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Lessons from Nature: A Personal Perspective

  • William W. AdamsIIIEmail author
  • Barbara Demmig-Adams
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 40)

Summary

This chapter highlights selected contributions to photosynthesis research made from an evolutionary and ecological perspective and, specifically, to the characterization of zeaxanthin-associated thermal energy dissipation. First, contributions of comparative ecophysiology to the discovery of different CO2 fixation pathways are examined, followed by a summary of the historical developments leading to documentation of the relationship between zeaxanthin and photoprotective energy dissipation. Evergreen species exhibit exceptionally strong non-photochemical quenching of chlorophyll fluorescence (NPQ) and very high levels of zeaxanthin formation. This enabled an unveiling of the correlation between zeaxanthin versus NPQ and/or photosystem II quantum efficiency (as inferred from the ratio of variable to maximal fluorescence, Fv/Fm), even prior to development of technology currently used in the assessment of these features. Results from characterization of the wide variety of different manifestations (with respect to extent and/or kinetics) of the conversion of xanthophylls, and changes in NPQ and/or Fv/Fm in different plant species and diverse environments are placed in an evolutionary and ecological context. Lastly, themes emerging from the international research community on NPQ and photoprotective thermal dissipation are summarized, and suggestions presented for how utilization of plants genetically adapted and acclimated to high levels of light stress may aid in addressing open questions.

Keywords

Energy Dissipation Chlorophyll Fluorescence Crassulacean Acid Metabolism Xanthophyll Cycle Thermal Dissipation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

CAM

Crassulacean acid metabolism

Car

Carotenoid

Chl

Chlorophyll

ELIP

Early light inducible protein

Fm, Fm

Maximal chlorophyll fluorescence in the dark- and light-adapted state, respectively

Fo, Fo

Minimal chlorophyll fluorescence in the dark- and light-adapted state, respectively

Fv, Fv

Variable chlorophyll fluorescence in the dark- (Fm – Fo) and light-adapted (Fm′ – Fo′) state, respectively

Fv/Fm, Fv′/Fm

Interpreted to be intrinsic efficiency (or quantum yield) of photosystem II in the dark and light-adapted state, respectively

hECN

3-hydroxy-echinenone as a xanthophyll bound to the orange carotenoid protein of cyanobacteria

HLIP

High light-inducible protein

HPLC

High-pressure liquid chromatography

LHC

Light-harvesting complex

LHCII

Light-harvesting complex of photosystem II

LHCSR

Light-harvesting complex stress-related

NPQ

Non-photochemical quenching of chlorophyll fluorescence

OCP

Orange carotenoid protein of cyanobacteria

PAM

Pulse-amplitude-modulated (chlorophyll fluorometry)

PS II

Photosystem II

VAZ cycle

The xanthophyll cycle involving the carotenoids violaxanthin (V) antheraxanthin (A), and zeaxanthin (Z)

Notes

Acknowledgments

We wish to thank our mentors, Olle Björkman and C. Barry Osmond, and the many colleagues and students who have contributed to the development of our work over three decades. We are grateful to J. I. García-Plazaola and Barry A. Logan for their thorough evaluation and suggested changes that have improved the chapter. We also acknowledge funding from various sources for three decades, including the University of Colorado at Boulder, the Australian National University, the Universität Würzburg, the Carnegie Institution of Washington, the National Science Foundation (including our current award, DEB-1022236), the David and Lucile Packard Foundation, the US Department of Agriculture, the Deutsche Forschungsgemeinschaft, the Andrew W. Mellon Foundation, the Alexander von Humboldt Stiftung, and a NATO Postdoctoral Fellowship to W.W.A.

