Photosynthesis Research

, Volume 117, Issue 1–3, pp 547–556 | Cite as

Age-dependent changes in the functions and compositions of photosynthetic complexes in the thylakoid membranes of Arabidopsis thaliana

  • Krishna Nath
  • Bong-Kwan Phee
  • Suyeong Jeong
  • Sun Yi Lee
  • Yoshio Tateno
  • Suleyman I. Allakhverdiev
  • Choon-Hwan Lee
  • Hong Gil Nam
Regular Paper


Photosynthetic complexes in the thylakoid membrane of plant leaves primarily function as energy-harvesting machinery during the growth period. However, leaves undergo developmental and functional transitions along aging and, at the senescence stage, these complexes become major sources for nutrients to be remobilized to other organs such as developing seeds. Here, we investigated age-dependent changes in the functions and compositions of photosynthetic complexes during natural leaf senescence in Arabidopsis thaliana. We found that Chl a/b ratios decreased during the natural leaf senescence along with decrease of the total chlorophyll content. The photosynthetic parameters measured by the chlorophyll fluorescence, photochemical efficiency (F v/F m) of photosystem II, non-photochemical quenching, and the electron transfer rate, showed a differential decline in the senescing part of the leaves. The CO2 assimilation rate and the activity of PSI activity measured from whole senescing leaves remained relatively intact until 28 days of leaf age but declined sharply thereafter. Examination of the behaviors of the individual components in the photosynthetic complex showed that the components on the whole are decreased, but again showed differential decline during leaf senescence. Notably, D1, a PSII reaction center protein, was almost not present but PsaA/B, a PSI reaction center protein is still remained at the senescence stage. Taken together, our results indicate that the compositions and structures of the photosynthetic complexes are differentially utilized at different stages of leaf, but the most dramatic change was observed at the senescence stage, possibly to comply with the physiological states of the senescence process.


Arabidopsis thaliana Chl contents and Chl a/b ratio Developmental stage and senescence Nutrient mobilization Photosynthetic performance Photosynthetic complexes and their components 



Blue-native polyacrylamide gel electrophoresis




Electron transport rate


Maximum photochemical efficiency of PSII for dark-adapted sample


Light-harvesting complex


Non-photochemical quenching


Photosynthetically active radiation




Reaction center



The authors thank Dr. Sunghyun Hong for providing critical feedback on this manuscript. This study was supported by the Research Center Program of IBS (Institute for Basic Science, No.CA1208) and the National Research Foundation of Korea (The National Honor Scientist Support Program, No.20100020417) funded by the Korea government (MEST) in Korea. SIA was supported by grants from the Russian Foundation for Basic Research and by the Molecular and Cell Biology Programs of the Russian Academy of Sciences. CHL was supported by a grant from the National Research Foundation of Korea (NRF), funded by MEST (No. 2012-0004968).

Supplementary material

11120_2013_9906_MOESM1_ESM.jpg (138 kb)
Supplementary material 1 (JPEG 137 kb). Suppl. Fig. 1 Light induction curve of ETR and NPQ during successive leaf ages under different intensities of PAR. a. ETR, electron transport rate, b. NPQ, non-photochemical quenching. PAR, photosynthetically active radiation. All measurements were carried out at room temperature. Each measurement was performed with five leaves. The means and standard errors (±SE) from three to five replicates are shown


