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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

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Abstract

The effect of dark-chilling and subsequent photoactivation on chloroplast structure and arrangements of chlorophyll–protein complexes in thylakoid membranes was studied in chilling-tolerant (CT) pea and in chilling-sensitive (CS) tomato. Dark-chilling did not influence chlorophyll content and Chl a/b ratio in thylakoids of both species. A decline of Chl a fluorescence intensity and an increase of the ratio of fluorescence intensities of PSI and PSII at 120 K was observed after dark-chilling in thylakoids isolated from tomato, but not from pea leaves. Chilling of pea leaves induced an increase of the relative contribution of LHCII and PSII fluorescence. A substantial decrease of the LHCII/PSII fluorescence accompanied by an increase of that from LHCI/PSI was observed in thylakoids from chilled tomato leaves; both were attenuated by photoactivation. Chlorophyll fluorescence of bright grana discs in chloroplasts from dark-chilled leaves, detected by confocal laser scanning microscopy, was more condensed in pea but significantly dispersed in tomato, compared with control samples. The chloroplast images from transmission-electron microscopy revealed that dark-chilling induced an increase of the degree of grana stacking only in pea chloroplasts. Analyses of O-J-D-I-P fluorescence induction curves in leaves of CS tomato before and after recovery from chilling indicate changes in electron transport rates at acceptor- and donor side of PS II and an increase in antenna size. In CT pea leaves these effects were absent, except for a small but irreversible effect on PSII activity and antenna size. Thus, the differences in chloroplast structure between CS and CT plants, induced by dark-chilling are a consequence of different thylakoid supercomplexes rearrangements.

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Abbreviations

Chl:

Chlorophyll

CLSM:

Fluorescence confocal laser scanning microscopy

CP:

Chlorophyll–protein

CS:

Chilling-sensitive

CT:

Chilling-tolerant

Em:

Emission wavelength

Ex:

Excitation wavelength

FFA:

Free fatty acids

PAR:

Photosynthetic active radiation

TEM:

Transmission electron microscopy

References

  • Albertsson P-Å, Andreasson E (2004) The constant proportion of grana and stroma lamellae in plant chloroplasts. Physiol Plant 121:334–342

    Article  PubMed  CAS  Google Scholar 

  • Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • van Buskirk HA, Thomashow MF (2006) Arabidopsis transcription factors regulating cold acclimation. Physiol Plant 126:72–80

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu J-K (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126:52–61

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39

    Article  PubMed  CAS  Google Scholar 

  • Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • van Heerden PDR, Krüger GHJ, Strasser RJ (2003b) Dark chilling effects on soybean genotypes during vegetative development: parallel studies of CO2 assimilation, chlorophyll a fluorescence kinetics O-J-I-P and nitrogen fixation. Physiol Plant 117:476–491

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hipkins MF, Baker NR (1986) Spectroscopy. In: Hipkins MF, Baker NR (eds) Photosynthesis energy transduction, a practical approach. IRL Press, Oxford, pp 63–64

    Google Scholar 

  • 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

    Google Scholar 

  • Jajoo A, Bharti S, Govindjee (1998) Inorganic anions induce state changes in spinach thylakoid membranes. FEBS Lett 434:193–196

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kaniuga Z (1997) Galactolipase and chilling sensitivity of plants. Acta Biochim Polon 44:21–39

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kim E-H, Chow WS, Horton P, Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes. Biochim Biophys Acta 1708:187–195

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kirchhoff H, Mukherjee U, Galla H-J (2002) Molecular architecture of the thylakoid membrane: lipid diffusion space for plastoquinone. Biochemistry 41:4872–4882

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Environ 23:337–350

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666:142–157

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mehta M, Sarafis V, Critchley C (1999) Thylakoid membrane architecture. Aust J Plant Physiol 26:709–716

    Article  CAS  Google Scholar 

  • Mustárdy L, Garab G (2003) Granum revisited. A three-dimensional model—where things fall into place. Trends Plant Sci 8:117–122

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Scheller HV, Haldrup A (2005) Photoinhibition of photosystem I. Planta 221:5–8

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Vredenberg WJ, Kasalicky V, Durchan M, Prasil O (2006) The chlorophyll a fluorescence induction pattern in chloroplasts upon repetitive single turnover excitations: accumulation and function of QB-nonreducing centers. Biochim Biophys Acta 1757:173–181

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant Cell Physiol 45:1595–1602

    Article  PubMed  CAS  Google Scholar 

  • Zhou YH, Yu JQ, Huang L F, Nogués S (2004) The relationship between CO2 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

    Article  Google Scholar 

  • 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

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Acknowledgments

We are grateful to Dr. E. Simeonova and Dr. A. Drozak (Department of Plant Physiology, University of Warsaw) for the excellent assistance in the preliminary experiments and to Prof. J. Bryla (Department of Metabolic Regulation, University of Warsaw) for critical reading of the manuscript and to Dr. P. R. van Hasselt (Laboratory of Plant Physiology, University of Groningen) for initiating the cooperation between University of Groningen and University of Warsaw. This work was supported by a grant from the Polish Ministry of Scientific Research and Information Technology (MNiI) No 3 PO4C 109 23 (MG) and partly by a grant from Netherlands Organizations (Productschap Tuinbouw, NOVEM, DLO, LNV and some private breeding companies) (JHV). The preliminary experiments were partly supported by grants of MNiI No 1521/14, 1561/20 (MG) and BST-1059/BF (BK). We wish to thank Dr. M. Kiersnowska (Department of Cytophysiology, University of Warsaw) for providing an access to the Huygens Suite software. The authors are also grateful to Dr. J. J. S. van Rensen (Department of Plant Physiology, Wageningen University and Research Centre) for using the Hansatech PEA fluorometer and Prof. J. T. M. Elzega (Laboratory of Plant Physiology, University of Groningen) for critical reading of the manuscript.

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  1. Malgorzata Rosiak

    Present address: Department of Biotechnology, Bioton Co. Ltd, 05-850, Ożarów Mazowiecki, Poland

Authors and Affiliations

  1. Department of Metabolic Regulation, Institute of Biochemistry, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096, Warsaw, Poland

    Maciej Garstka, Izabela Rumak, Katarzyna Gieczewska & Malgorzata Rosiak

  2. Department of Plant Anatomy and Cytology, Institute of Plant Experimental Biology, Faculty of Biology, University of Warsaw, 02-096, Warsaw, Poland

    Joanna Koziol-Lipinska & Agnieszka Mostowska

  3. Laboratory of Plant Physiology, University of Groningen, 9750, AA Haren, The Netherlands

    Jan Henk Venema

  4. Department of Biophysics, Institute of Experimental Physics, Faculty of Physics, University of Warsaw, Zwirki i Wigury 93, 02-089, Warsaw, Poland

    Borys Kierdaszuk

  5. Department of Plant Physiology, Wageningen University and Research Centre, 6703 BD, Wageningen, The Netherlands

    Wim J. Vredenberg

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  1. Maciej Garstka
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Correspondence to Maciej Garstka.

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Dedicated to Prof. Zbigniew Kaniuga on the 25th anniversary of his initiation of studies on chilling-induced stress in plants.

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Garstka, M., Venema, J.H., Rumak, I. et al. 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 226, 1165–1181 (2007). https://doi.org/10.1007/s00425-007-0562-7

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