Biologia 65/4: 587—594, 2010 Section Botany DOI: 10.2478/s11756-010-0058-y
Chromatic adaptation in lichen phyco- and photobionts Bazyli Czeczuga, Ewa Czeczuga-Semeniuk & Adrianna Semeniuk Department of General Biology, Medical University, Kili´ nskiego 1, PL-15-089 Bialystok, Poland; e-mail:
[email protected]
Abstract: The effect of light quality on the photosynthetic pigments as chromatic adaptation in 8 species of lichens were examined. The chlorophylls, carotenoids in 5 species with green algae as phycobionts (Cladonia mitis, Hypogymnia physodes, H. tubulosa var. tubulosa and subtilis, Flavoparmelia caperata, Xanthoria parietina) and the chlorophyll a, carotenoids and phycobiliprotein pigments in 3 species with cyanobacteria as photobionts (Peltigera canina, P. polydactyla, P. rufescens) were determined. The total content of photosynthetic pigments was calculated according to the formule and particular pigments were determined by means CC, TLC, HPLC and IEC chromatography. The total content of the photosynthetic pigments (chlorophylls, carotenoids) in the thalli was highest in red light (genus Peltigera), yellow light (Xanthoria parietina), green light (Cladonia mitis) and at blue light (Flavoparmelia caperata and both species of Hypogymnia). The biggest content of the biliprotein pigments at red and blue lights was observed. The concentration of C-phycocyanin increased at red light, whereas C-phycoerythrin at green light. In Trebouxia phycobiont of Hypogymnia and Nostoc photobiont of Peltigera species the presence of the phytochromes was observed. Key words: carotenoids; chlorophylls; chromatic adaptation; lichens; photobionts; phycobiliproteins; phycobionts; phytochromes.
Introduction Lichens can be found all over our planet, inhabiting diverse biotopes and tolerating even extreme environmental conditions (Kershaw 1985). A number of adaptive mechanisms allow them to exist in these conditions. As autotrophic organisms they need solar energy used by phyco- and photobionts in the process of photosynthesis. In different ecological niches, intensity of the light factor may vary depending on the season of the year or the time of day (Czeczuga et al. 2006a,b, 2007), not mentioning the differences observed between open and shadowed areas of a respective ecosystem (Smith 1981). Moreover, the type of shadowing itself differentiates the spectral composition of the visible light in the shadow (Czeczuga et al. 2007). The spectral composition of light is found to vary according to the shadow formed by various tree species in the vegetative period. The influence of the air pollution on content of chlorophylls have been examined by Arb et al. (1990) and on chlorophylls and carotenoids by Czeczuga & Krukowska (2001), and influence of high temperature Pisani et al. (2007). Whereas, the influence of the heavy metals on the content of chlorophylls in lichen species have been determined by Chettri et al. (1998), Bačkor & Zetikova (2003) and on carotenoids Bačkor et al. (2003). The light intensity investigated Czeczuga et al. (2004b) and Bačkor et al. (2006), and osmotic stress Vaczi & Bartak (2006).
c 2010 Institute of Botany, Slovak Academy of Sciences
Taking the above into account, we decided to investigate the chromatic adaptation of common lichen species in the Knyszy´ nska Forest to various light conditions during the vegetative period.
