Next Article in Journal
In Silico Analysis of Glutamate Receptors in Capsicum chinense: Structure, Evolution, and Molecular Interactions
Next Article in Special Issue
Improving Crop Yield through Increasing Carbon Gain and Reducing Carbon Loss
Previous Article in Journal
Quantifying the Individual and Combined Effects of Short-Term Heat Stress at Booting and Flowering Stages on Nonstructural Carbohydrates Remobilization in Rice
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 13
Issue 6
10.3390/plants13060811
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Assembly and Repair of Photosystem II in Chlamydomonas reinhardtii

by
Himanshu S. Mehra
†,
Xiaozhuo Wang
†,
Brandon P. Russell
,
Nidhi Kulkarni
,
Nicholas Ferrari
,
Brent Larson
and
David J. Vinyard
*
Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Plants 2024, 13(6), 811; https://doi.org/10.3390/plants13060811
Submission received: 25 January 2024 / Revised: 5 March 2024 / Accepted: 7 March 2024 / Published: 12 March 2024
(This article belongs to the Special Issue Photosynthesis and Carbon Metabolism in Higher Plants and Algae)
Browse Figures
Versions Notes

Abstract

:
Oxygenic photosynthetic organisms use Photosystem II (PSII) to oxidize water and reduce plastoquinone. Here, we review the mechanisms by which PSII is assembled and turned over in the model green alga Chlamydomonas reinhardtii. This species has been used to make key discoveries in PSII research due to its metabolic flexibility and amenability to genetic approaches. PSII subunits originate from both nuclear and chloroplastic gene products in Chlamydomonas. Nuclear-encoded PSII subunits are transported into the chloroplast and chloroplast-encoded PSII subunits are translated by a coordinated mechanism. Active PSII dimers are built from discrete reaction center complexes in a process facilitated by assembly factors. The phosphorylation of core subunits affects supercomplex formation and localization within the thylakoid network. Proteolysis primarily targets the D1 subunit, which when replaced, allows PSII to be reactivated and completes a repair cycle. While PSII has been extensively studied using Chlamydomonas as a model species, important questions remain about its assembly and repair which are presented here.

1. Introduction

In oxygenic photosynthesis, visible light is used to energize electrons stripped from water. Simultaneously, protons are pumped across a membrane generating proton motive force. The final products, NADPH and ATP, are used for cellular functions including the fixation of CO2 in the Calvin–Benson Cycle (reviewed in [1]).
Photosystem II (PSII) is the first component of the photosynthetic electron transport chain and acts as a water–plastoquinone (PQ) oxidoreductase (see [2,3]). PSII is a large membrane-bound complex consisting of approximately 20 unique protein subunits [4]. Within the PSII core, the P680 primary chlorophyll-a donor undergoes charge separation upon photoexcitation. On the donor side of PSII, the hole in the ground state of P680+ is filled by a redox-active tyrosine, YZ, which, is in turn, reduced by the Mn4CaO5 oxygen-evolving complex (OEC). Following four one-electron oxidation events, the OEC catalyzes the formation of O2 from two molecules of water. On the acceptor side of PSII, the excited electron in P680* is transferred to a pheophytin, a primary PQ acceptor, QA, and then to a secondary PQ acceptor, QB (reviewed in [5,6]).
PSII serves as a model system for multiple scientific fields. Protein biochemists study PSII to learn how membrane protein complexes assemble and function (see [7,8]). Bioinorganic chemists have been intrigued by the multiple metal cofactors in PSII including the OEC (see [9]), cytochrome(s) (see [10]) and a non-heme iron (see [11]). Biophysical chemists and biophysicists use PSII to study visible-to-chemical energy conversion and exciton and electron transfer reactions (see [12]). Molecular biologists have used differentially expressed PSII subunits to learn about bacterial and plastidal gene regulation (see [13]) and have used PSII to study protein turnover mechanisms (see [14]). Evolutionary biologists analyze the changes (or lack of changes) in PSII subunits from cyanobacteria to plants (see [15]). Geologists recognize the role of PSII as the sole biological source of O2 from water oxidation (see [16]). PSII’s ability to efficiently perform this reaction using only light as an energy input inspires synthetic chemists, materials chemists, and engineers to attempt to replicate this activity (see [17]). This incomplete list illustrates the significant interest in PSII and its application to multiple research areas.
PSII and other photosynthetic complexes are generally conserved from cyanobacteria to algae to plants, and researchers in this field use all three groups as model species. For example, many biophysical studies of PSII have used membrane preparations from market spinach [18,19,20,21]. The cyanobacterium Synechocystis sp. PCC 6803 has been widely used to study mutations in PSII subunits [22,23,24,25,26,27]. This mesophilic species is naturally transformable and has highly efficient homologous recombination making it a very practical genetic system [28,29]. Detergent-solubilized PSII core complexes from thermophilic cyanobacteria such as Thermosynechococcus vulcanus have been used for multiple influential structural studies [30,31,32] and biophysical studies [33,34,35,36]. While all this work is valuable, the structures [37] and assembly and repair mechanisms [7] of PSII are not identical between oxygenic phototrophs.
Over the past seventy years, the model green alga Chlamydomonas reinhardtii (hereafter Chlamydomonas) has been used to elucidate many discoveries in photosynthesis and other fields (see [38,39]). As a unicellular eukaryote, Chlamydomonas is a practical model species for studying chloroplast biology. First, this species can grow photoautotrophically, mixotrophically, or heterotrophically. This trait allows Chlamydomonas to be studied with genetic mutations in photosynthesis genes that would otherwise be lethal. In addition, Chlamydomonas can reproduce asexually or sexually. In the research laboratory, cultures are typically maintained vegetatively. However, sexual reproduction facilitates genetic approaches. Because of these features, Chlamydomonas has been and is used to discover key components and mechanisms of PSII function, assembly, and repair.
Here, we review research studies that have used Chlamydomonas to gain insights into PSII. We aim to highlight the influential role of this organism in multiple scientific fields that all use PSII as a model system. We compile PSII-specific data to facilitate future studies and bring attention to areas where more research is needed.

2. Discussion

2.1. Architecture of the Chlamydomonas chloroplast

In algae and plants, photosynthesis occurs in the chloroplast. Chlamydomonas cells develop one cup-shaped chloroplast occupying almost half of the volume of the cell [40,41] (Figure 1). The light-dependent photosynthetic reactions are localized to a network of membranes called thylakoids. These thylakoids are organized in appressed regions (regularly spaced stacks termed grana in land plants) and non-appressed regions. In Chlamydomonas, active dimeric PSII complexes are organized in appressed thylakoids, and Photosystem I and ATP synthase are localized to non-appressed regions [42,43].
The chloroplast emerged from the endosymbiosis of a cyanobacterium. Over the course of evolution, most of the genetic information from the original cyanobacterial genome was transferred to the host nuclear genome. In Chlamydomonas, only 72 unique protein-encoding genes are retained in the chloroplast genome [44]. As discussed below, most PSII subunits are chloroplast encoded. The synthesis of chloroplast-encoded photosystem proteins is concentrated at the Translation or T-zone, which is located near the pyrenoid [45,46,47] (Figure 1). Here, newly synthesized proteins are inserted directly into the membrane [48], which is facilitated by a complex containing Alb3.1 and Alb3.2 [49,50]. The Chlamydomonas chloroplast is a complex organelle with multiple sub-organellular structures [51].
Nuclear-encoded chloroplast proteins (including Chlamydomonas PSII subunits PsbO, PsbP, PsbQ [52], PsbW [53], and PsbX [54] (Figure 2)), are translated in the cytosol [55], targeted to the chloroplast [56], and then imported across the outer and inner chloroplast membranes using energy from ATP hydrolysis [57]. Chloroplast protein transport is facilitated by the translocon of the outer membrane (TOC) and translocon of the inner membrane (TIC) protein complexes [58,59,60,61] (Figure 1). Interestingly, the TOC and TIC complexes spatially align with the T-zone suggesting a highly coordinated system of protein import and translation in the Chlamydomonas chloroplast [62,63,64].