References

  1. Adams WW III (1988) Photosynthetic acclimation and photoinhibition of terrestrial and epiphytic CAM tissues growing in full sunlight and deep shade. Aust J Plant Physiol 15:123–134Google Scholar
  2. Adams WW III, Barker DH (1998) Seasonal changes in xanthophyll cycle-dependent energy dissipation in Yucca glauca Nuttall. Plant Cell Environ 21:501–512Google Scholar
  3. Adams WW III, Demmig-Adams B (1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Planta 186:390–398PubMedGoogle Scholar
  4. Adams WW III, Demmig-Adams B (1994) Carotenoid composition and down regulation of photosystem II in three conifer species during the winter. Physiol Plant 92:451–458Google Scholar
  5. Adams WW III, Demmig-Adams B (1995) The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter. Plant Cell Environ 18:117–127Google Scholar
  6. Adams WW III, Osmond CB (1988) Internal CO2 supply during photosynthesis of sun and shade grown CAM plants in relation to photoinhibition. Plant Physiol 86:117–123PubMedCentralPubMedGoogle Scholar
  7. Adams WW III, Smith SD, Osmond CB (1987) Photoinhibition of the CAM succulent Opuntia basilaris in Death Valley: evidence from 77K fluorescence and quantum yield. Oecologia 71:221–228Google Scholar
  8. Adams WW III, Terashima I, Brugnoli E, Demmig B (1988) Comparisons of photosynthesis and photoinhibition in the CAM vine Hoya australis and several C3 vines growing on the coast of Eastern Australia. Plant Cell Environ 11:173–181Google Scholar
  9. Adams WW III, Díaz M, Winter K (1989) Diurnal changes in photochemical efficiency, the reduction state of Q, radiationless energy dissipation, and nonphotochemical fluorescence quenching from cacti exposed to natural sunlight in Northern Venezuela. Oecologia 80:553–561Google Scholar
  10. Adams WW III, Demmig-Adams B, Winter K, Schreiber U (1990a) The ratio of variable to maximum chlorophyll fluorescence from photosystem II, measured in leaves at ambient temperature and at 77K, as an indicator of the photon yield of photosynthesis. Planta 180:166–174PubMedGoogle Scholar
  11. Adams WW III, Demmig-Adams B, Winter K (1990b) Relative contributions of zeaxanthin-related and zeaxanthin-unrelated types of “high-energy-state” quenching of chlorophyll fluorescence in spinach leaves exposed to various environmental conditions. Plant Physiol 92:302–309PubMedCentralPubMedGoogle Scholar
  12. Adams WW III, Volk M, Hoehn A, Demmig-Adams B (1992) Leaf orientation and the response of the xanthophyll cycle to incident light. Oecologia 90:404–410Google Scholar
  13. Adams WW III, Demmig-Adams B, Lange OL (1993) Carotenoid composition and metabolism in green and blue-green algal lichens in the field. Oecologia 94:576–584Google Scholar
  14. Adams WW III, Demmig-Adams B, Verhoeven AS, Barker DH (1995a) ‘Photoinhibition’ during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol 22:261–276Google Scholar
  15. Adams WW III, Hoehn A, Demmig-Adams B (1995b) Chilling temperatures and the xanthophyll cycle. A comparison of warm-grown and overwintering spinach. Aust J Plant Physiol 22:75–85Google Scholar
  16. Adams WW III, Demmig-Adams B, Barker DH, Kiley S (1996) Carotenoid and photosystem II characteristics of upper and lower halves of leaves acclimated to high light. Aust J Plant Physiol 23:669–677Google Scholar
  17. Adams WW III, Demmig-Adams B, Logan BA, Barker DH, Osmond CB (1999) Rapid changes in xanthophyll cycle-dependent energy dissipation and photosystem II efficiency in two vines, Stephania japonica and Smilax australis, growing in the understory of an open Eucalyptus forest. Plant Cell Environ 22:125–136Google Scholar
  18. Adams WW III, Demmig-Adams B, Rosenstiel TN, Ebbert V (2001) Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter. Photosynth Res 67:51–62PubMedGoogle Scholar
  19. Adams WW III, Demmig-Adams B, Rosenstiel TN, Brightwell AK, Ebbert V (2002) Photosynthesis and photoprotection in overwintering plants. Plant Biol 4:545–557Google Scholar
  20. Adams WW III, Zarter CR, Mueh KE, Amiard V, Demmig-Adams B (2006) Energy dissipation and photoinhibition: a continuum of photoprotection. In: Demmig-Adams B, Adams WW III, Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment. Advances in Photosynthesis and Respiration, Volume 21. Springer, Dordrecht, pp 49–64Google Scholar
  21. Adams WW III, Muller O, Cohu CM, Demmig-Adams B (2013a) May photoinhibition be a consequence, rather than a cause, of limited plant productivity? Photosynth Res 117:31–44PubMedGoogle Scholar
  22. Adams WW III, Cohu CM, Muller O, Demmig-Adams B (2013b) Foliar phloem infrastructure in support of photosynthesis. Front Plant Sci 4:194PubMedCentralPubMedGoogle Scholar
  23. Ågren J, Schemske DW (2012) Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range. New Phytol 194:1112–1122PubMedGoogle Scholar
  24. Armond PA, Schreiber U, Björkman O (1978) Photosynthetic acclimation to temperature in desert shrub, Larrea divaricata. 2. Light-harvesting efficiency and electron transport. Plant Physiol 61:411–415PubMedCentralPubMedGoogle Scholar
