Photobiology : the science of life and light,2nd ed

Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vii Contributors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xxi 1. The Nature of Light and Its Interaction with Matter . . . . . . . . . . . . . . 1 Lars Olof Björn 1.1. Introduction ................................................................................... 1 1.2. Particle and Wave Properties of Light ......................................... 1 1.3. Light as Particles and Light as Waves, and Some Definitions.... 6 1.4. Diffraction ..................................................................................... 7 1.5. Polarization.................................................................................... 8 1.6. Statistics of Photon Emission and Absorption ............................. 9 1.7. Heat Radiation............................................................................... 11 1.8. Refraction of Light........................................................................ 14 1.9. Reflection of Light ........................................................................ 15 1.10. Scattering of Light ........................................................................ 18 1.11. Propagation of Light in Absorbing and Scattering Media........... 19 1.12. Spectra of Isolated Atoms............................................................. 22 1.13. Energy Levels in Diatomic and Polyatomic Molecules............... 23 1.14. Quantum Yield of Fluorescence ................................................... 29 1.15. Relationship Between Absorption and Emission Spectra ............ 30 1.16. Molecular Geometry of the Absorption Process .......................... 31 1.17. Transfer of Electronic Excitation Energy Between Molecules.... 33 1.18. The Förster Mechanism for Energy Transfer............................... 34 1.19. Triplet States ................................................................................. 35 1.20. The Dioxygen Molecule................................................................ 36 1.21. Singlet Oxygen.............................................................................. 37 2. Principles and Nomenclature for the Quantification of Light . . . . . . 41 Lars Olof Björn 2.1. Introduction: Why This Chapter Is Necessary ............................. 41 2.2. The Wavelength Problem.............................................................. 42 2.3. The Problem of Direction and Shape ........................................... 43 2.4. Biological Weighting Functions and Units .................................. 46 ix x Contents 3. Generation and Control of Light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51 Lars Olof Björn 3.1. Introduction ................................................................................... 51 3.2. Light Sources................................................................................. 51 3.2.1. The Sun........................................................................... 51 3.2.2. Incandescent Lamps........................................................ 52 3.2.3. Electric Discharges in Gases of Low Pressure .............. 53 3.2.4. Medium- and High-Pressure Gas Discharge Lamps...... 54 3.2.5. Flashlamps ...................................................................... 55 3.2.6. Light-Emitting Diodes .................................................... 55 3.2.7. Lasers .............................................................................. 56 3.3. Selection of Light.......................................................................... 57 3.3.1. Filters with Light-Absorbing Substances ....................... 58 3.3.2. Interference Filters .......................................................... 61 3.3.3. Monochromators ............................................................. 62 4. The Measurement of Light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 Lars Olof Björn 4.1. Introduction ................................................................................... 69 4.2. Photothermal Devices ................................................................... 69 4.2.1. The Bolometer ................................................................ 69 4.2.2. The Thermopile............................................................... 71 4.2.3. Thermopneumatic Devices ............................................. 72 4.3. Photoelectric Devices.................................................................... 73 4.3.1. A Device Based on the Outer Photoelectric Effect: The Photomultiplier ......................................................... 73 4.3.2. Devices Based on Semiconductors (Inner Photoelectric Effect) ........................................................ 75 4.4. Photochemical Devices: Actinometers and Dosimeters............... 76 4.5. Fluorescent Wavelength Converters (“Quantum Counters”) ....... 79 4.6. Spectroradiometry ......................................................................... 80 4.6.1. General ............................................................................ 80 4.6.2. Input Optics..................................................................... 80 4.6.3. Example of a Spectroradiometer .................................... 