2.2. Transcription of PSII Subunits in the Chloroplast

The chloroplast genome encodes 16 of the 21 PSII subunits in Chlamydomonas [65] (see Figure 2). The most prevalent chloroplast transcript is psbA which encodes the PSII core subunit D1 [66,67]. However, little of this psbA mRNA is associated with ribosomes [68], indicating the tight control of translation initiation. The second most prevalent chloroplast transcript is psbD which encodes the D2 core subunit and is found at levels approximately five-fold less than psbA [65].
The PSII cytochrome b559 subunit is encoded by two genes, psbE and psbF. As described below, cytochrome b559 plays crucial roles in PSII translation control and assembly. In cyanobacteria [69], some algae [70,71], and plants [72], these genes are organized as part of a psbEFLJ operon. Surprisingly, in Chlamydomonas, psbE and psbF are separated and have reverse orientations [73,74]. psbF and psbL remain associated with each other and are co-transcribed [73]. psbJ is co-transcribed as part of a cluster that includes psbD [75,76].
In Arabidopsis, a mitochondrial transcription termination factor, mTERF5, controls the transcription of the psbEFLJ operon [77]. This regulatory mechanism is likely not conserved in Chlamydomonas given the differences in gene organization. Why Chlamydomonas evolved to have this unique cytochrome b559 expression system is not understood.

2.3. Translation of PSII Subunits in the Chloroplast—Control by Epistasy of Synthesis

The de novo synthesis of specific PSII subunits is regulated by the presence or absence of other PSII subunits through a mechanism termed Control by Epistasy of Synthesis (CES) (reviewed in [78]). Here, we discuss CES in Chlamdyomonas PSII assembly, but this mechanism is more general. In Chlamydomonas, CES has been observed in the assembly of cytochrome b6f, ATP synthase, ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), and PSI. It is also involved in the synthesis of Rubisco in plants and Cox1 in yeast mitochondria (see [79]).
In Chlamydomonas, the presence of the D2 subunit is required for D1 translation [80,81]. Subsequently, the presence of the D1 subunit is required for CP47 (psbB) translation [81]. This regulation is based on negative regulation of each unassembled polypeptide interacting with its own mRNA in the 5′ untranslated region (UTR) [68].
Regulation of cytochrome b559 translation in Chlamydomonas is more complicated. In a ΔpsbE strain, the translation of D1, D2, CP43, and CP47 was not observed or was strongly inhibited [82]. As discussed below, cytochrome b559 is a component of early PSII assembly intermediates. The phenotypes observed in ΔpsbE may reflect true CES and/or a defect in the assembly pathway.

2.4. Translation of PSII Subunits in the Chloroplast—Regulatory Elements

In the chloroplast, regulation occurs mostly at the translational level and requires both cis- and trans-regulating elements (see [83]). All characterized cis-regulatory elements are in the 5′ UTR of the genes [84,85,86]. Trans-regulating elements (translational activators) are crucial components of PSII core subunits’ translational control and are summarized in Table 1.
Clearly, the translational control of chloroplast-encoded PSII subunits is extensive. Table 1 is very likely incomplete, and more research is needed in this area. While trans-regulatory elements are discussed here for Chlamydomonas, similar regulation is present in plants (see [107]). In contrast to the chloroplast, cyanobacteria generally control PSII expression at the transcriptional level (see [108]).

2.5. Assembly of Protein Subunits and Cofactors

PSII subunits form discrete subcomplexes before assembling into monomeric then dimeric reaction centers (illustrated in Figure 1). First, D2 binds cytochrome b559 subunits PsbE and PsbF. D1 is then translated and binds with other subunits. The binding of the D1 subcomplex to D2-cytochrome b559 leads to the formation of the first reaction center (RC) complex. In Chlamydomonas, One-Helix Protein 2 (OHP2) stabilizes D1 during its translation by promoting chlorophyll association [109]. Another assembly factor, RBD1, promotes D1 stabilization [110,111] and is also involved in the delivery and/or reduction of the non-heme iron ion near the stromal surface of PSII [112]. Next, CP47 is translated and binds to create the RC47 complex. The binding of CP43, facilitated by the assembly factor LPA2 [113,114], low molecular weight subunits, and extrinsic subunits forms monomeric PSII.
After the PSII core is assembled, the OEC is assembled from Mn2+, Ca2+, and water in a stepwise process termed photo-assembly (reviewed in [115]). Here, metal ions and water molecules bind to the apo-OEC PSII protein. Light-driven oxidation events lead to higher valent Mn ions and the OEC cluster spontaneously assembles in situ. This process has mostly been studied in plants and cyanobacteria, but some groups have conducted experiments on Chlamydomonas whole cells [116] or isolated membranes [117]. The kinetics and efficiency of OEC photo-assembly are similar among these organisms suggesting a conserved mechanism [116,117].
The binding of the extrinsic subunits PsbO, PsbP, and PsbQ occurs late in the assembly process. (Note that the terms OEE1, OEE2, and OEE3, respectively, have also been used for these proteins [81,84,118]). PsbO is required for oxygen evolution and photoautotrophic growth in Chlamydomonas and acts by stabilizing the OEC [118]. This subunit is conserved in cyanobacteria, algae, and plants [119]. PsbP and PsbQ enhance oxygen evolution activity by promoting the binding of Ca2+ in the OEC and chloride near the OEC [120]. These subunits are conserved in algae and plants [121]. Mature PSII in cyanobacteria contains PsbO, PsbU, PsbV, and PsbQ [30,122]. The cyanobacterial PsbP homolog is an assembly intermediate [123] and not a component of the mature complex.
PSII reaction centers form supercomplexes with the light-harvesting complex (LHC) antenna proteins (see [3]) (Figure 2). In Chlamydomonas, the major complexes mature as trimers and are encoded by a family of nine genes (LHCBM1-9) with high sequence homology [124]. In addition, CP26 and CP29 subunits associate to control the linkage between the PSII core and LHC antenna proteins. Single and double mutants of CP26 and CP29 show impaired photosynthesis and photoprotection [125]. The PSII subunit PsbZ (also known as Ycf9) is also involved in supercomplex assembly, particularly under stress conditions [126].

2.6. PSII Phosphorylation and Dephosphorylation

In the chloroplast but not in cyanobacteria, phosphorylation of PSII subunits and the associated antennae plays a role in supercomplex formation and PSII migration within the thylakoid network. These properties affect both protein complex turnover and state transitions [127] (reviewed in [128]). In plants, the STN8 kinase phosphorylates PSII core subunits including D1 [129,130] which can be dephosphorylated by the PBCP phosphatase [131]. In plants, the STN7 kinase phosphorylates LHCs [132] (and to a lesser extent, PSII core subunits [133]) which can be dephosphorylated by the PPH1/TAP38 phosphatase [134,135].
The situation in Chlamydomonas is more complicated. The Chlamydomonas PSII subunits CP43, D2, and PsbH, but not D1, undergo phosphorylation at their N-termini [136]. The Chlamydomonas ortholog of STN8, STL1, has not been fully characterized but is likely to be the PSII core kinase. The phosphorylation of PSII subunits is independent of state transitions, and the specific trigger remains unknown [137]. Chlamydomonas LHCs are phosphorylated by the STT7 kinase [138]. Unlike plants which have distinct phosphatases for PSII subunits and LHCs, the Chlamydomonas phosphatases CrPPH1 and CrPBCP can dephosphorylate both PSII and LHC [139].
We note that PSII phosphorylation and dephosphorylation mechanisms increase in specificity over evolutionary time. These processes are absent in cyanobacteria. Algae use specialized kinases but redundant phosphatases. Plants use specialized kinases and phosphatases.