Material and methods Material The study was conducted on 10 species of lichens (Table 5), including three belonging to cyanolichens. The specimens were collected from ecological niches varying in the type of substratum, shade degree and substratum humidity, which included ground flora of the coniferous forest (spruce), leafy forest (hombeam), tree bark (epiphytes on poplar) and forest scarp by the road. Pieces of soil(5 × 10 cm) or branch covered with the particular lichens were collected in sommer (August) from the Knyszy´ nska Forest, and glued to small pieces of cardboard which were similar to that operating on the lichens in seasonal under field conditions. The experimental beakers were stored in boxes equipped with appropriate glass filters (Czeczuga 1986b), manufactured by the FPN-Bytom Works, wave-lengths being indicated by the producers. Four basic colours were used: red (λ = 700 nm), yellow (λ = 590 nm), green (λ = 500 nm), and blue (λ = 450 nm). A culture of lichens grown in a box provided with normal, “colourless” (white), glass served for the control. The boxes were placed on a table situated 1 metre from a window. In addition, the boxes containing the lichens were exposed to light of 2.7 W m−2 from a glow-tube lamp for 12 hours. After passing Unauthenticated Download Date | 4/22/18 8:38 PM
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588 through the different filters, light intensities were: colourless light – 95.5% (6.3 W m−2 ), red – 52.6% (4.1 W m−2 ), yellow – 21.1% (1.4 W m−2 ), green – 13.2% (0.9 W m−2 ), and blue – 7.9% (0.5 W m−2 ) of the all light in front of every filter. From time to time each lichens was moistened with a sprayer. After 4 weeks, the chlorophylls, particular carotenoids and biliproteins were measured. Analysis of lichen pigments The total amount of chlorophylls and carotenoids was calculated from the following formulae (E standing for extinction at the given wavelengts) (Czeczuga et al. 2006b): Chlorophyll a = 11.63 × E665 – 2.39 × E649 Chlorophyll b = 20.11 × E649 – 5.18 × E665 Total carotenoids = 4.695 × E440 – 0.268 × Ch a + b The presence of the respective carotenoids in the specimens of particular species of lichens assayed was identified by column (CC) and thin-layer chromatography (TLC) with different solvent systems (Czeczuga 1981) as well as highperformance liquid chromatography (HPLC). Prior to chromatography, the material was homogenized and hydrolized in nitrogen, at room temperature. The extract was subsequently placed on an Al2 O3 – filled Quickfit Co. column. The individual fractions were eluted using various solvent systems. The eluent was evaporated, and the residue was dissolved in an appropriate solvent to draw the maximum of absorption. In addition to CC, an acetone extract was divided into fractions with TLC Silicon gel covered glass plates (Merck Co.) and various solvent systems were used. The Rf values were established according to commonly accepted criteria (Kraus and Koch 1996). Pigments were also determined by ion-pairing in reverse-phase HPLC according to Mantoura & Llewellyn (1983). The HPLC equipment consisted of a Shimadzu SCL6B gradient programmer and a Rheodyne 7125 injector. Detection was achieved in a Schimadzu SPD–6AV UV-VIS spectrophotometric detector set at 440 nm and a Shimadzu
RF-535 fluorescence detector. CC, TLC, and HPLC are described in detail in Czeczuga et al. (2006b). Carotenoids were identified by comparison with standards from: a) the behavior in CC; b) their UV-VIS spectra; c) their partition between n-hexane and 95% ethanol; d) their Rf -values in TLC; e) the presence of the allylic OH group determined by the acid CHCl3 test; f) the epoxide test; g) the mass spectrum. Carotenoid pigment standards were purchased from the Hoffman-La Roche Co., Switzerland; the International Agency for 14 C Determinations, Denmark, and Sigma Chemical Co., USA. The structure of particular carotenoids was described by Straub (1987) and Czeczuga (1988). Protein analysis The phytochrome protein were isolated using method according to Tokuhisa et al. (1985) described by LópezFigueroa et al. (1989). The extraction of the phytochrome protein was performed ether according to Lindemann et al. (1989) with 50% ethylene glycol and 2 nM Triton X-100. After removal of contaminating material with polyethyleneimine concentration of the desired protein fraction was done using ammonium sulfate (45% saturation). Relative amounts of the photoreversible