Bid. Her. (1992), 67, p p . 199-284 Printed in Great Britain
EFFECTS OF GREEN LIGHT O N BIOLOGICAL SYSTEMS BY R I C H A R D M. KLEIN Botany Department, University of Vermont, Burlington, V T 0 540j, U S A (Received 24 June 1991; revised I 3 December 1991 ; 6 March 1992; accepted 10 March 1992) CONTENTS
I . Introduction
199
11. Physics and meteorology of green light . . . . . ( I ) Solar radiation . . . . . . . . . ( 2 ) Penetration of light into water . . . . . . ( 3 ) Penetration of light into animal tissues . . . . (4) Penetration of light into plant tissues , . . . I l l . Responses of aneural animal systems ( I ) Protozoans . _ _ _ _ _ . . ( 2 ) Blood and cells . . . . . . . . . I\'. Photoreceptors controlling nerve responses , . . . V. Phototactic and phototropic movements . . . . . ( I ) Phototasis and phototrophism in the absence of visible locomotor ( 2 ) Phototasis in organisms possessing locomotor structures . \'I. Chromatic adaptation in algae , . . . . . ( I ) Phycobilin pigments . . . . . . . . ( 2 ) Chromatic adaptation . . . . . . . ( 3 ) Molecular aspects of adaptation . . . . . (4) Ecological significance of chromatic adaptation . . V I I . Vegetative growth and development in plants . . . . ( I ) Llicroorganisms ( 2 ) Non-flowering embryophytic plants (3) Gymnosperms and flowering plants V I I I . Reproductive growth and development in plants ( I ) Fungi . . . . . . . . . . ( 2 ) Flowering plants _ _ _ _ _ . . IX. Metabolism in plants _ . . . . . . . ( I ) Respiration _ _ . . . . . . . ( 2 ) Pigment synthesis ( 3 ) Photosynthesis . . . . . . (4) LIembranes , . . . . . X, Evaluation of green light photoreceptors ( I ) Carotenoids . . . . . . . ( 2 ) Flavins . . . . . . . . ( 3 ) Porphyrins and tetrapyrroles . . . . (4) Phytochrome . . . . . . . . . X I . Summary . . . . . . . . . . X I I . Acknowledgements . . . . . . . . X I I I . References . . . , . . . . . . I
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Publication of a review implies that the topic has attained sufficient maturity to warrant an attempt to integrate available research, to evaluate concepts and to develop
R. M. KLEIK
200
150 >
z W
2 100 ._ c m a,
LT
50 400
500
600
700
Wavelength ( n m )
Fig.
I.
Aleraged spectral energy distribution f o r : (1. zenith skq ; b, s u n - s k y on a horizontal plane: c. overcast s k y ; d, direct sunlight. ( F r o m Taylor & Kcrr, 1 9 4 1 . )
heuristic models. T h e timespan covered may be brief - yearly reviews are common in rapidly-moving fields or a review may be a retrospective, covering a long period of research activity. T h e topic at hand does not fit these models. Study of responses to green light is not integrated, it is certainly not mature and it is not rapidly evolving. There is probably no unifying theory binding the disparate studies into a cohesi1.e \\.hole. T h u s , one is justified in asking why there should be B review on the biological responses to green light. T h e rejoinder is provided by mountain climbers whose answer to a similar question is ‘Because it is there.’ T h e human-visible electromagnetic spectrum - light is dominated by wavelengths that fall roughly into the green range, extending from ca. joo n m in the blue-green to about 570 n m in the yellow-green (Gates, 1980). Assuming 40’ north latitude and I O O klx of combined direct sunlight and skylight, close to half the radiant flux from 390 to 720 n m as iV mP2and a quarter of the quantum flux as / t E m P 2s-l is green or greenish light. Responding to this broad wavelength band are pigments whose biological roles have been investigated for kvell over a century. Among these, the visual pigments have been examined most extensively (cf. Fein & Szutz, 1982; Applebury & Hargrave, 1986); vision will not be considered here. Photodynamic actions (Moreno, Pottier & Truscott, 1988) will also be excluded as will some other systems whose photochemistry and photobiology are well defined such as the green light absorbing, rhodopsin-related pigments of Halobacterium (Traulich e t al., 1983). T h i s review will focus on plant and animal green-light photosystems about which relatively little is known. Reports falling within the scope of the review are \videly scattered throughout the literature with virtuall>-no integration e\’en among related organisms. There is, in fact, no evidence that remotely suggests a commonality among green light responsive pigment systems, the physico-chemical mechanisms of radiation absorption or the biological responses occasioned by reception of the radiation. There are perils inherent in reviewing green-light photobiology. hZany reports, particularly those published in the early decades of this century, utilized apparatus and methods recognized today as being inadequate. Radiation sources, filters, and/or measurements of flux are suspect and quantitative, statistically-validated results are ~
~
Eflects of green light on biological systems
20I
rarely seen. Nevertheless, there is ample internal evidence that most, if not all, of these reports contain at least a core of reality and provide an interested reader with a comprehensive overview of the amazingly broad range of biological responses to green light that may serve to spark interest in the topic. I t is difficult to organize the avaiIable information. Maily organisms and many different responses have been studied and only rarely have these studies been placed into a context that is applicable to the behaviour of the organism. T h u s , this review is more of a compilation or compendium than an integrated survey. While it would have been conceptually more valuable to group green light responses by photochemical categories, the paucity of information on the chemical nature of most of the photoreceptor pigments precluded such an organization. Hence the use of a response approach, e.g. phototaxis, growth and development, etc. Only with additional research, will a more satisfying review be possible. 11. PHYSICS AND METEOROLOGY OF GREEN LIGHT
( I ) Solar radiation
Solar radiation has a spectral distribution that closely follows Planck's Law where :
i,h
=
217hc2 h5[exp (hc/hK,)-']
'
Maximum spectral emittance is at 480 n m for a 6000 K source, the approximate radiant temperature of the sun's surface (Gates, 1965). T h e average colour temperature of direct, unimpeded sunlight is about 5800 K in midsummer and ca. 5500 K in winter. Diffuse radiation increases the colour temperature to 6500 K and overcast skylight raises the temperature to 6950 K (Fig. I ) . North skylight temperatures are a 10000K with no significant change in the spectral energy distribution between 520 and 600 n m (Taylor & Kerr, 1941). Solar radiation is extensively filtered before reaching the earth's surface. As are other wavelengths, green wavelengths are attenuated by Rayleigh and Mie scattering (Taylor & Kerr, 1941). T h e spectral energy distribution varies with solar angle, time of the year, air mass (the ratio of slant path of solar light to vertical path length through the atmosphere) (Fig. 2) and atmospheric clarity as affected by cloud cover, smoke, water vapour content and elevation (Fig. 3 ) . Radiant flux may vary by a factor of 10 with changes in ambient conditions, but shapes of the curves remain qualitatively similar (Smith, 1982, 1986). Midsummer irradiances on cloudless days range from 20 to 30 mJ m-' (500-700 cal-') as a function of solar elevation and atmospheric transparency (Ross, I 975). I n the photosynthetically active radiation (PAR) range (400-700 nm), direct radiation is close to 40 0 4 of the total, and is reduced by half on a fully overcast day (Ross, 1975). Green wavelengths are usually scattered less than either red or blue, although this depends on solar angle and the sizes and distribution of scattering particles (Taylor & Kerr, 1941). (2)
Penetration of light into water
T h e distribution of various wavelengths as light penetrates into water has been extensively analysed. Molecular scattering by dissolved salts follows Rayleigh scattering, i.e. is proportional to the wavelength raised to the power of -4 (Morel,
R. >I. KLEIN
202 I
1.5
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1 .o
E E
3 0.5
I
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400
1 P'ig.
2.
I
500 600 700 Wavelength (nrn)
8C
Spectral energ? d i s t r i b u t i o n of full, dircct solar irradiation as a f u n c t i o n o f air mass.
