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Photosynthesis Research

, Volume 103, Issue 3, pp 175–182 | Cite as

The different effects of chilling stress under moderate light intensity on photosystem II compared with photosystem I and subsequent recovery in tropical tree species

  • Wei Huang
  • Shi-Bao Zhang
  • Kun-Fang CaoEmail author
Regular Paper

Abstract

Tropical plants are sensitive to chilling temperatures above zero but it is still unclear whether photosystem I (PSI) or photosystem II (PSII) of tropical plants is mainly affected by chilling temperatures. In this study, the effect of 4°C associated with various light densities on PSII and PSI was studied in the potted seedlings of four tropical evergreen tree species grown in an open field, Khaya ivorensis, Pometia tomentosa, Dalbergia odorifera, and Erythrophleum guineense. After 8 h chilling exposure at the different photosynthetic flux densities of 20, 50, 100, 150 μmol m−2 s−1, the maximum quantum yield of PSII (F v /F m) in all of the four species decreased little, while the quantity of efficient PSI complex (P m) remained stable in all species except E. guineense. However, after chilling exposure under 250 μmol m−2 s−1 for 24 h, F v /F m was severely photoinhibited in all species whereas P m was relative stable in all plants except E. guineense. At the chilling temperature of 4°C, electron transport from PSII to PSI was blocked because of excessive reduction of primary electron acceptor of PSII. F v /F m in these species except E. guineense recovered to ~90% after 8 h recovery in low light, suggesting the dependence of the recovery of PSII on moderate PSI and/or PSII activity. These results suggest that PSII is more sensitive to chilling temperature under the moderate light than PSI in tropical trees, and the photoinhibition of PSII and closure of PSII reaction centers can serve to protect PSI.

Keywords

Tropical trees Photosystem I Photosystem II Photoinhibition Recovery 

Abbreviations

CEF

Cyclic electron flow

Fo

Minimum chlorophyll fluorescence

Fm

Maximum chlorophyll fluorescence

Fv/Fm

Maximum quantum yield of PSII

NPQ

Non-photochemical quenching

PSI

Photosystem I

PSII

Photosystem II

Pm

Maximal change of P700 signal upon quantitative transformation of P700 from the fully reduced to the fully oxidized state

qP

Photochemical quenching

QA

Primary quinone electron acceptor of PSII

Notes

Acknowledgments

The CAS-XTBG plant germplasm bank provided the cold storage room for the chilling experiment, and Xishuangbanna Station for Tropical Rain Forest Ecosystem Studies (XSTRE) provided climatic data. This study was supported through an open project grant funded by the Key Laboratory of National Forestry Bureau for Fast-growing Tree Breeding and Cultivation in Central South China.

