Skip to main content
SpringerLink
Log in

Simultaneous regulation of antenna size and photosystem I/II stoichiometry in Arabidopsis thaliana

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

The photosystem I/II ratio increased when antenna size was enlarged by transient induction of CAO in chlorophyll b -less mutants, thus indicating simultaneous regulation of antenna size and photosystem I/II stoichiometry.

Regulation of antenna size and photosystem I/II stoichiometry is an indispensable strategy for plants to acclimate to changes to light environments. When plants grown in high-light conditions are transferred to low-light conditions, the peripheral antennae of photosystems are enlarged. A change in the photosystem I/II ratio is also observed under the same light conditions. However, our knowledge of the correlation between antenna size modulation and variation in photosystem I/II stoichiometry remains limited. In this study, chlorophyll a oxygenase was transiently induced in Arabidopsis thaliana chlorophyll b-less mutants, ch1-1, to alter the antenna size without changing environmental conditions. In addition to the accumulation of chlorophyll b, the levels of the peripheral antenna complexes of both photosystems gradually increased, and these were assembled to the core antenna of both photosystems. However, the antenna size of photosystem II was greater than that of photosystem I. Immunoblot analysis of core antenna proteins showed that the number of photosystem I increased, but not that of photosystem II, resulting in an increase in the photosystem I/II ratio. These results clearly indicate that antenna size adjustment was coupled with changes in photosystem I/II stoichiometry. Based on these results, the physiological importance of simultaneous regulation of antenna size and photosystem I/II stoichiometry is discussed in relation to acclimation to light conditions.

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
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Anderson JM, Andersson B (1988) The dynamic photosynthetic membrane and regulation of solar energy conversion. Trends Biochem Sci 13:351–355

    Article  CAS  PubMed  Google Scholar 

  • Anderson JM, Chow WS, Park YI (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46:129–139

    Article  CAS  PubMed  Google Scholar 

  • Bailey S, Walters R, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801

    Article  CAS  PubMed  Google Scholar 

  • Bellafiore S, Barneche F, Peltier G, Rochaix J-D (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895

    Article  CAS  PubMed  Google Scholar 

  • Bellemare G, Bartlett SG, Chua NH (1982) Biosynthesis of chlorophyll a/b-binding polypeptides in wild type and the chlorina f2 mutant of barley. J Biol Chem 257:7762–7767

    CAS  PubMed  Google Scholar 

  • Biswal AK, Pattanayak GK, Pandey SS, Leelavathi S, Reddy VS, Govindjee Tripathy BC (2012) Light intensity-dependent modulation of chlorophyll b biosynthesis and photosynthesis by overexpression of chlorophyllide a oxygenase in tobacco. Plant Physiol 159:433–449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonente G, Howes BD, Caffarri S, Smulevich G, Bassi R (2008) Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro. J Biol Chem 283:8434–8445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bossmann B, Knoetzel J, Jansson S (1997) Screening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: absence of specific antenna proteins. Photosynth Res 52:127–136

    Article  CAS  Google Scholar 

  • Brestic M, Zivcak M, Kunderlikova K, Sytar O, Shao H, Kalaji H, Allakhverdiev S (2015) Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. Photosynth Res 125:151–166

    Article  CAS  PubMed  Google Scholar 

  • Caffarri S, Kouril R, Kereiche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J 28:3052–3063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chow WS, Melis A, Anderson JM (1990) Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis. Proc Natl Acad Sci 87:7502–7506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chow WS, Funk C, Hope AB, Govindjee (2000) Greening of intermittent-light-grown bean plants in continuous light: thylakoid components in relation to photosynthetic performance and capacity for photoprotection. Indian J Biochem Biophys 37:395–404

    CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Craft J, Samalova M, Baroux C, Townley H, Martinez A, Jepson I, Tsiantis M, Moore I (2005) New pOp/LhG4 vectors for stringent glucocorticoid-dependent transgene expression in Arabidopsis. Plant J 41:899–918

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Depege N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575

    Article  CAS  PubMed  Google Scholar 

  • Dietzel L, Bräutigam K, Pfannschmidt T (2008) Photosynthetic acclimation: state transitions and adjustment of photosystem stoichiometry—functional relationships between short-term and long-term light quality acclimation in plants. FEBS J 275:1080–1088

    Article  CAS  PubMed  Google Scholar 

  • Espineda CE, Linford AS, Devine D, Brusslan JA (1999) The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:10507–10511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan D-Y, Hope AB, Smith PJ, Jia H, Pace RJ, Anderson JM, Chow WS (2008) The stoichiometry of photosystem II to photosystem I in higher plants. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the sun: 14th international congress on photosynthesis. Springer Netherlands, Dordrecht, pp 7–10

    Chapter  Google Scholar 

  • Floris M, Bassi R, Robaglia C, Alboresi A, Lanet E (2013) Post-transcriptional control of light-harvesting genes expression under light stress. Plant Mol Biol 82:147–154

    Article  CAS  PubMed  Google Scholar 

  • Fujita Y (1997) A study on the dynamic features of photosystem stoichiometry: accomplishments and problems for future studies. Photosynth Res 53:83–93