5000
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(111 :I
Iiorimiitiil
siirl;i, haemoglobin, reducing internal transmittance of green Lvavelengths (Fig. 8). In mammals, attention has focused on reflectance of skin and penetration into the brain. Rallowitz & Avery ( I 970) reported that skin reflectance, proceeding from 3 5 0 nm in the near-U\' (U\--4) to the far red at 700 n m , shoiied a peak betkveen 490 and 5 2 0 nm. T h e reflectance curve was similar in lightly and head!- pigmented skins except that in heavily melanized skins the reflection peak was at or belo\\ 490 nm. Infants reflect less radiation in the 460-600 n m band for reasons not understood. Hardy, Hammel & Nlurgatroyd (1956) found a light scattering peak in human skin at .joo nm due to the presence of pigment granules. Penetration into internal organs or muscle has rcceived little attention, although it is assumcd that littlc light is pi- nt in the internal organs. T h i s may not be true for the abdomen area; light reaching a foetus ma?- have still unknown effects. Of particular medical interest is the penetration of light into mammalian brains \\.here the pineal contains photoreceptors with absorption peaks in the j2.j-56-j rim range (Ganong et a l . , 1963; Hartwig & Baumann, 1974; Eldred & S o l t e , 1978). Van ljrunt rt a / . (1964) and Viggian, Giesla & Kusso (1968) found that rat skulls transmit
EfSects of green light on biological systems
207
Table 2 . Effect on canopy shade on percentage distribution of wavelength bands of visible radiation at the soil surface beneath the canopy. After Smith (1986) Photon flux as percent of totdl flux
Photon
nux .+oo-800 n m
Sunlight dboxe canopx Sunlight a t soil surface
I
700 60
-
~ O O - ~ OnOm
21 l'o 0
04 i ) o
--
500-600
~~~~~
nm
0 Ij
600-700 nm
26 ' c j
26 u\\ substance (gelhstom a nd its contribution t n the attenuation of pliotos~ntlicticall~ active radiation in some inland and coastal southeastern Australian waters. Atrstrultnn Jozirnnl of M n r i n e und Frcslizcntrr Research 27,6 I 3 I . K I R K .J . 'I' 0 . ( I 9x3). Light and Photos~~rrthesis in Aquatic ~ ~ c o s y s t e ~ rCambridge rs. Ynil-ersity 1'1-ess, 1\lelhnurnc K I R KM , .11. b K I R K D. , L. ( r g 8 j ) . Translational regulation of protein synthesis in response to llght, at a critical stage of 1701?~o.vdevelopment. ('el/ 41,419-428. KITIVOTO,Y., SL~ ~ ' I c'4. I , b Fr Rl-KA\vA, S. (1972). An action spectrum for light-induced primordium formation in :I basidiom) cetr. /'m.olns nrcitlaviirs (Fr.) Ames. f'lont Physiologv 49,338 340. Kt\-ok[.&[{.-\,-F., FTJ I T A , Y.,H A T I W HAI ,. b W.i I ' A S X I W , .A, (1960). Heterotrophic culture 0 1 21 blue-green alga, Trilypothrr\ tenitis. JozrInal of IIT(:HEI.I., B. G . & KIEFER, L). A. (1984). Photoadaptation in marine phytoplankton. Changes in spectral absorption and excitation of chlorophyll a fluorescence. Plant Physiology 76, 508 524.
