Photostasis and cold acclimation: Sensing low temperature through photosynthesis

Physiologia Plantarum

Volumn 126, Issue 1, 2006, Pages 28-44

  Ensminger, Ingo ^a,b   Busch, Florian ^a,c   Huner, Norman P A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON TRANSPORT PROPERTIES; METABOLISM; PHOTONS; PLANTS (BOTANY); REDOX REACTIONS; SUGARS;

COLD ACCLIMATION; METABOLIC SINK; PHOTOSTASIS; PHOTOSYSTEMS;

PHOTOSYNTHESIS;

EID: 33645108251     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/j.1399-3054.2006.00627.x     Document Type: Review

References (87)

1. Adams WW Demmig-Adams B Rosenstiel TN Brightwell AK Ebbert V 2002 Photosynthesis and photoprotection in overwintering plants Plant Biol 4 545 557
2. Allen JF Nilsson A 1997 Redox signalling and the structural basis of regulation of photosynthesis by protein phosphorylation Physiol Plant 100 863 868
3. Ball MC Hodges VS Laughlin GP 1991 Cold-induced photoinhibition limits regeneration of snow gum at tree-line Funct Ecol 5 663 668
4. Bauer H Nagele M Comploj M Galler V Mair M Unterpertinger E 1994 Photosynthesis in cold-acclimated leaves of plants with various degrees of freezing tolerance Physiol Plant 91 403 412
5. Briantais JM Vernotte C Picaud M Krause GH 1979 Quantitative study of the slow decline of chlorophyll alpha-fluorescence in isolated-chloroplasts Biochim Biophys Acta 548 128 138
6. Browse J Xin Z 2001 Temperature sensing and cold acclimation Curr Opin Plant Biol 4 241 246
7. Carlberg I Hansson M Kieselbach T Schröder WP Andersson B Vener AV 2003 A novel plant protein undergoing light-induced phosphorylation and release from the photosynthetic thylakoid membranes Proc Natl Acad Sci USA 100 757 762
8. Collett H Shen A Gardner M Farrant JM Denby KJ Illing N 2004 Towards transcript profiling of desiccation tolerance in Xerophyta humilis: construction of a normalized 11 k X. humilis cDNA set and microarray expression analysis of 424 cDNAs in response to dehydration Physiol Plant 122 39 53
9. Crosatti C Soncini C Stanca AM Cattivelli L 1995 The accumulation of a cold-regulated chloroplastic protein is light-dependent Planta 196 458 463
10. Crosatti C de Laureto PP Bassi R Cattivelli L 1999 The interaction between cold and light controls the expression of the cold-regulated barley gene cor14b and the accumulation of the corresponding protein Plant Physiol 119 671 680
11. Dal Bosco C Busconi M Covoni C Baldi P Stanca AM Crosatti C Bassi R Cattivelli L 2003 cor gene expression in barley mutants affected in chloroplast development and photosynthetic electron transport Plant Physiol 131 793 802
12. Demmig-Adams B Adams WW 1996 The role of xanthophyll cycle carotenoids in the protection of photosynthesis Trends Plant Sci 1 21 26
13. Depege N Bellafiore S Rochaix JD 2003 Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas Science 299 1572 1575
14. Dolman AJ Moors EJ Elbers JA 2002 The carbon uptake of a mid latitude pine forest growing on sandy soil Agric For Met 111 157 170
15. Dubacq JP Tremolieres A 1983 Occurrence and function of phosphatidylglycerol containing delta3-trans-hexadecenoic acid in photosynthetic lamellae Physiol Veg 21 293 312
16. Ebbert V Adams WW Mattoo AK Sokolenko A Demmig-Adams B 2005 Up-regulation of a photosystem II core protein phosphatase inhibitor and sustained D1 phosphorylation in zeaxanthin-retaining, photoinhibited needles of overwintering Douglas fir Plant Cell Environ 28 232 240
17. Elrad D Niyogi KK Grossman AR 2002 A major light-harvesting polypeptide of photosystem II functions in thermal dissipation Plant Cell 14 1801 1816
18. Ensminger I Sveshnikov D Campbell DA Funk C Jansson S Lloyd J Shibistova O Öquist G 2004 Intermittent low temperatures constrain spring recovery of photosynthesis in boreal Scots pine forests Glob Change Biol 10 995 1008
19. Ensminger I Schmidt L Tittmann S Lloyd J 2005 Will photosynthetic gain of boreal evergreen conifers increase in response to a potentially longer growing season? In: Carpentier R Bruce D van der Est A (eds) Photosynthesis: Fundamental Aspects to Global Perspectives Vol. 2 Allen Press Inc. Lawrence KS, pp 976 978
