Photosynthetica 2004, 42(2):263-271 | DOI: 10.1023/B:PHOT.0000040599.63773.ef

High Irradiance Induced Changes of Photosystem 2 in Young and Mature Needles of Cypress (Cupressus sempervirens L.)

N. La Porta1, M. Bertamini1, N. Nedunchezhian2, K. Muthuchelian1
1 Istituto Agrario di San Michele all' Adige, 38010, San Michele all' Adige, Italy
2 Centre for Biodiversity and Forest Studies, School of Energy, Environment and Natural Resources, Madurai Kamaraj University, Madurai Kamaraj University, Madurai-625 021, India

Photoinhibition of photosynthesis was studied in young and mature detached sun needles of cypress under high irradiance (HI) of about 1 900 μmol m-2 s-1. The degree of photoinhibition was determined by means of the ratio of variable to maximum chlorophyll (Chl) fluorescence (Fv/Fm) and electron transport measurements. Compared with the mature needles, the young needles, containing about half the amount of Chl a+b per unit area, exhibited a higher proportion of total carotenoids (Car) as xanthophyll cycle pigments and had an increased ratio of Car/Chl a+b. The potential efficiency of photosystem (PS) 2, Fv/Fm, markedly declined in HI-treated young needles without significant increase of F0 level. In contrast, the Fv/Fm ratio declined with significant increase of F0 level in mature needles. In isolated thylakoids, the rate of whole chain and PS2 activity markedly decreased in young HI-needles in comparison with mature needles. A smaller inhibition of PS1 activity was observed in both needles. In the subsequent dark incubation, fast recovery was found in both needle Types that reached maximum PS2 efficiencies similar to those observed in non-photoinhibited needles. The artificial exogenous electron donors DPC, NH2OH, and Mn2+ failed to restore the HI-induced loss of PS2 activity in mature needles, while DPC and NH2OH significantly restored it in young needles. Hence, HI-inactivation was on the donor side of PS2 in young needles and on the acceptor side of PS2 in mature needles. Quantification of the PS2 reaction centre proteins D1 and 33 kDa protein of water splitting complex following HI-exposure of needles showed pronounced differences between young and mature needles. The large loss of PS2 activity in HI-needles was due to the marked loss of D1 protein of the PS2 reaction centre in mature needles and of the 33 kDa protein in young needles.

Additional key words: acclimation to irradiance; chlorophyll fluorescence; D1 protein; donor side; electron transport; photoinhibition; photosystem 2; proteins

Published: June 1, 2004  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
La Porta, N., Bertamini, M., Nedunchezhian, N., & Muthuchelian, K. (2004). High Irradiance Induced Changes of Photosystem 2 in Young and Mature Needles of Cypress (Cupressus sempervirens L.). Photosynthetica42(2), 263-271. doi: 10.1023/B:PHOT.0000040599.63773.ef
Download citation