NE\\ 11.~5, I . X. (1974). Electric responses of oats to phytochrome transformation. In Mechanisms of Regulation uf Plnnt Growth (cd. R. I,. Hieleski, A . R. Fergeson and 3%.XI. Cresswell), pp. 35 j -360, Bulletin 1 2 , Royal Society of New Zealand, \Vellington. NLXTON,J . E. & BIACKRIAN, G . E. (1970). T h e penetration of solar radiation through leaf canopies of different structures. Annals of Botan-v 34, 320-318. NI(.HOI.S,K. E. & BO(:OR.AD, L. (1962). Action spectrum studies of phycocyanin formation in a mutant of (’ynnidinm caldarium. Botanical Gazette 124,85-93. N I E S ~I).,, REISSER, \\’. & ~VIESSNER, W. (1982). Photobehaviour of Paramecium bursaria infected with different symbiotic and aposymbiotic species of Chlorella. Planta 156,47j-480. Noc:cr.r;, G. K. & FRITZ, G. J . (1976). Introductory Plant Physiology, 2nd edn. Prentice-Hall Publishing Co., Engel\zood Cliffs, New Jersey. NOHXI.AY, c‘. Sr Gni.i>iiERc, E. ( 1 9 ; ~ ) .Effect of light on motility, life span and respiration o f bovine spermatozoa. Science 130,Ozo~~Oz5 NOHMAS, C . , GOIJUERC,,E. & I’ORTERI:IEI.~, I. D. (1962). T h e effect of visible radiation on the functional life-span of mammalian and avian spermatozoa. Experimental C e l l Research 28, 69-84. X O K I I ILV. , J . & PASI[X,C. F. A. (1958). Sensitivity to light in the sea anemone ,\/letridium senile L.: adaptation and action spectrum. Proceedings of the Royal Society of L,ondon B 148,385-396. NORTOY, T. .I.. MC.~I.I.ISTFR, H. .I.,CON\~.AY, E. & IRVINE, L. X I . (1969). T h e marine algae of the Hebridean island o f Colonsay. British Journal of Phycology 4, 125 136. NII.TS(.H, \V. ( 1 9 7 1 ) .Phototactic and photokinetic action spectra of the diatom Nitzschia conrmunis. Photochenzistrj, cmd Photobiology 14,705-71 2 . NI-IT W H , \V. (1974). Der Einfluss des Lichts auf Bewegung phototropher Mikroorganismen. I . Photokinesis. Abhandlung von den Marburger Gelehrtner Gesellschaft, Jahrgang 1972 2, 143-2 I 3. NI-I,TSCH,\V. ( I 97 j ) . Phototaxis and photokinesis. In Primitive Sensor-v and Communication Systems (ed. X I . J . Carlile), pp. 29 90. Academic Press, London. N r I.TSCCI, LV. (198;). Photosensing in cyanobacteria. In Sensory Perception and Transduction in Aneural Organisms (ed. G. Colomhetti, F. Lenci and P.-S. Song), pp. 147-164. Plenum Press, New York. N ~ . i . s c . ~ i\V. , & HADER,D.-P. (1980). Light perceptions and sensory transduction in photosynthetic prokaryotes. I n Structure and Bonding. Volume 4 1 , Molecular Structure and Sensory Physiology (ed. P. Hemmerich), pp. I I I 139. Springer Verlag, Berlin. NYI-TSCH, \V. & II.XDER, D . - P . (1988). Photomovements in motile microorganisms. 11. Photochemistry and Photohiology 47,837--86g. NI-I.TWH,\V., S(.HIWART, \V. & I-Iiir.r., > I . ( I 979). Investigations on the phototactic orientation of Anabaena wriabilrs. Archires of Microbiology 122,8;-9 I . N ~ - I . T S C \V. H , & HCI.I.M.ANN, W. (1972). Untersuchungen zum Photokinese von Anabaena i.wriabilis Kutzing. A r d i k f i i r .2likrobio/o~ie82, 76-90. Nt ILIM’I~, I!., S(.irL( ‘ H A K ’ I , H. & DII.LESUERGER, >!I(1979). . Photomovement of the red alga Porpliyiidinm cruentum (Ag.) Naegeli. 1. Photokinesis. Archi7~esof Microbiology 122,207-21 2 . Nr.i:rscti, IT.,SCHLCHAKI., H . & K o e ~ i c F. , (1983). Effects of sodium azide on phototaxis of the blue-green alga ;lnuhncnn 7.~ri(ihi/isand consequences to the two-photoreceptor-system-hypothesis. A r c h i w s of Microbiology 134, 3 3 - 3 7 .