protein were determined by measurement of the absorbtion of difference spectrum of A660 nm – A730 nm determined after saturating far-red irradiation, minus the difference A660 nm – A730 nm determined after saturatin red irradiation. In the Nostoc punctiforme photobiont of Peltigera investigated species of the photoreversible protein were determined by measurement of the changes in the absorbance at A540 nm and A650 nm (MacColl & Guard-Friar 1987). Absorption spectra was recorded with a Beckman spectrophotometr model 2400 DU. Further purification on a CC from hydroxyapatite was achieved with the extract from investigated material. Sodium dodecyl sulphate gel electrophoresis with 10%
Table 1. Percentage contain of different coloured light. Type of light (in %) Specification
1. In the months (10–11h) January June December 2. Sunny day (July 9, 10 h) 3. Cloudy day (July 11, 10 h) 4. In the different time of day (July 10) 500 1400 2030 5. In the shade of particular trees (July 7–10, 10–14 h) Alnus glutinosa (L.) Gear. Betula verrucosa Ehrh. Carpinus betulus L. Picea excelsa (Lam.) Lk. Pinus sylvestris L. Populus tremula L. Quercus robur L. Tilia cordata Mill. sunny day cloudy day Acer pseudoplatanus L. (October 29; yellow leaves)
Intensity of sunlight (in W m−2 )
Red
Yellow
Green
Blue
0.75 6.45 0.47 6.36 3.91
25.4 23.1 26.8 23.8 18.4
30.2 28.5 30.6 29.9 26.1
34.4 33.5 32.0 37.6 38.6
10.0 14.9 10.6 8.7 16.9
31.0 22.0 30.8
32.3 31.9 36.0
28.9 31.5 26.5
7.8 14.6 6.7
21.0 22.6 21.0 22.7 20.5 25.0 23.5
31.7 26.1 28.2 27.2 30.8 28.2 29.5
26.3 37.4 36.8 36.5 34.2 34.3 35.3
21.0 13.9 14.0 13.6 14.5 12.5 11.7
31.0 21.2 33.3
25.0 27.2 41.6
31.4 36.5 20.8
12.6 15.1 4.3
3.32 – 4.38
1.70
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Chromatic adaptation in lichen phyco- and photobionts
589
Table 2. Chlorophylls and carotenoids content in lichens from green algae as phycobiont (mg g−1 dry weight, means from 3 determinations). Light
White Red Yellow Green Blue White Red Yellow Green Blue White Red Yellow Green Blue White Red Yellow Green Blue White Red Yellow Green Blue White Red Yellow Green Blue White Red Yellow Green Blue
Chlorophyll a
Chlorophyll b
Carotenoids
Ratio chl. a/chl. b
Cladonia mitis (Sandst.) Hustich – Trebouxia glomerata (Warén) Ahm.∗ 4.3632 3.8872 2.0144 3.2453 3.0618 1.5023 3.8142 3.6661 1.9391 4.8568 4.4894 2.1902 3.6167 3.2252 1.9627 Flavoparmelia caperata (L.) Hale – Trebouxia crenulata Arch. 1.3691 0.3425 0.6963 0.9002 0.3038 0.4801 1.3571 0.4431 0.7852 1.3343 0.3580 0.7578 4.0469 1.0734 1.8204 Hypogymnia physodes (L.) Nyl. – Trebouxia jamesii spp. jamesii Beck 0.3812 0.2108 0.2036 0.4184 0.3176 0.2941 0.6323 0.4244 0.3485 0.8942 0.6026 0.4122 1.2360 0.8207 0.5448 Hypogymnia tubulosa (Schaer) Hav. var. subtile (spruce) – Trebouxia sp. 1.4520 0.8362 1.0924 1.6342 0.8440 1.1360 1.8136 0.9324 1.2092 2.1380 1.0840 1.3140 2.6178 1.2136 1.5188 Hypogymnia tubulosa (Schaer) Hav. var. tubulosa (larch) – Trebouxia sp. 0.4984 0.2542 0.2772 0.4380 0.3002 0.2926 0.5175 0.3132 0.2798 0.5563 0.3236 0.2878 0.5888 0.3381 0.3318 Hypogymnia tubulosa (Schaer) Hav. var. tubulosa (pine) – Trebouxia sp. 0.8099 0.2297 0.3552 0.6809 0.2329 0.2481 0.6702 0.2919 0.2587 0.7886 0.3154 0.3145 2.3661 0.8507 0.7812 Xanthoria parietina (L.) Th. Fr.- Trebouxia arboricola de Puymaly 0.3821 0.2108 0.1432 0.6746 0.3841 0.2186 0.9642 0.7128 0.4382 0.7124 0.5410 0.3174 0.6215 0.3934 0.2283
1.12 1.06 1.04 1.08 1.12 4.00 2.96 3.06 3.73 3.77 1.80 1.32 1.49 1.48 1.51 1.74 1.94 1.95 1.97 2.16 1.96 1.46 1.65 1.72 1.74 3.53 2.92 2.30 2.50 2.78 1.81 1.77 1.35 1.32 1.58
* names of phycobionts according to Bhattacharya et al. (1996) and Beck et al. (1998) (molecular studies)
polyacrylamide gels (0.75 nm) and immunoblotting were performed as described by Schneider-Poetsch et al. (1988). The phycobiliproteins were separated from lichen thalli according to the earlier methods with ammonium sulphate (Czeczuga 1985). After centrifugation, the material was dissolved in a 0.1 M phosphate buffer at pH 7 and purified by ion exchange chromatography (IEC) using a Sephadex G100 column. Elution was carried out in a phosphate buffer at pH 7 using a linear gradient of concentration within the range 0.005–0.1 M. the identification of the phycobiliproteins moiety was achieved by a visible absorption and fluorescence emission maxima (Ray et al. 1978). Relative amounts of particular phycobiliproteins were determined by the method of Bennett and Bogorad (1973).
