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Photomorphogenesis—a term designating photoregulation or photocontrol by plants
J. Photo&em,
Photobiol. B: Bid.,
11 (1991)
377
377-382
News and Views
Photomorphogenesis - a term designating photocontrol by plants
photoregulation
or
Sneiana Obrenovii: Institute for Biolugicd (yilgoslavia..
Research
“Sini..fa Stankovic,
29. nmembm
142, 11060 Belgrade
The list of photobiological disciplines adopted by both the European [ 1] and American [2] Societies of Photobiology includes the term photo-
morphogenesis, which is also used at the annual European meetings and in books concerning the regulation of various processes in plants by light. The term was introduced soon after the discovery of phytochrome, the only known pigment with features matching those of a photoreceptor in plants [3]. The discovery was made using photoresponses involving visible morphogenic changes such as flowering [ 41, stem elongation [ 5 ] and germination [6]. However, the 6rst physiological localization of phytochrome was investigated in the chloroplast movement of an alga (Mougeotia) [ 71, a response not related to any morphogenic change. The synthesis of various pigments, such as anthocyanin [ 8 1, betacyanin [91 and chlorophyll [ 10 ], which is controlled by phytochrome, also does not refer to a change in shape of either cells or organs and thus cannot be designated as a morphogenic response. In addition, the regulation of stomatal opening by phytochrome [ 111 relates to a distinct physiological process -transpiration-while the light-dependent movement of leaves in mimosas and some other plants [12] is a nastic motion quite distinct from growth-mediated tropisms. Both kinds of responses to light involve changes in turgor pressure, and both belong to the class of photoperiodic phenomena which, although initially defined in developmental responses, such as flowering, were also discovered in the photoperiodic control of CAM and C4 metabolism in plants living in arid regions [ 131. Thus, a number of phytochrome-regulated phenomena of plants cannot be designated as morphogenic responses, and thus remain outside the term photomorphogenesis. The above-mentioned problems concern the subject of the scientific discipline called photomorphogenesis. The ambiguity of the general subject is also problematic because the term morphogenesis refers to animals as well. Some developmental stages in animals may be influenced by light and thus represent a subject of photomorphogenesis, although the people working in this field limit the meaning of the term to plants and fungi. The term morphogenesis implies a descriptive approach to developmental processes Elsevier Sequoia, Lausanne
378
NEWS AND VIEWS
like histogenesis, organogenesis, plastochrone etc., whereas the underlying regulatory mechanisms belong to the physiology or molecular biology of development, which implies a functional approach. The crucial physiological problems in plant morphogenesis concern the roles and mechanisms of action of the plant growth substances which, with high probability, mediate the action of light (phytochrome) in the regulation of plant growth and development. However, the same responses are controlled by temperature and humidity as well, also involving plant growth substances, but there has been no attempt to date to designate research into these problems by the terms thermomorphogenesis or hygromorphogenesis. The crucial problems in so-called photomorphogenesis are the sensing of wavelength, fluence rate [ 141 and day length [ 151, which are variable but universal for all hinds of photoresponses, Le. they are not restricted to developmental processes. These phenomena can be merely described, with only a speculative attempt at explanation, thus matching the approach of morphogenesis. In contrast, a physiological approach addresses the underlying biophysical (photophysical) and biochemical mechanisms of these phenomena, which exert similar features and occur merely during induction of the physiological and developmental processes in plants. The explanation requires a photochemical characterization of the photoreceptor(s), identification of the signal transduction components and, if possible, reconstitution of the phototransduction chain in vitro. The whole photoreceptor system appears to operate during the so-called inductive phase, controlling the engagement of subsequent regulatory mechanisms (plant growth substances) or in direct regulation of some cellular functions. Consequently, the most appropriate term to designate the discipline concerned with these general problems would be photocontrol and/or photoregulation by plants, which was originally and intuitively used by the authors of phytochrome discovery [ 3 ]. The same holds for the analogous phenomena occurring in fungi, which are controlled by other photoreceptors. Therefore, I would suggest to the European Society for Photobiology that it should adopt this new terminology for the sake of clarity and scientific exactness. The 40-year long research into this field cannot be a reason for the unquestioning use of confusing and inadequate terms just because they are “traditional” or “classic” , particularly because, in the meantime, the units used in photobiology research have been changed several times with the aim of ilnding those which are most exact. 1 Photo&em. Ph&obioL, 52 (1990). 2 J. Photo&em. PhotobioL, B: BioL, 1 (1987). 3 W. L. Butler, S. B. Hendricks and H. W. Siegelman, Action spectra of phytochrome in vitro, Photochmn. PhotobioL, 3 (1964) 621-528. 4 H. A. Borthwick, S. B. Hendricks and M. W. Parker, Action spectrum for the control of flowering in winter barley, a long day plant, Am. J. Bot., 34 (1947) 598. 6 H. A. Borthwick, S. B. Hendricks and M. W. Parker, Action spectrum for inhibition of stem growth in dark-grown seedlings of albino and nonalbino barley (Hordeurn vuIgure~, Bot. Guz., 223 (1951) 96-106.
