Characterization of photosystem II assembly complexes containing ONE-HELIX PROTEIN1 in Arabidopsis thaliana

Maeda, Hanaki; Takahashi, Koharu; Ueno, Yoshifumi; Sakata, Kei; Yokoyama, Akari; Yarimizu, Kozue; Myouga, Fumiyoshi; Shinozaki, Kazuo; Ozawa, Shin-Ichiro; Takahashi, Yuichiro; Tanaka, Ayumi; Ito, Hisashi; Akimoto, Seiji; Takabayashi, Atsushi; Tanaka, Ryouichi

doi:10.1007/s10265-022-01376-x

Regular Paper – Physiology/Biochemistry/Molecular and Cellular Biology
Published: 10 February 2022

Characterization of photosystem II assembly complexes containing ONE-HELIX PROTEIN1 in Arabidopsis thaliana

Journal of Plant Research volume 135, pages 361–376 (2022)Cite this article

435 Accesses
5 Altmetric
Metrics details

Abstract

The assembly process of photosystem II (PSII) requires several auxiliary proteins to form assembly intermediates. In plants, early assembly intermediates comprise D1 and D2 subunits of PSII together with a few auxiliary proteins including at least ONE-HELIX PROTEIN1 (OHP1), OHP2, and HIGH-CHLOROPHYLL FLUORESCENCE 244 (HCF244) proteins. Herein, we report the basic characterization of the assembling intermediates, which we purified from Arabidopsis transgenic plants overexpressing a tagged OHP1 protein and named the OHP1 complexes. We analyzed two major forms of OHP1 complexes by mass spectrometry, which revealed that the complexes consist of OHP1, OHP2, and HCF244 in addition to the PSII subunits D1, D2, and cytochrome b₅₅₉. Analysis of chlorophyll fluorescence showed that a major form of the complex binds chlorophyll a and carotenoids and performs quenching with a time constant of 420 ps. To identify the localization of the auxiliary proteins, we solubilized thylakoid membranes using a digitonin derivative, glycodiosgenin, and separated them into three fractions by ultracentrifugation, and detected these proteins in the loose pellet containing the stroma lamellae and the grana margins together with two chlorophyll biosynthesis enzymes. The results indicated that chlorophyll biosynthesis and assembly may take place in the same compartments of thylakoid membranes. Inducible suppression of the OHP2 mRNA substantially decreased the OHP2 protein in mature Arabidopsis leaves without a significant reduction in the maximum quantum yield of PSII under low-light conditions, but it compromised the yields under high-light conditions. This implies that the auxiliary protein is required for acclimation to high-light conditions.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