82 4.6.4. Calibration of Spectroradiometers.................................. 84 4.7. Special Methods for Measurement of Very Weak Light............. 87 4.7.1. Introduction ..................................................................... 87 4.7.2. Direct Current Mode....................................................... 87 4.7.3. Chopping of Light and Use of Lock-In Amplifier ........ 88 4.7.4. Measurement of Shot Noise ........................................... 88 4.7.5. Pulse Counting................................................................ 88 4.8. A Sensor for Catching Images: The Charge-Coupled Device..... 89 5. Light as a Tool for Biologists: Recent Developments . . . . . . . . . . . . . . 93 Lars Olof Björn 5.1. Introduction ................................................................................... 93 Contents xi 5.2. Optical Tweezers and Related Techniques................................... 93 5.3. Use of Lasers for Ablation, Desorption, Ionization, and Dissection ................................................................................ 95 5.4. Fluorescent Labeling ..................................................................... 96 5.5. Abbe’s Diffraction Limit to Spatial Resolution in Microscopy ................................................................................ 97 5.6. Two-Photon Excitation Fluorescence Microscopy....................... 99 5.7. Stimulated Emission Depletion ................................................... 100 5.8. Near-Field Microscopy ................................................................. 101 5.9. Quantum Dots ............................................................................... 103 5.10. Photochemical Internalization....................................................... 108 5.11. Photogating of Membrane Channels ............................................ 110 5.12. Photocrosslinking and Photolabeling............................................ 113 5.13. Fluorescence-Aided DNA Sequencing ......................................... 115 6. Terrestrial Daylight . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 Lars Olof Björn 6.1. Introduction ................................................................................... 123 6.2. Principles for the Modification of Sunlight by the Earth’s Atmosphere........................................................................ 123 6.3. The UV-A, Visible, and Infrared Components of Daylight in the Open Terrestrial Environment Under Clear Skies ..................................................................................... 124 6.4. Cloud Effects................................................................................. 127 6.5. Effects of Ground and Vegetation................................................ 127 6.6. The UV-B Daylight Spectrum and Biological Action of UV-B.......................................................................................... 128 7. Underwater Light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 131 Raymond C. Smith and Curtis D. Mobley 7.1. Introduction ................................................................................... 131 7.2. Inherent Optical Properties ........................................................... 132 7.3. Apparent Optical Properties.......................................................... 133 7.4. Estimation of In-Water Radiant Energy ....................................... 134 8. Action Spectroscopy in Biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 139 Lars Olof Björn 8.1. Introduction ................................................................................... 139 8.2. The Oldest History: Investigation of Photosynthesis by Means of Action Spectroscopy...................................................... 141 8.3. Investigation of Respiration Using Action Spectroscopy ............ 143 8.4. The DNA That Was Forgotten ..................................................... 144 8.5. Plant Vision ................................................................................... 147 8.6. Protochlorophyllide Photoreduction to Chlorophyllide a ............ 151 xii Contents 8.7. Limitations of Action Spectroscopy: The Elusive Blue Light Receptor................................................................................ 152 8.8. Another Use for Action Spectra ................................................... 153 9. Spectral Tuning in Biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155 Lars Olof Björn and Helen Ghiradella 9.1. Introduction ................................................................................... 155 9.2. Why Are Plants Green? ................................................................ 156 9.3. What Determines Spectra of Pigments? ....................................... 157 9.4. Relation Between the Absorption and Molecular Structure of Chlorophylls .............................................................................. 159 9.5. Tuning of Chlorophyll a and b Absorption Peaks by the Molecular Environment...................................................... 161 9.6. Phycobiliproteins and Phycobilisomes ......................................... 162 9.7. Chromatic Adaptation of Cyanobacterial Phycobilisomes........... 