20. Escoubas J Lomas M LaRoche J Falkowski PG 1995 Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool Proc Natl Acad Sci USA 92 10237 10241
21. Falkowski PG Chen Y-B 2003 Photoacclimation of light harvesting systems in eukaryotic algae. In: Green BR Parson WW (eds) Advances in Photosynthesis and Respiration: Light Harvesting Antennas in Photosynthesis Vol. 13 Kluwer Academic Publishers The Netherlands, pp 423 447
22. Farage PK Long SP 1991 The occurrence of photoinhibition in an over-wintering crop of oilseed rape (Brassica-Napus L) and its correlation with changes in crop growth Planta 185 279 286
23. Fey V Wagner R Bräutigam K Pfannschmidt T 2005a Photosynthetic redox control of nuclear gene expression J Exp Bot 56 1491 1498
24. Fey V Wagner R Bräutigam K Wirtz M Hell R Dietzmann A Leister D Oelmüller R Pfannscmidt T 2005b Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins Arabidopsis thaliana J Biol Chem 280 5318 5328
25. Frank HA Cua A Chynwat V Young A Gosztola D Wasielewski MR 1994 Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis Photosyn Res 41 389 395
26. Gilmore AM Ball MC 2000 Protection and storage of chlorophyll in overwintering evergreens Proc Natl Acad Sci USA 97 11098 11101
27. Gray GR Heath D 2005 A global reorganization of the metabolome in Arabidopsis during cold acclimation is revealed by metabolic fingerprinting Physiol Plant 124 236 248
28. Gray GR Boese SR Huner NPA 1994 A comparison of low temperature growth vs low temperature shifts to induce resistance to photoinhibition in spinach (Spinacia oleracea) Physiol Plant 90 560 566
29. Gray GR Chauvin L-P Sarhan F Huner NPA 1997 Cold acclimation and freezing tolerance. A complex interaction of light and temperature Plant Physiol 114 467 474
30. Gray GR Ivanov AG Krol M Huner NPA 1998 Adjustment of thylakoid plastoquinone content and electron donor pool size in response to growth temperature and growth irradiance in Winter Rye (Secale Cereale L.) Photosyn Res 56 209 221
31. Gray GR Ivanov AG Krol M Williams JP Khan MU Myscich EG Huner NPA 2005 Temperature and light modulate trans-delta3-hexadecenoic acid content of phosphatidylglycerol: light-harvesting complex II organization and non-photochemical quenching Plant Cell Physiol 46 1272 1282
32. Haldrup A Jensen PE Lunde C Scheller HV 2001 Balance of power: a view of the mechanism of photosynthetic state transitions Trends Plant Sci 6 301 305
33. Hjelm U Ögren E 2003 Is photosynthetic acclimation to low temperature controlled by capacities for storage and growth at low temperature? Results from comparative studies of grasses and trees Physiol Plant 119 113 120
34. Holt NE Zigmantas D Valkunas L Li X-P Niyogi KK Fleming GR 2005 Carotenoid cation formation and the regulation of photosynthetic light harvesting Science 307 433 436
35. Horton P Ruban AV Young AJ 1999 Regulation of the structure and function of the light harvesting complexes of photosystem II by the xanthophyll cycle. In: Frank HA Young AJ Britton G Cogdell RJ (eds) Advances in Photosynthesis and Respiration: the Photochemistry of Carotenoids Vol. 8 Kluwer Academic Publishers The Netherlands, pp 271 291
36. Huner NPA Krol M Williams JP Maissan E Low P Roberts D Thompson JE 1987 Low temperature development induces a specific decrease in trans-D3-hexadecenoic acid content which influences LHCII organization Plant Physiol 84 12 18
37. Huner NPA Williams JP Maissan EE Myscich EG Krol M Larouche A Singh J 1989 Low temperature-induced decrease in trans-D3-hexadecenoic acid content is correlated with freezing tolerance in cereals Plant Physiol 89 144 150
38. Huner NPA Öquist G Hurry V Krol M Falk S Griffith M 1993 Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants Photosyn Res 37 19 39
39. Huner NPA Öquist G Sarhan F 1998 Energy balance and acclimation to light and cold Trends Plant Sci 3 224 230