  25. Badger MR, Björkman O, Armond PA (1982) An analysis of photosynthetic response and adaptation to temperature in higher plants: temperature acclimation in the desert evergreen Nerium oleander L. Plant Cell Environ 5:85–99Google Scholar
  26. Baker NR, Long SP (eds) (1986) Photosynthesis in Contrasting Environments. Topics in Photosynthesis, Volume 7. Elsevier, AmsterdamGoogle Scholar
  27. Barker DH, Adams WW III (1997) The xanthophyll cycle and energy dissipation in differently oriented faces of the cactus Opuntia macrorhiza. Oecologia 109:353–361Google Scholar
  28. Barker DH, Adams WW III, Demmig-Adams B, Logan BA, Verhoeven AS, Smith SD (2002) Nocturnally retained zeaxanthin does not remain engaged in a state primed for energy dissipation during the summer in two Yucca species growing in the Mojave Desert. Plant Cell Environ 25:95–103Google Scholar
  29. Bassham JA (2005) Mapping the carbon reduction cycle: a personal retrospective. In: Govindjee, Beatty JT, Gest H, Allen JF (eds) Discoveries in Photosynthesis. Advances in Photosynthesis and Respiration, Volume 20. Springer, Dordrecht, pp 815–832Google Scholar
  30. Benson AA (2005) Following the path of carbon in photosynthesis: a personal story. In: Govindjee, Beatty JT, Gest H, Allen JF (eds) Discoveries in Photosynthesis. Advances in Photosynthesis and Respiration, Volume 20. Springer, Dordrecht, pp 793–813Google Scholar
  31. Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543Google Scholar
  32. Beyschlag W, Ryel RJ (2007) Plant physiological ecology: an essential link for integrating across disciplines and scales in plant ecology. Flora 202:606–623Google Scholar
  33. Bilger W, Björkman O (1991) Temperature dependence of violaxanthin de-epoxidation and non-photochemical fluorescence quenching in intact leaves of Gossypium hirsutum L. and Malva parviflora L. Planta 184:226–234PubMedGoogle Scholar
  34. Björkman O (1968) Carboxydismutase activity in shade-adapted and sun-adapted species of higher plants. Physiol Plant 21:1–10Google Scholar
  35. Björkman O, Gauhl E (1969) Carboxydismutase activity in plants with and without β-carboxylation photosynthesis. Planta 88:197–203PubMedGoogle Scholar
  36. Björkman O, Holmgren P (1963) Adaptability of photosynthetic apparatus to light intensity in ecotypes from exposed and shaded habitats. Physiol Plant 16:889–914Google Scholar
  37. Björkman O, Holmgren P (1966) Photosynthetic adaptation to light intensity in plants native to shaded and exposed habitats. Physiol Plant 19:854–859Google Scholar
  38. Björkman O, Powles SP (1984) Inhibition of photosynthetic reactions under water stress: interaction with light level. Planta 161:490–504PubMedGoogle Scholar
  39. Björkman O, Pearcy RW, Mooney H, Harrison AT (1972) Photosynthetic adaptation to high temperatures: a field study in Death Valley, California. Science 175:786–789PubMedGoogle Scholar
  40. Björkman O, Troughton J, Nobs M (1973) Photosynthesis in relation to leaf structure. Brookhaven Symp Biol 25:206–226Google Scholar
  41. Black CC, Osmond CB (2005) Crassulacean acid metabolism photosynthesis: ‘working the night shift’. In: Govindjee, Beatty JT, Gest H, Allen JF (eds) Discoveries in Photosynthesis. Advances in Photosynthesis and Respiration, Volume 20. Springer, Dordrecht, pp 881–893Google Scholar
  42. Clausen J, Hiesey WM (1960) The balance between coherence and variation in evolution. Proc Natl Acad Sci 46:494–506PubMedCentralPubMedGoogle Scholar
  43. Clausen J, Keck DD, Hiesey WM (1941) Regional differentiation in plant species. Am Nat 75:231–250Google Scholar
  44. Clausen J, Keck DD, Hiesey WM (1947) Heredity of geographically and ecologically isolated races. Am Nat 81:114–133PubMedGoogle Scholar
  45. Cleland RE, Demmig-Adams B, Adams WW III, Winter K (1990) Phosphorylation state of the light-harvesting chlorophyll-protein complex of photosystem II and fluorescence characteristics in Monstera deliciosa Liebm. and Glycine max (L.) Merrill in response to light. Aust J Plant Physiol 17:589–599Google Scholar
  46. Cockburn W, Goh CJ, Avadhani PN (1985) Photosynthetic carbon assimilation in a shootless orchid, Chiloschista usneoides (DON) LDL. Plant Physiol 77:83–86PubMedCentralPubMedGoogle Scholar
  47. Cohu CM, Muller O, Demmig-Adams B, Adams WW III (2013a) Minor loading vein acclimation for three Arabidopsis thaliana ecotypes in response to growth under different temperature and light regimes. Front Plant Sci 4:240PubMedCentralPubMedGoogle Scholar
  48. Cohu CM, Muller O, Demmig-Adams B, Adams WW III (2013b) Association between minor loading vein architecture and light- and CO2-saturated rates of photosynthetic oxygen evolution among Arabidopsis thaliana ecotypes from different latitudes. Front Plant Sci 4:264PubMedCentralPubMedGoogle Scholar
  49. Cohu CM, Muller O, Adams WW III, Demmig-Adams B (2014) Leaf anatomical and photosynthetic acclimation to cool temperature and high light in two winter versus two summer annuals. Physiol Plant 152:164–173. doi:  10.1111/ppl.121154
  50. Dall’Osto L, Lico C, Alric J, Gioliano G, Havaux M, Bassi R (2006) Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biol 6:32PubMedCentralPubMedGoogle Scholar
