Plant Biol (Stuttg) 2002; 4(5): 545-557
DOI: 10.1055/s-2002-35434
Review Article
Georg Thieme Verlag Stuttgart ·New York

Photosynthesis and Photoprotection in Overwintering Plants

W. W. Adams III, B. Demmig-Adams, T. N. Rosenstiel, A. K. Brightwell, V. Ebbert
  • Department of Environmental, Population and Organismic Biology, University of Colorado, Boulder, USA
Further Information

Publication History

Received: July 1, 2002

Accepted: September 27, 2002

Publication Date:
15 November 2002 (online)

Abstract

Seasonal differences in the capacity of photosynthetic electron transport, leaf pigment composition, xanthophyll cycle characteristics and chlorophyll fluorescence emission were investigated in two biennial mesophytes (Malva neglecta and Verbascum thapsus) that grow in full sunlight, and in leaves/needles of sun and shade populations of several broad-leafed evergreens and conifers (Vinca minor, Euonymus kiautschovicus, Mahonia repens, Pseudotsuga menziesii [Douglas fir], and Pinus ponderosa). Both mesophytic species maintained or upregulated photosynthetic capacity in the winter and exhibited no upregulation of photoprotection. In contrast, photosynthetic capacity was downregulated in sun leaves/needles of V. minor, Douglas fir, and Ponderosa pine, and even in shade needles of Douglas fir. Interestingly, photosynthetic capacity was upregulated during the winter in shade leaves/needles of V. minor, Ponderosa pine and Euonymus kiautschovicus. Nocturnal retention of zeaxanthin and antheraxanthin, and their sustained engagement in a state primed for energy dissipation, were observed largely in the leaves/needles of sun-exposed evergreen species during winter. Factors that may contribute to these differing responses to winter stress, including chloroplast redox state, the relative levels of source and sink activity at the whole plant level, and apoplastic versus symplastic phloem loading, are discussed.

