Contrasting effect of dark-chilling on chloroplast structure and arrangement of chlorophyll-protein complexes in pea and tomato: Plants with a different susceptibility to non-freezing temperature

Planta

Volumn 226, Issue 5, 2007, Pages 1165-1181

  Garstka, Maciej ^a   Venema, Jan Henk ^c   Rumak, Izabela ^a   Gieczewska, Katarzyna ^a   Rosiak, Malgorzata ^a,b   Koziol Lipinska, Joanna ^a   Kierdaszuk, Borys ^a   Vredenberg, Wim J ^d   Mostowska, Agnieszka ^a  

^a UNIVERSITY OF WARSAW   (Poland)

^b Bioton Co Ltd   (Poland)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Cation induced thylakoid stacking; Chilling tolerant; Chilling sensitive; Chlorophyll protein complexes; Chloroplast and thylakoid membrane structure; Confocal laser scanning microscopy; Dark chilling stress; O J D I P chlorophyll fluorescence; Pea; Tomato

Indexed keywords

CHLOROPHYLL; VEGETABLE PROTEIN;

ARTICLE; CHLOROPLAST; COLD; DARKNESS; METABOLISM; PEA; POLYACRYLAMIDE GEL ELECTROPHORESIS; SPECTROFLUOROMETRY; TOMATO; ULTRASTRUCTURE;

CHLOROPHYLL; CHLOROPLASTS; COLD; DARKNESS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; LYCOPERSICON ESCULENTUM; PEAS; PLANT PROTEINS; SPECTROMETRY, FLUORESCENCE;

LYCOPERSICON ESCULENTUM; PISUM SATIVUM;

EID: 34548522744     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-007-0562-7     Document Type: Article

References (68)