379
NEWS AND VIEWS
6 H. A. Borthwick, S. B. Hendricks, E. H. Toole and V. K. Toole, Action-of light on lettuceseed germination, Bot. Gaz, 115 (1954) 205-225. 7 W. Haupt, Die Chloroplastendrehung bei Mougeotia. II. Die Induktion der Schwachlichtbewegung durch linear polarisiertes Licht, Planta, 55 (1960) 465-479. 8 S. B. Hendricks and H. A. Borthwick, Photocontrol of plant development by the simultaneous excitation of two interconvertible pigments. II: Theory and control of anthocyanln synthesis. Bot. Gaz., 102 (1959) 187-193. 9 K.-H. Kohler, Die Steuerung der Amamnthinbiosynthese durch das Phytochromsystem, Biol. Zentralbl., 92 (1973) 307-336. 10 H. Virgin, Action spectrum for the elimination of the lag phase in chlorophyll formation in previously dark grown leaves of wheat, Physiol. Plant., 14 (1961) 439-452. 11 H. Meidner, The comparative effects of blue and red light on the stomata of Allium cepa and Xanthium pensylvanicum, J. Exp. Bot., I9 (1968) 146-l 51. 12 A. W. GaIston, Leaf movements in Samanea. In J. D. Cosens and D. Vince-Prue (eds.), TheBiology ofPhotoreception, Cambridge University Press, Cambridge, 1983, pp. 541-560. 13 J. Brulfert, J. Vidal, E. Kreyer, M. Thomas, P. Gadal and 0. Queiroz, Phytochrome control of phosphoenolpyruvate carboxylase synthesis and specific RNA level during photoperiodic induction of a CAM plant and during greening in a C, plant, Physiol. Veg., 23 (1985) 921-928. 14 A. L. Mancinelli and I. Rabino, The “high irradiance responses” of plant photomorphogenesis, Bot. Rev., 44 (1978) 129-180. 15 D. Vince-Prue, Photoperiodi-sm in Plants, McGraw Hill, London, 1975.
Comment on “Photomorphogenesis - a term designating photoregulation or photocontrol by plants” by S. Obrenovik W. Nultsch Fachbereich Biologic-Botanik, Philipps-Universitiit W-3550 Mar&rg /Lahn (F.R. G.)
Marburg,
Lahnberge,
S. Obrenovie is certainly right when she states that light-induced chloroplast movements in Mo24.geotia, nyktinastic leaf movements of Mimosa and nastic movements of stomata are not photomorphogenic processes. However, I would also not call the latter two photoperiodic phenomena. Of course they follow the night-day change and are governed by the circadian clock, but they do so all year and do not measure the day length in order to Ilnd out the time of the year, as is the case in flowering induction which is a true photoperiodic phenomenon. I think all photobiologists will agree that not all phytochrome regulated phenomena can be regarded as photomorphoses, e.g. the phytochrome controlled attachment and detachment of root tips to wet glass surfaces (Tanada, ref. l), just as not all photomorphoses are controlled by phytochrome, but by, for example, blue light photoreceptors. However, it seems highly problematic to distinguish between descriptive and functional approaches to
Photobiol. B: Bid.,
11 (1991)
377
377-382
News and Views
Photomorphogenesis - a term designating photocontrol by plants
photoregulation
or
Sneiana Obrenovii: Institute for Biolugicd (yilgoslavia..