2.7. Proteolysis of the D1 Subunit

PSII in Chlamydomonas is undergoing frequent damage and repair. When PSII is isolated from Chlamydomonas cultures grown under optimal conditions, the observed manganese content is lower than expected suggesting that up to 20% of centers are in damaged or assembly states [140,141]. The PSII D1 subunit is most prone to oxidative damage and is rapidly turned over. In Chlamydomonas under saturating light conditions, the half-life of D1 is as short as 20 min [142]. While D1 repair is costly in terms of ATP equivalents [143], replacing only this single subunit is more efficient than degrading and reassembling the entire PSII reaction center. D2 turns over at a slightly slower, but significantly rapid rate under high light conditions [144].
The D1 degradation process is well understood in plants where soluble DEG proteases clip loops and the FtsH proteases degrade the resulting fragments. Arabidopsis DEG2 clips a stromal D1 loop to generate ~23 kDa and ~10 kDa fragments [145], although D1 is still degraded in the absence of this protease [146]. DEG1 clips a lumenal loop or loops to generate ~16 kDa and ~5 kDa fragments [147]. DEG5 and DEG8 form a complex and DEG8 clips a lumenal loop to generate ~16 kDa and ~18 kDa fragments [148]. In cyanobacteria, DEG proteases are not required for D1 degradation, but do protect cells from heat and light stresses [149].
FtsH is essential for D1 degradation in Chlamydomonas. In a Chlamydomonas FtsH mutant strain exposed to light, D1 fragments of ~23 kDa, ~16 kDa, and ~6 kDa accumulate (Figure 3) [150]. However, it is not known which proteases are responsible for these fragments. The Chlamydomonas genome encodes 12 DEG proteases with predicted active protease domains and up to seven are predicted to be localized to the chloroplast [151]. DEG1C [152] and DEG9 (unpublished) are active proteases localized to the chloroplast stroma but are not involved in PSII repair or biogenesis. DEG8 and DEG5 are colocalized to the pyrenoid tubules (thylakoids) [51] but have not been further characterized. The identity of the specific protease(s) involved in processing D1 before FtsH remains unknown.
Intriguingly, a 23 kDa D1 fragment is also accumulated in a Chlamydomonas double mutant of FtsH and RBD1 in darkness. In this situation, D1 degradation is not the result of photodamage and instead may be induced by a conformational change from the lack of RBD1 [110].

2.8. PSII Repair

Following D1 damage, CP43 dissociates from the PSII reaction center, which makes D1 more accessible to proteolysis [81]. A new D1 polypeptide is synthesized and inserted, and CP43 rebinds (reviewed in [153]). This process occurs in non-appressed regions of the thylakoids. In Chlamydomonas, the factor TEF30 facilitates D1 insertion and/or CP43 binding during repair of monomeric PSII [154]. Another factor, REP27 (homologous to LPA1 in plants), is also involved in D1 insertion during PSII repair [155,156].

3. Conclusions

As shown here, Chlamydomonas has remained an important tool for studying PSII from the 1980s to the present. The studies reviewed here have provided deeper insights into biochemical and evolutionary processes:
  • PSII assembly in Chlamydomonas provides an excellent model system for the evolution and interplay between nuclear and organellar genomes.
  • The CES mechanism, which is well studied in terms of PSII assembly in Chlamydomonas, is applicable to multiple protein complexes in the chloroplast and other systems.
  • Analogously, the extensive translational control of PSII subunits in the Chlamydomonas chloroplast has revealed gene regulation strategies.
  • The PSII phosphorylation, dephosphorylation, and degradation pathways in Chlamydomonas show intermediate mechanisms between cyanobacteria and plants, thus providing insights into evolution of photosynthetic organisms.

4. Remaining Questions

While Chlamydomonas has clearly contributed much to our understanding of PSII assembly and repair, key questions remain unanswered. These include:
  • What are the molecular mechanisms that allow chloroplast protein import and chloroplast protein synthesis to be coordinated?
  • Why are the genes that encode cytochrome b559 separated in the Chlamydomonas chloroplast genome?
  • What is the full suite of regulatory elements that control the translation of PSII subunits in the chloroplast?
  • What are the specific triggers for PSII core subunit phosphorylation and dephosphorylation?
  • Which protease(s) degrades D1 into fragments before FtsH processing?
With these questions and others, Chlamydomonas will continue to be a practical and powerful system for PSII research.

Funding

This work was funded the U.S. Department of Energy, Office of Science, Office of Basic Energy Science, Division of Chemical Sciences, Geosciences, and Biosciences, Photosynthetic Systems through Grant DE-SC0020119. B.P.R. and D.J.V. received partial support from the National Science Foundation EPSCoR RII Track-4 Award Number 2131863.

Data Availability Statement

Not applicable.