N I - Inew, !I-., T m w A i , G . Sr RIRIOCHA, I . (1971). Phototaktische untersuchungen an Chlaniydonzonas reinhardtii Dangeard in homokontinuierlicher kultur. Arkiz fiir Mikrohiologie 80, 3 j I 369. NII.TS(-H, \V. & RICHTER, G . (1963). Aktionsspectrum des photosynthetischen “CO,-Einbau \ o n Phownidium rincinatum. i l r k i r .fiir Il.likrobiologie 47,207- 21 3. O’HENAR, J . 1). & ~I.ATSZ.RIOTO, Y. (1976). Light-induced neural activity and musclc contraction in the marine orm Golfiryicc grncldii. Cornparatire Biochemistry and Physiology 5 5 A , 77-8 I . Orrwuovi, S. ( i c l q i ) . Molecular basis for navelength fluence rate and daylength sensing b y plants. Journal qf Photochemistvy and Photobiolog). B 9 , 237 239. 0 ~ 1 . 1 i 1 1 i . i . R., ~ ~ . 1 ~
Eflects of green light on biological systems
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OHAD,I . , SCHNEIDER, H. J. A. W., GENDEL, S. & BOGORAD, L . (1980).Light-induced changes in allophycocyanin. Plant Physiology 65,6-12. O’HEOCHA, C. (1965). Phycobilins. In Chemistry and Biochemistry of Plant Pigments (ed. T. W. Goodwin), pp. 175-196. Academic Press, London. O’HEOCHA,C. & RAFFERTY, M. ( I 959). Phycoerythrins and phycocyanins of cryptomonads. Nature 184, 1049- 1 0 5 0 . OKHI,K. & FUJITA, Y. (1979a). Photoreversible absorption changes of guanidine-HCI-treated phycocyanin and allophycocyanin isolated from the blue-green alga Tolypothrix tenuis. Plant and Cell Physiology 20, 483-490. OKHI,K. & FUJITA, Y . (1979b). In aico transformation of phycobiliprotein during photobleaching of Tolypothrix tenuis in forms active in photoreversible absorption changes. Plant and Cell Physiology 20, 1341-1347. OKAGAMI, N. & KAWAI,M. (1977). Dormancy in Dioscorea. Gibberellin-inhibitors or promoters in seed germination of D . tokoro and D . tenuipes in relation to light quality. Plant Physiology 60,360-362. OKAYAMA, S. & BUTLER, W. L . (1972). Extraction and reconstitution of photosystem 11. Plant Physiology 49. 769-774. O’KELLY, J . C. & HARDMAN, J. K. (1977).A blue light reaction involving flavin nucleotides and plastocyanin from Protosiphon botryoides. Photochemistry and Photobiology 25, 559-564. OLTMANS, F. (1892).ii‘ber die kultur- und lebensbedingungen der Meeresalgen. Jarhbucherfur Wissensrhaftlichen Botanik 23,349-440. ORTH,R. (1937). Zur Keimungsphysiologie der Farnsporen in verschiedenen Spektralbezerken. Jahrbucher fur Wissenschaftlichen Botanik 86,358-426. OSBORNE, B. A. & RAVEN, J. A. (1986). LIght absorption by plants and its implications for photosynthesis. Biological Reviews 61,1-6 I . OSTER,G., BELLIN, J . S. & HOLMSTROM, B. (1962). Photochemistry of riboflavin. Experientia 18,249-253. PAGE,R. M. (1962). Light and the asexual reproduction of Pilobolus. Science 138, 1238-1245. PAGE,R. M. & BRUNGARD, J. ( 1 9 6 1 ) .Phototropism in Conidiobolus, some preliminary observations. Science 134. 733-734. PEARCY, R.W. (1988).Photosynthetic utilization of light flecks by understory plants. In Ecology of Photosynthesis in Sun and Shade (ed. S . von Cammerer and W. W. Adams), pp. 223-238. CSIRO, Melbourne. G. I . (1966). T h e reflection of visible radiation from leaves of some western Australian species. PEARMAN, Australian Journal of Biological Sciences 19,97-103. POFF, K. L. & BUTLER,W. L. (1974). Spectral characteristics of the photoreceptor pigment of phototaxis in Dictylostelium discoideum. Photochemistry and Photobiology 20, 24 1-244. POFF, K. L. & BUTLER,W. L. (1975). Spectral characterization of the photoreducible b-type cytochrome of Dictylostelium discoideum. Plant Physiology 55, 427-429. POFF, K. L. & HADER,D.