1. Albertsson P-Å, Andreasson E (2004) The constant proportion of grana and stroma lamellae in plant chloroplasts. Physiol Plant 121:334-342
2. Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36-42
3. Allen KD, Staehelin LA (1991) Resolution of 16 to 20 chlorophyll-protein complexes using a low ionic strength native green gel system. Anal Biochem 194:214-222
4. Andreeva A, Stoitchkova K, Busheva M, Apostolova E (2003) Changes in the energy distribution between chlorophyll-protein complexes of thylakoid membranes from pea mutants with modified pigment content I. Changes due to the modified pigment content. J Photochem Photobiol B:Biology 70:153-162
5. Barth C, Krause GH (1999) Inhibition of photosystems I and II in chilling-sensitive and chilling-tolerant plants under light and low-temperature stress. Z Naturforsch 54c:645-657
6. Brüggemann W (1995) Long-term chilling of young tomato plants under low light. VI. Differential chilling sensitivity of ribulose-1,5-bisphosphate carboxylase/oxygenase is linked to the oxidation of cystein residues. Plant Cell Physiol 36:733-736
7. Brüggemann W, Daubhorn B, Klauke S, Linger P, Maas-Kantel K, Wenner A (1995) Chilling sensitivity of photosynthesis: ecophysiological studies in two Lycopersicon species of different chilling tolerance. Acta Physiol Plant 17:113-122
8. van Buskirk HA, Thomashow MF (2006) Arabidopsis transcription factors regulating cold acclimation. Physiol Plant 126:72-80
9. Caffarri S, Frigerio S, Olivieri E, Righetti PG, Bassi R (2005) Differential accumulation of Lhcb gene products in thylakoid membranes of Zea mays plants grown under contrasting light and temperature conditions. Proteomics 5:758-768
10. Chinnusamy V, Zhu J, Zhu J-K (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126:52-61
11. Choi SM, Jeong SW, Jeong WJ, Kwon SY, Chow WS, Park Y-I (2002) Chloroplast Cu/Zn-superoxide dismutase is a highly sensitive site in cucumber leaves chilled in the light. Planta 216:315-324
12. Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA 101:15243-15248
13. Danielsson R, Albertsson P-Å, Mamedov F, Styring S (2004) Quantifications of photosystem I and II in different parts of the thylakoid membrane from spinach. Biochim Biophys Acta 1608:53-61
14. Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12-39
15. Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28-44
16. Foyer ChH, Vanacker H, Gomez LD, Harbinson J (2002) Regulation of photosynthesis and antioxidant metabolism in maize leaves at optimal and chilling temperatures: review. Plant Physiol Biochem 40:659-668
17. Gang L, Knowles PF, Murphy DJ, Marsh D (1990) Lipid-protein interaction in thylakoid membranes of chilling-resistant and -sensitive plants studied by spin label electron resonance spectroscopy. J Biol Chem 265:16867-16872
18. Garstka M, Kaniuga Z (1991) Reversal by light of deleterious effects of chilling on oxygen evolution, manganese and free fatty acid content in tomato thylakoids is not accompanied by restoration of the original membrane conformation. Physiol Plant 82:292-298
19. Garstka M, Drozak A, Rosiak M, Venema JH, Kierdaszuk B, Simeonova E, van Hasselt PR, Dobrucki J, Mostowska A (2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-protein complexes in bean thylakoid membranes. Biochim Biophys Acta 1710:13-23
20. Gemel J, Kaniuga Z (1987) Comparison of galactolipase activity and free fatty acid levels in chloroplasts of chill-sensitive and chill-resistant plants. Eur J Biochem 166:229-233
21. Gemel J, Golinowski W, Kaniuga Z (1986) Low-temperature induced changes in chloroplast ultrastructure in relation to changes of Hill reaction activity, manganese and free fatty acid levels in chloroplasts of chilling-sensitive and chilling-resistant plants. Acta Physiol Plant 8:135-143
22. Govindachary S, Bukhov NG, Joly D, Carpentier R (2004) Photosystem II inhibition by moderate light under low temperature in intact leaves of chilling-sensitive and -tolerant plants. Physiol Plant 121:322-333
23. Havaux M, Davaud A (1994) Photoinhibition of photosynthesis in chilled potato leaves is not correlated with a loss of photosystem-II activity. Photosynth Res 40:75-92
24. van Heerden PDR, Krüger GHJ, Loveland JE, Parry MAJ, Foyer CH (2003a) Dark chilling imposes metabolic restrictions on photosynthesis in soybean. Plant Cell Environ 26:323-337
25. 2 assimilation, chlorophyll a fluorescence kinetics O-J-I-P and nitrogen fixation. Physiol Plant 117:476-491
26. Higuchi M, Noguchi T, Sonoike K (2003) Over-reduced states of the Mn-cluster in cucumber leaves induced by dark-chilling treatment. Biochim Biophys Acta 1604:151-158
27. Hipkins MF, Baker NR (1986) Spectroscopy. In: Hipkins MF, Baker NR (eds) Photosynthesis energy transduction, a practical approach. IRL Press, Oxford, pp 63-64
28. Ivanov AG, Morgan RG, Gray GR, Velitchkova MY, Huner NPA (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 215:541-548
29. Jajoo A, Bharti S, Govindjee (1998) Inorganic anions induce state changes in spinach thylakoid membranes. FEBS Lett 434:193-196
30. Joliot P, Joliot A (1964) Etude cinétique de la réaction photochimique libérant l'oxygene au cours de la photosynthese. C R Acad Sci (Paris) 258:4622-4625
31. Jones TL, Tucker DE, Ort DR (1998) Chilling delays circadian pattern of sucrose phosphate synthase and nitrate reductase activity in tomato. Plant Physiol 118:149-158
32. Kaftan D, Brumfeld V, Nevo R, Scherz A, Reich Z (2002) From chloroplasts to photosystems: in situ scanning force microscopy on intact thylakoid membranes. EMBO J 21:6146-6153
33. Kaniuga Z (1997) Galactolipase and chilling sensitivity of plants. Acta Biochim Polon 44:21-39
34. Kaniuga Z, Zabek J, Sochanowicz B (1978) Photosynthetic apparatus in chilling-sensitive plants. III. Contribution of loosely bound manganese to the mechanism of reversible inactivation of Hill reaction activity following cold and dark storage and illumination of leaves. Planta 144:49-56