  1. Allakhverdiev SI (2011) Recent progress in the studies of structure and function of photosystem II. J Photochem Photobiol B: Biol 104:1–385CrossRefGoogle Scholar
  2. Allakhverdiev SI (2012) Photosynthesis research for sustainability: from natural to artificial. Biochim Biophys Acta 1817:1107–1524PubMedCrossRefGoogle Scholar
  3. Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6:317–326PubMedCrossRefGoogle Scholar
  4. Bhanumathi G, Murthy SDS (2011) Senescence induced alterations in the photosynthetic electron transport activities in maize primary leaves. Bot Res Intl 4:65–68Google Scholar
  5. Biswal UC, Mohanty P (1976) Aging induced changes in photosynthetic electron transport of detached barley leaves. Plant Cell Physiol 17:323–332Google Scholar
  6. Camp PJ, Huber SC, Burke JJ, Moreland DE (1982) Biochemical changes that occur during senescence of wheat leaves. I. Basis for the reduction of photosynthesis. Plant Physiol 70:1641–1646PubMedCrossRefGoogle Scholar
  7. Chen Z, Gallie DR (2008) Dehydroascorbate reductase affects non-photochemical quenching and photosynthetic performance. JBC 283:21347–21361CrossRefGoogle Scholar
  8. Crafts-Brandner SJ, Salvucci ME, Egli DB (1990) Changes in ribulose bisphosphate carboxylase/oxygenase and ribulose 5-phosphate kinase abundances and photosynthetic capacity during leaf senescence. Photosynth Res 23:223–230CrossRefGoogle Scholar
  9. Croce R, Bassi R (1998) The light harvesting complex of photosystem I: pigment composition and stoichiometry. In: Garab G (ed) Photosynthesis: mechanisms and effects 1:421–424. Kluwer Academic, DordrechtGoogle Scholar
  10. Croce R, van Amerongen H (2013) Light-harvesting in photosystem I. Photosynth Res. doi: 10.1007/s11120-013-9838-x Google Scholar
  11. Diaz C, Purdy S, Christ A, Gaudry MJF, Wingler A, Daubresse MC (2005) Characterization of markers to determine the extent and variability of leaf senescence in arabidopsis. A metabolic profiling approach. Plant Physiol 138:898–908PubMedCrossRefGoogle Scholar
  12. Feller U, Fischer A (1994) Nitrogen metabolism in senescing leaves. Crit Rev Plant Sci 13:241–273Google Scholar
  13. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92CrossRefGoogle Scholar
  14. Gepstein S (1988) Photosynthesis in senescence and aging in plants. In: Leopold AC, Nooden L (eds) Senescence and aging in plants. Academic Press, San Diego, pp 85–109Google Scholar
  15. Ghosh S, Mahoney SR, Penterman JN, Peirson D, Dumbroff EB (2001) Ultrastructural and biochemical changes in chloroplasts during Brassica napus senescence. Plant Physiol Biochem 39:777–784CrossRefGoogle Scholar
  16. Grassl J, Pruzinska A, Hortensteiner S, Taylor NL, Millar AH (2012) Early events in plastid protein degradation in stay-green arabidopsis reveal differential regulation beyond the retention of LHCII and chlorophyll. J Proteome Res 11:5443–5452PubMedCrossRefGoogle Scholar
  17. Green BR, Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47:685–714PubMedCrossRefGoogle Scholar
  18. Holloway PJ, Maclean DJ, Scott KJ (1983) Rate-limiting steps of electron transport in chloroplasts during ontogeny and senescence of barley. Plant Physiol 72:795–801PubMedCrossRefGoogle Scholar
  19. Huang W, Chen Q, Zhu Y, Hu F, Zhang L, Ma Z, He Z, Jirong Huang (2013) Arabidopsis thylakoid formation 1 is a critical regulator for dynamics of PSII-LHCII complexes in leaf senescence and excess light. Mol Plant. doi: 10.1093/mp/sst069 Google Scholar
  20. Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4:236–240PubMedCrossRefGoogle Scholar
  21. Kim JH, Kim SJ, Cho SH, Chow WS, Lee CH (2005) Photosystem I acceptor side limitation is a prerequisite for the reversible decrease in the maximum extent of P700 oxidation after short-term chilling in the light in four plant species with different chilling sensitivities. Physiol Plant 123:100–107CrossRefGoogle Scholar
  22. Lepeduš H, Jurković V, Štolfa I, Ćurković-Perica M, Fulgosi H, Cesar V (2010) Changes in photosystem II photochemistry in senescing maple leaves. Croat Chem Acta 83:379–386Google Scholar
  23. Li J, Pandeya D, Nath K, Zulfugarov IS, Yoo SC, Zhang H, Yoo JH, Cho SH, Koh HJ, Kim DS, Seo HS, Kang BC, Lee CH, Paek NC (2010) ZEBRA-NECROSIS, a thylakoid-bound protein, is critical for the photoprotection of developing chloroplasts during early leaf development. Plant J 62:713–725PubMedCrossRefGoogle Scholar
  24. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136PubMedCrossRefGoogle Scholar
  25. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428:287–292PubMedCrossRefGoogle Scholar
  26. Matile P, Schellenberg M, Peisker C (1992) Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187:230–235PubMedCrossRefGoogle Scholar
  27. Morita R, Sato Y, Masuda Y, Nishimura M, Kusaba M (2009) Defect in non-yellow coloring 3, an α/β hydrolase-fold family protein, causes a stay-green phenotype during leaf senescence in rice. Plant J 59:940–952PubMedCrossRefGoogle Scholar