    Article  CAS  Google Scholar 

  • Fujita Y, Ohki K, Murakami A (1985) Chromatic regulation of photosystem composition in the photosynthetic system of red and blue-green algae. Plant Cell Physiol 26:1541–1548

    CAS  Google Scholar 

  • Greene BA, Staehelin LA, Melis A (1988) Compensatory alterations in the photochemical apparatus of a photoregulatory, chlorophyll b-deficient mutant of maize. Plant Physiol 87:365–370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Havaux M, Dall’Osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horie Y, Ito H, Kusaba M, Tanaka R, Tanaka A (2009) Participation of chlorophyll b reductase in the initial step of the degradation of light-harvesting chlorophyll a/b-protein complexes in Arabidopsis. J Biol Chem 284:17449–17456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horton P, Ruban AV (1992) Regulation of photosystem II. Photosynth Res 34:375–385

    Article  CAS  PubMed  Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    Article  CAS  PubMed  Google Scholar 

  • Hu X, Tanaka A, Tanaka R (2013) Simple extraction methods that prevent the artifactual conversion of chlorophyll to chlorophyllide during pigment isolation from leaf samples. Plant Methods 9:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Ihalainen JA, Klimmek F, Ganeteg U, van Stokkum IHM, van Grondelle R, Jansson S, Dekker JP (2005) Excitation energy trapping in photosystem I complexes depleted in Lhca1 and Lhca4. FEBS Lett 579:4787–4791

    Article  CAS  PubMed  Google Scholar 

  • Jia T, Ito H, Hu X, Tanaka A (2015) Accumulation of the NON-YELLOW COLORING 1 protein of the chlorophyll cycle requires chlorophyll b in Arabidopsis thaliana. Plant J 81:586–596

    Article  CAS  PubMed  Google Scholar 

  • Kawamura M, Mimuro M, Fujita Y (1979) Quantitative relationship between two reaction centersin the photosynthetic system of blue-green algae. Plant Cell Physiol 20:697–705

    CAS  Google Scholar 

  • Kim JH, Glick RE, Melis A (1993) Dynamics of photosystem stoichiometry adjustment by light quality in chloroplasts. Plant Physiol 102:181–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim E-H, Li X-P, Razeghifard R, Anderson JM, Niyogi KK, Pogson BJ, Chow WS (2009) The multiple roles of light-harvesting chlorophyll a/b-protein complexes define structure and optimize function of Arabidopsis chloroplasts: a study using two chlorophyll b-less mutants. Biochim Biophys Acta 1787:973–984

    Article  CAS  PubMed  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Krol M, Spangfort MD, Huner N, Oquist G, Gustafsson P, Jansson S (1995) Chlorophyll a/b-binding proteins, pigment conversions, and early light-induced proteins in a chlorophyll b-less barley mutant. Plant Physiol 107:873–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulheim C, Agren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93

    Article  PubMed  Google Scholar 

  • Masuda T, Tanaka A, Melis A (2003) Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and Lhcb gene expression. Plant Mol Biol 51:757–771

    Article  CAS  PubMed  Google Scholar 

  • Melis A, Homann PH (1978) A selective effect of Mg2+ on the photochemistry at one type of reaction center in photosystem II of chloroplasts. Arch Biochem Biophys 190:523–530

    Article  CAS  PubMed  Google Scholar 

  • Melis A, Murakami A, Nemson JA, Aizawa K, Ohki K, Fujita Y (1996) Chromatic regulation in Chlamydomonas reinhardtii alters photosystem stoichiometry and improves the quantum efficiency of photosynthesis. Photosynth Res 47:253–265

    Article  CAS  PubMed  Google Scholar 

  • Murakami A, Fujita Y (1991) Steady state of photosynthetic electron transport in cells of the Cyanophyti Synechocystis PCC 6714 having different stoichiometry between PS I and PS II: analysis of flash-induced oxidation-reduction of cytochrome f and P700 under steady state of photosynthesis. Plant Cell Physiol 32:213–222

    CAS  Google Scholar 

  • Myers J, Graham JR, Wang RT (1980) Light harvesting in Anacystis nidulans studied in pigment mutants. Plant Physiol 66:1144–1149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niyogi KK, Grossman AR, Bjorkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Plumley GF, Schmidt GW (1995) Light-harvesting chlorophyll a/b complexes: interdependent pigment synthesis and protein assembly. Plant Cell 7:689–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polle JE, Benemann JR, Tanaka A, Melis A (2000) Photosynthetic apparatus organization and function in the wild type and a chlorophyll b-less mutant of Chlamydomonas reinhardtii. Dependence on carbon source. Planta 211:335–344

    Article  CAS  PubMed  Google Scholar 

  • Pribil M, Pesaresi P, Hertle A, Barbato R, Leister D (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol 8:e1000288

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin X, Suga M, Kuang T, Shen J-R (2015) Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348:989–995