  51. Demmig B, Björkman O (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77K) and photon yield of O2 evolution in leaves of higher plants. Planta 171:171–184PubMedGoogle Scholar
  52. Demmig B, Winter K (1988) Characterisation of three components of non-photochemical fluorescence quenching and their response to photoinhibition. Aust J Plant Physiol 15:163–177Google Scholar
  53. Demmig B, Winter K, Krüger A, Czygan F-C (1987a) Photoinhibition and zeaxanthin formation in intact leaves. A possible role for the xanthophyll cycle in the dissipation of excess light. Plant Physiol 84:218–224PubMedCentralPubMedGoogle Scholar
  54. Demmig B, Cleland RE, Björkman O (1987b) Photoinhibition, 77K chlorophyll fluorescence quenching and phosphorylation of the light-harvesting chlorophyll-protein complex of photosystem II in soybean leaves. Planta 172:378–385PubMedGoogle Scholar
  55. Demmig B, Winter K, Krüger A, Czygan F-C (1988) Zeaxanthin and the heat dissipation of excess light energy in Nerium oleander exposed to a combination of high light and water stress. Plant Physiol 87:17–24PubMedCentralPubMedGoogle Scholar
  56. Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39:474–482Google Scholar
  57. Demmig-Adams B, Adams WW III (1990) The carotenoid zeaxanthin and “high-energy-state” quenching of chlorophyll fluorescence. Photosynth Res 25:187–197PubMedGoogle Scholar
  58. Demmig-Adams B, Adams WW III (1992a) Carotenoid composition in sun and shade leaves of plants with different life forms. Plant Cell Environ 15:411–419Google Scholar
  59. Demmig-Adams B, Adams WW III (1992b) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626Google Scholar
  60. Demmig-Adams B, Adams WW III (1994) Capacity for energy dissipation in the pigment bed in leaves with different xanthophyll pools. Aust J Plant Physiol 21:575–588Google Scholar
  61. Demmig-Adams B, Adams WW III (1996a) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198:460–470Google Scholar
  62. Demmig-Adams B, Adams WW III (1996b) Chlorophyll and carotenoid composition in leaves of Euonymus kiautschovicus acclimated to different degrees of light stress in the field. Aust J Plant Physiol 23:649–659Google Scholar
  63. Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21PubMedGoogle Scholar
  64. Demmig-Adams B, Winter K, Krüger A, Czygan F-C (1989a) Light response of CO2 assimilation, dissipation of excess excitation energy, and zeaxanthin content of sun and shade leaves. Plant Physiol 90:881–886PubMedCentralPubMedGoogle Scholar
  65. Demmig-Adams B, Winter K, Krüger A, Czygan F-C (1989b) Zeaxanthin and the induction and relaxation kinetics of the dissipation of excess excitation energy in leaves in 2% O2, 0% CO2. Plant Physiol 90:887–893PubMedCentralPubMedGoogle Scholar
  66. Demmig-Adams B, Winter K, Krüger A, Czygan F-C (1989c) Zeaxanthin synthesis, energy dissipation, and photoprotection of photosystem II at chilling temperatures. Plant Physiol 90:894–898PubMedCentralPubMedGoogle Scholar
  67. Demmig-Adams B, Adams WW III, Winter K, Meyer A, Schreiber U, Pereira JS, Krüger A, Czygan F-C, Lange OL (1989d) Photochemical efficiency of photosystem II, photon yield of O2 evolution, photosynthetic capacity, and carotenoid composition during the “midday depression” of net CO2 uptake in Arbutus unedo growing in Portugal. Planta 177:377–387PubMedGoogle Scholar
  68. Demmig-Adams B, Winter K, Winkelmann E, Krüger A, Czygan F-C (1989e) Photosynthetic characteristics and the ratio of chlorophyll, β-carotene, and the components of the xanthophyll cycle upon a sudden increase in growth light regime in several plant species. Bot Acta 102:319–325Google Scholar
  69. Demmig-Adams B, Adams WW III, Heber U, Neimanis S, Winter K, Krüger A, Czygan F-C, Bilger W, Björkman O (1990a) Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol 92:293–301PubMedCentralPubMedGoogle Scholar
  70. Demmig-Adams B, Adams WW III, Czygan F-C, Schreiber U, Lange OL (1990b) Differences in the capacity for radiationless energy dissipation in green and blue-green algal lichens associated with differences in carotenoid composition. Planta 180:582–589PubMedGoogle Scholar
  71. Demmig-Adams B, Adams WW III, Green TGA, Czygan F-C, Lange OL (1990c) Differences in the susceptibility to light stress in two lichens, one possessing and one lacking the xanthophyll cycle. Oecologia 84:451–456Google Scholar
  72. Demmig-Adams B, Adams WW III, Logan BA, Verhoeven AS (1995) Xanthophyll cycle-dependent energy dissipation and flexible photosystem II efficiency in plants acclimated to light stress. Aust J Plant Physiol 22:249–260Google Scholar
  73. Demmig-Adams B, Adams WW III, Barker DH, Logan BA, Bowling DR, Verhoeven AS (1996a) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal energy dissipation of excess excitation. Physiol Plant 98:253–264Google Scholar
  74. Demmig-Adams B, Gilmore AM, Adams WW III (1996b) In vivo functions of carotenoids in higher plants. FASEB J 10:403–412PubMedGoogle Scholar
  75. Demmig-Adams B, Moeller DL, Logan BA, Adams WW III (1998) Positive correlation between levels of retained zeaxanthin + antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola. Planta 205:367–374Google Scholar