35. Kim JC, Lee SH, Cheong YH, Yoo C-M, Lee SI, Chun HJ, Yun D-J, Hong JC, Lee SY, Lim CO, Cho MJ (2001) A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. Plant J 25:247-259
36. Kim E-H, Chow WS, Horton P, Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes. Biochim Biophys Acta 1708:187-195
37. Kirchhoff H, Horstmann S, Weis E (2000) Control of the photosynthetic electron transport by PQ diffusion microdomains in thylakoids of higher plants. Biochim Biophys Acta 1459:148-168
38. Kirchhoff H, Mukherjee U, Galla H-J (2002) Molecular architecture of the thylakoid membrane: lipid diffusion space for plastoquinone. Biochemistry 41:4872-4882
39. Kirchhoff H, Tremmel I, Haase W, Kubitscheck U (2004a) Supramolecular photosystem II organization in grana thylakoid membranes: evidence for a structured arrangement. Biochemistry 43:9204-9213
40. Kirchhoff H, Borinski M, Lenhert S, Chi L, Büchel C (2004b) Transversal and lateral exciton energy transfer in grana thylakoids of spinach. Biochemistry 43:14508-14516
41. Klimmek F, Ganeteg U, Ihalainen J, van Roon H, Jensen PE, Scheller HV, Dekker JP, Jansson S (2005) Structure of the higher plant light harvesting complex I: in vivo characterization and structural interpendence of the Lhca proteins. Biochemistry 44:3065-3073
42. Kouril R, Zygadlo A, Arteni AA, de Wit ChD, Dekker JP, Jensen PE, Scheller HV, Boekema EJ (2005) Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44:10935-10940
43. Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Environ 23:337-350
44. Kudoh H, Sonoike K (2002) Irreversible damage to photosystem I by chilling in the light: cause of the degradation of chlorophyll after returning to normal growth temperature. Planta 215:541-548
45. Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666:142-157
46. Maroc J, Trèmoltères A, Garnier J, Guyon D (1987) Oligomeric form of the light-harvesting chlorophyll a + b-protein complex CP II, phosphatidyldiacylglycerol, Δ 3-trans-hexadecenoic acid and energy transfer in Chlamydomonas reinhardtii, wild type and mutants. Biochim Biophys Acta 893:91-99
47. Mehta M, Sarafis V, Critchley C (1999) Thylakoid membrane architecture. Aust J Plant Physiol 26:709-716
48. Mustárdy L, Garab G (2003) Granum revisited. A three-dimensional model-where things fall into place. Trends Plant Sci 8:117-122
49. Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541-568
50. Pesaresi P, Lunde Ch, Jahns P, Tarantino D, Meurer J, Varotto C, Hirtz R-D, Soave C, Scheller HV, Salamini F, Leister D (2002) A stable LHCII-PSI aggregate and suppression of photosynthetic state transition in the psae1-1 mutant of Arabidopsis thaliana. Planta 215:940-948
51. Rozak PR, Seiser RM, Wacholtz WF, Wise RR (2002) Rapid, reversible alterations in spinach thylakoid appression upon changes in light intensity. Plant Cell Environ 25:421-429
52. Ruban AV, Dekker JP, Horton P, van Grondelle R (1995) Temperature dependence of the chlorophyll fluorescence from light harvesting complex II of higher plants. Photochem Photobiol 61:216-221
53. Ruban AV, Calkoen F, Kwa SLS, van Grondelle R, Horton P, Dekker JP (1997) Characterisation of LHCII in the aggregated state by linear and circular dichroism spectroscopy. Biochim Biophys Acta 1932:61-70
54. Scheller HV, Haldrup A (2005) Photoinhibition of photosystem I. Planta 221:5-8
55. Schreiber U (2004) Pulse-amplitude modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou G, Govindjee (ed) Advances in photosynthesis and respiration. Chlorophyll a fluorescence a signature of photosynthesis, vol 19. Springer, Dordrecht, pp 279-319
56. Shen J-R, Terashina I, Katoh S (1990) Cause for dark, chilling-induced inactivation of photosynthetic oxygen-evolving system in cucumber leaves. Plant Physiol 93:1354-1357
57. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou G, Govindjee (ed) Advances in photosynthesis and respiration. Chlorophyll a fluorescence: a signature of photosynthesis, vol 19. Springer, Dordrecht, pp 321-362
58. Tjus SE, Møller BL, Scheller HV (1998) Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol 116:755-764
59. Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou H-E, Rajashekar CB, Williams TD, Wang X (2002) Profiling membrane lipids in plant stress responses. J Biol Chem 277:31994-32002
60. van Heerden PDR, Viljoen MM, de Villiers MF, Krüger GHJ (2004) Limitation of photosynthetic carbon metabolism by dark chilling in temperate and tropical soybean genotypes. Plant Physiol Biochem 42:117-124
61. Venema JH, Linger P, van Heusden AW, van Hasselt PR, Brüggemann W (2005) The inheritance of chilling tolerance in tomato (Lycopersicon spp.). Plant Biol 7:118-130
62. Vredenberg WJ (2004) System analysis and photo-electrochemical control of chlorophyll fluorescence in terms of trapping models of photosystem II: a challenging view. In: Papageorgiou G, Govindjee (ed) Advances in photosynthesis and respiration. Chlorophyll a fluorescence a signature of photosynthesis, vol 19. Springer, Dordrecht, pp 133-172
63. Vredenberg WJ, van Rensen JJS, Rodrigues GC (2005) On the sub-maximal yield and photo-electric stimulation of chlorophyll a fluorescence in single turnover excitations in plant cells. Bioelectrochemistry 68:81-88
64. B-nonreducing centers. Biochim Biophys Acta 1757:173-181
65. Yang M-T, Chen S-L, Lin C-Y, Chen Y-M (2005) Chilling stress suppresses chloroplast development and nuclear gene expression in leaves of mung bean seedlings. Planta 221:374-385
66. Zhang S, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant Cell Physiol 45:1595-1602
67. 2 assimilation, photosynthetic electron transport and water-water cycle in chill-exposed cucumber leaves under low light and subsequent recovery. Plant Cell Environ 27:1503-1514
68. Zhu X-G, Govindjee, Baker NR, deSturler E, Ort DR, Long SP (2005) Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with photosystem II. Planta 223:114-133