References

Andersson U, Heddad M, Adamska I (2003) Light stress-induced one-helix protein of the chlorophyll a/b-binding family associated with photosystem I. Plant Phys 132:811–820. https://doi.org/10.1104/pp.102.019281
CAS Article Google Scholar
Baena-González E, Aro E-M (2002) Biogenesis, assembly and turnover of photosystem II units. Philos Trans R Soc Lond B Biol Sci 357:1451–1460. https://doi.org/10.1098/rstb.2002.1141
CAS Article PubMed PubMed Central Google Scholar
Beck J, Lohscheider JN, Albert S, Andersson U, Mendgen KW, Rojas-Stütz MC, Adamska I, Funck D (2017) Small one-helix proteins are essential for photosynthesis in arabidopsis. Front Plant Sci 8:487. https://doi.org/10.3389/fpls.2017.00007
Article Google Scholar
Chotewutmontri P, Barkan A (2020) Light-induced psbA translation in plants is triggered by photosystem II damage via an assembly-linked autoregulatory circuit. Proc Natl Acad Sci USA 117:21775–21784. https://doi.org/10.1073/pnas.2007833117
CAS Article PubMed PubMed Central Google Scholar
Chotewutmontri P, Williams-Carrier R, Barkan A (2020) Exploring the link between photosystem ii assembly and translation of the chloroplast psbA mRNA. Plants 9:152. https://doi.org/10.3390/plants9020152
CAS Article PubMed Central Google Scholar
Clough S, Bent A (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
CAS Article PubMed Google Scholar
Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26:1367–1372. https://doi.org/10.1038/nbt.1511
CAS Article PubMed Google Scholar
Danielsson R, Suorsa M, Paakkarinen V, Albertsson PÅ, Styring S, Aro EM, Mamedov F (2006) Dimeric and monomeric organization of photosystem II: distribution of five distinct complexes in the different domains of the thylakoid membrane. J Biol Chem 281:14241–14249. https://doi.org/10.1074/jbc.M600634200
CAS Article PubMed Google Scholar
Furukawa R, Aso M, Fujita T, Akimoto S, Tanaka R, Tanaka A, Yokono M, Takabayashi A (2019) Formation of a PSI–PSII megacomplex containing LHCSR and PsbS in the moss Physcomitrella patens. J Plant Res 132:867–880. https://doi.org/10.1007/s10265-019-01138-2
CAS Article PubMed Google Scholar
García-Cerdán JG, Furst AL, McDonald KL, Schünemann D, Francis MB, Niyogi KK (2019) A thylakoid membrane-bound and redox-active rubredoxin (RBD1) functions in de novo assembly and repair of photosystem II. Proc Natl Acad Sci USA 1817:201903314–201916640. https://doi.org/10.1073/pnas.1903314116
CAS Article 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 - Gen Subj 990:87–92. https://doi.org/10.1016/S0304-4165(89)80016-9
CAS Article Google Scholar
Heinz S, Liauw P, Nickelsen J, Nowaczyk M (2016) Analysis of photosystem II biogenesis in cyanobacteria. Biochim Biophys Acta Bioenerg 1857:274–287. https://doi.org/10.1016/j.bbabio.2015.11.007
CAS Article Google Scholar
Hey D, Grimm B (2018) ONE-HELIX PROTEIN2 (OHP2) is required for the stability of OHP1 and assembly factor HCF244 and is functionally linked to PSII biogenesis. Plant Physiol 177:1453–1472. https://doi.org/10.1104/pp.18.00540
CAS Article PubMed PubMed Central Google Scholar
Hooper CM, Castleden IR, Tanz SK, Aryamanesh N, Millar AH (2017) SUBA4: The interactive data analysis centre for Arabidopsis subcellular protein locations. Nucleic Acids Res 45:D1064–D1074. https://doi.org/10.1093/nar/gkw1041
CAS Article PubMed Google Scholar
Järvi S, Suorsa M, Paakkarinen V, Aro E-M (2011) Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochem J 439:207–214. https://doi.org/10.1042/BJ20102155
CAS Article Google Scholar
Järvi S, Suorsa M, Aro EM (2015) Photosystem II repair in plant chloroplasts—regulation, assisting proteins and shared components with photosystem II biogenesis. Biochim Biophys Acta Bioenerg 1847:900–909. https://doi.org/10.1016/j.bbabio.2015.01.006
CAS Article Google Scholar
Kiss E, Knoppová J, Pascual Aznar G, Pilny J, Yu J, Halada P, Nixon PJ, Sobotka R, Komenda J (2019) A Photosynthesis-specific rubredoxin-like protein is required for efficient association of the D1 and D2 proteins during the initial steps of photosystem II assembly. Plant Cell 31:2019–2258. https://doi.org/10.1105/tpc.19.00155
CAS Article Google Scholar
Knoppová J, Sobotka R, Tichý M, Yu J, Konik P, Halada P, Nixon PJ, Komenda J (2014) Discovery of a chlorophyll binding protein complex involved in the early steps of Photosystem II assembly in Synechocystis. Plant Cell 26:1200–1212. https://doi.org/10.1105/tpc.114.123919