References

  • 01 Adams,  W. W. III., and Barker,  D. H.. (1998);  Seasonal changes in xanthophyll cycle-dependent energy dissipation in Yucca glauca Nuttall.  Plant, Cell and Environment. 21 501-512
  • 02 Adams,  W. W. III., and Demmig-Adams,  B.. (1992);  Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight.  Planta. 186 390-398
  • 03 Adams,  W. W. III., and Demmig-Adams,  B.. (1994);  Carotenoid composition and down regulation of photosystem II in three conifer species during the winter.  Physiologia Plantarum. 92 451-458
  • 04 Adams,  W. W. III., and Demmig-Adams,  B.. (1995);  The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter.  Plant, Cell and Environment. 18 117-127
  • 05 Adams,  W. W. III.,, Winter,  K.,, Schreiber,  U.,, and Schramel,  P.. (1990);  Photosynthesis and chlorophyll fluorescence characteristics in relationship to changes in pigment and elemental composition of leaves of Platanus occidentalis L. during autumnal leaf senescence.  Plant Physiology. 93 1184-1190
  • 06 Adams,  W. W. III.,, Demmig-Adams,  B.,, Verhoeven,  A. S.,, and Barker,  D. H.. (1995 a);  “Photoinhibition” during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation.  Australian Journal of Plant Physiology. 22 261-276
  • 07 Adams,  W. W. III.,, Hoehn,  A.,, and Demmig-Adams,  B.. (1995 b);  Chilling temperatures and the xanthophyll cycle. A comparison of warm-grown and overwintering spinach.  Australian Journal of Plant Physiology. 22 75-85
  • 08 Adams,  W. W. III.,, Demmig-Adams,  B.,, Rosenstiel,  T. N.,, and Ebbert,  V.. (2001 a);  Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter.  Photosynthesis Research. 67 51-62
  • 09 Adams,  W. W. III.,, Demmig-Adams,  B.,, Rosenstiel,  T. N.,, Ebbert,  V.,, Brightwell,  A. K.,, Barker,  D. H.,, and Zarter,  C. R.. (2001 b) Photosynthesis, xanthophylls, and D1 phosphorylation under winter stress. PS2001 Proceedings. 12th International Congress on Photosynthesis, Melbourne; CSIRO Publishing. Available at http://www.publish.csiro.au/ps2001
  • 10 Baroli,  I., and Niyogi,  K. K.. (2000);  Molecular genetics of xanthophyll-dependent photoprotection in green algae and plants. Philosophical Transactions of the Royal Society of London. Series B.  Biological Sciences. 355 1385-1393
  • 11 Bauer,  H.,, Nagele,  M.,, Comploj,  M.,, Galler,  V.,, Mair,  M.,, and Unterpertinger,  E.. (1994);  Photosynthesis in cold acclimated leaves of plants with various degrees of freezing tolerance.  Physiologia Plantarum. 91 403-412
  • 12 Björkman,  O.. (1981) Responses to different quantum flux densities. Encyclopedia of plant physiology, new series, Vol. 12 A, physiological plant ecology I. Lange, O.-L., Nobel, P. S., Osmond, C. B., and Ziegler, H., eds. Berlin; Springer-Verlag pp. 57-107
  • 13 Blennow,  K.,, Lang,  A. R. G.,, Dunne,  P.,, and Ball,  M. C.. (1998);  Cold-induced photoinhibition and growth of seedling snow gum (Eucalyptus pauciflora) under differing temperature and radiation regimes in fragmented forests.  Plant, Cell and Environment. 21 407-416
  • 14 Boardman,  N. K.. (1977);  Comparative photosynthesis of sun and shade plants.  Annual Review of Plant Physiology. 28 355-377
  • 15 Bruick,  R. K., and Mayfield,  S. P.. (1999);  Light-activated translation of chloroplast mRNAs.  Trends in Plant Science. 4 190-195
  • 16 Cushman,  R. C.,, Jones,  S. R.,, and Knopf,  J.. (1993) Boulder Nature Almanac. Boulder; Pruet 340 pp.
  • 17 Demmig-Adams,  B.. (1998);  Survey of thermal energy dissipation and pigment composition in sun and shade leaves.  Plant and Cell Physiology. 39 474-482
  • 18 Demmig-Adams,  B., and Adams,  W. W. III.. (1996);  The role of the xanthophyll cycle carotenoids in the protection of photosynthesis.  Trends in Plant Science. 1 21-26
  • 19 Demmig-Adams,  B.,, Adams,  W. W. III.,, Barker,  D. H.,, Logan,  B. A.,, Verhoeven,  A. S.,, and Bowling,  D. R.. (1996);  Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation.  Physiologia Plantarum. 98 253-265
  • 20 Demmig-Adams,  B.,, Adams,  W. W. III.,, Ebbert,  V.,, and Logan,  B. A.. (1999) Ecophysiology of the xanthophyll cycle. The Photochemistry of Carotenoids. Frank, H. A., Young, A. J., Britton, G., and Cogdell, R. J., eds. Dordrecht; Kluwer Academic Publishers pp. 245-269
  • 21 Ebbert,  V.,, Demmig-Adams,  B.,, Adams,  W. W. III.,, Mueh,  K. E.,, and Staehelin,  L. A.. (2001);  Association between persistent forms of zeaxanthin-dependent energy dissipation and thylakoid protein phosphorylation.  Photosynthesis Research. 67 63-78
  • 22 Finkelstein,  R. R., and Gibson,  S. I.. (2001);  ABA and sugar interactions regulating development: cross-talk or voices in a crowd?.  Current Opinion on Plant Biology. 5 26-32