Research
“Sini..fa Stankovic,
29. nmembm
142, 11060 Belgrade
The list of photobiological disciplines adopted by both the European [ 1] and American [2] Societies of Photobiology includes the term photo-
morphogenesis, which is also used at the annual European meetings and in books concerning the regulation of various processes in plants by light. The term was introduced soon after the discovery of phytochrome, the only known pigment with features matching those of a photoreceptor in plants [3]. The discovery was made using photoresponses involving visible morphogenic changes such as flowering [ 41, stem elongation [ 5 ] and germination [6]. However, the 6rst physiological localization of phytochrome was investigated in the chloroplast movement of an alga (Mougeotia) [ 71, a response not related to any morphogenic change. The synthesis of various pigments, such as anthocyanin [ 8 1, betacyanin [91 and chlorophyll [ 10 ], which is controlled by phytochrome, also does not refer to a change in shape of either cells or organs and thus cannot be designated as a morphogenic response. In addition, the regulation of stomatal opening by phytochrome [ 111 relates to a distinct physiological process -transpiration-while the light-dependent movement of leaves in mimosas and some other plants [12] is a nastic motion quite distinct from growth-mediated tropisms. Both kinds of responses to light involve changes in turgor pressure, and both belong to the class of photoperiodic phenomena which, although initially defined in developmental responses, such as flowering, were also discovered in the photoperiodic control of CAM and C4 metabolism in plants living in arid regions [ 131. Thus, a number of phytochrome-regulated phenomena of plants cannot be designated as morphogenic responses, and thus remain outside the term photomorphogenesis. The above-mentioned problems concern the subject of the scientific discipline called photomorphogenesis. The ambiguity of the general subject is also problematic because the term morphogenesis refers to animals as well. Some developmental stages in animals may be influenced by light and thus represent a subject of photomorphogenesis, although the people working in this field limit the meaning of the term to plants and fungi. The term morphogenesis implies a descriptive approach to developmental processes Elsevier Sequoia, Lausanne
378
NEWS AND VIEWS
like histogenesis, organogenesis, plastochrone etc., whereas the underlying regulatory mechanisms belong to the physiology or molecular biology of development, which implies a functional approach. The crucial physiological problems in plant morphogenesis concern the roles and mechanisms of action of the plant growth substances which, with high probability, mediate the action of light (phytochrome) in the regulation of plant growth and development. However, the same responses are controlled by temperature and humidity as well, also involving plant growth substances, but there has been no attempt to date to designate research into these problems by the terms thermomorphogenesis or hygromorphogenesis. The crucial problems in so-called photomorphogenesis are the sensing of wavelength, fluence rate [ 141 and day length [ 151, which are variable but universal for all hinds of photoresponses, Le. they are not restricted to developmental processes. These phenomena can be merely described, with only a speculative attempt at explanation, thus matching the approach of morphogenesis. In contrast, a physiological approach addresses the underlying biophysical (photophysical) and biochemical mechanisms of these phenomena, which exert similar features and occur merely during induction of the physiological and developmental processes in plants. The explanation requires a photochemical characterization of the photoreceptor(s), identification of the signal transduction components and, if possible, reconstitution of the phototransduction chain in vitro. The whole photoreceptor system appears to operate during the so-called inductive phase, controlling the engagement of subsequent regulatory mechanisms (plant growth substances) or in direct regulation of some cellular functions. Consequently, the most appropriate term to designate the discipline concerned with these general problems would be photocontrol and/or photoregulation by plants, which was originally and intuitively used by the authors of phytochrome discovery [ 3 ]. The same holds for the analogous phenomena occurring in fungi, which are controlled by other photoreceptors. Therefore, I would suggest to the European Society for Photobiology that it should adopt this new terminology for the sake of clarity and scientific exactness. The 40-year long research into this field cannot be a reason for the unquestioning use of confusing and inadequate terms just because they are “traditional” or “classic” , particularly because, in the meantime, the units used in photobiology research have been changed several times with the aim of ilnding those which are most exact. 1 Photo&em. Ph&obioL, 52 (1990). 2 J. Photo&em. PhotobioL, B: BioL, 1 (1987). 3 W. L. Butler, S. B. Hendricks and H. W. Siegelman, Action spectra of phytochrome in vitro, Photochmn. PhotobioL, 3 (1964) 621-528. 4 H. A. Borthwick, S. B. Hendricks and M. W. Parker, Action spectrum for the control of flowering in winter barley, a long day plant, Am. J. Bot., 34 (1947) 598. 6 H. A. Borthwick, S. B. Hendricks and M. W. Parker, Action spectrum for inhibition of stem growth in dark-grown seedlings of albino and nonalbino barley (Hordeurn vuIgure~, Bot. Guz., 223 (1951) 96-106.