CAS Article PubMed PubMed Central Google Scholar
Knoppová J, Yu J, Janouškovec J, Halada P, Nixon PJ, Whitelegge JP, Komenda J (2021) The photosystem II assembly factor Ycf48 from the Cyanobacterium Synechocystis sp. PCC 6803 is lipidated usingan atypical lipobox sequence. Int J Mol Sci 22:3733. https://doi.org/10.3390/ijms22073733
CAS Article PubMed PubMed Central Google Scholar
Komenda J, Sobotka R (2016) Cyanobacterial high-light-inducible proteins—protectors of chlorophyll-protein synthesis and assembly. Biochim Biophys Acta Bioenerg 1857:288–295. https://doi.org/10.1016/j.bbabio.2015.08.011
CAS Article Google Scholar
Komenda J, Sobotka R, Nixon PJ (2012) Assembling and maintaining the Photosystem II complex in chloroplasts and cyanobacteria. Curr Opin Plant Biol 15:245–251. https://doi.org/10.1016/j.pbi.2012.01.017
CAS Article PubMed Google Scholar
Li Y, Liu B, Zhang J, Kong F, Zhang L, Meng H, Li W, Rochaix JD, Li D, Peng L (2019) OHP1, OHP2, and HCF244 form a transient functional complex with the photosystem II reaction center. Plant Physiol 179:195–208. https://doi.org/10.1104/pp.18.01231
CAS Article PubMed Google Scholar
Liang Z, Zhu N, Mai KK, Liu ZY, Tzeng D, Osteryoung KW, Zhong S, Staehelin LA, Kang BH (2018) Thylakoid-bound polysomes and a dynamin-related protein, FZL, mediate critical stages of the linear chloroplast biogenesis program in greening Arabidopsis cotyledons. Plant Cell 30:1476–1495. https://doi.org/10.1105/tpc.17.00972
CAS Article PubMed PubMed Central Google Scholar
Link S, Engelmann K, Meierhoff K, Westhoff P (2012) The atypical short-chain dehydrogenases HCF173 and HCF244 are jointly involved in translational initiation of the psbA mRNA of Arabidopsis. Plant Phys 160:2202–2218. https://doi.org/10.1104/pp.112.205104
CAS Article 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. https://doi.org/10.1038/nature02373
CAS Article PubMed Google Scholar
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:405–498. https://doi.org/10.1006/meth.2001.1262
CAS Article Google Scholar
Llansola-Portoles MJ, Sobotka R, Kish E, Shukla MK, Pascal AA, Polívka T, Robert B (2017) Twisting a β-carotene, an adaptive trick from nature for dissipating energy during photoprotection. J Biol Chem 292:1396–1403. https://doi.org/10.1074/jbc.M116.753723
CAS Article PubMed Google Scholar
Lu Y (2016) Identification and roles of photosystem ii assembly, stability, and repair factors in Arabidopsis. Front Plant Sci 7:209. https://doi.org/10.3389/fpls.2016.00168
Article Google Scholar
McDermott JJ, Watkins KP, Williams-Carrier R, Barkan A (2019) Ribonucleoprotein capture by in vivo expression of a designer pentatricopeptide repeat protein in Arabidopsis. Plant Cell 31:1723–1733. https://doi.org/10.1105/tpc.19.00177
CAS Article PubMed PubMed Central Google Scholar
Mimuro M, Yamazaki I, Itoh S, Tamai N, Satoh K (1988) Dynamic fluorescence properties of Dl-D2-cytochrome b-559 complex isolated from spinach chloroplasts: analysis by means of the time-resolved fluorescence spectra in picosecond time range. Biochim Biophys Acta Bioenerg 933:478–486. https://doi.org/10.1016/0005-2728(88)90083-7
CAS Article Google Scholar
Mimuro M, Akimoto S, Tomo T, Yokono M, Miyashita H, Tsuchiya T (2007) Delayed fluorescence observed in the nanosecond time region at 77 K originates directly from the photosystem II reaction center. Biochim Biophys Acta Bioenerg 1767:327–334. https://doi.org/10.1016/j.bbabio.2007.02.012
CAS Article Google Scholar
Myouga F, Takahashi K, Tanaka R, Nagata N, Kiss AZ, Funk C, Nomura Y, Nakagami H, Jansson S, Shinozaki K (2018) Stable accumulation of photosystem II requires ONE-HELIX PROTEIN1 (OHP1) of the light harvesting-like family. Plant Physiol 176:2277–2291. https://doi.org/10.1104/pp.17.01782
CAS Article PubMed PubMed Central Google Scholar
Nelson N, Yocum C (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565. https://doi.org/10.1146/annurev.arplant.57.032905.105350
CAS Article PubMed Google Scholar
Nickelsen J, Rengstl B (2013) Photosystem II assembly: from cyanobacteria to plants. Annu Rev Plant Biol 64:609–635. https://doi.org/10.1146/annurev-arplant-050312-120124
CAS Article PubMed Google Scholar
Niedzwiedzki DM, Tronina T, Liu H, Staleva H, Komenda J, Sobotka R, Blankenship RE, Polívka T (2016) Carotenoid-induced non-photochemical quenching in the cyanobacterial chlorophyll synthase-HliC/D complex. Biochim Biophys Acta Bioenerg 1857:1430–1439. https://doi.org/10.1016/j.bbabio.2016.04.280