  28. Neilson JAD, Durnford DG (2010) Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth Res 106:57–71PubMedCrossRefGoogle Scholar
  29. Nelson N, Yocum CF (2006) Structure and function of photosystem I and II. Annu Rev Plant Biol 57:521–565PubMedCrossRefGoogle Scholar
  30. Noodén LD, Guiamét JJ, John I (1997) Senescence mechanisms. Physiol Plant 101:746–753CrossRefGoogle Scholar
  31. Oh MH, Lee CH (1996) Dissambly of chloropyll-protein complexes in Arabidopsis thaliana during dark induced foliar senescence. J Plant Biol 39:301–307Google Scholar
  32. Oh MH, Kim YJ, Lee CH (2000) Leaf senescence in stay-green mutant of Arabidopsis thaliana: disassembly process of photosystem I and II during dark- incubation. J Biochem Mol Biol 33:256–262Google Scholar
  33. Ono Y, Wada S, Izumi M, Makino A, Ishida H (2013) Evidence for contribution of autophagy to Rubisco degradation during leaf senescence in Arabidopsis thaliana. Plant Cell Environ 36(6):1147–1159PubMedCrossRefGoogle Scholar
  34. Oster U, Tanaka R, Tanaka A, Rudiger W (2000) Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J 21:305–310PubMedCrossRefGoogle Scholar
  35. Park SY, Yu JW, Park JS, Li J, Yoo SC, Lee NY, Lee SK, Jeong SW, Seo HS, Koh HJ, Jeon JS, Park YI, Paek NC (2007) The senescence-induced stay-green protein regulates chlorophyll degradation. Plant Cell 19:1649–1664PubMedCrossRefGoogle Scholar
  36. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and chlorophyll b extracted with 4 different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394CrossRefGoogle Scholar
  37. Sabat SC, Grover A, Mohanty P (1989) Senescence induced alterations in the electron transport in wheat leaf chloroplasts. J Photochem Photobiol B3:175–183Google Scholar
  38. Sakuraba Y, Schelbert S, Park SY, Han SH, Lee BD, Andrès CB, Kessler F, Hörtensteiner S, Paek NC (2012) STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis. Plant Cell 24:507–518PubMedCrossRefGoogle Scholar
  39. Schägger H, van Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 99:223–231CrossRefGoogle Scholar
  40. Schelbert S, Aubry S, Burla B, Agne B, Kessler F, Krupinska K, Hörtensteinera S (2009) Pheophytin pheophorbide hydrolase (Pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21:767–785PubMedCrossRefGoogle Scholar
  41. Smart CM (1994) Gene expression during leaf senescence. New Phytol 126:419–448CrossRefGoogle Scholar
  42. Stoddart JL, Thomas H (1982) Leaf senescence. In: Boulter D, Parthier B (eds) Encyclopedia of plant physiology, Vol 14A. Springer, Berlin, pp 592–636Google Scholar
  43. Tang Y, Wen X, Lu C (2005) Differential changes in degradation of chlorophyll–protein complexes of photosystem I and photosystem II during flag leaf senescence of rice. Plant Physiol Biochem 43:193–201PubMedCrossRefGoogle Scholar
  44. Thomas H, Ougham HJ, Wagstaff C, Stead AD (2003) Defining senescence and death. J Exp Bot 54:1127–1132PubMedCrossRefGoogle Scholar
  45. Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886PubMedCrossRefGoogle Scholar
  46. Wientjes E, Croce R (2011) The light-harvesting complexes of higher-plant photosystem I: lhca1/4 and Lhca2/3 form two redemitting heterodimers. Biochem J 433:477–485PubMedCrossRefGoogle Scholar
  47. Wientjes E, Oostergetel GT, Jansson S, Boekema EJ, Croce R (2009) The role of Lhca complexes in the supramolecular organization of higher plant photosystem I. J Biol Chem 284:7803–7810PubMedCrossRefGoogle Scholar
  48. Wollman FA, Minai L, Nechushtai R (1999) The biogenesis and assembly of photosynthetic proteins in thylakoid membranes. Biochim Biophys Acta 1141:21–85Google Scholar
  49. Zhang Z, Li G, Gao H, Zhang L, Yang C, Liu P, Meng Q (2012) Characterization of photosynthetic performance during, senescence in stay-green and quick-leaf-senescence Zea mays L. Inbred Lines. PLoS One 7:e42936PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Krishna Nath
    • 1
  • Bong-Kwan Phee
    • 1
  • Suyeong Jeong
    • 2
    • 3
  • Sun Yi Lee
    • 4
  • Yoshio Tateno
    • 1
  • Suleyman I. Allakhverdiev
    • 5
    • 6
  • Choon-Hwan Lee
    • 7
  • Hong Gil Nam
    • 1
    • 3
  1. 1.Department of New BiologyDGISTDaeguRepublic of Korea
  2. 2.Department of Molecular and Life SciencePOSTECHPohangRepublic of Korea
  3. 3.Academy of New Biology for Plant Senescence and Life HistoryInstitute for Basic ScienceDaejeonRepublic of Korea
  4. 4.Protected Horticulture Research StationNational Institute of Horticultural & Herbal Science, RDABusanRepublic of Korea
  5. 5.Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  6. 6.Institute of Basic Biological ProblemsRussian Academy of SciencesPushchinoRussia
  7. 7.Department of Molecular BiologyPusan National UniversityBusanRepublic of Korea

Personalised recommendations