References

  1. Adir, N., Zer, H., Shochat, S., Ohad, I.: Photoinhibition-a his-torical perspective.-Photosynth. Res. 76: 343-370, 2003. Go to original source...
  2. Allakhverdiev, S.I., Šetlíková, E., Klimov, V.V., Šetlík, I.: In photoinhibited photosystem II particles pheophytin photo-reduction remains unimpaired.-FEBS Lett. 226: 186-190, 1987. Go to original source...
  3. Anderson, J.M., Aro, E.-M.: Grana stacking and protection of Photosystem II in thylakoid membranes of higher plant leaves under sustained high irradiance: An hypothesis.-Photosynth. Res. 41: 315-326, 1994. Go to original source...
  4. Anderson, J.M., Park, Y.-I., Chow, W.S.: Photoinactivation and photoprotection of photosystem II in nature.-Physiol. Plant. 100: 214-223, 1997. Go to original source...
  5. Andersson, B., Styring, S.: Photosystem II. Molecular organiza-tion, function and acclimation.-Curr. Topics Bioenerget. 16: 2-81, 1991. Go to original source...
  6. Aro, E.-M., Virgin, I., Andersson, B.: Photoinhibition of Pho-tosystem II. Inactivation, protein damage and turnover.-Biochim. biophys. Acta 1143: 113-134, 1993. Go to original source...
  7. Asada, K., Heber, U., Schreiber, U.: Pool size of electrons that can be donated to P700 +, as determined in intact leaves: donation to P700 + from stromal components via the inter-system chain.-Plant Cell Physiol. 33: 927-932, 1992.
  8. Barber, J.: Molecular basis of photoinhibition.-In: Mathis, P. (ed.): Photosynthesis, From Light to Biosphere. Vol. IV. Pp. 159-164. Kluwer Academic Publishers, Dordrecht-Boston-London 1995. Go to original source...
  9. Belay, A.: An experimental investigation of inhibition of phyto-plankton at lake surface.-New Phytol. 89: 61-74, 1981. Go to original source...
  10. Bertamini, M., Nedunchezhian, N.: Photoinhibition of photosynthesis in Vitis berlandieri and Vitis rupestris leaves under field conditions.-Photosynthetica 40: 597-603, 2002. Go to original source...
  11. Berthold, D.A., Babcock, G.T., Yocum, C.A.: A highly resol-ved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. EPR and electron-transport properties.-FEBS Lett. 134: 231-234, 1981. Go to original source...
  12. Bolhàr-Nordenkampf, H.R., Hofer, M., Lechner, E.G.: Analysis of light induced reduction of the photochemical capacity in field grown plants. Evidence for photoinhibition?-Photo-synth. Res. 27: 31-39, 1991. Go to original source...
  13. Bratt, C.E., Arvidsson, P.-O., Carlsson, M., Åkerlund, H.-E.: Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration.-Photosynth. Res. 45: 169-175, 1995. Go to original source...
  14. Carpentier, R.: Influence of high light intensity on photo-synthesis: photoinhibition and energy dissipation.-In: Pessarakli, M. (ed.): Handbook of Photosynthesis. Pp. 443-450. Marcel Dekker, New York-Basel-Hong Kong 1995.
  15. Chow, W.S., Osmond, C.B., Huang, L.K.: Photosystem II func-tion and herbicide binding sites during photoinhibition of spi-nach chloroplasts in-vivo and in-vitro.-Photosynth. Res. 21: 17-26, 1989. Go to original source...
  16. Cleland, R.E., Melis, A., Neale, P.J.: Mechanism of photo-inhibition: photochemical reaction center inactivation in sys-tem II of chloroplasts.-Photosynth. Res. 9: 79-88, 1986. Go to original source...
  17. Critchley, C., Russell, A.W.: Photoinhibition of photosynthesis in vivo: The role of protein turnover in photosystem II.-Phy-siol. Plant. 92: 188-196, 1994. Go to original source...
  18. Demmig-Adams, B., Adams, W.W., III: The role of xanthophyll cycle carotenoids in the protection of photosynthesis.-Trends Plant Sci. 1: 21-26, 1996. Go to original source...
  19. Eckert, H.-J., Geiken, B., Bernarding, J., Napiwotzki, A., Eichler, H.-J., Renger, G.: Two sites of photoinhibition of the electron transfer in oxygen evolving and Tris-treated PS II membrane fragments from spinach.-Photosynth. Res. 27: 97-108, 1991. Go to original source...
  20. Enami, I., Kitamura, M., Tomo, T., Isokawa, Y., Ohta, H., Katoh, S.: Is the primary cause of thermal inactivation of oxy-gen evolution in spinach PS II membranes release of the ex-trinsic 33 kDa protein or of Mn?-Biochim. biophys. Acta 1186: 52-58, 1994. Go to original source...
  21. Eskling, M., Arvidsson, P.-O., Åkerlund, H.-E.: The xantho-phyll cycle, its regulation and components.-Physiol. Plant. 100: 806-816, 1997. Go to original source...
  22. Flexas, J., Hendrickson, L., Chow, W.S.: Photoinactivation of photosystem II in high light-acclimated cypresss.-Aust. J. Plant Physiol. 28: 755-764, 2001. Go to original source...