Results In varied light of photosynthetically active radiation (PAR) (Table 1), the total content of chlorophylls and carotenoids in lichen thalli with green algae as phy-
cobionts has been presented in Table 2, whereas with cyanobacteria as photobionts in Table 3. Data concerning the content of phycobiliprotein pigments have been listed in Table 3. In such species as Hypogymnia physodes, Hypogymnia tubulosa (var. subtilis and tubulosa) and Flavoparmelia caperata, with green algae as phycobionts, the chlorophyll and carotenoid content in the thalli was the highest in blue light. Moreover, the thalli of H. tubulosa var. tubulosa and var. subtilis from more shady sites (pine, spruce) showed higher content of these pigments as compared to more insolated places (var. tubulosa from larch). In the thalli of Cladonia mitis the content of the photosynthesizing pigments was the highest in green light, whereas in the thalli of Xanthoria parietina in yellow light. In the thalli of three species of the genus Peltigera, with cyanobacteria Nostoc punctiforme as photobiont, the greatest amounts of chlorophyll a and carotenoids were found in red light. The thalli of Peltigera rufescens growing in a shadowed Unauthenticated Download Date | 4/22/18 8:38 PM
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Table 3. Chlorophyll a, carotenoids and phycobiliproteins in lichens from cyanobacteria as photobiont (mg g−1 dry weight, means from 3 determinations). Light
White Red Yellow Green Blue White Red Yellow Green Blue White Red Yellow Green Blue White Red Yellow Green Blue
Chlorophyll a
Carotenoids
Phycobiliproteins
C – phycocyanin (%)
C – phycoerythrin (%)
Peltigera canina (L.) Willd. – Nostoc punctiforme (K¨ utz.) Hariot. * 0.3161 1.1181 39.1 0.8248 2.1074 42.8 0.6156 1.3126 40.9 0.5417 0.9180 32.5 0.6724 1.8347 38.7 Peltigera polydactyla (Necker) Hoffm. – Nostoc punctiforme (K¨ utz.) Hariot. 0.8632 0.2816 1.0842 58.4 0.9826 0.3432 1.2878 60.2 0.7654 0.2186 1.1946 56.9 0.6146 0.1848 1.1160 55.3 0.7242 0.2634 1.8042 58.1 Peltigera rufescens (Weiss) Humb. (meadow) – Nostoc punctiforme (K¨ utz.) Hariot. 0.6830 0.2428 0.7142 62.8 0.9283 0.3810 1.5220 63.0 0.6910 0.2782 0.8544 61.2 0.5742 0.2640 0.5162 40.4 0.8824 0.3261 0.9786 43.2 Peltigera rufescens (Weiss) Humb. (forest) – Nostoc punctiforme (K¨ utz.) Hariot. 0.7058 0.2202 1.0260 65.4 1.0058 0.4008 2.0924 67.8 1.2267 0.4314 1.2136 63.1 0.4811 0.2306 0.9960 51.6 0.6251 0.2643 1.5128 55.2 0.9124 1.1481 0.8412 0.7148 0.8046
60.9 57.2 59.1 67.5 61.3 41.6 39.8 43.1 44.7 41.9 37.2 37.0 38.8 59.6 56.8 34.6 32.2 36.9 48.4 44.8
* name of photobiont according to Tschermack-Woess (1988)
place (forest) showed the highest content of these pigments in yellow and blue light. The highest content of phycobiliprotein pigments was detected in the thalli of the three Peltigera species in red and blue light. The content of C-phycocyanin was found to increase in red light, whereas that of C-phycoerythrin – in green light. The thalli of the investigated lichens contained 14 carotenoids (Table 4), among which β-carotene, βcryptoxanthin, lutein, zeaxanthin and astaxanthin occurred in the all species (Table 5). The phytochrome content was 0.085 µg g−1 of fresh weight of Hypogymnia tubulosa and 0.061 of Peltigera investigated species. The molecular weight of isolated phytochrome protein was 131 kDa (Hypogymnia) and 128 kDa (Peltigera). Discussion In the Knyszy´ nska Forest, being the site of our current study, pine and spruce are the predominant tree species, with birch and alder growing on lower terrains. As found in the present study, the spectral composition of PAR light varies depending on tree species casting their