  76. Demmig-Adams B, Ebbert V, Mellman DL, Mueh KE, Schaffer L, Funk C, Zarter RC, Adamska I, Jansson S, Adams WW III (2006) Modulation of PsbS and flexible vs sustained energy dissipation by light environment in different species. Physiol Plant 127:670–680Google Scholar
  77. Demmig-Adams B, Cohu CM, Muller O, Adams WW III (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth Res 113:75–88PubMedGoogle Scholar
  78. Demmig-Adams B, Amiard V, Cohu CM, Muller O, van Zadelhoff G, Veldink GA, Adams WW III (2013) Emerging trade-offs – impact of photoprotectants (PsbS, xanthophylls, and vitamin E) on oxylipins as regulators of development and defense. New Phytol 197:720–729PubMedGoogle Scholar
  79. Ebbert V, Demmig-Adams B, Adams WW III, Mueh KE, Staehelin LA (2001) Association between persistent forms of zeaxanthin-dependent energy dissipation and thylakoid protein phosphorylation. Photosynth Res 67:63–78PubMedGoogle Scholar
  80. Ebbert V, Adams WW III, Mattoo AK, Sokolenko A, Demmig-Adams B (2005) Upregulation of a PSII core protein phosphatase inhibitor and sustained D1 phosphorylation in zeaxanthin-retaining, photoinhibited needles of overwintering Douglas fir. Plant Cell Environ 28:232–240Google Scholar
  81. Edwards G, Walker DA (1983) C3, C4: Mechanisms, Cellular and Environmental Regulation of Photosynthesis. University of California Press, BerkeleyGoogle Scholar
  82. Ehleringer J, Björkman O (1977) Quantum yields for CO2 uptake in C3 and C4 plants. Dependence on temperature, CO2, and O2 concentration. Plant Physiol 59:86–90PubMedCentralPubMedGoogle Scholar
  83. Esteban R, Olano JM, Castresana J, Fernández-Marín B, Hernández A, Becerril JM, García-Plazaola JI (2009) Distribution and evolutionary trends of photoprotective isoprenoids (xanthophylls and tocopherols) within the plant kingdom. Physiol Plant 135:379–389PubMedGoogle Scholar
  84. Feder ME (2002) Plant and animal physiological ecology, comparative physiology/biochemistry, and evolutionary physiology: opportunities for synergy: an introduction to the symposium. Integr Comp Biol 42:409–414PubMedGoogle Scholar
  85. García-Plazaola JI, Matsubara S, Osmond CB (2007) The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Funct Plant Biol 34:759–773Google Scholar
  86. García-Plazaola JI, Esteban R, Fernández-Marín B, Kranner I, Porcar-Castell A (2012) Thermal energy dissipation and xanthophyll cycles beyond the Arabidopsis model. Photosynth Res 113:89–103PubMedGoogle Scholar
  87. Gilmore AM, Ball MC (2000) Protection and storage of chlorophyll in overwintering evergreens. Proc Natl Acad Sci USA 87:11098–11101Google Scholar
  88. Gilmore AM, Hazlett TL, Govindjee (1995) Xanthophyll cycle-dependent quenching of photosystem II chlorophyll a fluorescence: formation of a quenching complex with a short fluorescence lifetime. Proc Natl Acad Sci USA 92:2273–2277PubMedCentralPubMedGoogle Scholar
  89. Gorsuch PA, Pandey S, Atkin OK (2010) Temporal heterogeneity of cold acclimation phenotypes in Arabidopsis leaves. Plant Cell Environ 33:244–258Google Scholar
  90. Govindjee, Amesz J, Fork DC (eds) (1986) Light Emission by Plants and Bacteria. Academic Press, OrlandoGoogle Scholar
  91. Greenway H, Osmond CB (1972) Salt responses of enzymes from species differing in salt tolerance. Plant Physiol 49:256–259PubMedCentralPubMedGoogle Scholar
  92. Hager A (1980) The reversible, light-induced conversions of xanthophylls in the chloroplast. In: Czygan F-C (ed) Pigments in Plants, 2nd edn. Gustav Fischer Verlag, Stuttgart, pp 57–79Google Scholar
  93. Harris FS, Martin CE (1991a) Plasticity in the degree of CAM-cycling and its relationship to drought stress in 5 species of Talinum (Portulacaceae). Oecologia 86:575–584Google Scholar
  94. Harris FS, Martin CE (1991b) Correlation between CAM-cycling and photosynthetic gas exchange in 5 species of Talinum (Portulacaceae). Plant Physiol 96:1118–1124PubMedCentralPubMedGoogle Scholar
  95. Hatch MD (1992) I can’t believe my luck. Photosynth Res 33:1–14Google Scholar
  96. Hatch MD (2005) C4 photosynthesis: discovery and resolution. In: Govindjee, Beatty JT, Gest H, Allen JF (eds) Discoveries in Photosynthesis. Advances in Photosynthesis and Respiration, Volume 20. Springer, Dordrecht, pp 875–893Google Scholar
  97. Hiesey WM, Clausen J, Keck DD (1942) Relations between climate and intraspecific variation in plants. Am Nat 76:5–22Google Scholar
  98. Holaday AS, Shieh Y-J, Lee KW, Chollet R (1981) Anatomical, ultrastructural and enzymatic studies of leaves of Moricandia arvensis, a C3-C4 intermediate species. Biochim Biophys Acta 637:334–341Google Scholar
  99. Hultine KR, Williams DG, Burgess SSO, Keefer TO (2003) Contrasting patterns of hydraulic redistribution in three desert phreatophytes. Oecologia 136:167–175Google Scholar
  100. Hultine KR, Koepke DF, Pockman WT, Fravolini A, Sperry JS, Williams DG (2005) Influence of soil texture on hydraulic properties and water relations of a dominant warm-desert phreatophyte. Tree Physiol 26:313–323Google Scholar
  101. Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193PubMedGoogle Scholar