40. Huner NPA Öquist G Melis A 2003 Photostasis in plants, green algae and cyanobacteria: the role of light harvesting antenna complexes In: Green BR Parson WW (eds) Advances in Photosynthesis and Respiration Light Harvesting Antennas in Photosynthesis Kluwer Academic Publishers Dordrecht, pp 401 421
41. Hurry VM Malmberg G Gardeström P Öquist G 1994 Effects of a short-term shift to low temperature and of long-term cold hardening on photosynthesis and ribulose-1,5-bisphosphate carboxylase/oxygenase and sucrose phosphate synthase activity in leaves of winter rye (Secale cereale L.) Plant Physiol 106 983 990
42. Hurry V Strand A Furbank R Stitt M 2000 The role of inorganic phosphate in the development of freezing tolerance and the acclimation of photosynthesis to low temperature is revealed by the pho mutants of Arabidopsis thaliana Plant J 24 383 396
43. Ivanov AG Sane PV Zeinalov Y Malmberg G Gardeström P Huner NPA Öquist G 2001 Photosynthetic electron transport adjustments in overwintering Scots pine (Pinus sylvestris L) Planta 213 575 585
44. Ivanov AG Sane PV Zeinalov Y Simidjiev I Huner NPA Öquist G 2002 Seasonal responses of photosynthetic electron transport in Scots pine (Pinus sylvestris L.) studies by thermoluminescence Planta 215 457 465
45. Kacperska A 2004 Sensor types in signal transduction pathways in plant cells responding to abiotic stressors: do they depend on stress intensity? Physiol Plant 122 159 168
46. Karpinski S Reynolds H Karpinska B Wingsle G Creissen G Mullineaux P 1999 Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis Science 284 654 657
47. Krause GH Weis E 1991 Chlorophyll fluorescence and photosynthesis: the basics Annu Rev Plant Physiol Plant Mol Biol 42 313 349
48. Krol M Huner NPA Williams JP Maissan E 1988 Chloroplast biogenesis at cold hardening temperatures. Kinetics of trans-3-hexadecenoic acid accumulation and the assembly of LHCII Photosyn Res 15 115 132
49. Krol M Huner NPA Williams JP Maissan EE 1989 Prior accumulation of phosphatidylglycerol high in trans-D3-hexadecenoic acid enhances the in vitro stability of oligomeric light harvesting complex II J Plant Physiol 135 75 90
50. Lee HY Hong YN Chow WS 2001 Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves Planta 212 332 342
51. Leonardos ED Savitch LV Huner NPA Öquist G Grodzinski B 2003 Daily photosynthetic and C-export patterns in winter wheat leaves during cold stress and acclimation Physiol Plant 117 521 531
52. Lloyd J Shibistova O Zolotoukhine D Kolle O Arneth A Wirth C Styles JM Tchebakova NM Schulze ED 2002 Seasonal and annual variations in the photosynthetic productivity and carbon balance of a central Siberian pine forest Tellus B 54 590 610
53. Lunde C Jensen PE Haldrup A Knoetzel J Scheller HV 2000 The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis Nature 408 613 615
54. Lundmark T Bergh J Strand M Koppel A 1998 Seasonal variation of maximum photochemical efficiency in boreal Norway spruce stands Trees-Struct Funct 13 63 67
55. Maxwell DP Laudenbach DE Huner NPA 1995 Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina Plant Physiol 109 787 795
56. Melis A 1999 Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4 130 135
57. Monroy AF Dhindsa RS 1995 Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25 degrees C Plant Cell 7 321 331
58. Murata N Los DA 1997 Membrane fluidity and temperature perception Plant Physiol 115 875 879
59. Murata N Los DA 2006 Histidine Kinase Hik33 is an important participant in cold-signal transduction in cyanobacteria Physiol Plant 126 17 27
60. NDong C Danyluk J Huner NPA Sarhan F 2001 Survey of gene expression in winter rye during changes in either growth temperature, irradiance or excitation pressure Plant Mol Biol 45 691 703
61. Niyogi KK Li X-P Rosenberg V Jung H-S 2005 Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56 375 382
62. Öquist G Huner NPA 1993 Cold-hardening induced resistance to photoinhibition in winter rye is dependent upon an increased capacity for photosynthesis Planta 189 150 156