165 9.8. Visual Tuning................................................................................ 166 9.9. Tuning of Anthocyanins................................................................ 171 9.10. Living Mirrors and the Tuning of Structural Color ..................... 177 9.10.1. Introduction ..................................................................... 177 9.10.2. Reflection in a Single Thin Layer.................................. 178 9.10.3. Reflection by Multilayer Stacks ..................................... 183 9.11. The Interplay of Spectra in the Living World.............................. 188 10. Photochemical Reactions in Biological Light Perception and Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197 Lars Olof Björn 10.1. Introduction ................................................................................... 197 10.2. Cis-Trans and Trans-Cis Isomerization........................................ 198 10.2.1. Urocanic Acid ................................................................. 199 10.2.2. Eukaryotic Rhodopsin..................................................... 200 10.2.3. Archaean Rhodopsins ..................................................... 203 10.2.4. Photoactive Yellow Proteins (PYPs, Xanthopsins) ....... 205 10.2.5. Phytochrome ................................................................... 207 10.2.6. Photosensor for Chromatic Adaptation of Cyanobacteria.............................................................. 209 10.2.7. Violaxanthin as a Blue-light Sensor in Stomatal Regulation ........................................................ 210 10.3. Other Types of Photosensors ........................................................ 211 10.3.1. Cryptochromes ................................................................ 211 10.3.2. Phototropin...................................................................... 212 10.3.3. The Plant UV-B Receptor .............................................. 215 11. The Diversity of Eye Optics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223 Lars Olof Björn 11.1. Introduction ................................................................................... 223 Contents xiii 11.2. The Human Eye ............................................................................ 223 11.3. An Eye in Water: The Problem .................................................... 227 11.4. An Eye in Water: The Solution .................................................... 228 11.5. Another Problem: Chromatic Aberration ..................................... 230 11.6. Problems and Solutions for Amphibious Animals....................... 231 11.7. Feedback Regulation During Eye Development .......................... 234 11.8. Eyes with Extreme Light Sensitivity ............................................ 234 11.9. Compound Eyes ............................................................................ 235 11.10. Nipple Arrays on Insect Eyes ....................................................... 240 11.11. Eyes with Mirror Optics ............................................................... 241 11.12. Scanning Eyes ............................................................................... 242 11.13. Evolution of Eyes.......................................................................... 246 12. The Evolution of Photosynthesis and Its Environmental Impact . . . 255 Lars Olof Björn and Govindjee 12.1. Introduction ................................................................................... 256 12.2. A Short Review of Plant Photosynthesis...................................... 257 12.3. The Domains of Life..................................................................... 258 12.4. Predecessors of the First Photosynthetic Organisms.................... 259 12.5. The First Photosynthesis ............................................................... 260 12.6. Appearance of Oxygenic Photosynthesis ..................................... 262 12.7. From Cyanobacteria to Chloroplasts ............................................ 265 12.8. Evolution of Photosynthetic Pigments and Chloroplast Structure ..................................................................... 267 12.9. Many Systems for the Assimilation of Carbon Dioxide Have Been Tried in the Course of Evolution ............................... 270 12.10. C4 Metabolism .............................................................................. 272 12.11. Crassulacean Acid Metabolism..................................................... 274 12.12. Evolution of ATP-Synthesizing Enzymes .................................... 275 12.13. The Journey onto Land ................................................................. 275 12.14. Impact of Photosynthesis on the Biospheric Environment .......... 277 12.15. Conclusion..................................................................................... 280 13. Photosynthetic Light Harvesting, Charge Separation, and Photoprotection: The Primary Steps . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 289 Villy Sundström 13.1. Introduction ................................................................................... 289 13.2. Photosynthetic Antennas: Light-Harvesting and Energy Transfer .......................................................................................... 