-P. (1984). An action spectrum for phototaxis by pseudoplasmodia of Dictylostelium discoideum. Photochemistry and Photobiology 39,433-436. POFF, K. L. & LOOMIS,W. F. JR. (1973). Control of phototactic migration in Dictylostelium discoideum. Experimental Cell Research 82, 236-240. POFF,K. L . & WHITAKER, B. D. (1979).Movement of slime molds. In Physiology of Movement (ed. W. Haupt and M. E. Feinleib), pp. 355-382. Springer-Verlag, Berlin. W. L. & LOOMIS, W. F. JR. (1973). Light-induced absorbance changes associated with POFF, K. J., BUTLER, Dhototaxis in Dictylostelium. Proceedings of the National Academy of Sciences of the United States of America 70, 8 13-816. POFF,K. L., LOOMIS, W. F. JR. & BUTLER, W. L. (1974). Isolation and purification of the photoreceptor pigment associated with phototaxis in Dictylostelium discoideum. Journal of Biological Chemistry 249,2 1 64-2 167. PORTER, C. L. & BOCKSTABLER, H. W. (1929). Concerning the reaction of certain fungi to various wavelengths of light. Proceedings of the Indiana Academy of Sciences 38, 133-135. PRATT,L. H. & BRIGGS, W. R. (1966). Photochemical and nonphotochemical reactions of phytochrome in vitro. Plant Physiology 41,467-474. PREZELN, B. B. & HAXO,F. T. (1976). Purification and characterization of peridinin-chlorophyll a-protein from the marine dinoflagellates Glenodinium sp. and Gonyaulax polyedra. Planta 128,133-141. PRUSTI, R. K., SONG,P.-S., HADER,D.-P. & HADER,M. (1984). Caffeine-enhanced photomovement in the ciliate Stentor coerula. Photochemistry and Photobiology 40,369-375. PURVIS, J. E. & WARWICK, G. R. (1908). The influence of spectral colours on the sporulation of Saccharyomyces. Proceedings of the Cambridge Philosophical Society 14,30-40. RACUSEN, R.& MILLER,K. (1972).Phytochrome-induced adhesion of mung bean root tips to platinum electrodes in a direct current field. Plant Physiology 49, 654-655. B. ( 1 9 7 s ) . Role of membrane-bound, fixed-charge changes in phytochromeRACUSEN, R. H. & ETHERTON, mediated mung bean root tip adherance phenomenon. Plant Physiology 5 5 , 49 1-495.
278
R. M.KLEIN
I
EFFECTS OF GREEN LIGHT O N BIOLOGICAL SYSTEMS BY R I C H A R D M. KLEIN Botany Department, University of Vermont, Burlington, V T 0 540j, U S A (Received 24 June 1991; revised I 3 December 1991 ; 6 March 1992; accepted 10 March 1992) CONTENTS
I . Introduction
199
11. Physics and meteorology of green light . . . . . ( I ) Solar radiation . . . . . . . . . ( 2 ) Penetration of light into water . . . . . . ( 3 ) Penetration of light into animal tissues . . . . (4) Penetration of light into plant tissues , . . . I l l . Responses of aneural animal systems ( I ) Protozoans . _ _ _ _ _ . . ( 2 ) Blood and cells . . . . . . . . . I\'. Photoreceptors controlling nerve responses , . . . V. Phototactic and phototropic movements . . . . . ( I ) Phototasis and phototrophism in the absence of visible locomotor ( 2 ) Phototasis in organisms possessing locomotor structures . \'I. Chromatic adaptation in algae , . . . . . ( I ) Phycobilin pigments . . . . . . . . ( 2 ) Chromatic adaptation . . . . . . . ( 3 ) Molecular aspects of adaptation . . . . . (4) Ecological significance of chromatic adaptation . . V I I . Vegetative growth and development in plants . . . . ( I ) Llicroorganisms ( 2 ) Non-flowering embryophytic plants (3) Gymnosperms and flowering plants V I I I . Reproductive growth and development in plants ( I ) Fungi . . . . . . . . . . ( 2 ) Flowering plants _ _ _ _ _ . . IX. Metabolism in plants _ . . . . . . . ( I ) Respiration _ _ . . . . . . . ( 2 ) Pigment synthesis ( 3 ) Photosynthesis . . . . . . (4) LIembranes , . . . . . X, Evaluation of green light photoreceptors ( I ) Carotenoids . . . . . . . ( 2 ) Flavins . . . . . . . . ( 3 ) Porphyrins and tetrapyrroles . . . . (4) Phytochrome . . . . . . . . . X I . Summary . . . . . . . . . . X I I . Acknowledgements . . . . . . . . X I I I . References . . . , . . . . . . I
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243 245 245
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248 248 250 25 1 252
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256 259 262
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262
I. I N T R O D U C T I O N
Publication of a review implies that the topic has attained sufficient maturity to warrant an attempt to integrate available research, to evaluate concepts and to develop
R. M. KLEIK
200
150 >
z W
2 100 ._ c m a,
LT
50 400
500
600
700
Wavelength ( n m )
Fig.