  • 23 Gal,  A.,, Zer,  H.,, and Ohad,  I.. (1997);  Redox-controlled thylakoid protein phosphorylation.  Physiologia Plantarum. 100 869-885
  • 24 Gamalei,  Y. V.. (1991);  Phloem loading and its development related to plant evolution from trees to herbs.  Trees. 5 50-64
  • 25 Gilmore,  A. M., and Ball,  M. C.. (2000);  Protection and storage of chlorophyll in overwintering evergreens.  Proceedings of the National Academy of Science USA. 97 11098-11101
  • 26 Gilmore,  A. M., and Yamamoto,  H. Y.. (1991);  Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column.  Journal of Chromatography. 543 137-145
  • 27 Graves,  J. D.. (1990);  A model of the seasonal pattern of carbon acquisition in two woodland herbs, Mercurialis perennis L. and Geum urbanum L.  Oecologia. 83 479-484
  • 28 Holaday,  A. S.,, Martindale,  W.,, Alred,  R.,, Brooks,  A.,, and Leegood,  R. C.. (1992);  Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature.  Plant Physiology. 98 1105-1114
  • 29 Hovenden,  M. J., and Warren,  C. R.. (1998);  Photochemistry, energy dissipation and cold-hardening in Eucalyptus nitens and E. pauciflora. .  Australian Journal of Plant Physiology. 25 581-589
  • 30 Huner,  N. P. A.,, Öquist,  G.,, Hurry,  V. M.,, Krol,  M.,, Falk,  S.,, and Griffith,  M.. (1993);  Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants.  Photosynthesis Research. 37 19-39
  • 31 Huner,  N. P. A.,, Öquist,  G.,, and Sarhan,  F.. (1998);  Energy balance and acclimation to light and cold.  Trends in Plant Science. 3 224-230
  • 32 Hurry,  V. M.,, Keerberg,  O.,, Pärnik,  T.,, Gardeström,  P.,, and Öquist,  G.. (1995 a);  Cold-hardening results in increased activity of enzymes involved in carbon metabolism in leaves of winter rye (Secale cereale L.).  Planta. 195 554-562
  • 33 Hurry,  V. M.,, Strand,  Å.,, Tobiæson,  M.,, Gardeström,  P.,, and Öquist,  G.. (1995 b);  Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism, and carbohydrate content.  Plant Physiology. 109 697-706
  • 34 Hymus,  G. J.,, Ellsworth,  D. S.,, Baker,  N. R.,, and Long,  S. P.. (1999);  Does free-air carbon dioxide enrichment affect photochemical energy use by evergreen trees in different seasons? A chlorophyll fluorescence study of mature loblolly pine.  Plant Physiology. 120 1183-1191
  • 35 Ivanov,  A. G.,, Sane,  P. V.,, Zeinalov,  Y.,, Malmberg,  G.,, Gardeström,  P.,, Huner,  N. P. A.,, and Öquist,  G.. (2001);  Photosynthetic electron transport adjustments in overwintering Scots pine (Pinus sylvestris L.).  Planta. 213 575-585
  • 36 Königer,  M.,, Harris,  G. C.,, and Kibler,  E.. (2000);  Seasonal changes in the physiology of shade leaves of Acer saccharum. .  Journal of Plant Physiology. 157 627-636
  • 37 Körner,  C.,, Pelaez-Riedl,  S.,, and van Bel,  A. J. E.. (1995);  CO2 responsiveness of plants: a possible link to phloem loading.  Plant, Cell and Environment. 18 595-600
  • 38 Lambers,  H.,, Chapin,  F. S. III.,, and Pons,  T. L.. (1998) Plant Physiological Ecology. New York; Springer-Verlag pp. 540
  • 39 Leverenz,  J. W., and Öquist,  G.. (1987);  Quantum yields of photosynthesis at temperatures between - 2 °C and 35 °C in a cold-tolerant C3 plant (Pinus sylvestris) during the course of one year.  Plant, Cell and Environment. 10 287-295
  • 40 Logan,  B. A.,, Grace,  S. C.,, Adams,  W. W. III.,, and Demmig-Adams,  B.. (1998);  Seasonal differences in xanthophyll cycle characteristics and antioxidants in Mahonia repens growing in different light environments.  Oecologia. 116 9-17
  • 41 Martindale,  W., and Leegood,  R. C.. (1997);  Acclimation of photosynthesis to low temperature in Spinacia oleracea L. I. Effects of acclimation on CO2 assimilation and carbon partitioning.  Journal of Experimental Botany. 48 1865-1872
  • 42 Møller,  S. G., and Chua,  N.-H.. (1999);  Interactions and intersections of plant signaling pathways.  Journal of Molecular Biology. 293 219-234
  • 43 Monson,  R. K.,, Turnipseed,  A. A.,, Sparks,  J. P.,, Harley,  P. C.,, Scott-Denton,  L. E.,, Sparks,  K.,, and Huxman,  T. E.. (2002);  Carbon sequestration in a high-elevation, subalpine forest.  Global Change Biology. 8 459-478
  • 44 Mullineaux,  P., and Karpinski,  S.. (2002);  Signal transduction in response to excess light: getting out of the chloroplast.  Current Opinion in Plant Biology. 5 43-48
  • 45 Oberhuber,  W., and Bauer,  H.. (1991);  Photoinhibition of photosynthesis under natural conditions in ivy (Hedera helix L.) growing in an understory of deciduous trees.  Planta. 185 545-553
  • 46 Öquist,  G., and Huner,  N. P. A.. (1993);  Cold-hardening-induced resistance to photoinhibition of photosynthesis in winter rye is dependent upon an increased capacity for photosynthesis.  Planta. 189 150-156
  • 47 Ottander,  C., and Öquist,  G.. (1991);  Recovery of photosynthesis in winter-stressed Scots pine.  Plant, Cell and Environment. 14 345-349