Acknowledgments

Figure 1 and Figure 3 were prepared in part using BioRender.com (accessed on 15 January 2024). We thank James V. Moroney for his comments on this manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Blankenship, R.E. Molecular Mechanisms of Photosynthesis, 3rd, ed.; Wiley: Hoboken, NJ, USA, 2021. [Google Scholar]
  2. Shevela, D.; Kern, J.F.; Govindjee, G.; Whitmarsh, J.; Messinger, J. Photosystem II. In eLS; Wiley: Hoboken, NJ, USA, 2021; pp. 1–16. [Google Scholar]
  3. Redding, K.E.; Santabarbara, S. Photosystems I and II. In The Chlamydomonas Sourcebook; Elsevier: Amsterdam, The Netherlands, 2023; pp. 525–560. [Google Scholar]
  4. Shen, J.-R. The Structure of Photosystem II and the Mechanism of Water Oxidation in Photosynthesis. Annu. Rev. Plant Biol. 2015, 66, 23–48. [Google Scholar] [CrossRef] [PubMed]
  5. Lubitz, W.; Chrysina, M.; Cox, N. Water oxidation in photosystem II. Photosynth. Res. 2019, 142, 105–125. [Google Scholar] [CrossRef] [PubMed]
  6. Vinyard, D.J.; Brudvig, G.W. Progress toward a Molecular Mechanism of Water Oxidation in Photosystem II. Annu. Rev. Phys. Chem. 2017, 68, 101–116. [Google Scholar] [CrossRef] [PubMed]
  7. Nickelsen, J.; Rengstl, B. Photosystem II Assembly: From Cyanobacteria to Plants. Annu. Rev. Plant Biol. 2013, 64, 609–635. [Google Scholar] [CrossRef] [PubMed]
  8. Johnson, V.M.; Pakrasi, H.B. Advances in the Understanding of the Lifecycle of Photosystem II. Microorganisms 2022, 10, 836. [Google Scholar] [CrossRef]
  9. Young, K.J.; Brennan, B.J.; Tagore, R.; Brudvig, G.W. Photosynthetic Water Oxidation: Insights from Manganese Model Chemistry. Acc. Chem. Res. 2015, 48, 567–574. [Google Scholar] [CrossRef]
  10. Chiu, Y.-F.; Chu, H.-A. New Structural and Mechanistic Insights into Functional Roles of Cytochrome b559 in Photosystem II. Front. Plant Sci. 2022, 13, 914922. [Google Scholar] [CrossRef] [PubMed]
  11. Müh, F.; Zouni, A. The nonheme iron in photosystem II. Photosynth. Res. 2013, 116, 295–314. [Google Scholar] [CrossRef]
  12. Sirohiwal, A.; Pantazis, D.A. Reaction Center Excitation in Photosystem II: From Multiscale Modeling to Functional Principles. Acc. Chem. Res. 2023, 56, 2921–2932. [Google Scholar] [CrossRef] [PubMed]
  13. Allen, J.F. Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression. Proc. Natl. Acad. Sci. USA 2015, 112, 10231–10238. [Google Scholar] [CrossRef] [PubMed]
  14. Su, J.; Jiao, Q.; Jia, T.; Hu, X. The photosystem-II repair cycle: Updates and open questions. Planta 2023, 259, 20. [Google Scholar] [CrossRef] [PubMed]
  15. Oliver, T.; Kim, T.D.; Trinugroho, J.P.; Cordón-Preciado, V.; Wijayatilake, N.; Bhatia, A.; Rutherford, A.W.; Cardona, T. The Evolution and Evolvability of Photosystem II. Annu. Rev. Plant Biol. 2023, 74, 225–257. [Google Scholar] [CrossRef] [PubMed]
  16. Fischer, W.W.; Hemp, J.; Johnson, J.E. Evolution of Oxygenic Photosynthesis. Annu. Rev. Earth Planet. Sci. 2016, 44, 647–683. [Google Scholar] [CrossRef]
  17. Moore, G.F.; Brudvig, G.W. Energy Conversion in Photosynthesis: A Paradigm for Solar Fuel Production. Annu. Rev. Condens. Matter Phys. 2011, 2, 303–327. [Google Scholar] [CrossRef]
  18. Berthold, D.A.; Babcock, G.T.; Yocum, C.F. A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. FEBS Lett. 1981, 134, 231–234. [Google Scholar] [CrossRef]
  19. Greife, P.; Schönborn, M.; Capone, M.; Assunção, R.; Narzi, D.; Guidoni, L.; Dau, H. The electron–proton bottleneck of photosynthetic oxygen evolution. Nature 2023, 617, 623–628. [Google Scholar] [CrossRef] [PubMed]
  20. Mino, H.; Asada, M. Location of two Mn2+ affinity sites in photosystem II detected by pulsed electron–electron double resonance. Photosynth. Res. 2022, 152, 289–295. [Google Scholar] [CrossRef]
  21. Wang, J.; Perez-Cruet, J.M.; Huang, H.-L.; Reiss, K.; Gisriel, C.J.; Banerjee, G.; Kaur, D.; Ghosh, I.; Dziarski, A.; Gunner, M.R.; et al. Identification of a Na+-Binding Site near the Oxygen-Evolving Complex of Spinach Photosystem II. Biochemistry 2020, 59, 2823–2831. [Google Scholar] [CrossRef]
  22. Debus, R.J. Protein ligation of the photosynthetic oxygen-evolving center. Coord. Chem. Rev. 2008, 252, 244–258. [Google Scholar] [CrossRef]
  23. Nixon, P.J.; Michoux, F.; Yu, J.; Boehm, M.; Komenda, J. Recent advances in understanding the assembly and repair of photosystem II. Ann. Bot. 2010, 106, 1–16. [Google Scholar] [CrossRef]
  24. Williams, J.G.K. [85] Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. In Methods in Enzymology; Academic Press: Cambridge, MA, USA, 1988; Volume 167, pp. 766–778. [Google Scholar]
  25. Ghosh, I.; Khan, S.; Banerjee, G.; Dziarski, A.; Vinyard, D.J.; Debus, R.J.; Brudvig, G.W. Insights into Proton-Transfer Pathways during Water Oxidation in Photosystem II. J. Phys. Chem. B 2019, 123, 8195–8202. [Google Scholar] [CrossRef] [PubMed]
  26. Avramov, A.P.; Hwang, H.J.; Burnap, R.L. The role of Ca2+ and protein scaffolding in the formation of nature’s water oxidizing complex. Proc. Natl. Acad. Sci. USA 2020, 117, 28036–28045. [Google Scholar] [CrossRef]
  27. Russell, B.P.; Vinyard, D.J. Conformational changes in a Photosystem II hydrogen bond network stabilize the oxygen-evolving complex. Biochim. Et Biophys. Acta (BBA) Bioenerg. 2024, 1865, 149020. [Google Scholar] [CrossRef] [PubMed]
  28. Ikeuchi, M.; Tabata, S. Synechocystis sp. PCC 6803—A useful tool in the study of the genetics of cyanobacteria. Photosynth. Res. 2001, 70, 73–83. [Google Scholar] [CrossRef] [PubMed]
  29. Vermaas, W. Molecular genetics of the cyanobacterium Synechocystis sp. PCC 6803: Principles and possible biotechnology applications. J. Appl. Phycol. 1996, 8, 263–273. [Google Scholar] [CrossRef]
  30. Umena, Y.; Kawakami, K.; Shen, J.-R.; Kamiya, N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 2011, 473, 55–60. [Google Scholar] [CrossRef] [PubMed]
  31. Guskov, A.; Kern, J.; Gabdulkhakov, A.; Broser, M.; Zouni, A.; Saenger, W. Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 2009, 16, 334–342. [Google Scholar] [CrossRef] [PubMed]
  32. Ferreira, K.N.; Iverson, T.M.; Maghlaoui, K.; Barber, J.; Iwata, S. Architecture of the Photosynthetic Oxygen-Evolving Center. Science 2004, 303, 1831–1838. [Google Scholar] [CrossRef]
  33. Kato, Y.; Noguchi, T. Redox properties and regulatory mechanism of the iron-quinone electron acceptor in photosystem II as revealed by FTIR spectroelectrochemistry. Photosynth. Res. 2022, 152, 135–151. [Google Scholar] [CrossRef]
  34. Noguchi, T. Fourier transform infrared difference and time-resolved infrared detection of the electron and proton transfer dynamics in photosynthetic water oxidation. Biochim. Et Biophys. Acta (BBA) Bioenerg. 2015, 1847, 35–45. [Google Scholar] [CrossRef]