I.
Aleraged spectral energy distribution f o r : (1. zenith skq ; b, s u n - s k y on a horizontal plane: c. overcast s k y ; d, direct sunlight. ( F r o m Taylor & Kcrr, 1 9 4 1 . )
heuristic models. T h e timespan covered may be brief - yearly reviews are common in rapidly-moving fields or a review may be a retrospective, covering a long period of research activity. T h e topic at hand does not fit these models. Study of responses to green light is not integrated, it is certainly not mature and it is not rapidly evolving. There is probably no unifying theory binding the disparate studies into a cohesi1.e \\.hole. T h u s , one is justified in asking why there should be B review on the biological responses to green light. T h e rejoinder is provided by mountain climbers whose answer to a similar question is ‘Because it is there.’ T h e human-visible electromagnetic spectrum - light is dominated by wavelengths that fall roughly into the green range, extending from ca. joo n m in the blue-green to about 570 n m in the yellow-green (Gates, 1980). Assuming 40’ north latitude and I O O klx of combined direct sunlight and skylight, close to half the radiant flux from 390 to 720 n m as iV mP2and a quarter of the quantum flux as / t E m P 2s-l is green or greenish light. Responding to this broad wavelength band are pigments whose biological roles have been investigated for kvell over a century. Among these, the visual pigments have been examined most extensively (cf. Fein & Szutz, 1982; Applebury & Hargrave, 1986); vision will not be considered here. Photodynamic actions (Moreno, Pottier & Truscott, 1988) will also be excluded as will some other systems whose photochemistry and photobiology are well defined such as the green light absorbing, rhodopsin-related pigments of Halobacterium (Traulich e t al., 1983). T h i s review will focus on plant and animal green-light photosystems about which relatively little is known. Reports falling within the scope of the review are \videly scattered throughout the literature with virtuall>-no integration e\’en among related organisms. There is, in fact, no evidence that remotely suggests a commonality among green light responsive pigment systems, the physico-chemical mechanisms of radiation absorption or the biological responses occasioned by reception of the radiation. There are perils inherent in reviewing green-light photobiology. hZany reports, particularly those published in the early decades of this century, utilized apparatus and methods recognized today as being inadequate. Radiation sources, filters, and/or measurements of flux are suspect and quantitative, statistically-validated results are ~
~
Eflects of green light on biological systems
20I
rarely seen. Nevertheless, there is ample internal evidence that most, if not all, of these reports contain at least a core of reality and provide an interested reader with a comprehensive overview of the amazingly broad range of biological responses to green light that may serve to spark interest in the topic. I t is difficult to organize the avaiIable information. Maily organisms and many different responses have been studied and only rarely have these studies been placed into a context that is applicable to the behaviour of the organism. T h u s , this review is more of a compilation or compendium than an integrated survey. While it would have been conceptually more valuable to group green light responses by photochemical categories, the paucity of information on the chemical nature of most of the photoreceptor pigments precluded such an organization. Hence the use of a response approach, e.g. phototaxis, growth and development, etc. Only with additional research, will a more satisfying review be possible. 11. PHYSICS AND METEOROLOGY OF GREEN LIGHT
( I ) Solar radiation
Solar radiation has a spectral distribution that closely follows Planck's Law where :
i,h
=
217hc2 h5[exp (hc/hK,)-']
'
Maximum spectral emittance is at 480 n m for a 6000 K source, the approximate radiant temperature of the sun's surface (Gates, 1965). T h e average colour temperature of direct, unimpeded sunlight is about 5800 K in midsummer and ca. 5500 K in winter. Diffuse radiation increases the colour temperature to 6500 K and overcast skylight raises the temperature to 6950 K (Fig. I ) . North skylight temperatures are a 10000K with no significant change in the spectral energy distribution between 520 and 600 n m (Taylor & Kerr, 1941). Solar radiation is extensively filtered before reaching the earth's surface. As are other wavelengths, green wavelengths are attenuated by Rayleigh and Mie scattering (Taylor & Kerr, 1941). T h e spectral energy distribution varies with solar angle, time of the year, air mass (the ratio of slant path of solar light to vertical path length through the atmosphere) (Fig. 2) and atmospheric clarity as affected by cloud cover, smoke, water vapour content and elevation (Fig. 3 ) . Radiant flux may vary by a factor of 10 with changes in ambient conditions, but shapes of the curves remain qualitatively similar (Smith, 1982, 1986). Midsummer irradiances on cloudless days range from 20 to 30 mJ m-' (500-700 cal-') as a function of solar elevation and atmospheric transparency (Ross, I 975). I n the photosynthetically active radiation (PAR) range (400-700 nm), direct radiation is close to 40 0 4 of the total, and is reduced by half on a fully overcast day (Ross, 1975). Green wavelengths are usually scattered less than either red or blue, although this depends on solar angle and the sizes and distribution of scattering particles (Taylor & Kerr, 1941). (2)
Penetration of light into water
T h e distribution of various wavelengths as light penetrates into water has been extensively analysed. Molecular scattering by dissolved salts follows Rayleigh scattering, i.e. is proportional to the wavelength raised to the power of -4 (Morel,
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3 0.5
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L
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I
500 600 700 Wavelength (nrn)
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Spectral energ? d i s t r i b u t i o n of full, dircct solar irradiation as a f u n c t i o n o f air mass.