63. Öquist G Huner NPA 2003 Photosynthesis of overwintering evergreen plants Annu Rev Plant Biol 54 329 355
64. Oswald O Martin T Dominy PJ Graham IA 2001 Plastid redox state and sugars: Interactive regulators of nuclear-encoded photosynthetic gene expression Proc Natl Acad Sci USA 98 2047 2052
65. Ottander C Campbell D Öquist G 1995 Seasonal-changes in photosystem II organization and pigment composition in Pinus sylvestris Planta 197 176 183
66. Paul MJ Foyer CH 2001 Sink regulation of photosynthesis J Exp Bot 52 1383 1400
67. Pfannschmidt 2003 Chloroplast redox signals: how photosynthesis controls its own genes Trends Plant Sci 8 33 41
68. Pfannschmidt T Nilsson A Allen JF 1999 Photosynthetic control of chloroplast gene expression Nature 397 625 628
69. Sane PV Ivanov AG Hurry V Huner NPA Öquist G 2003 Changes in the redox potential of primary and secondary electron-accepting quinones in photosystem II confer increased resistance to photoinhibition in low-temperature-acclimated Arabidopsis Plant Physiol 132 2144 2151
70. Savitch LV Harney T Huner NPA 2000 Sucrose metabolism in spring and winter wheat in response to high irradiance, cold stress and cold acclimation Physiol Plant 108 270 278
71. Savitch LV Leonardos ED Krol M Jansson S Grodzinski B Huner NPA Öquist G 2002 Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation Plant Cell Environ 25 761 771
72. Savitch LV Allard G Seki M Robert LS Tinker NA Huner NPA Shinozaki K Singh J 2005 The effect of over-expression of two Brassica CBF/DREB1-like transcription factors on photosynthetic capacity and freezing tolerance in Brassica napus Plant Cell Physiol 46 1525 1539
73. Scheible WR Morcuende R Czechowski T Fritz C Osuna D Palacios-Rojas N Schindelasch D Thimm O Udvardi MK Stitt M 2004 Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen Plant Physiol 136 2483 2499
74. Shinozaki K Yamaguchi-Shinozaki K Seki M 2003 Regulatory network of gene expression in the drought and cold stress responses Curr Opin Plant Biol 6 410 417
75. Singh AK Li H Sherman LA 2004 Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803 Physiol Plant 120 27 35
76. Slot M Wirth C Schumacher J Mohren GMJ Shibistova O Lloyd J Ensminger I 2005 Regeneration patterns in boreal Scots pine glades linked to cold-induced photoinhibition Tree Physiol 25 1139 1150
77. Stitt M Hurry V 2002 A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis Curr Opin Plant Biol 5 199 206
78. Strand A Hurry V Gustafsson P Gardestrom P 1997 Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates Plant J 12 605 614
79. Strand A Hurry V Henkes S Huner N Gustafsson P Gardestrom P Stitt M 1999 Acclimation of Arabidopsis leaves developing at low temparatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway Plant Physiol 119 1387 1397
80. Strand A Foyer CH Gustafsson P Gardestrom P Hurry V 2003 Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance Plant Cell Environ 26 523 535
81. Suzuki I Kanesaki Y Mikami K Kanehisa M Murata N 2001 Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis Mol Microbiol 40 235 244
82. Sveshnikov D Ensminger I Ivanov AG Campbell DA Lloyd J Funk C Hüner NPA Öquist G 2006 Excitation energy partitioning and quenching during cold acclimation in Scots pine Tree Physiol 26 325 336
83. Thomashow MF 1999 Plant cold acclimation: freezing tolerance genes and regulatory mechanisms Annu Rev Plant Physiol Plant Mol Biol 50 571 599
84. Urao T Yamaguchi-Shinozaki K Shinozaki K 2000 Two-component systems in plant signal transduction Trends Plant Sci 5 67 74
85. Walters RG Horton P 1994 Acclimation of Arabidopsis thaliana to the light environment: changes in composition of the photosynthetic apparatus Planta 195 248 256
86. Wilson KE Krol M Huner NPA 2003 Temperature-induced greening of Chlorella vulgaris. The role of the cellular energy balance and zeaxanthin-dependent nonphotochemical quenching Planta 217 616 627
87. Zeeman SC Smith SM Smith AM 2004 The breakdown of starch in leaves New Phytol 163 247 261