293 13.2.1. Theoretical Considerations for Energy Transfer and Spectroscopy............................................................. 294 13.2.2. Energy Transfer Between Weakly Dipole-Coupled Chromophores: B800–B800 and B800–B850 Transfer in LH2............................................................... 295 xiv Contents 13.2.3. Energy Transfer Between Strongly Coupled Chromophores: B850 of LH2.......................................... 296 13.2.4. The Photosynthetic Unit: Intercomplex Excitation Transfer .......................................................... 298 13.3. Photosynthetic Charge Separation: The Photosynthetic Reaction Center.............................................................................. 300 13.3.1. The Structure and Function of the Bacterial Reaction Center ............................................................... 300 13.3.2. The Mechanism of Primary Electron Transfer .............. 301 13.4. Carotenoid Photophysics and Excited State Dynamics: The Basis of Carotenoid Light-Harvesting and Non-Photochemical Quenching ..................................................... 303 13.4.1. Excited States of Carotenoids......................................... 305 13.5. Energy Transfer from Carotenoids to (Bacterio)Chlorophyll ...... 309 13.6. Quenching of Chlorophyll Excited States by Carotenoids: Non-Photochemical Quenching ..................................................... 313 14. The Biological Clock and Its Resetting by Light . . . . . . . . . . . . . . . . . . 321 Anders Johnsson and Wolfgang Engelmann 14.1. Biological Clocks .......................................................................... 321 14.1.1. Spectrum of Rhythms ..................................................... 322 14.1.2. Function of Clocks.......................................................... 322 14.1.3. Current Concepts and Caveats ....................................... 323 14.1.4. Adaptive Significance and Evolutionary Aspects of Circadian Clocks ......................................................... 324 14.1.5. Properties and Formal Structures of the Circadian System.............................................................................. 324 14.2. Synchronization of Clocks............................................................ 325 14.3. Clocks and Light in Cyanobacteria .............................................. 328 14.3.1. Photoreceptors and Zeitgeber ......................................... 328 14.3.2. Molecular Clock Model and Temporal Orchestration of Gene Expression .................................. 330 14.4. Clocks in the Dinoflagellate Lingulodinium ............................... 331 14.5. Light Effects on Circadian Clocks in Plants: Arabidopsis .......... 332 14.5.1. Light as the Most Important Zeitgeber .......................... 333 14.5.2. Photoreceptors................................................................. 334 14.5.3. Clock Mechanism and Clock-Controlled Genes............ 336 14.5.4. Photoperiodism ............................................................... 337 14.6. Fungal Clocks and Light Resetting: Neurospora ........................ 338 14.6.1. The Circadian System of Neurospora............................ 338 14.6.2. Entrainment of the Circadian System ............................ 341 14.6.3. Photoreceptors of the Circadian System ........................ 342 14.6.4. Outputs of the Circadian System and Photoperiodism ................................................................ 343 14.7. How Light Affects Drosophila’s Circadian System .................... 344 Contents xv 14.7.1. Circadian Eclosion.......................................................... 344 14.7.2. Locomotor Activity Controlled by Several Circadian Oscillators ....................................................... 345 14.7.3. Mechanism of Circadian Clock...................................... 347 14.7.4. Photoreceptors for the Entrainment of the Locomotion Clock ................................................ 347 14.8. Light and Circadian Clocks in Mammals..................................... 351 14.8.1. SCN and Its Incoming and Outgoing Pathways ............ 351 14.8.2. Circadian Photoreceptors in the Retina.......................... 353 14.8.3. Pineal Organ, Melatonin, and Photoperiodism .............. 355 14.8.4. Clocks Outside the SCN................................................. 357 14.9. Light and the Human Circadian System ...................................... 358 14.9.1. Light Synchronizes the Human Circadian System ........ 359 14.9.2. Significance of Light in Shift Work and Jetlag ............. 360 14.9.3. Light Treatment in Sleep Disorders ............................... 361 14.9.4. Seasonal Affective Disorders and Endogenous Depressions ...................................................................... 362 14.10. Models ........................................................................................... 363 14.10.1. Simple Model Description.............................................. 363 14.10.2. Some Mathematical Properties of Circadian Models .... 365 14.10.3. Single Versus Multioscillator Models—Outlook........... 366 15. Photoperiodism in Insects and Other Animals . . . . . . . . . . . . . . . . . . . . 