  35. Sugiura, M.; Boussac, A. Variants of photosystem II D1 protein in Thermosynechococcus elongatus. Res. Chem. Intermed. 2014, 40, 3219–3229. [Google Scholar] [CrossRef]
  36. Sugiura, M.; Inoue, Y. Highly Purified Thermo-Stable Oxygen-Evolving Photosystem II Core Complex from the Thermophilic Cyanobacterium Synechococcus elongatus Having His-Tagged CP43. Plant Cell Physiol. 1999, 40, 1219–1231. [Google Scholar] [CrossRef] [PubMed]
  37. Nelson, N.; Junge, W. Structure and Energy Transfer in Photosystems of Oxygenic Photosynthesis. Annu. Rev. Biochem. 2015, 84, 659–683. [Google Scholar] [CrossRef] [PubMed]
  38. Goodenough, U. The Chlamydomonas Sourcebook: Volume 1: Introduction to Chlamydomonas and Its Laboratory Use, 3rd ed.; Elsevier Science: Amsterdam, The Netherlands, 2023. [Google Scholar]
  39. Dupuis, S.; Merchant, S.S. Chlamydomonas reinhardtii: A model for photosynthesis and so much more. Nat. Methods 2023, 20, 1441–1442. [Google Scholar] [CrossRef] [PubMed]
  40. Sager, R.; Palade, G.E. Structure and development of the chloroplast in Chlamydomonas. I. The normal green cell. J. Cell Biol. 1957, 3, 463–488. [Google Scholar] [CrossRef]
  41. Gaffal, K.; Arnold, C.-G.; Friedrichs, G.; Gemple, W. Morphodynamical changes of the chloroplast of Chlamydomonas reinhardtii during the 1st round of division. Arch. Für Protistenkd. 1995, 145, 10–23. [Google Scholar] [CrossRef]
  42. Vallon, O.; Wollman, F.A.; Olive, J. Laterial distribution of the main protein complexes of the photosynthetic apparatus in Chlamydomonas reinhardtii and in spinach: An immunocytochemical study using intact thylakoid membranes and a PS II enriched membrane preparation. Photobiochem. Photobiophys. 1986, 12, 203–220. [Google Scholar]
  43. Wietrzynski, W.; Schaffer, M.; Tegunov, D.; Albert, S.; Kanazawa, A.; Plitzko, J.M.; Baumeister, W.; Engel, B.D. Charting the native architecture of Chlamydomonas thylakoid membranes with single-molecule precision. Elife 2020, 9, e53740. [Google Scholar] [CrossRef] [PubMed]
  44. Maul, J.E.; Lilly, J.W.; Cui, L.; DePamphilis, C.W.; Miller, W.; Harris, E.H.; Stern, D.B. The Chlamydomonas reinhardtii plastid chromosome: Islands of genes in a sea of repeats. Plant Cell 2002, 14, 2659–2679. [Google Scholar] [CrossRef] [PubMed]
  45. Uniacke, J.; Zerges, W. Photosystem II assembly and repair are differentially localized in Chlamydomonas. Plant Cell 2007, 19, 3640–3654. [Google Scholar] [CrossRef]
  46. Uniacke, J.; Zerges, W. Chloroplast protein targeting involves localized translation in Chlamydomonas. Proc. Natl. Acad. Sci. USA 2009, 106, 1439–1444. [Google Scholar] [CrossRef]
  47. Sun, Y.; Valente-Paterno, M.; Bakhtiari, S.; Law, C.; Zhan, Y.; Zerges, W. Photosystem Biogenesis Is Localized to the Translation Zone in the Chloroplast of Chlamydomonas. Plant Cell 2019, 31, 3057–3072. [Google Scholar] [CrossRef] [PubMed]
  48. Zhang, L.; Paakkarinen, V.; van Wijk, K.J.; Aro, E.M. Co-translational assembly of the D1 protein into photosystem II. J. Biol. Chem. 1999, 274, 16062–16067. [Google Scholar] [CrossRef]
  49. Gohre, V.; Ossenbühl, F.; Crevecoeur, M.; Eichacker, L.A.; Rochaix, J.-D. One of two alb3 proteins is essential for the assembly of the photosystems and for cell survival in Chlamydomonas. Plant Cell 2006, 18, 1454–1466. [Google Scholar] [CrossRef]
  50. Ossenbühl, F.; Gohre, V.; Meurer, J.; Krieger-Liszkay, A.; Rochaix, J.-D.; Eichacker, L.A. Efficient assembly of photosystem II in Chlamydomonas reinhardtii requires Alb3. 1p, a homolog of Arabidopsis ALBINO3. Plant Cell 2004, 16, 1790–1800. [Google Scholar] [CrossRef]
  51. Wang, L.; Patena, W.; Van Baalen, K.A.; Xie, Y.; Singer, E.R.; Gavrilenko, S.; Warren-Williams, M.; Han, L.; Harrigan, H.R.; Hartz, L.D.; et al. A chloroplast protein atlas reveals punctate structures and spatial organization of biosynthetic pathways. Cell 2023, 186, 3499–3518.e3414. [Google Scholar] [CrossRef] [PubMed]
  52. Delepelaire, P. Partial characterization of the biosynthesis and integration of the Photosystem II reaction centers in the thylakoid membrane of Chlamydomonas reinhardtii. EMBO J. 1984, 3, 701–706. [Google Scholar] [CrossRef] [PubMed]
  53. Bishop, C.L.; Purton, S.; Nugent, J.H. Molecular analysis of the Chlamydomonas nuclear gene encoding PsbW and demonstration that PsbW is a subunit of photosystem II, but not photosystem I. Plant Mol. Biol. 2003, 52, 285. [Google Scholar] [CrossRef] [PubMed]
  54. Sheng, X.; Watanabe, A.; Li, A.; Kim, E.; Song, C.; Murata, K.; Song, D.; Minagawa, J.; Liu, Z. Structural insight into light harvesting for photosystem II in green algae. Nat. Plants 2019, 5, 1320–1330. [Google Scholar] [CrossRef]
  55. Westhoff, P.; Jansson, C.; Klein-Hitpaß, L.; Berzborn, R.; Larsson, C.; Bartlett, S.G. Intracellular coding sites of polypeptides associated with photosynthetic oxygen evolution of photosystem II. Plant Mol. Biol. 1985, 4, 137–146. [Google Scholar] [CrossRef] [PubMed]
  56. Bruce, B.D. Chloroplast transit peptides: Structure, function and evolution. Trends Cell Biol. 2000, 10, 440–447. [Google Scholar] [CrossRef] [PubMed]
  57. Theg, S.M.; Bauerle, C.; Olsen, L.J.; Selman, B.R.; Keegstra, K. Internal ATP Is the Only Energy Requirement for the Translocation of Precursor Proteins across Chloroplastic Membranes. J. Biol. Chem. 1989, 264, 6730–6736. [Google Scholar] [CrossRef] [PubMed]
  58. Shi, L.-X.; Theg, S.M. The chloroplast protein import system: From algae to trees. Biochim. Et Biophys. Acta (BBA) Mol. Cell Res. 2013, 1833, 314–331. [Google Scholar] [CrossRef] [PubMed]
  59. Ramundo, S.; Asakura, Y.; Salomé, P.A.; Strenkert, D.; Boone, M.; Mackinder, L.C.; Takafuji, K.; Dinc, E.; Rahire, M.; Crèvecoeur, M. Coexpressed subunits of dual genetic origin define a conserved supercomplex mediating essential protein import into chloroplasts. Proc. Natl. Acad. Sci. USA 2020, 117, 32739–32749. [Google Scholar] [CrossRef] [PubMed]
  60. Liu, H.; Li, A.; Rochaix, J.-D.; Liu, Z. Architecture of chloroplast TOC-TIC translocon supercomplex. Nature 2023, 615, 349–357. [Google Scholar] [CrossRef] [PubMed]
  61. Jin, Z.; Wan, L.; Zhang, Y.; Li, X.; Cao, Y.; Liu, H.; Fan, S.; Cao, D.; Wang, Z.; Li, X.; et al. Structure of a TOC-TIC supercomplex spanning two chloroplast envelope membranes. Cell 2022, 185, 4788–4800.e4713. [Google Scholar] [CrossRef] [PubMed]
  62. Schottkowski, M.; Peters, M.; Zhan, Y.; Rifai, O.; Zhang, Y.; Zerges, W. Biogenic membranes of the chloroplast in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 2012, 109, 19286–19291. [Google Scholar] [CrossRef] [PubMed]
