Skip to main content

Advertisement

SpringerLink
Log in

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

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

BN-PAGE:

Blue-native polyacrylamide gel electrophoresis

Chl:

Chlorophyll

ETR:

Electron transport rate

F v/F m :

Maximum photochemical efficiency of PSII for dark-adapted sample

LHC:

Light-harvesting complex

NPQ:

Non-photochemical quenching

PAR:

Photosynthetically active radiation

PS:

Photosystem

RC:

Reaction center

References

  • Allakhverdiev SI (2011) Recent progress in the studies of structure and function of photosystem II. J Photochem Photobiol B: Biol 104:1–385

    Article  CAS  Google Scholar 

  • Allakhverdiev SI (2012) Photosynthesis research for sustainability: from natural to artificial. Biochim Biophys Acta 1817:1107–1524

    Article  PubMed  CAS  Google Scholar 

  • Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6:317–326

    Article  PubMed  CAS  Google Scholar 

  • Bhanumathi G, Murthy SDS (2011) Senescence induced alterations in the photosynthetic electron transport activities in maize primary leaves. Bot Res Intl 4:65–68

    CAS  Google Scholar 

  • Biswal UC, Mohanty P (1976) Aging induced changes in photosynthetic electron transport of detached barley leaves. Plant Cell Physiol 17:323–332

    CAS  Google Scholar 

  • 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 70:1641–1646

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Gallie DR (2008) Dehydroascorbate reductase affects non-photochemical quenching and photosynthetic performance. JBC 283:21347–21361

    Article  CAS  Google Scholar 

  • 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 23:223–230

    Article  CAS  Google Scholar 

  • 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, Dordrecht

    Google Scholar 

  • Croce R, van Amerongen H (2013) Light-harvesting in photosystem I. Photosynth Res. doi:10.1007/s11120-013-9838-x

    Google Scholar 

  • 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 138:898–908

    Article  PubMed  CAS  Google Scholar 

  • Feller U, Fischer A (1994) Nitrogen metabolism in senescing leaves. Crit Rev Plant Sci 13:241–273

    CAS  Google Scholar 

  • 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 990:87–92

    Article  CAS  Google Scholar 

  • 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 85–109

    Google Scholar 

  • Ghosh S, Mahoney SR, Penterman JN, Peirson D, Dumbroff EB (2001) Ultrastructural and biochemical changes in chloroplasts during Brassica napus senescence. Plant Physiol Biochem 39:777–784

    Article  CAS  Google Scholar 

  • 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 11:5443–5452

    Article  PubMed  CAS  Google Scholar 

  • Green BR, Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47:685–714

    Article  PubMed  CAS  Google Scholar 

  • Holloway PJ, Maclean DJ, Scott KJ (1983) Rate-limiting steps of electron transport in chloroplasts during ontogeny and senescence of barley. Plant Physiol 72:795–801

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4:236–240

    Article  PubMed  Google Scholar 

  • 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 123:100–107

    Article  CAS  Google Scholar 

  • 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 83:379–386

    Google Scholar 

  • 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 62:713–725

    Article  PubMed  CAS  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  PubMed  CAS  Google Scholar 

  • 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 428:287–292

    Article  PubMed  CAS  Google Scholar 

  • Matile P, Schellenberg M, Peisker C (1992) Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187:230–235

    Article  PubMed  CAS  Google Scholar 

  • 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 59:940–952

    Article  PubMed  CAS  Google Scholar 

  • Neilson JAD, Durnford DG (2010) Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth Res 106:57–71

    Article  PubMed  CAS  Google Scholar 

  • Nelson N, Yocum CF (2006) Structure and function of photosystem I and II. Annu Rev Plant Biol 57:521–565

    Article  PubMed  CAS  Google Scholar 

  • Noodén LD, Guiamét JJ, John I (1997) Senescence mechanisms. Physiol Plant 101:746–753

    Article  Google Scholar 

  • Oh MH, Lee CH (1996) Dissambly of chloropyll-protein complexes in Arabidopsis thaliana during dark induced foliar senescence. J Plant Biol 39:301–307

    CAS  Google Scholar 

  • 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 33:256–262

    CAS  Google Scholar 

  • 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):1147–1159

    Article  PubMed  CAS  Google Scholar 

  • 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 21:305–310

    Article  PubMed  CAS  Google Scholar 

  • 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 19:1649–1664

    Article  PubMed  CAS  Google Scholar 

  • 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 975:384–394

    Article  CAS  Google Scholar 

  • Sabat SC, Grover A, Mohanty P (1989) Senescence induced alterations in the electron transport in wheat leaf chloroplasts. J Photochem Photobiol B3:175–183

    Google Scholar 

  • 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 24:507–518

    Article  PubMed  CAS  Google Scholar 

  • Schägger H, van Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 99:223–231

    Article  Google Scholar 

  • 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 21:767–785

    Article  PubMed  CAS  Google Scholar 

  • Smart CM (1994) Gene expression during leaf senescence. New Phytol 126:419–448

    Article  CAS  Google Scholar 

  • Stoddart JL, Thomas H (1982) Leaf senescence. In: Boulter D, Parthier B (eds) Encyclopedia of plant physiology, Vol 14A. Springer, Berlin, pp 592–636

    Google Scholar 

  • 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 43:193–201

    Article  PubMed  CAS  Google Scholar 

  • Thomas H, Ougham HJ, Wagstaff C, Stead AD (2003) Defining senescence and death. J Exp Bot 54:1127–1132

    Article  PubMed  CAS  Google Scholar 

  • Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886

    Article  PubMed  CAS  Google Scholar 

  • 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 433:477–485

    Article  PubMed  CAS  Google Scholar 

  • 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 284:7803–7810

    Article  PubMed  CAS  Google Scholar 

  • Wollman FA, Minai L, Nechushtai R (1999) The biogenesis and assembly of photosynthetic proteins in thylakoid membranes. Biochim Biophys Acta 1141:21–85

    Google Scholar 

  • 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:e42936

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

  1. Department of New Biology, DGIST, Daegu, 711-873, Republic of Korea

    Krishna Nath, Bong-Kwan Phee, Yoshio Tateno & Hong Gil Nam

  2. Department of Molecular and Life Science, POSTECH, Pohang, 790-784, Republic of Korea

    Suyeong Jeong

  3. Academy of New Biology for Plant Senescence and Life History, Institute for Basic Science, Daejeon, Republic of Korea

    Suyeong Jeong & Hong Gil Nam

  4. Protected Horticulture Research Station, National Institute of Horticultural & Herbal Science, RDA, Busan, 618-800, Republic of Korea

    Sun Yi Lee

  5. Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow, 127276, Russia

    Suleyman I. Allakhverdiev

  6. Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, 142290, Russia

    Suleyman I. Allakhverdiev

  7. Department of Molecular Biology, Pusan National University, Busan, 609-735, Republic of Korea

    Choon-Hwan Lee

Authors
  1. Krishna Nath
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bong-Kwan Phee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suyeong Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sun Yi Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoshio Tateno
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Suleyman I. Allakhverdiev
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Choon-Hwan Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hong Gil Nam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Choon-Hwan Lee or Hong Gil Nam.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11120_2013_9906_MOESM1_ESM.jpg

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

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nath, K., Phee, BK., Jeong, S. et al. Age-dependent changes in the functions and compositions of photosynthetic complexes in the thylakoid membranes of Arabidopsis thaliana . Photosynth Res 117, 547–556 (2013). https://doi.org/10.1007/s11120-013-9906-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-013-9906-2

Keywords

Search

Navigation