  102. Keeley JE (1998) CAM photosynthesis in submerged aquatic plants. Bot Rev 64:121–175Google Scholar
  103. Keeley JE, Osmond CB, Raven JA (1984) Stylites, a vascular land plant without stomata absorbs CO2 via its roots. Nature 310:694–695Google Scholar
  104. Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115PubMedGoogle Scholar
  105. Kluge M, Osmond CB (1971) Pyruvate P i dikinase in Crassulacean acid metabolism. Naturwissenschaften 58:414–415Google Scholar
  106. Kluge M, Osmond CB (1972) Studies on phosphoenolpyruvate carboxylase and other enzymes of crassulacean acid metabolism of Bryophyllum tubiflorum and Sedum praealtum. Z Pflanzenphysiol 66:97–105Google Scholar
  107. Kluge M, Ting IP (1978) Crassulacean Acid Metabolism (CAM): Analysis of an Ecological Adaptation. Springer, BerlinGoogle Scholar
  108. Königer M, Harris GC, Virgo A, Winter K (1995) Xanthophyll-cycle pigments and photosynthetic capacity in tropical forest species: a comparative field study on canopy, gap and understory plants. Oecologia 104:280–290Google Scholar
  109. Krause GH, Grube E, Koroleva OY, Barth C, Winter K (2004) Do mature shade leaves of tropical tree seedlings acclimate to high sunlight and UV radiation? Funct Plant Biol 31:743–756Google Scholar
  110. Ku MSB, Monson RK, Littlejohn RO, Nakamoto H, Fisher DB, Edwards GE (1983) Photosynthetic characteristics of C3-C4 intermediate Flaveria species. 1. Leaf anatomy, photosynthetic responses to O2 and CO2, and activities of key enzymes in the C3 and C4 pathways. Plant Physiol 71:944–948PubMedCentralPubMedGoogle Scholar
  111. Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) (1981a) Physiological Plant Ecology I. Responses to the Physical Environment. Encyclopedia of Plant Physiology, New Series, Volume 12A. Springer, BerlinGoogle Scholar
  112. Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) (1981b) Physiological Plant Ecology II. Water Relations and Carbon Assimilation. Encyclopedia of Plant Physiology, New Series, Volume 12B. Springer, BerlinGoogle Scholar
  113. Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) (1981c) Physiological Plant Ecology III. Responses to the Chemical and Biological Environment. Encyclopedia of Plant Physiology, New Series, Volume 12C. Springer, BerlinGoogle Scholar
  114. Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) (1981d) Physiological Plant Ecology IV. Ecosystem Processes: Mineral Cycling, Productivity and Man’s Influence. Encyclopedia of Plant Physiology, New Series, Volume 12D. Springer, BerlinGoogle Scholar
  115. Larcher W (2003) Physiological Plant Ecology. Ecophysiology and Stress Physiology of Functional Groups, 4th edn. Springer, BerlinGoogle Scholar
  116. Leegood RC, von Caemmerer S (1994) Regulation of photosynthetic carbon assimilation in leaves of C3-C4 intermediate species of Moricandia and Flaveria. Planta 192:232–238Google Scholar
  117. Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395PubMedGoogle Scholar
  118. Li X-P, Gilmore AM, Niyogi KK (2002a) Molecular and global time-resolved analysis of a psbS gene dosage effect on pH- and xanthophyll cycle-dependent nonphotochemical quenching in photosystem II. J Biol Chem 277:33590–33597PubMedGoogle Scholar
  119. Li X-P, Müller-Moulé P, Gilmore AM, Niyogi KK (2002b) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci USA 99:15222–15227PubMedCentralPubMedGoogle Scholar
  120. Li X-P, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279:22866–22874PubMedGoogle Scholar
  121. Logan BA, Barker DH, Demmig-Adams B, Adams WW III (1996) Acclimation of leaf carotenoid composition and ascorbate levels to gradients in the light environment within an Australian rainforest. Plant Cell Environ 19:1083–1090Google Scholar
  122. Logan BA, Demmig-Adams B, Rosenstiel TN, Adams WW III (1999) Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics. Planta 209:213–220PubMedGoogle Scholar
  123. Logan BA, Barker DH, Adams WW III, Demmig-Adams B (1997) The response of xanthophyll cycle-dependent energy dissipation in Alocasia brisbanensis to sunflecks in a subtropical rainforest. Aust J Plant Physiol 24:27–33Google Scholar
  124. Lokstein H, Tian L, Polle JEW, DellaPenna D (2002) Xanthophyll biosynthetic mutants of Arabidopsis thaliana: altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in photosystem II antenna size and stability. Biochim Biophys Acta 1553:309–319PubMedGoogle Scholar
  125. Lüttge U (2006) Photosynthetic flexibility and ecophysiological plasticity: questions and lessons from Clusia, the only CAM tree, in the neotropics. New Phytol 171:7–25PubMedGoogle Scholar
  126. Matsubara S, Förster B, Waterman M, Robinson SA, Pogson BJ, Gunning B, Osmond B (2012) From ecophysiology to phenomics: some implication of photoprotection and shade-sun acclimation in situ for dynamics of thylakoids in vitro. Philos Trans R Soc Lond B Biol Sci 367:3503–3514PubMedCentralPubMedGoogle Scholar
  127. Mooney HA (1991) Plant physiological ecology – determinants of progress. Funct Ecol 5:127–135Google Scholar
  128. Mooney HA, Billings WD (1961) Comparative physiological ecology of arctic and alpine populations of Oxyria digyna. Ecol Monogr 31:1–29Google Scholar