  • 48 Ottander,  C.,, Campbell,  D.,, and Öquist,  G.. (1995);  Seasonal changes in photosystem II organization and pigment composition in Pinus sylvestris. .  Planta. 197 176-183
  • 49 Pei,  Z. M.,, Murata,  Y.,, Benning,  G.,, Thomine,  S.,, Klusener,  B.,, Allen,  G. J.,, Grill,  E.,, and Schroeder,  J. I.. (2000);  Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells.  Nature. 406 731-734
  • 50 Pfannschmidt,  T.,, Allen,  J. F.,, and Oelmüller,  R.. (2001);  Principles of redox control in photosynthesis gene expression.  Physiologia Plantarum. 112 1-9
  • 51 Roden,  J. S.,, Egerton,  J. J.,, and Ball,  M. C.. (1999);  Effect of elevated (CO2) on photosynthesis and growth of snow gum (Eucalyptus pauciflora) seedlings during winter and spring.  Australian Journal of Plant Physiology. 26 37-46
  • 52 Savitch,  L. V.,, Leonardos,  E. D.,, Krol,  M.,, Jansson,  S.,, Grodzinski,  B.,, Huner,  N. P. A.,, and Öquist,  G.. (2002);  Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation.  Plant, Cell and Environment. 25 761-771
  • 53 Schreiber,  U.,, Bilger,  W.,, and Neubauer,  C.. (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. Ecophysiology of Photosynthesis. Schulze, E.-D. and Caldwell, M. M., eds. Berlin; Springer-Verlag pp. 49-70
  • 54 Siefermann-Harms,  D.. (1994);  Light and temperature control of season-dependent changes in the α- and β-carotene content of spruce needles.  Journal of Plant Physiology. 143 488-494
  • 55 Skillman,  J. B.,, Strain,  B. R.,, and Osmond,  C. B.. (1996);  Contrasting patterns of photosynthetic acclimation and photoinhibition in two evergreen herbs from a winter deciduous forest.  Oecologia. 107 446-455
  • 56 Strand,  Å.,, Hurry,  V.,, Gustafsson,  P.,, and Gardeström,  P.. (1997);  Development of Arabidopsis thaliana leaves at low temperature releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates.  The Plant Journal. 12 605-614
  • 57 Strand,  Å.,, Hurry,  V. M.,, Henkes,  S.,, Huner,  N. P. A.,, Gustafsson,  P.,, Gardeström,  P.,, and Stitt,  M.. (1999);  Acclimation of Arabidopsis leaves developing at low temperatures: Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway.  Plant Physiology. 119 1387-1397
  • 58 Turgeon,  R.,, Beebe,  D. U.,, and Gowan,  E.. (1993);  The intermediary cell: minor vein anatomy and raffinose oligosaccharide synthesis in the Scrophulariaceae.  Planta. 191 446-456
  • 59 Turgeon,  R.,, Medville,  R.,, and Nixon,  K. C.. (2001);  The evolution of minor vein phloem and phloem loading.  American Journal of Botany. 88 1331-1339
  • 60 Van Bel,  A. J. E.. (1992);  Different phloem loading machineries correlated with the climate.  Acta Botanica Neerlandica. 41 121-141
  • 61 Van Bel,  A. J. E., and Gamalei,  Y. V.. (1992);  Ecophysiology of phloem loading in source leaves.  Plant, Cell and Environment. 15 265-270
  • 62 Vener,  A. V.,, Ohad,  I.,, and Andersson,  B.. (1998);  Protein phosphorylation and redox sensing in chloroplast thylakoids.  Current Opinion in Plant Biology. 1 217-223
  • 63 Verhoeven,  A. S.,, Adams,  W. W. III.,, and Demmig-Adams,  B.. (1996);  Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress.  Physiologia Plantarum. 96 567-576
  • 64 Verhoeven,  A. S.,, Adams,  W. W. III.,, and Demmig-Adams,  B.. (1998);  Two forms of sustained xanthophyll cycle-dependent energy dissipation in overwintering Euonymus kiautschovicus. .  Plant, Cell and Environment. 21 893-903
  • 65 Verhoeven,  A. S.,, Adams,  W. W. III.,, and Demmig-Adams,  B.. (1999);  The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress.  Oecologia. 118 277-287
  • 66 Warren,  C. R.,, Hovenden,  M. J.,, Davidson,  N. J.,, and Beadle,  C. L.. (1998);  Cold hardening reduces photoinhibition of Eucalyptus nitens and E. pauciflora at frost temperatures.  Oecologia. 113 350-359
  • 67 Williams,  L. E.,, Lemoine,  R.,, and Sauer,  N.. (2000);  Sugar transporters in higher plants - a diversity of roles and complex regulation.  Trends in Plant Science. 5 283-290
  • 68 Yamamoto,  H. Y., and Bassi,  R.. (1996) Carotenoids: localization and function. Oxygenic Photosynthesis: The Light Reactions. Ort, D. R. and Yocum, C. F., eds. Dordrecht; Kluwer Academic Publishers pp. 539-563
  • 69 Zimmermann,  M. H., and Ziegler,  H.. (1975) List of sugars and sugar alcohols in sieve-tube exudates. Encyclopedia of Plant Physiology, New Series, Vol. 1, Transport in Plants 1, Phloem Transport. Zimmermann, M. H. and Milburn, J. A., eds. Berlin; Springer-Verlag pp. 480-503

W. W. Adams III

Department of Environmental, Population and Organismic Biology
University of Colorado

Boulder
CO 80309-0334
USA

Email: william.adams@colorado.edu

Section Editor: U. Lüttge

    >