  23. Gilmore, A.M.: Mechanistic aspects of xanthophyll cycle de-pendent photoprotection in higher plant chloroplasts and leaves.-Physiol. Plant. 99: 197-209, 1997. Go to original source...
  24. Gilmore, A.M., Björkman, O.: Adenine nucleotides and the xanthophyll cycle in leaves. II. Comparison of the effects of CO2-and temperature-limited photosynthesis on photosystem II fluorescence quenching, the adenylate energy charge and violaxanthin de-epoxidation in cotton.-Planta 192: 537-544, 1994. Go to original source...
  25. Gong, H., Nilsen, S.: Effect of temperature on photoinhibitiuon of photosynthesis, recovery, and turnover of the 32 kDa chlo-roplast protein in Lemna gibba.-J. Plant Physiol. 135: 9-14, 1989. Go to original source...
  26. Hager, A.: Lichtbedingte pH-Erniedrigung in einem Chloro-plasten-Kompartiment als Ursache der enzymatischen Viola-xanthin-Zeaxanthin-Umwandlung; Beziehungen zur Photo-phosphorylierung.-Planta 89: 224-243, 1969. Go to original source...
  27. Hong, S.-S., Xu, D.-Q.: Light-induced increase in initial chloro-phyll fluorescence Fo level and the reversible inactivation of PS II reaction centers in soybean leaves.-Photosynth. Res. 61: 269-280, 1999. Go to original source...
  28. Horton, P., Ruban, A.V., Walters, R.G.: Regulation of light har-vesting in green plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 655-684, 1999. Go to original source...
  29. Hundal, T., Virgin, I., Styring, S., Andersson, B.: Changes in the organization of photosystem II following light-induced D1-protein degradation.-Biochim. biophys. Acta 1017: 235-241, 1990. Go to original source...
  30. Huner, N.P.A., Öquist, G., Sarhan, F.: Energy balance and acclimation to light and cold.-Trends Plant Sci. 3: 224-230, 1998. Go to original source...
  31. Krause, G.H.: Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms.-Physiol. Plant. 74: 566-574, 1988. Go to original source...
  32. Krause, G.H., Virgo, A., Winter, K.: High susceptibility to pho-toinhibition of young needles of tropical forest trees.-Planta 197: 583-591, 1995. Go to original source...
  33. Krause, G.H., Weis, E.: Chlorophyll fluorescence and photo-synthesis: The basics.-Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 313-349, 1991. Go to original source...
  34. Kyle, D.J., Kuang, T.-Y., Watson, J.L., Arntzen, C.J..: Movement of a sub-population of the light harvesting complex (LHII) from grana to stroma lamellae as a consequence of its phosphorylation.-Biochim. biophys. Acta 765: 89-96, 1984. Go to original source...
  35. Laemmli, U.K.: Cleavage of structural proteins during the as-sembly of the head of bacteriophage T4.-Nature 227: 680-685, 1970. Go to original source...
  36. Lichtenthaler, H.K.: Chlorophylls and carotenoids-pigments of photosynthetic biomembranes.-In: Colowick, S.P., Kaplan, N.O. (ed.): Methods in Enzymology. Vol. 148. Pp. 351-382. Academic Press, San Diego-New York-Berkeley-Boston-London-Sydney-Tokyo-Toronto 1987. Go to original source...
  37. Lutz, C., Steiger, A., Godde, D.: Influence of air pollutants and nutrient deficiency on D1 protein content and photosynthesis in young spruce trees.-Physiol. Plant. 85: 611-617, 1992. Go to original source...
  38. Melis, A.: Functional properties of Photosystem II â in spinach chloroplasts.-Biochim. biophys. Acta 808: 334-342, 1985. Go to original source...
  39. Millner, P.A., Gogel, G., Barber, J.: Investigation of the spatial relationships between photosystem 2 polypeptides by rever-sible crosslinking and diagonal electrophoresis.-Photosynth. Res. 13: 185-198, 1987. Go to original source...
  40. Mulkey, S.S., Pearcy, R.W.: Interactions between acclimation and photoinhibition of photosynthesis of a tropical forest understorey herb, Alocasia macrorrhiza, during simulated ca-nopy gap formation.-Funct. Ecol. 6: 719-729, 1992. Go to original source...
  41. Murata, N., Miyao, M., Omata, T., Matsunami, H., Kuwabara, T.: Stoichiometry of components in the photosynthetic oxy-gen evolution system of Photosystem II particles prepared with Triton X-100 from spinach chloroplasts.-Biochim. bio-phys. Acta 765: 363-369, 1984. Go to original source...
  42. Nedunchezhian, N., Morales, F., Abadia, A., Abadia, J.: Decline in photosynthetic electron transport activity and changes in thylakoid protein pattern in field grown iron deficient peach (Prunus persica L.).-Plant Sci. 129: 29-38, 1997. Go to original source...