  129. Mooney HA, Johnson AW (1965) Comparative physiological ecology of an arctic and alpine population of Thalictrum alpinum L. Ecology 46:721–727Google Scholar
  130. Mooney HA, Strain BR (1964) Bark photosynthesis in ocotillo. Madrono 17:230–233Google Scholar
  131. Mooney HA, Björkman O, Collatz GJ (1978) Photosynthetic acclimation to temperature in desert shrub, Larrea divaricata. 1. Carbon dioxide exchange characteristics of intact leaves. Plant Physiol 61:406–410PubMedCentralPubMedGoogle Scholar
  132. Mooney HA, Pearcy RW, Ehleringer J (1987) Plant physiological ecology today. Bioscience 37:18–29Google Scholar
  133. Mozzo M, Dall’Osto L, Hienerwadel R, Bassi R, Croce R (2008) Photoprotection in the antenna complexes of photosystem II. Role of individual xanthophylls in chlorophyll triplet quenching. J Biol Chem 283:6184–6192PubMedGoogle Scholar
  134. Nedoff JA, Ting IP, Lord EM (1985) Structure and function of the green stem tissue in ocotillo (Fouquieria splendens). Am J Bot 72:143–151Google Scholar
  135. Nilsen ET, Sharifi MR, Rundel PW, Jarrell WM, Virginia RA (1983) Diurnal and seasonal water relations of the desert phreatophyte Prosopis glandulosa (Honey Mesquite) in the Sonoran Desert of California. Ecology 64:1381–1393Google Scholar
  136. Nilsen ET, Sharifi MR, Rundel PW (1984) Comparative water relations of phreatophytes in the Sonoran Desert of California. Ecology 65:767–778Google Scholar
  137. Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Annu Rev Plant Biol 54:329–355PubMedGoogle Scholar
  138. Osmond CB (1966) Divalent cation absorption and interaction in Atriplex. Aust J Biol Sci 19:37–48Google Scholar
  139. Osmond CB (1967) β-carboxylation during photosynthesis in Atriplex. Biochim Biophys Acta 141:197–199PubMedGoogle Scholar
  140. Osmond CB (1970) C4 photosynthesis in the Chenopodiaceae. Z Pflanzenphysiol 62:129–132Google Scholar
  141. Osmond CB (1971) Metabolite transport in C4 photosynthesis. Aust J Biol Sci 24:159–163PubMedGoogle Scholar
  142. Osmond CB (1974) Leaf anatomy of Australian saltbushes in relation to photosynthetic pathways. Aust J Bot 22:39–44Google Scholar
  143. Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annu Rev Plant Physiol 29:379–414Google Scholar
  144. Osmond CB (1981) Photorespiration and photoinhibition: some implications for the energetics of photosynthesis. Biochim Biophys Acta 639:77–98Google Scholar
  145. Osmond CB (1983) Interactions between irradiance, nitrogen nutrition, and water stress in the sun-shade responses of Solanum dulcamara. Oecologia 57:316–321Google Scholar
  146. Osmond CB, Greenway H (1972) Salt responses of carboxylation enzymes from species differing in salt tolerance. Plant Physiol 49:260–263PubMedCentralPubMedGoogle Scholar
  147. Osmond CB, Harris B (1971) Photorespiration during C4 photosynthesis. Biochim Biophys Acta 234:270–282PubMedGoogle Scholar
  148. Osmond CB, Allaway WG, Sutton BG, Troughton JH, Queiroz O, Lüttge U, Winter K (1973) Carbon isotope discrimination in photosynthesis of CAM plants. Nature 246:41–42Google Scholar
  149. Osmond CB, Björkman O, Anderson DJ (1980) Physiological Processes in Plant Ecology: Toward a Synthesis with Atriplex. Springer, New YorkGoogle Scholar
  150. Ottander C, Campbell D, Öquist G (1995) Seasonal changes in photosystem II organisation and pigment composition in Pinus sylvestris. Planta 197:176–183Google Scholar
  151. Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration, Volume 19. Springer, DordrechtGoogle Scholar
  152. Patten DT (1978) Productivity and production efficiency of an upper Sonoran Desert ephemeral community. Am J Bot 65:891–895Google Scholar
  153. Powles SP, Björkman O (1982) Photoinhibition of photosynthesis: effect on chlorophyll fluorescence at 77K in intact leaves and in chloroplast membranes of Nerium oleander. Planta 156:97–107PubMedGoogle Scholar
  154. Powles SP, Osmond CB (1978) Inhibition of capacity and efficiency of photosynthesis in bean leaflets illuminated in a CO2-free atmosphere at low oxygen: a possible role for photorespiration. Aust J Plant Physiol 5:619–629Google Scholar
  155. Powles SB, Osmond CB, Thorne SW (1979) Photoinhibition of intact attached leaves of C3 plants illuminated in the absence of both carbon dioxide and photorespiration. Plant Physiol 64:982–988PubMedCentralPubMedGoogle Scholar
  156. Powles SP, Berry JA, Björkman O (1983) Interaction between light and chilling temperatures on the inhibition of photosynthesis in chilling-sensitive plants. Plant Cell Environ 6:117–123Google Scholar
  157. Raghavendra AS, Sage RF (eds) (2011) C4 Photosynthesis and Related CO2 Concentrating Mechanisms. Advances in Photosynthesis and Respiration, Volume 32. Springer, DordrechtGoogle Scholar
  158. Sage FR, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106PubMedGoogle Scholar
  159. Sage RF, Zhu XG (2011) Exploiting the engine of C4 photosynthesis. J Exp Bot 62:2989–3000PubMedGoogle Scholar
  160. Sala A, Smith SD, Devitt DA (1996) Water use by Tamarix ramosissima and associated phreatophytes in a Mojave Desert floodplain. Ecol Appl 6:888–898Google Scholar