  63. Sun, Y.; Bakhtiari, S.; Valente-Paterno, M.; Wu, Y.; Law, C.; Dai, D.; Dhaliwal, J.; Bui, K.H.; Zerges, W. Chloroplast-localized translation for protein targeting in Chlamydomonas reinhardtii. bioRxiv 2021. [Google Scholar] [CrossRef]
  64. Willmund, F.; Hauser, C.; Zerges, W. Translation and protein synthesis in the chloroplast. In The Chlamydomonas Sourcebook; Elsevier: Amsterdam, The Netherlands, 2023; pp. 467–508. [Google Scholar]
  65. Gallaher, S.D.; Fitz-Gibbon, S.T.; Strenkert, D.; Purvine, S.O.; Pellegrini, M.; Merchant, S.S. High-throughput sequencing of the chloroplast and mitochondrion of Chlamydomonas reinhardtii to generate improved de novo assemblies, analyze expression patterns and transcript speciation, and evaluate diversity among laboratory strains and wild isolates. Plant J. 2018, 93, 545–565. [Google Scholar] [CrossRef]
  66. Erickson, J.M.; Rahire, M.; Rochaix, J.-D. Chlamydomonas reinhardii gene for the 32 000 mol. wt. protein of photosystem II contains four large introns and is located entirely within the chloroplast inverted repeat. EMBO J. 1984, 3, 2753–2762. [Google Scholar] [CrossRef] [PubMed]
  67. Bedbrook, J.R.; Link, G.; Coen, D.M.; Bogorad, L. Maize plastid gene expressed during photoregulated development. Proc. Natl. Acad. Sci. USA 1978, 75, 3060–3064. [Google Scholar] [CrossRef] [PubMed]
  68. Minai, L.; Wostrikoff, K.; Wollman, F.-A.; Choquet, Y. Chloroplast biogenesis of photosystem II cores involves a series of assembly-controlled steps that regulate translation. Plant Cell 2006, 18, 159–175. [Google Scholar] [CrossRef]
  69. Pakrasi, H.B.; Williams, J.G.; Arntzen, C.J. Targeted mutagenesis of the psbE and psbF genes blocks photosynthetic electron transport: Evidence for a functional role of cytochrome b559 in photosystem II. EMBO J. 1988, 7, 325–332. [Google Scholar] [CrossRef]
  70. Cantrell, A.; Bryant, D.A. Nucleotide sequence of the genes encoding cytochrome b-559 from the cyanelle genome of Cyanophora paradoxa. Photosynth. Res. 1988, 16, 65–81. [Google Scholar] [CrossRef] [PubMed]
  71. Cushman, J.C.; Christopher, D.A.; Little, M.C.; Hallick, R.B.; Price, C.A. Organization of the psbE, psbF, orf38, and orf42 gene loci on the Euglena gracilis chloroplast genome. Curr. Genet. 1988, 13, 173–180. [Google Scholar] [CrossRef] [PubMed]
  72. Herrmann, R.G.; Alt, J.; Schiller, B.; Widger, W.R.; Cramer, W.A. Nucleotide sequence of the gene for apocytochrome b-559 on the spinach plastid chromosome: Implications for the structure of the membrane protein. FEBS Lett. 1984, 176, 239–244. [Google Scholar] [CrossRef]
  73. Mor, T.S.; Ohad, I.; Hirschberg, J.; Pakrasi, H.B. An unusual organization of the genes encoding cytochrome b559 in Chlamydomonas reinhardtii: psbE and psbF genes are separately transcribed from different regions of the plastid chromosome. Mol. Gen. Genet. MGG 1995, 246, 600–604. [Google Scholar] [CrossRef] [PubMed]
  74. Alizadeh, S.; Nechushtai, R.; Barber, J.; Nixon, P. Nucleotide sequence of the psbE, psbF and trnM genes from the chloroplast genome of Chlamydomonas reinhardtii. Biochim. Et Biophys. Acta (BBA) Bioenerg. 1994, 1188, 439–442. [Google Scholar] [CrossRef]
  75. Liu, X.Q.; Gillham, N.W.; Boynton, J.E. Chloroplast Ribosomal Protein Gene rps12 of Chlamydomonas reinhardtii: Wild-type sequence, mutation to streptomycin resistance and dependence, and function in escherichia coli. J. Biol. Chem. 1989, 264, 16100–16108. [Google Scholar] [CrossRef] [PubMed]
  76. Cavaiuolo, M.; Kuras, R.; Wollman, F.A.; Choquet, Y.; Vallon, O. Small RNA profiling in Chlamydomonas: Insights into chloroplast RNA metabolism. Nucleic Acids Res. 2017, 45, 10783–10799. [Google Scholar] [CrossRef]
  77. Ding, S.; Zhang, Y.; Hu, Z.; Huang, X.; Zhang, B.; Lu, Q.; Wen, X.; Wang, Y.; Lu, C. mTERF5 Acts as a Transcriptional Pausing Factor to Positively Regulate Transcription of Chloroplast psbEFLJ. Mol. Plant 2019, 12, 1259–1277. [Google Scholar] [CrossRef]
  78. Wollman, F.-A.; Minai, L.; Nechushtai, R. The biogenesis and assembly of photosynthetic proteins in thylakoid membranes. Biochim. Et Biophys. Acta (BBA) Bioenerg. 1999, 1411, 21–85. [Google Scholar] [CrossRef]
  79. Choquet, Y.; Wollman, F.-A. The assembly of photosynthetic proteins. In The Chlamydomonas Sourcebook; Elsevier: Amsterdam, The Netherlands, 2023; pp. 615–646. [Google Scholar]
  80. Erickson, J.M.; Rahire, M.; Malnoë, P.; Girard-Bascou, J.; Pierre, Y.; Bennoun, P.; Rochaix, J.-D. Lack of the D2 protein in a Chlamydomonas reinhardtii psbD mutant affects photosystem II stability and D1 expression. EMBO J. 1986, 5, 1745–1754. [Google Scholar] [CrossRef]
  81. de Vitry, C.; Olive, J.; Drapier, D.; Recouvreur, M.; Wollman, F.-A. Posttranslational events leading to the assembly of photosystem II protein complex: A study using photosynthesis mutants from Chlamydomonas reinhardtii. J. Cell Biol. 1989, 109, 991–1006. [Google Scholar] [CrossRef] [PubMed]
  82. Morais, F.; Barber, J.; Nixon, P.J. The Chloroplast-encoded α Subunit of Cytochromeb-559 Is Required for Assembly of the Photosystem Two Complex in both the Light and the Dark in Chlamydomonas reinhardtii. J. Biol. Chem. 1998, 273, 29315–29320. [Google Scholar] [CrossRef] [PubMed]
  83. Bohne, A.-V.; Nickelsen, J. Control of organellar gene expression by nucleus-encoded proteins. In The Chlamydomonas Sourcebook; Elsevier: Amsterdam, The Netherlands, 2023; pp. 443–466. [Google Scholar]
  84. Mayfield, S.P.; Rahire, M.; Frank, G.; Zuber, H.; Rochaix, J.-D. Expression of the nuclear gene encoding oxygen-evolving enhancer protein 2 is required for high levels of photosynthetic oxygen evolution in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 1987, 84, 749–753. [Google Scholar] [CrossRef] [PubMed]
  85. Nickelsen, J.; van Dillewijn, J.; Rahire, M.; Rochaix, J.-D. Determinants for stability of the chloroplast psbD RNA are located within its short leader region in Chlamydomonas reinhardtii. EMBO J. 1994, 13, 3182–3191. [Google Scholar] [CrossRef] [PubMed]
  86. Rochaix, J.-D.; Kuchka, M.; Mayfield, S.; Schirmer-Rahire, M.; Girard-Bascou, J.; Bennoun, P. Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii. EMBO J. 1989, 8, 1013–1021. [Google Scholar] [CrossRef] [PubMed]
  87. Danon, A.; Mayfield, S.P. Light regulated translational activators: Identification of chloroplast gene specific mRNA binding proteins. EMBO J. 1991, 10, 3993–4001. [Google Scholar] [CrossRef] [PubMed]