CAS Article Google Scholar
Nishioka K, Kato Y, Ozawa SI, Takahashi Y, Sakamoto W (2021) Phos-tag-based approach to study protein phosphorylation in the thylakoid membrane. Photosyn Res 147:107–124. https://doi.org/10.1007/s11120-020-00803-1
CAS Article Google Scholar
Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46. https://doi.org/10.1111/j.1399-3054.2011.01457.x
CAS Article PubMed Google Scholar
Nishiyama Y, Murata N (2014) Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Appl Microbiol Biotech 98:8777–8796. https://doi.org/10.1007/s00253-014-6020-0
CAS Article Google Scholar
Plöchinger M, Schwenkert S, von Sydow L, Schröder WP, Meurer J (2016) Functional update of the auxiliary proteins PsbW, PsbY, HCF136, PsbN, TerC and ALB3 in maintenance and assembly of PSII. Front Plant Sci 7:423. https://doi.org/10.3389/fpls.2016.00423
Article PubMed PubMed Central Google Scholar
Psencik J, Hey D, Grimm B, Lokstein H (2020) Photoprotection of photosynthetic pigments in plant one-helix protein 1/2 heterodimers. J Phys Chem Lett 11:9387–9392. https://doi.org/10.1021/acs.jpclett.0c02660
CAS Article PubMed Google Scholar
Puthiyaveetil S, Tsabari O, Lowry T, Lenhert S, Lewis RR, Reich Z, Kirchhoff H (2014) Compartmentalization of the protein repair machinery in photosynthetic membranes. Proc Natl Acad Sci USA 111:15839–15844. https://doi.org/10.1073/pnas.1413739111
CAS Article PubMed PubMed Central Google Scholar
Schult K, Meierhoff K, Paradies S, Töller T, Wolff P, Westhoff P (2007) The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell 19:1329–1346. https://doi.org/10.1105/tpc.106.042895
CAS Article PubMed PubMed Central Google Scholar
Staleva H, Komenda J, Shukla MK, Šlouf V, Kaňa R, Polívka T, Sobotka R (2015) Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins. Nat Chem Biol 11:287–291. https://doi.org/10.1038/nchembio.1755
CAS Article PubMed Google Scholar
Su X, Ma J, Wei X, Cao P, Zhu D, Chang W, Liu Z, Zhang X, Li M (2017) Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex. Science 357:815–820. https://doi.org/10.1126/science.aan0327
CAS Article PubMed Google Scholar
Suorsa M, Rantala M, Danielsson R, Järvi S, Paakkarinen V, Schröder WP, Styring S, Mamedov F, Aro EM (2014) Dark-adapted spinach thylakoid protein heterogeneity offers insights into the photosystem II repair cycle. Biochim Biophys Acta Bioenerg 1837:1463–1471. https://doi.org/10.1016/j.bbabio.2013.11.014
CAS Article Google Scholar
Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60. https://doi.org/10.1038/nature09913
CAS Article PubMed Google Scholar
Walters RG, Shephard F, Rogers JJM, Rolfe SA, Horton P (2003) Identification of mutants of arabidopsis defective in acclimation of photosynthesis to the light environment. Plant Physiol 131:472–481. https://doi.org/10.1104/pp.015479
CAS Article PubMed PubMed Central Google Scholar
Wang L, Kim C, Xu X, Piskurewicz U, Dogra V, Singh S, Mahler H, Apel K (2016) Singlet oxygen- and EXECUTER1-mediated signaling is initiated in grana margins and depends on the protease FtsH2. Proc Natl Acad Sci U S A 113:E3792–E3800. https://doi.org/10.1073/pnas.1603562113
CAS Article 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. https://doi.org/10.1111/j.1467-7652.2005.00149.x
CAS Article PubMed Google Scholar
Williams-Carrier R, Brewster C, Belcher SE, Rojas M, Chotewutmontri P, Ljungdahl S, Barkan A (2019) The Arabidopsis pentatricopeptide repeat protein LPE1 and its maize ortholog are required for translation of the chloroplast psbJ RNA. Plant J 99:56–66. https://doi.org/10.1111/tpj.14308
CAS Article PubMed Google Scholar
Wu HY, Liu MS, Lin TP, Cheng YS (2011) Structural and functional assays of AtTLP18.3 identify its novel acid phosphatase activity in thylakoid lumen. Plant Phys 157:1015–1025. https://doi.org/10.1104/pp.111.184739
CAS Article Google Scholar
Yokono M, Takabayashi A, Akimoto S, Tanaka A (2015) A megacomplex composed of both photosystem reaction centres in higher plants. Nat Commun 6:6675. https://doi.org/10.1038/ncomms7675
CAS Article PubMed Google Scholar
Yu J, Knoppová J, Michoux F, Bialek W, Cota E, Shukla MK, Strašková A, Aznar GP, Sobotka R, Komenda J, Murray JW, Nixon PJ (2018) Ycf48 involved in the biogenesis of the oxygen-evolving photosystem II complex is a seven-bladed beta-propeller protein. Proc Natl Acad Sci USA 115:E7824–E7833. https://doi.org/10.1073/pnas.1800609115
CAS Article PubMed PubMed Central Google Scholar