  161. Sapozhnikov DI (1973) Investigations of the violaxanthin cycle. Pure Appl Chem 35:697–703Google Scholar
  162. Savage JA, Cavender-Bares J, Verhoeven A (2009) Willow species (genus: Salix) with contrasting habitat affinities differ in their photoprotective responses to water stress. Funct Plant Biol 36:300–309Google Scholar
  163. Schreiber U (1986) Detection of rapid induction kinetics with a new type of high-frequency modulated chlorophyll fluorometer. Photosynth Res 9:261–272PubMedGoogle Scholar
  164. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62PubMedGoogle Scholar
  165. Schulze E-D, Caldwell MM (1994) Ecophysiology of Photosynthesis. Ecological Studies, Volume 100. Springer, BerlinGoogle Scholar
  166. Silvera K, Neubig KM, Whitten WM, Williams NH, Winter K, Cushman JC (2010) Evolution along the crassulacean acid metabolism continuum. Funct Plant Biol 37:995–1010Google Scholar
  167. Smith SD, Hartsock TL, Nobel PS (1983) Ecophysiology of Yucca brevifolia, an arborescent monocot of the Mojave Desert. Oecologia 60:10–17Google Scholar
  168. Verhoeven AS, Adams WW III, Demmig-Adams B (1996) Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress. Physiol Plant 96:567–576Google Scholar
  169. Verhoeven AS, Demmig-Adams B, Adams WW III (1997) Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and nitrogen stress. Plant Physiol 113:817–824PubMedCentralPubMedGoogle Scholar
  170. Verhoeven AS, Adams WW III, Demmig-Adams B (1998) Two forms of sustained xanthophyll cycle-dependent energy dissipation in overwintering Euonymus kiautschovicus. Plant Cell Environ 21:893–903Google Scholar
  171. Verhoeven AS, Adams WW III, Demmig-Adams B (1999) The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress. Oecologia 118:277–287Google Scholar
  172. Wang X, Peng YH, Singer JW, Fessehaie A, Krebs SL, Arora R (2009) Seasonal changes in photosynthesis, antioxidant systems and ELIP expression in a thermonastic and non-thermonastic Rhododendron species: a comparison of photoprotective strategies in overwintering plants. Plant Sci 177:607–617Google Scholar
  173. Went F (1926) On growth-accelerating substances in the coleoptile of Avena sativa. Proc Kon Ned Akad Wet 30:10–19Google Scholar
  174. Went FW (1968) The mobile laboratories of the Desert Research Institute. Bioscience 18:293–297Google Scholar
  175. Winter K (1985) Crassulacean acid metabolism. In: Barber J, Baker NR (eds) Photosynthetic Mechanisms and the Environment. Elsevier, Amsterdam, pp 329–387Google Scholar
  176. Winter K, Lüttge U, Winter E, Troughton JH (1978) Seasonal shift from C3 photosynthesis to crassulacean acid metabolism in Mesembryanthenum crystallinum growing in its natural environment. Oecologia 34:225–237Google Scholar
  177. Winter K, Medina E, Garcia V, Mayoral ML, Muniz R (1985) Crassulacean acid metabolism in roots of a leafless orchid, Campylocentrum tyrridion Caray & Dunsterv. J Plant Physiol 118:73–78PubMedGoogle Scholar
  178. Winter K, Garcia M, Holtum JAM (2008) On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoë, and Opuntia. J Exp Bot 59:1829–1840PubMedGoogle Scholar
  179. Woo KC, Downton WJS, Osmond CB, Anderson JM, Boardman NK, Thorne SW (1970) Deficient photosystem II in agranal bundle sheath chloroplasts of C4 plants. Proc Natl Acad Sci 67:18–25PubMedCentralPubMedGoogle Scholar
  180. Yamamoto HY (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure Appl Chem 51:639–648Google Scholar
  181. Yamamoto HY (2006) A random walk to and through the xanthophyll cycle. In: Demmig-Adams B, Adams WW III, Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment. Advances in Photosynthesis and Respiration, Volume 21. Springer, Dordrecht, pp 1–10Google Scholar
  182. Yamamoto HY, Bugos RC, Hieber AD (1999) Biochemistry and molecular biology of the xanthophyll cycle. In: Frank HA, Young AJ, Britton G, Cogdell RJ (eds) The Photochemistry of Carotenoids. Advances in Photosynthesis, Volume 8. Kluwer Academic (now Springer), Dordrecht, pp 293–303Google Scholar
  183. Yoder CK, Nowak RS (1999) Soil moisture extraction by evergreen and drought-deciduous shrubs in the Mojave Desert during wet and dry years. J Arid Environ 42:81–96Google Scholar
  184. Zarter CR, Adams WW III, Ebbert V, Adamska I, Jansson S, Demmig-Adams B (2006a) Winter acclimation of PsbS and related proteins in the evergreen Arctostaphylos uva-ursi as influenced by altitude and light environment. Plant Cell Environ 29:869–878PubMedGoogle Scholar
  185. Zarter CR, Adams WW III, Ebbert V, Cuthbertson D, Adamska I, Demmig-Adams B (2006b) Winter downregulation of intrinsic photosynthetic capacity coupled with upregulation of Elip-like proteins and persistent energy dissipation in a subalpine forest. New Phytol 172:272–282PubMedGoogle Scholar
  186. Zarter CR, Demmig-Adams B, Ebbert V, Adamska I, Adams WW III (2006c) Photosynthetic capacity and light harvesting efficiency during the winter-to-spring transition in subalpine conifers. New Phytol 172:283–292PubMedGoogle Scholar

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© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

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