  88. Yohn, C.B.; Cohen, A.; Danon, A.; Mayfield, S.P. A poly(A) binding protein functions in the chloroplast as a message-specific translation factor. Proc. Natl. Acad. Sci. USA 1998, 95, 2238–2243. [Google Scholar] [CrossRef] [PubMed]
  89. Yohn, C.B.; Cohen, A.; Rosch, C.; Kuchka, M.R.; Mayfield, S.P. Translation of the Chloroplast psbA mRNA Requires the Nuclear-encoded Poly(A)-binding Protein, RB47. J. Cell Biol. 1998, 142, 435–442. [Google Scholar] [CrossRef] [PubMed]
  90. Kim, J.; Mayfield, S.P. Protein disulfide isomerase as a regulator of chloroplast translational activation. Science 1997, 278, 1954–1957. [Google Scholar] [CrossRef] [PubMed]
  91. Somanchi, A.; Barnes, D.; Mayfield, S.P. A nuclear gene of Chlamydomonas reinhardtii, Tba1, encodes a putative oxidoreductase required for translation of the chloroplast psbA mRNA. Plant J. 2005, 42, 341–352. [Google Scholar] [CrossRef] [PubMed]
  92. Barnes, D.; Cohen, A.; Bruick, R.K.; Kantardjieff, K.; Fowler, S.; Efuet, E.; Mayfield, S.P. Identification and Characterization of a Novel RNA Binding Protein That Associates with the 5‘-Untranslated Region of the Chloroplast psbA mRNA. Biochemistry 2004, 43, 8541–8550. [Google Scholar] [CrossRef] [PubMed]
  93. Yohn, C.B.; Cohen, A.; Danon, A.; Mayfield, S.P. Altered mRNA binding activity and decreased translational initiation in a nuclear mutant lacking translation of the chloroplast psbA mRNA. Mol. Cell. Biol. 1996, 16, 3560–3566. [Google Scholar] [CrossRef] [PubMed]
  94. Ossenbühl, F.; Hartmann, K.; Nickelsen, J. A chloroplast RNA binding protein from stromal thylakoid membranes specifically binds to the 5′ untranslated region of the psbA mRNA. Eur. J. Biochem. 2002, 269, 3912–3919. [Google Scholar] [CrossRef] [PubMed]
  95. Bohne, A.-V.; Schwarz, C.; Schottkowski, M.; Lidschreiber, M.; Piotrowski, M.; Zerges, W.; Nickelsen, J. Reciprocal Regulation of Protein Synthesis and Carbon Metabolism for Thylakoid Membrane Biogenesis. PLoS Biol. 2013, 11, e1001482. [Google Scholar] [CrossRef] [PubMed]
  96. Neusius, D.; Kleinknecht, L.; Teh, J.T.; Ostermeier, M.; Kelterborn, S.; Eirich, J.; Hegemann, P.; Finkemeier, I.; Bohne, A.-V.; Nickelsen, J. Lysine acetylation regulates moonlighting activity of the E2 subunit of the chloroplast pyruvate dehydrogenase complex in Chlamydomonas. Plant J. 2022, 111, 1780–1800. [Google Scholar] [CrossRef]
  97. Kafri, M.; Patena, W.; Martin, L.; Wang, L.; Gomer, G.; Ergun, S.L.; Sirkejyan, A.K.; Goh, A.; Wilson, A.T.; Gavrilenko, S.E.; et al. Systematic identification and characterization of genes in the regulation and biogenesis of photosynthetic machinery. Cell 2023, 186, 5638–5655.e5625. [Google Scholar] [CrossRef]
  98. Kuchka, M.R.; Mayfield, S.P.; Rochaix, J.-D. Nuclear mutations specifically affect the synthesis and/or degradation of the chloroplast-encoded D2 polypeptide of photosystem II in Chlamydomonas reinhardtii. EMBO J. 1988, 7, 319–324. [Google Scholar] [CrossRef]
  99. Rattanachaikunsopon, P.; Rosch, C.; Kuchka, M.R. Cloning and characterization of the nuclear AC115 gene of Chlamydomonas reinhardtii. Plant Mol. Biol. 1999, 39, 1–10. [Google Scholar] [CrossRef] [PubMed]
  100. Kuchka, M.R.; Goldschmidt-Clermont, M.; van Dillewijn, J.; Rochaix, J.-D. Mutation at the chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell 1989, 58, 869–876. [Google Scholar] [CrossRef] [PubMed]
  101. Ossenbühl, F.; Nickelsen, J. cis- and trans-Acting Determinants for Translation of psbD mRNA in Chlamydomonas reinhardtii. Mol. Cell. Biol. 2000, 20, 8134–8142. [Google Scholar] [CrossRef] [PubMed]
  102. Schwarz, C.; Elles, I.; Kortmann, J.; Piotrowski, M.; Nickelsen, J. Synthesis of the D2 protein of photosystem II in Chlamydomonas is controlled by a high molecular mass complex containing the RNA stabilization factor Nac2 and the translational activator RBP40. Plant Cell 2007, 19, 3627–3639. [Google Scholar] [CrossRef] [PubMed]
  103. Monod, C.; Goldschmidt-Clermont, M.; Rochaix, J.-D. Accumulation of chloroplast psbB RNA requires a nuclear factor in Chlamydomonas reinhardtii. Mol. Gen. Genet. 1992, 231, 449–459. [Google Scholar] [CrossRef] [PubMed]
  104. Vaistij, F.E.; Goldschmidt-Clermont, M.; Wostrikoff, K.; Rochaix, J.-D. Stability determinants in the chloroplast psbB/T/H mRNAs of Chlamydomonas reinhardtii. Plant J. 2000, 21, 469–482. [Google Scholar] [CrossRef]
  105. Zerges, W.; Rochaix, J.-D. The 5′ leader of a chloroplast mRNA mediates the translational requirements for two nucleus-encoded functions in Chlamydomonas reinhardtii. Mol. Cell. Biol. 1994, 14, 5268–5277. [Google Scholar] [CrossRef] [PubMed]
  106. Zerges, W. Translation of the psbC mRNA and incorporation of its polypeptide product into photosystem II is controlled by interactions between the psbC 5′leader and the NCT loci in Chlamydomonas reinhardtii. Mol. Cell. Biol. 1997, 17, 3440–3448. [Google Scholar] [CrossRef] [PubMed]
  107. Zoschke, R.; Bock, R. Chloroplast Translation: Structural and Functional Organization, Operational Control, and Regulation. Plant Cell 2018, 30, 745–770. [Google Scholar] [CrossRef] [PubMed]
  108. Wilde, A.; Hihara, Y. Transcriptional and posttranscriptional regulation of cyanobacterial photosynthesis. Biochim. Et Biophys. Acta (BBA) Bioenerg. 2016, 1857, 296–308. [Google Scholar] [CrossRef] [PubMed]
  109. Wang, F.; Dischinger, K.; Westrich, L.D.; Meindl, I.; Egidi, F.; Trösch, R.; Sommer, F.; Johnson, X.; Schroda, M.; Nickelsen, J.; et al. One-helix protein 2 is not required for the synthesis of photosystem II subunit D1 in Chlamydomonas. Plant Physiol. 2023, 191, 1612–1633. [Google Scholar] [CrossRef] [PubMed]
  110. Calderon, R.H.; de Vitry, C.; Wollman, F.-A.; Niyogi, K.K. Rubredoxin 1 promotes the proper folding of D1 and is not required for heme b559 assembly in Chlamydomonas photosystem II. J. Biol. Chem. 2023, 299, 102968. [Google Scholar] [CrossRef]
  111. Calderon, R.H.; García-Cerdán, J.G.; Malnoë, A.; Cook, R.; Russell, J.J.; Gaw, C.; Dent, R.M.; de Vitry, C.; Niyogi, K.K. A Conserved Rubredoxin Is Necessary for Photosystem II Accumulation in Diverse Oxygenic Photoautotrophs. J. Biol. Chem. 2013, 288, 26688–26696. [Google Scholar] [CrossRef] [PubMed]
  112. García-Cerdán, J.G.; Furst, A.L.; McDonald, K.L.; Schünemann, D.; Francis, M.B.; Niyogi, K.K. A thylakoid membrane-bound and redox-active rubredoxin (RBD1) functions in de novo assembly and repair of photosystem II. Proc. Natl. Acad. Sci. USA 2019, 116, 16631–16640. [Google Scholar] [CrossRef] [PubMed]