shadows (Table 1). The least red light can be found in the shadow of pine, yellow light in the shadow of birch, green in the shadow of alder and blue in the shadow of oak. The greatest amount of red light can be observed in the shadow caused by aspen, blue and green by birch. This is also weather-dependent, especially in relation to red light. On a sunny day, in a shadow formed by e.g. linden, red light accounts for 31.0% whereas on a cloudy day – only for 21.2%. The differences are even greater in the autumn period, when leaves become yellow, e.g. the shadows formed by yellow leaves of maple Acer pseudoplatanus show a char-
acteristic pattern. In such ecological niches with diverse light conditions, numerous lichen species can be found to grow. In the Knyszy´ nska Forest, 315 taxons, including 251 tree epiphytes, have been identified (Czeczuga & Lengiewicz 2001). As revealed by the current study, the most substantial increase in photosynthesizing pigments in all the epiphytic species, except for Xanthoria parietina, occurred in blue light, despite different phycobiont species in these lichens. Worthy of note is the finding of two varieties of Hypogymnia tubulosa var. subtilis on spruce branches, and tubulosa on pine branches and larches growing in the forest peripheries (Czeczuga & Lengiewicz 2001). The thalli of the Hypogymnia tubulosa variety growing in more shady sites (pine, spruce) had higher pigment content in blue light as compared to less shady sites (larch). In the other two species having green algae as phycobionts and growing in semi-shady sites, the content of chlorophylls and carotenoids was found to increase in another than blue light. In the thalli of Xanthoria parietina growing as an epiphyte on poplar-tree, the pigment content was the highest in yellow light. Also in yellow light, the phycobiont of Xanthoria parientina, i.e. green alga Trebouxia arboricola, has the largest cells (Czeczuga & Czeczuga-Semeniuk 2003). Moreover, cells of this phycobiont contain the greatest amount of yellow carotenoid, namely lutein (Czeczuga et al. 2004a,b), which is known to absorb shorter wavelength light beams than those captured by chlorophylls (Yokohama 1982). It should be emphasized that a shade-loving monocellular epiphyte Desmococcus vulgaris shows the largest amount of photosynthesizing pigments in yellow light (Czeczuga 1986b) and lutein predominance (Czeczuga 1978). In the thalli of Unauthenticated Download Date | 4/22/18 8:38 PM
Chromatic adaptation in lichen phyco- and photobionts
591
Table 4. List of the carotenoids from investigated lichens. Carotenoid
1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.
β-carotene α-carotene β-cryptoxanthin α-cryptoxanthin lutein zeaxanthin mutatoxanthin violaxanthin neoxanthin echinenone 3’-hydroxyechinenone adonixanthin canthaxanthin astaxanthin
Structure (see Fig. 1)
Summary formula
Semisystematic name
A–R–A A–R–B A–R–C B–R–C C–R–D C–R–C C – R1 - G E–R–E F – R1 – E A–R -H C–R–H C–R–I H–R–H I–R–I
C40 H56 C40 H56 C40 H56 O C40 H56 O C40 H56 O2 C40 H56 O2 C40 H56 O3 C40 H56 O4 C40 H56 O4 C40 H54 O C40 H54 O2 C40 H54 O3 C40 H52 O2 C40 H52 O4
β, β-Carotene β, ε-Carotene β, β-Caroten-3–ol β, ε-Caroten-3–ol β, ε-Carotene-3,3’-diol β, β-Carotene-3,3’-diol 5,8–Epoxy-5,8–dihydro-β, β-carotene-3,3’-diol 5,6,5’,6’-Diepoxy-5,6,5’,6’-tetrahydro-β, β-carotene-3,3’-diol 5’,6’-Epoxy-6,7–didehydro-5,6,5’,6’-tetrahydro-β, β-carotene-3,5,3’-triol β, β-Caroten-4–one 3–Hydroxy-β, β-carotene-4–one 3,3’-Dihydroxy-β, β-caroten-4–one β, β-Carotene-4,4’-dione 3,3’-Dihydroxy-β, β-carotene-4,4’-dione
Table 5. Carotenoid distribution in the investigated lichens. Species
1. 2. 3. 4. 5. 6. 7. 8. 9. 10.
