and thereby reducing gravitropic responsiveness. Water deficiency is a probable cause of amyloplast degradation. Second, the gravitropic responsiveness of Arabidopsis hypocotyls is greatly inhibited by the action of phytochrome and, as a consequence of this response, the growth direction under directional light stimulus is almost entirely determined by phototropism. This type of regulatory mechanism, which has not been found in other investigated plants, might be related to the rosette lifestyle of Arabidopsis. It has also become clearer that plants germinating and growing within the dark environment of the soil generally have little ability to express functional phototropism (i.e. time-dependent phototropism) and that phytochrome is used to establish phototropic responsiveness. Furthermore, it appears that phototropic signaling involves sensory adaptation mechanisms that are mediated by phytochrome and a blue-light-absorbing photoreceptor. Further investigations should clarify the response components that are involved in the photocontrol of tropisms. Such components are expected to include key players in tropic signal transduction. www.sciencedirect.com
Ecological functions of tropisms Iino 93
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