389 David Saunders 15.1. Introduction ................................................................................... 389 15.2. Photoperiodic Regulation of Diapause and Seasonal Morphs in Insects........................................................................... 391 15.3. Models for Photoperiodism........................................................... 393 15.4. Evidence for the Involvement of the Circadian System in Photoperiodic Time Measurement................................................. 396 15.4.1. Nanda-Hamner Experiments........................................... 396 15.4.2. Night Interruption Experiments and the Bünsow Protocol ............................................................................ 397 15.4.3. Skeleton Photoperiods and Bistability Phenomenon ..... 400 15.4.4. The Effects of Transient or Non–Steady-State Entrainment on Diapause Induction................................ 401 15.5. Using Overt “Indicator” Rhythms as “Hands of the Clock” ....... 403 15.6. The “Hourglass” Alternative: Damping Oscillations ................... 404 15.7. Photoreception and Clock Location.............................................. 405 15.8. Diapause Induction in Drosophila melanogaster and the Potential Molecular Analysis of Photoperiodic Induction ............ 408 16. Photomorphogenesis and Photoperiodism in Plants . . . . . . . . . . . . . . . 417 James L. Weller and Richard E. Kendrick 16.1. Introduction ................................................................................... 417 xvi Contents 16.2. Photomorphogenic Photoreceptors ............................................... 418 16.2.1. Phytochromes.................................................................. 418 16.2.2. Cryptochromes ................................................................ 423 16.2.3. Phototropins .................................................................... 424 16.2.4. Other Photoreceptors ...................................................... 425 16.3. Physiological Roles of Photoreceptors ......................................... 425 16.3.1. Germination .................................................................... 426 16.3.2. Seedling Establishment................................................... 427 16.3.3. Phototropism ................................................................... 429 16.3.4. Shade Avoidance ............................................................ 430 16.4. Photoreceptor Signal Transduction............................................... 431 16.4.1. Primary Reactions of Photoreceptors ............................. 431 16.4.2. Mutants and Interacting Factors ..................................... 432 16.4.3. Expression Profiling ....................................................... 436 16.4.4. Pharmacological Approaches ......................................... 437 16.5. Photoperiodism.............................................................................. 438 16.5.1. Light and the Circadian Clock ....................................... 438 16.5.2. Signaling in Photoperiodism .......................................... 445 16.6. Photomorphogenesis and Photoperiodism in the Natural Environment ................................................................................... 447 16.6.1. Improving Energy Capture ............................................. 448 16.6.2. Light and the Seed Habit................................................ 449 16.6.3. Avoidance or Survival of Unfavorable Conditions ....... 450 16.7. Concluding Remarks..................................................................... 451 17. The Light-Dependent Magnetic Compass . . . . . . . . . . . . . . . . . . . . . . . . . 465 Rachel Muheim 17.1. The Involvement of Light in the Magnetic Compass Orientation in Animals................................................................... 465 17.1.1. The Magnetic Inclination Compass................................ 466 17.2. Light-Dependent Effects on Orientation at Different Wavelengths and Irradiances ......................................................... 467 17.2.1. Evidence for an Antagonistic Spectral Mechanism Mediating Magnetic Compass Orientation in Newts...... 467 17.2.2. Magnetic Compass Orientation of Birds Depends on Wavelength and Irradiance ........................................ 468 17.3. Localization of the Light-Dependent Magnetoreceptor ............... 469 17.4. Mechanisms of Light-Dependent Magnetoreception ................... 470 17.4.1. Chemical Magnetoreception Based on a Radical Pair Mechanism ............................................................... 471 17.4.2. Involvement of Cryptochromes as Magneto-Sensitive Photoreceptors?............................ 471 17.4.3. RF Fields as Diagnostic Tool for Testing the Radical Pair Mechanism............................................ 473 17.5. Outlook .......................................................................................... 474 Contents xvii 18. Phototoxicity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 479 Lars Olof Björn and Pirjo Huovinen 18.1. Introduction ................................................................................... 479 18.2. Phototoxicity in Plant Defense ..................................................... 