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siirl;i, haemoglobin, reducing internal transmittance of green Lvavelengths (Fig. 8). In mammals, attention has focused on reflectance of skin and penetration into the brain. Rallowitz & Avery ( I 970) reported that skin reflectance, proceeding from 3 5 0 nm in the near-U\' (U\--4) to the far red at 700 n m , shoiied a peak betkveen 490 and 5 2 0 nm. T h e reflectance curve was similar in lightly and head!- pigmented skins except that in heavily melanized skins the reflection peak was at or belo\\ 490 nm. Infants reflect less radiation in the 460-600 n m band for reasons not understood. Hardy, Hammel & Nlurgatroyd (1956) found a light scattering peak in human skin at .joo nm due to the presence of pigment granules. Penetration into internal organs or muscle has rcceived little attention, although it is assumcd that littlc light is pi- nt in the internal organs. T h i s may not be true for the abdomen area; light reaching a foetus ma?- have still unknown effects. Of particular medical interest is the penetration of light into mammalian brains \\.here the pineal contains photoreceptors with absorption peaks in the j2.j-56-j rim range (Ganong et a l . , 1963; Hartwig & Baumann, 1974; Eldred & S o l t e , 1978). Van ljrunt rt a / . (1964) and Viggian, Giesla & Kusso (1968) found that rat skulls transmit
EfSects of green light on biological systems
207
Table 2 . Effect on canopy shade on percentage distribution of wavelength bands of visible radiation at the soil surface beneath the canopy. After Smith (1986) Photon flux as percent of totdl flux
Photon
nux .+oo-800 n m
Sunlight dboxe canopx Sunlight a t soil surface
I
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-
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--
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26 u\\ substance (gelhstom a nd its contribution t n the attenuation of pliotos~ntlicticall~ active radiation in some inland and coastal southeastern Australian waters. Atrstrultnn Jozirnnl of M n r i n e und Frcslizcntrr Research 27,6 I 3 I . K I R K .J . 'I' 0 . ( I 9x3). Light and Photos~~rrthesis in Aquatic ~ ~ c o s y s t e ~ rCambridge rs. Ynil-ersity 1'1-ess, 1\lelhnurnc K I R KM , .11. b K I R K D. , L. ( r g 8 j ) . Translational regulation of protein synthesis in response to llght, at a critical stage of 1701?~o.vdevelopment. ('el/ 41,419-428. KITIVOTO,Y., SL~ ~ ' I c'4. I , b Fr Rl-KA\vA, S. (1972). An action spectrum for light-induced primordium formation in :I basidiom) cetr. /'m.olns nrcitlaviirs (Fr.) Ames. f'lont Physiologv 49,338 340. Kt\-ok[.&[{.-\,-F., FTJ I T A , Y.,H A T I W HAI ,. b W.i I ' A S X I W , .A, (1960). Heterotrophic culture 0 1 21 blue-green alga, Trilypothrr\ tenitis. JozrInal of IIT(:HEI.I., B. G . & KIEFER, L). A. (1984). Photoadaptation in marine phytoplankton. Changes in spectral absorption and excitation of chlorophyll a fluorescence. Plant Physiology 76, 508 524.
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