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181

    Article  CAS  PubMed  Google Scholar 

  • Sato R, Ito H, Tanaka A (2015) Chlorophyll b degradation by chlorophyll b reductase under high-light conditions. Photosynth Res 126:249–259

    Article  CAS  PubMed  Google Scholar 

  • Schmid VH (2008) Light-harvesting complexes of vascular plants. Cell Mol Life Sci 65:3619–3639

    Article  CAS  PubMed  Google Scholar 

  • Shapiguzov A, Ingelsson B, Samol I, Andres C, Kessler F, Rochaix J-D, Vener AV, Goldschmidt-Clermont M (2010) The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc Natl Acad Sci USA 107:4782–4787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takabayashi A, Kurihara K, Kuwano M, Kasahara Y, Tanaka R, Tanaka A (2011) The oligomeric states of the photosystems and the light-harvesting complexes in the Chl b-less mutant. Plant Cell Physiol 52:2103–2114

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Iwai M, Takahashi Y, Minagawa J (2006) Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 103:477–482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka R, Tanaka A (2005) Effects of chlorophyllide a oxygenase overexpression on light acclimation in Arabidopsis thaliana. Photosynth Res 85:327–340

    Article  CAS  PubMed  Google Scholar 

  • Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346

    Article  CAS  PubMed  Google Scholar 

  • Tanaka A, Yamamoto Y, Tsuji H (1991) Formation of chlorophyll–protein complexes during greening 2. Redistribution of chlorophyll among apoproteins. Plant Cell Physiol 32:195–204

    CAS  Google Scholar 

  • Tanaka A, Ito H, Tanaka R, Tanaka NK, Yoshida K, Okada K (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc Natl Acad Sci USA 95:12719–12723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thornber JP, Highkin HR (1974) Composition of the photosynthetic apparatus of normal barley leaves and a mutant lacking chlorophyll b. Eur J Biochem 41:109–116

    Article  CAS  PubMed  Google Scholar 

  • Tikkanen M, Grieco M, Aro E-M (2011) Novel insights into plant light-harvesting complex II phosphorylation and ‘state transitions’. Trends Plant Sci 16:126–131

    Article  CAS  PubMed  Google Scholar 

  • Tzvetkova-Chevolleau T, Franck F, Alawady AE, Dall’Osto L, Carriere F, Bassi R, Grimm B, Nussaume L, Havaux M (2007) The light stress-induced protein ELIP2 is a regulator of chlorophyll synthesis in Arabidopsis thaliana. Plant J 50:795–809

    Article  CAS  PubMed  Google Scholar 

  • Webb MR, Melis A (1995) Chloroplast response in Dunaliella salina to irradiance stress (effect on thylakoid membrane protein assembly and function). Plant Physiol 107:885–893

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wielopolska A, Townley H, Moore I, Waterhouse P, Helliwell C (2005) A high-throughput inducible RNAi vector for plants. Plant Biotechnol J 3:583–590

    Article  CAS  PubMed  Google Scholar 

  • Wientjes E, Croce R (2011) The light-harvesting complexes of higher-plant photosystem I: Lhca1/4 and Lhca2/3 form two red-emitting heterodimers. Biochem J 433:477–485

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm C, Krämer P, Lenartz-Weiler I (1989) The energy distribution between the photosystems and light-induced changes in the stoichiometry of system I and II reaction centers in the chlorophyll b-containing alga Mantoniella squamata (Prasinophyceae). Photosynth Res 20:221–233

    CAS  PubMed  Google Scholar 

  • Wittig I, Braun HP, Schagger H (2006) Blue native PAGE. Nat Protoc 1:418–428

    Article  CAS  PubMed  Google Scholar 

  • Yamasato A, Nagata N, Tanaka R, Tanaka A (2005) The N-terminal domain of chlorophyllide a oxygenase confers protein instability in response to chlorophyll b accumulation in Arabidopsis. Plant Cell 17:1585–1597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zapata M, Rodríguez F, Garrido JL (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar Ecol Prog Ser 195:29–45

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Makio Yokono, Yukako Kato and Junko Kishimoto for technical assistance for antenna-size measurement. Finance of this study was provided by Core Research for Evolutional Science and Technology and the Japan Society for the Scientific Research 24370017 to A.T. T. J. was supported by a scholarship from China Scholarship Council.

Author information

Authors and Affiliations

  1. Institute of Low Temperature Science, Hokkaido University, N19 W8, Kita-ku, Sapporo, 060-0819, Japan

    Ting Jia, Hisashi Ito & Ayumi Tanaka

  2. CREST, Japan Science and Technology Agency, N19 W8, Kita-ku, Sapporo, 060-0819, Japan

    Hisashi Ito & Ayumi Tanaka

Authors
  1. Ting Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hisashi Ito
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ayumi Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hisashi Ito.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 1550 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jia, T., Ito, H. & Tanaka, A. Simultaneous regulation of antenna size and photosystem I/II stoichiometry in Arabidopsis thaliana . Planta 244, 1041–1053 (2016). https://doi.org/10.1007/s00425-016-2568-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-016-2568-5

Keywords

Search

Navigation