Cladonia mitis (Sandst.) Hustich Flavoparmelia caperata (L.) Hale Hypogymnia physodes (L.) Nyl. H. tubulosa (Schaer) Hav. var. subtile H. tubulosa (Schaer) Hav. var. tubulosa (larch) H. tubulosa (Schaer) Hav. var. tubulosa (pine) Xanthoria parietina (L.) Th. Fr. Peltigera canina (L.) Willd. P. polydactyla (Necker) Hoffm. P. rufescens (Weiss) Humb.
Carotenoid detected (see Table 4)
Major carotenoid (%)
1,3,5,6,8,12,14 1,2,3,4,5,6,7,8,13,14 1,3,5,6,7,8,14 1,3,5,6,9,12,14 1,3,5,6,8,13,14 1,3,5,6,8 ,13,14 1,3,5,6,7,8,14 1,3,5,6,9,10,13,14 1,3,5,6,9,11,13,14 1,3,5,6,9,10,13,14
6(31.4) 3(21.2) 3(30.5) 1(19.4) 6(28.7) 8(24.5) 7(31.3) 13(18.6) 13(21.1) 14(30.7)
Cladonia mitis growing in the Knyszy´ nska Forest in well-lit woods, the content of photosynthesizing pigments was the highest in green light predominating (34.2%) in the shadow of pines in the Forest. An increase in photosynthesizing pigments has been also observed in other species of the genus Cladonia growing in shadowed places (Karenlampi 1970; Rundel 1972; Legaz et al. 1986; Czeczuga 1993; Czeczuga et al. 2004b). It has to be mentioned that phycobionts of such lichen species as Cetraria islandica and Hypogymnia physodes had the largest cells in blue light, whereas in Cladonia furcata – in green light (Czeczuga & CzeczugaSemeniuk 2003). In all the three lichen species of the genus Peltigera, the cyanobacterium Nostoc punctiforme is a photobiont (Tschermak-Woess 1988). In the thalli of the species examined the highest concentrations of chlorophyll a, phycobilin pigments and carotenoids were found in red light. In the thalli of Peltigera rufescens collected for analysis from a shadowed site with less red light, the largest amounts of chlorophyll a and carotenoids were observed in yellow light whereas of phycobiliprotein pigments in red and blue light, like in the other two species. The content of C-phycocyanin was the highest in red light and C-phycoerythrin in green light. In the thalli of Peltigera rufescens collected from a shadier site, the content of phycobilin pigments in general and that of C-phycocyanin in particular were higher as compared
Total content (µg g−1 dry wt) 10.92 9.12 12.54 18.91 15.12 21.32 14.71 9.92 11.41 14.12
Fig. 1. Structural features of carotenoids from investigated materials (see Table 4).
to a more insolated site. It should be underlined that in two species of Anabaena (cylindrica and variabilis), the content of phycobilin pigments was the highest in blue and red light. In red light, the cells contained Cphycocyanins, whereas in blue light – C-phycoerythrins (Czeczuga 1986a). Light conditions in every larger or smaller forest in the vegetative period depend to a great extent on the species composition of tree stands (Barnes et al. 1998). PAR in the understory ranges from 50% to 80% of full Unauthenticated Download Date | 4/22/18 8:38 PM
592 sunlight under leafless deciduous trees, to 10–15% in even-aged pine stands, 2.5% in closed spruce canopies, 0.2–0.4% in dense beach forests, and even less than 0.1% in certain tropical rainforests (Valladares 2003). Shade tolerance by plants appears to involve three principal tracts: efficient light harvesting at constant low irradiance; – efficient harvesting of sunflecks and – efficient blue light capture (Hugh & Aarssen 1997). Plants have three main photoreceptors, one sensitive to visible light (phytochrome B, sensitive to red light, 660 nm), one to both blue-light and ultraviolet A (chryptochromes, 450 nm and