  43. Ögren, E., Öquist, G., Hällgren, J.-E.: Photoinhibition of photo-synthesis in Lemna gibba as induced by the interaction between light and temperature. I. Photosynthesis in vivo.-Physiol. Plant. 62: 181-186, 1984. Go to original source...
  44. Ohad, I., Kyle, D.J., Hirschberg, J.: Light-dependent degrada-tion of the QB-protein in isolated pea thylakoids.-EMBO J. 4: 1655-1659, 1985. Go to original source...
  45. Öquist, G., Anderson, J.M., McCaffery, S., Chow, W.S.: Me-chanistic differences in photoinhibition of sun and shade plants.-Planta 188: 422-431, 1992. Go to original source...
  46. Ottander, C., Campbell, D., Öquist, G.: Seasonal changes in photosystem II organisation and pigment composition in Pinus sylvestris.-Planta 197: 176-183, 1995. Go to original source...
  47. Powles, S.B.: Photoinhibition of photosynthesis induced by vi-sible light.-Annu. Rev. Plant Physiol. 35: 15-44, 1984. Go to original source...
  48. Powles, S.B., Berry, J.A., Björkman, O.: Interaction between light and chilling temperature on the inhibition of photo-synthesis in chilling sensitive plants.-Plant Cell Environ. 6: 117-123, 1983. Go to original source...
  49. Prasil, O., Adir, N., Ohad, I.: Dynamics of photosystem II: me-chanism of photoinhibition and recovery process.-In: Barber, J. (ed.): The Photosystems: Structure, Function and Molecular Biology. Pp. 295-348. Elsevier, Amsterdam-London-New York-Tokyo 1992. Go to original source...
  50. Richter, M., Rühle, W., Wild, A.: Studies on the mechanism of photosystem II photoinhibition. II. The involvement of toxic oxygen species.-Photosynth. Res. 24: 237-243, 1990. Go to original source...
  51. Rintamäki, E., Salo, R., Lehtonen, E., Aro, E.-M.: Regulation of D1 protein degradation during photoinhibition of photosystem II in vivo: Phosphorylation of D1 protein in various plant groups.-Planta 195: 379-386, 1995. Go to original source...
  52. Schiefthaler, U., Russell, A.W., Bolhàr-Nordenkampf, H.R., Critchley, C.: Photoregulation and photodamage in Scheflera arboricola leaves adapted to different light environments.-Aust. J. Plant Physiol. 26: 485-494, 1999. Go to original source...
  53. Schnettger, B., Critchley, C., Santore, U.J., Graf, M., Krause, G.H.: Relationship between photoinhibition of photosyn-thesis, D1 protein turnover and chloroplast structure: effects of protein synthesis inhibitors.-Plant Cell Physiol. 17: 55-64, 1994. Go to original source...
  54. Šetlík, I., Allakhverdiev, S.I., Nedbal, L., Šetlíková, E., Klimov, V.V.: Three Types of photosystem II photoinactivation. 1. Da-maging processes on the acceptor side.-Photosynth. Res. 23: 39-48, 1990. Go to original source...
  55. Smith, B.M., Morrissey, P.J., Guenther, J.E., Nemson, J.A., Harrison, M.A., Allen, J.F., Melis, A.: Response of the photo-synthetic apparatus in Dunaliella salina (green algae) to irra-diance stress.-Plant Physiol. 93: 1433-1440, 1990. Go to original source...
  56. Somersalo, S., Krause, G.H.: Reversible photoinhibition of un-hardened and cold-acclimated spinach leaves at chilling tem-peratures.-Planta 180: 181-187, 1990. Go to original source...
  57. Thiele, A., Schirwitz, K., Winter, K., Krause, G.H.: Increased xanthophyll cycle activity and reduced D1 protein inactivation related to photoinhibition in two plant systems acclimated to excess light.-Plant Sci. 115: 237-250, 1996. Go to original source...
  58. Thiele, A., Winter, K., Krause, H.: Low inactivation of D1 pro-tein of photosystem II in young canopy leaves of Anacardium excelsum under high-light stress.-J. Plant Physiol. 151: 286-292, 1997. Go to original source...
  59. Tyystjärvi, E., Ali-Yrkkö, K., Kettunen, R., Aro, E.-M.: Slow degradation of the D1 protein is related to the susceptibility of low light-grown pumpkin plants to photoinhibition.-Plant Physiol. 100: 1310-1317, 1992. Go to original source...
  60. Wydrzynski, T., Govindjee: A new site of bicarbonate effect in photosystem II of photosynthesis: Evidence from chlorophyll fluorescence transients in spinach chloroplasts.-Biochim. biophys. Acta 387: 403-408, 1975. Go to original source...
  61. Yamamoto, H.Y.: Biochemistry of the violaxanthin cycle in higher plants.-Pure appl. Chem. 51: 639-648, 1979. Go to original source...
  62. Yamane, Y., Kashino, Y., Koike, H., Satoh, K.: Increases in the fluorescence Fo level and reversible inhibition of Photosystem II reaction center by high-temperature treatments in higher plants.-Photosynth. Res. 52: 57-64, 1997. Go to original source...