Download references

Acknowledgements

The authors would like to thank Ms. Junko Kishimoto for her excellent technical assistance. We also thank Dr. Seiko Oka from the Open Facility, Global Facility Center, Creative Research Institution, Hokkaido University for allowing us to conduct mass spectroscopic analysis of protein samples using LTQ Orbitrap Discovery and providing insight and expertise that greatly assisted with our research. We thank Dr. Yusuke Kato (Okayama University) for providing the anti-D1 antibody, and Dr. Yao-Pin Lin and Dr. Yee-yung Charng (Academia Sinica, Taiwan) for providing the anti-ChlG antibody.

Funding

This study was supported by funding from the Japan Society for the Promotion of Science (JSPS) through the KAKENHI Grant numbers 16H06554 and 20H03017 to RT, 21K06217 to SIO, and 16H06553 and 20H03017 to SA, respectively.

Author information

Shin-Ichiro Ozawa
Present address: Institute of Plant Science and Resources, Okayama University, 2-20-1 Chuo, Kurashiki, Okayama, 710-0046, Japan

Authors and Affiliations

Institute of Low Temperature Science, N19W8 Kita-ku, Sapporo, 060-0819, Japan
Hanaki Maeda, Koharu Takahashi, Kei Sakata, Akari Yokoyama, Kozue Yarimizu, Ayumi Tanaka, Hisashi Ito, Atsushi Takabayashi & Ryouichi Tanaka
Graduate School of Science, Kobe University, Kobe, 657‑8501, Japan
Yoshifumi Ueno & Seiji Akimoto
RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, 230-0045, Japan
Fumiyoshi Myouga & Kazuo Shinozaki
Research Institute for Interdisciplinary Science, Okayama University, 3-1-1 Tsushima-naka, Kita-ku, Okayama, 700-8530, Japan
Shin-Ichiro Ozawa & Yuichiro Takahashi

Authors

Hanaki Maeda
View author publications
You can also search for this author in PubMed Google Scholar
Koharu Takahashi
View author publications
You can also search for this author in PubMed Google Scholar
Yoshifumi Ueno
View author publications
You can also search for this author in PubMed Google Scholar
Kei Sakata
View author publications
You can also search for this author in PubMed Google Scholar
Akari Yokoyama
View author publications
You can also search for this author in PubMed Google Scholar
Kozue Yarimizu
View author publications
You can also search for this author in PubMed Google Scholar
Fumiyoshi Myouga
View author publications
You can also search for this author in PubMed Google Scholar
Kazuo Shinozaki
View author publications
You can also search for this author in PubMed Google Scholar
Shin-Ichiro Ozawa
View author publications
You can also search for this author in PubMed Google Scholar
Yuichiro Takahashi
View author publications
You can also search for this author in PubMed Google Scholar
Ayumi Tanaka
View author publications
You can also search for this author in PubMed Google Scholar
Hisashi Ito
View author publications
You can also search for this author in PubMed Google Scholar
Seiji Akimoto
View author publications
You can also search for this author in PubMed Google Scholar
Atsushi Takabayashi
View author publications
You can also search for this author in PubMed Google Scholar
Ryouichi Tanaka
View author publications
You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: RT; Experimentation: HM, KT, YU, KS, AY, KY, S-IO, HI, SA, AT; Writing—original draft preparation: HM and RT; Writing—review and editing: HM, SA, RT; Funding acquisition: S-IO, SA, RT; Resources: FM, KS; Supervision: YT, AT, RT.

Corresponding author

Correspondence to Ryouichi Tanaka.

Ethics declarations

Competing Interests

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 775 KB)

Supplementary file2 (XLSX 47 KB)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Maeda, H., Takahashi, K., Ueno, Y. et al. Characterization of photosystem II assembly complexes containing ONE-HELIX PROTEIN1 in Arabidopsis thaliana. J Plant Res 135, 361–376 (2022). https://doi.org/10.1007/s10265-022-01376-x

Download citation

Received: 12 November 2021
Accepted: 20 January 2022
Published: 10 February 2022
Issue Date: March 2022
DOI: https://doi.org/10.1007/s10265-022-01376-x

Keywords

Arabidopsis
Chlorophyll
One-helix proteins
Photosystem II