References

  1. Adir N, Shochat S, Ohad I (1990) Light-dependent D1 protein synthesis and translocation is regulated by reaction center II. J Biol Chem 265:12563–12568PubMedGoogle Scholar
  2. Aro EM, Virgin I, Andersson B (1993a) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134CrossRefPubMedGoogle Scholar
  3. Aro EM, McCaffery S, Anderson J (1993b) Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol 103:835–843PubMedGoogle Scholar
  4. Barbato R, Friso G, Rigoni F, Dalla VF, Giacometti GM (1992) Structural changes and lateral redistribution of photosystem II during donor side photoinhibition of thylakoids. J Cell Biol 119:325–335CrossRefPubMedGoogle Scholar
  5. Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66CrossRefPubMedGoogle Scholar
  6. Barth C, Krause GH (1999) Inhibition of photosystem I and II in chilling-sensitive and chilling-tolerant plants under light and low-temperature stress. Z Naturforsch C 54:645–657Google Scholar
  7. Briantais LM, Comic G, Hodges M (1988) The modification of chlorophyll fluorescence of Chlamydomonas reinhardtii by photoinhibition and chloramphenicol addition suggests a form of PS II less susceptible to degradation. FEBS Lett 236:226–230CrossRefGoogle Scholar
  8. Gilmore AM, Bjorkman O (1995) Temperature-sensitive coupling and uncoupling of ATPase-mediated, nonradiative energy dissipation: similarities between chloroplasts and leaves. Planta 197:646–654CrossRefGoogle Scholar
  9. Guenther JE, Melis A (1990) The physiological significance of photosystem II heterogeneity in chloroplasts. Photosynth Res 23:105–109CrossRefGoogle Scholar
  10. Havaux M, Davaud A (1994) Photoinhibition of photosynthesis in chilled potato leaves is not correlated with a loss of photosystem II activity—preferential inactivation of photosystem I. Photosynth Res 40:75–92CrossRefGoogle Scholar
  11. Huner NPA, Maxwell DP, Gray GR, Savitch LV, Krol M, Ivanov AG, Falk S (1996) Sensing environmental temperature change through imbalances between energy supply and energy consumption: redox state of photosystem II. Physiol Plant 98:358–364CrossRefGoogle Scholar
  12. Ivanov AG, Morgan RM, Gray GR, Velitchkova MY, Huner NPA (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 430:288–292CrossRefPubMedGoogle Scholar
  13. Kim SJ, Lee CH, Hope AB, Chow WS (2001) Inhibition of photosystem I and II and enhanced back flow of photosystem I electrons in cucumber leaf discs chilled in the light. Plant Cell Physiol 42:842–848CrossRefPubMedGoogle Scholar
  14. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basis. Annu Rev Plant Physiol Plant Mol Biol 42:313–349CrossRefGoogle Scholar
  15. 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 215:541–548CrossRefPubMedGoogle Scholar
  16. Miyake C, Horiguchi S, Makino A, Shinzaki Y, Yamamoto H, Tomizawa K (2005) Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of chl fluorescence in tobacco leaves. Plant Cell Physiol 46:1819–1830CrossRefPubMedGoogle Scholar
  17. Neidhardt J, Benemann JR, Zhang L-P, Melis A (1998) Photosystem II repair and chloroplast recovery from irradiance stress: relationship between chronic photoinhibition, light-harvesting chlorophyll antenna size and photosynthetic productivity in Dunaliella sallia (green algae). Photosynth Res 56:175–184CrossRefGoogle Scholar
  18. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359CrossRefPubMedGoogle Scholar
  19. Oquist G, Hurry VM, Huner NPA (1993) The temperature dependence of the redox state of QA and susceptibility of photosynthesis to photoinhibition. Plant Physiol Biochem 31:683–691Google Scholar
  20. Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44CrossRefGoogle Scholar
  21. Prasil O, Adir N, Ohad I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. In: Barber J (ed) Topics in photosynthesis, Elsevier, Amsterdam, The Netherlands, pp 295–348Google Scholar
  22. Salonen M, Aro EM, Rintamäki E (1998) Reversible phosphorylation and turnover of the D1 protein under various redox states of photosystem II induced by low temperature photoinhibition. Photosynth Res 58:143–151CrossRefGoogle Scholar
  23. Sonoike K (1995) Selective photoinhibition of photosystem I in isolated thylakoid membranes from cucumber and spinach. Plant Cell Physiol 36:825–830Google Scholar
  24. Sonoike K (1999) The different roles of chilling temperatures in the photoinhibition of photosystem I and photosystem II. J Photochem Photobiol B 48:136–141CrossRefGoogle Scholar
  25. Sonoike K (2006) Photoinhibition and protection of photosystem I. In: Golbeck JH (ed) Photosystem I: the light-driven plastocyanin: ferredoxin oxidoreductase, series advances in photosynthesis and respiration, vol 24. Springer, Dordrecht, pp 657–668Google Scholar
  26. Sonoike K, Terashima I (1994) Mechanism of photosystem-I photoinhibition in leaves of Cucumis sativus L. Planta 194:287–293CrossRefGoogle Scholar
  27. Sun Z-L, Lee H-Y, Matsubara S, Hope AB, Pogson BJ, Hong Y-N, Chow WS (2006) Photoprotection of residual functional photosystem II units that survive illumination in the absence of repair, and their critical role in subsequent recovery. Physiol Plant 128:415–424CrossRefGoogle Scholar
  28. Sundby C, McCaffery S, Anderson JM (1993) Turnover of the photosystem II D1 protein in higher plants under photoinhibitory and nonphotoinhibitory irradiance. J Biol Chem 268:25476–25482PubMedGoogle Scholar
  29. Taniguchi M, Kuroda H, Satoh K (1993) ATP-dependent protein synthesis in isolated pea chloroplasts. FEBS Lett 317:57–61CrossRefPubMedGoogle Scholar
  30. Teicher HB, Møller BL, Scheller HV (2000) Photoinhibition of photosystem I in field-grown barley (Hordeum vulgare L.): induction, recovery and acclimation. Photosynth Res 64:53–61CrossRefGoogle Scholar
  31. Terashima I, Funayama S, Sonoike K (1994) The site of photoinhibition in leaves of Cucumis-sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193:300–306CrossRefGoogle Scholar
  32. Tjus SE, Møller BL, Scheller HV (1998) Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol 116:755–764CrossRefPubMedGoogle Scholar
  33. Tjus SE, Møller BL, Scheller HV (1999) Photoinhibition of photosystem I damages both reaction centre proteins PSI-A and PSI-B and acceptor side located small photosystem I polypeptides. Photosynth Res 60:75–86CrossRefGoogle Scholar
  34. Tyystjarvi E, Aro EM (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93:2213–2218CrossRefPubMedGoogle Scholar
  35. van Wijk KJ, Bingsmark S, Aro EM, Andersson B (1995) In vitro synthesis and assembly of photosystem II core proteins. The D1 protein can be incorporated into photosystem II in isolated chloroplasts and thylakoids. J Biol Chem 270:25685–25695CrossRefPubMedGoogle Scholar
  36. Zhang S-P, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis. Plant Cell Physiol 45:1595–1602CrossRefPubMedGoogle Scholar
  37. Zhang Y-P, Xu Z-F (2000) Analysis on meteorological cause of cold damaging to tropical crops in Xishuangbanna in 1999. J Yunnan Trop Crop Sci Technol (China) 23(2):6–8Google Scholar
  38. Zhou J, Lan Q-J, Tang J-H, Lu Y-C (2008) Survey of chilling injury to tropical and subtropical plant germplasm resources in Guangxi. Guangxi Trop Agric (China) 117:25–29Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical GardenChinese Academy of SciencesMenglaChina
  2. 2.School of Life ScienceUniversity of Science and Technology of ChinaHefeiChina

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