379
NEWS AND VIEWS
6 H. A. Borthwick, S. B. Hendricks, E. H. Toole and V. K. Toole, Action-of light on lettuceseed germination, Bot. Gaz, 115 (1954) 205-225. 7 W. Haupt, Die Chloroplastendrehung bei Mougeotia. II. Die Induktion der Schwachlichtbewegung durch linear polarisiertes Licht, Planta, 55 (1960) 465-479. 8 S. B. Hendricks and H. A. Borthwick, Photocontrol of plant development by the simultaneous excitation of two interconvertible pigments. II: Theory and control of anthocyanln synthesis. Bot. Gaz., 102 (1959) 187-193. 9 K.-H. Kohler, Die Steuerung der Amamnthinbiosynthese durch das Phytochromsystem, Biol. Zentralbl., 92 (1973) 307-336. 10 H. Virgin, Action spectrum for the elimination of the lag phase in chlorophyll formation in previously dark grown leaves of wheat, Physiol. Plant., 14 (1961) 439-452. 11 H. Meidner, The comparative effects of blue and red light on the stomata of Allium cepa and Xanthium pensylvanicum, J. Exp. Bot., I9 (1968) 146-l 51. 12 A. W. GaIston, Leaf movements in Samanea. In J. D. Cosens and D. Vince-Prue (eds.), TheBiology ofPhotoreception, Cambridge University Press, Cambridge, 1983, pp. 541-560. 13 J. Brulfert, J. Vidal, E. Kreyer, M. Thomas, P. Gadal and 0. Queiroz, Phytochrome control of phosphoenolpyruvate carboxylase synthesis and specific RNA level during photoperiodic induction of a CAM plant and during greening in a C, plant, Physiol. Veg., 23 (1985) 921-928. 14 A. L. Mancinelli and I. Rabino, The “high irradiance responses” of plant photomorphogenesis, Bot. Rev., 44 (1978) 129-180. 15 D. Vince-Prue, Photoperiodi-sm in Plants, McGraw Hill, London, 1975.
Comment on “Photomorphogenesis - a term designating photoregulation or photocontrol by plants” by S. Obrenovik W. Nultsch Fachbereich Biologic-Botanik, Philipps-Universitiit W-3550 Mar&rg /Lahn (F.R. G.)
Marburg,
Lahnberge,
S. Obrenovie is certainly right when she states that light-induced chloroplast movements in Mo24.geotia, nyktinastic leaf movements of Mimosa and nastic movements of stomata are not photomorphogenic processes. However, I would also not call the latter two photoperiodic phenomena. Of course they follow the night-day change and are governed by the circadian clock, but they do so all year and do not measure the day length in order to Ilnd out the time of the year, as is the case in flowering induction which is a true photoperiodic phenomenon. I think all photobiologists will agree that not all phytochrome regulated phenomena can be regarded as photomorphoses, e.g. the phytochrome controlled attachment and detachment of root tips to wet glass surfaces (Tanada, ref. l), just as not all photomorphoses are controlled by phytochrome, but by, for example, blue light photoreceptors. However, it seems highly problematic to distinguish between descriptive and functional approaches to