482 18.3. Phototoxins of Fungal Plant Parasites .......................................... 484 18.4. Phototoxic Drugs and Cosmetics.................................................. 485 18.5. Metabolic Disturbances Leading to Phototoxic Effects of Porphyrins or Related Compounds................................................ 487 18.6. Polycyclic Aromatic Hydrocarbons as Phototoxic Contaminants in Aquatic Environments........................................ 489 18.6.1. Nature and Occurrence of PAHs.................................... 489 18.6.2. Mechanisms of PAH Phototoxicity................................ 490 18.6.3. Factors Affecting Exposure to Phototoxicity of PAHs in Aquatic Systems........................................... 492 18.6.4. Phototoxicity of PAHs to Aquatic Biota........................ 493 19. Ozone Depletion and the Effects of Ultraviolet Radiation . . . . . . . . . . 503 Lars Olof Björn and Richard L. McKenzie 19.1. Introduction ................................................................................... 503 19.2. The Ozone Layer........................................................................... 504 19.3. Ozone Depletion............................................................................ 506 19.4. Molecular Effects of UV-B Radiation.......................................... 508 19.4.1. Effects of Ultraviolet Radiation on DNA ...................... 511 19.4.2. Photolyases and Photoreactivation ................................. 513 19.4.3. Formation and Effects of Reactive Oxygen Species ..... 515 19.4.4. Effects of Ultraviolet Radiation on Lipids..................... 517 19.4.5. Photodestruction of Proteins........................................... 518 19.4.6. UV Absorption Affecting Regulative Processes............ 518 19.4.7. UV-Induced Apoptosis ................................................... 519 19.5. Ultraviolet Effects on Inanimate Matter of Biological Relevance ....................................................................................... 519 19.6. UV-B Radiation in an Ecological Context................................... 520 19.6.1. Aquatic Life .................................................................... 520 19.6.2. Terrestrial Life ................................................................ 522 19.7. Effects on Human Eyes................................................................. 523 20. Vitamin D: Photobiological and Ecological Aspects . . . . . . . . . . . . . . . 531 Lars Olof Björn 20.1. Introduction ................................................................................... 531 20.2. Chemistry and Photochemistry of Provitamin and Vitamin D.... 532 20.3. Transport and Transformation of Vitamin D in the Human Body .................................................................................. 536 20.4. Physiological Roles of 1,25-Dihydroxyvitamin D in Vertebrates ..................................................................................... 536 xviii Contents 20.5. Cellular Effects and the Vitamin D Receptor: Two Basic Modes of Action ............................................................................ 537 20.6. Evolutionary Aspects .................................................................... 538 20.7. Distribution of Provitamin and Vitamin D in the Plant Kingdom ............................................................................... 540 20.8. Physiological Effects of Provitamin and Vitamin D in Plants and Algae ............................................................................ 541 20.9. Roles of Provitamin and Vitamin D in Plants.............................. 541 20.10. Biogeographical Aspects............................................................... 542 20.11. The Bright and Dark Sides of Sunlight........................................ 545 20.12. Non-Photochemical Production of Vitamin D ............................. 546 21. The Photobiology of Human Skin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 553 Mary Norval 21.1. Introduction ................................................................................... 553 21.2. The Structure of Skin and the Skin Immune System................... 554 21.2.1. Skin Structure ................................................................. 554 21.2.2. The Skin Immune System .............................................. 555 21.2.3. Contact and Delayed-Type Hypersensitivity ................. 556 21.2.4. Effect of Solar UV Radiation on the Skin: Action Spectra.............................................................................. 557 21.3. Pigmentation and Sunburn............................................................ 557 21.3.1. Pigmentation and Phototypes ......................................... 557 21.3.2. Sunburn and Minimal Erythema Dose........................... 558 21.4. Photoageing ................................................................................... 559 21.5. Photocarcinogenesis ...................................................................... 560 21.5.1. Nonmelanoma Skin Cancer ............................................ 561 21.5.2. Malignant Melanoma...................................................... 563 21.5.3. Animal Studies of Skin Cancer...................................... 564