  113. Spaniol, B.; Lang, J.; Venn, B.; Schake, L.; Sommer, F.; Mustas, M.; Geimer, S.; Wollman, F.-A.; Choquet, Y.; Mühlhaus, T. Complexome profiling on the Chlamydomonas lpa2 mutant reveals insights into PSII biogenesis and new PSII associated proteins. J. Exp. Bot. 2022, 73, 245–262. [Google Scholar] [CrossRef] [PubMed]
  114. Cecchin, M.; Jeong, J.; Son, W.; Kim, M.; Park, S.; Zuliani, L.; Cazzaniga, S.; Pompa, A.; Young Kang, C.; Bae, S. LPA2 protein is involved in photosystem II assembly in Chlamydomonas reinhardtii. Plant J. 2021, 107, 1648–1662. [Google Scholar] [CrossRef] [PubMed]
  115. Oliver, N.; Avramov, A.P.; Nürnberg, D.J.; Dau, H.; Burnap, R.L. From manganese oxidation to water oxidation: Assembly and evolution of the water-splitting complex in photosystem II. Photosynth. Res. 2022, 152, 107–133. [Google Scholar] [CrossRef]
  116. Rova, E.M.; McEwen, B.; Fredriksson, P.O.; Styring, S. Photoactivation and photoinhibition are competing in a mutant of Chlamydomonas reinhardtii lacking the 23-kDa extrinsic subunit of photosystem II. J. Biol. Chem. 1996, 271, 28918–28924. [Google Scholar] [CrossRef]
  117. Vinyard, D.J.; Sun, J.S.; Gimpel, J.; Ananyev, G.M.; Mayfield, S.P.; Charles Dismukes, G. Natural isoforms of the Photosystem II D1 subunit differ in photoassembly efficiency of the water-oxidizing complex. Photosynth. Res. 2016, 128, 141–150. [Google Scholar] [CrossRef]
  118. Mayfield, S.P.; Bennoun, P.; Rochaix, J.-D. Expression of the nuclear encoded OEE1 protein is required for oxygen evolution and stability of photosystem II particles in Chlamydomonas reinhardtii. EMBO J. 1987, 6, 313–318. [Google Scholar] [CrossRef]
  119. Popelkova, H.; Yocum, C.F. PsbO, the manganese-stabilizing protein: Analysis of the structure–function relations that provide insights into its role in photosystem II. J. Photochem. Photobiol. B Biol. 2011, 104, 179–190. [Google Scholar] [CrossRef] [PubMed]
  120. Rova, M.; Franzen, L.G.; Fredriksson, P.O.; Styring, S. Photosystem II in a mutant of Chlamydomonas reinhardtii lacking the 23 kDa psbP protein shows increased sensitivity to photoinhibition in the absence of chloride. Photosynth. Res. 1994, 39, 75–83. [Google Scholar] [CrossRef]
  121. Enami, I.; Okumura, A.; Nagao, R.; Suzuki, T.; Iwai, M.; Shen, J.-R. Structures and functions of the extrinsic proteins of photosystem II from different species. Photosynth. Res. 2008, 98, 349–363. [Google Scholar] [CrossRef] [PubMed]
  122. Gisriel, C.J.; Wang, J.; Liu, J.; Flesher, D.A.; Reiss, K.M.; Huang, H.-L.; Yang, K.R.; Armstrong, W.H.; Gunner, M.R.; Batista, V.S.; et al. High-resolution cryo-electron microscopy structure of photosystem II from the mesophilic cyanobacterium, Synechocystis sp. PCC 6803. Proc. Natl. Acad. Sci. USA 2022, 119, e2116765118. [Google Scholar] [CrossRef] [PubMed]
  123. Knoppová, J.; Yu, J.; Konik, P.; Nixon, P.J.; Komenda, J. CyanoP is Involved in the Early Steps of Photosystem II Assembly in the Cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 2016, 57, 1921–1931. [Google Scholar] [CrossRef] [PubMed]
  124. Minagawa, J.; Takahashi, Y. Structure, function and assembly of Photosystem II and its light-harvesting proteins. Photosynth. Res. 2004, 82, 241–263. [Google Scholar] [CrossRef] [PubMed]
  125. Cazzaniga, S.; Kim, M.; Bellamoli, F.; Jeong, J.; Lee, S.; Perozeni, F.; Pompa, A.; Jin, E.; Ballottari, M. Photosystem II antenna complexes CP26 and CP29 are essential for nonphotochemical quenching in Chlamydomonas reinhardtii. Plant Cell Environ. 2020, 43, 496–509. [Google Scholar] [CrossRef] [PubMed]
  126. Swiatek, M.; Kuras, R.; Sokolenko, A.; Higgs, D.; Olive, J.; Cinque, G.; Muller, B.; Eichacker, L.A.; Stern, D.B.; Bassi, R.; et al. The chloroplast gene ycf9 encodes a photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture. Plant Cell 2001, 13, 1347–1367. [Google Scholar] [CrossRef] [PubMed]
  127. Delosme, R.; Olive, J.; Wollman, F.-A. Changes in light energy distrubution upon state transitions: An in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii. Biochim. Et Biophys. Acta (BBA) Bioenerg. 1996, 1273, 150–158. [Google Scholar] [CrossRef]
  128. Tikkanen, M.; Aro, E.-M. Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim. Et Biophys. Acta (BBA) Bioenerg. 2012, 1817, 232–238. [Google Scholar] [CrossRef] [PubMed]
  129. Vainonen, J.P.; Hansson, M.; Vener, A.V. STN8 protein kinase in Arabidopsis thaliana is specific in phosphorylaton of photosystem II core proteins J. Biol. Chem. 2005, 280, 33679–33686. [Google Scholar] [CrossRef] [PubMed]
  130. Bonardi, V.; Pesaresi, P.; Becker, T.; Schleiff, E.; Wagner, R.; Pfannschmidt, T.; Jahns, P.; Leister, D. Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 2005, 437, 1179–1182. [Google Scholar] [CrossRef] [PubMed]
  131. Samol, I.; Shapiguzov, A.; Ingelsson, B.; Fucile, G.; Crèvecoeur, M.; Vener, A.V.; Rochaix, J.-D.; Goldschmidt-Clermont, M. Identification of a Photosystem II Phosphatase Involved in Light Acclimation in Arabidopsis. Plant Cell 2012, 24, 2596–2609. [Google Scholar] [CrossRef] [PubMed]
  132. Bellafiore, S.; Barneche, F.; Peltier, G.; Rochaix, J.-D. State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 2005, 433, 892–895. [Google Scholar] [CrossRef] [PubMed]
  133. Tikkanen, M.; Nurmi, M.; Kangasjärvi, S.; Aro, E.-M. Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim. Et Biophys. Acta (BBA) Bioenerg. 2008, 1777, 1432–1437. [Google Scholar] [CrossRef] [PubMed]
  134. Shapiguzov, A.; Ingelsson, B.; Samol, I.; Andres, C.; Kessler, F.; Rochaix, J.-D.; Vener, A.V.; Goldschmidt-Clermont, M. The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc. Natl. Acad. Sci. USA 2010, 107, 4782–4787. [Google Scholar] [CrossRef] [PubMed]
  135. Pribil, M.; Pesaresi, P.; Hertle, A.; Barbato, R.; Leister, D. Role of Plastid Protein Phosphatase TAP38 in LHCII Dephosphorylation and Thylakoid Electron Flow. PLoS Biol. 2010, 8, e1000288. [Google Scholar] [CrossRef]
  136. de Vitry, C.; Diner, B.A.; Popot, J.-L. Photosystem II Particle from Chlamydomonas reinhardtii. J. Biol. Chem. 1991, 266, 16614–16621. [Google Scholar] [CrossRef] [PubMed]
  137. Lemeille, S.; Turkina, M.V.; Vener, A.V.; Rochaix, J.-D. Stt7-dependent phosphorylation during state transitions in the green alga Chlamydomonas reinhardtii. Mol. Cell Proteom. 2010, 9, 1281–1295. [Google Scholar] [CrossRef]
  138. Depège, N.; Bellafiore, S.; Rochaix, J.-D. Role of Chloroplast Protein Kinase Stt7 in LHCII Phosphorylation and State Transition in Chlamydomonas. Science 2003, 299, 1572–1575. [Google Scholar] [CrossRef]
  139. Cariti, F.; Chazaux, M.; Lefebvre-Legendre, L.; Longoni, P.; Ghysels, B.; Johnson, X.; Goldschmidt-Clermont, M. Regulation of Light Harvesting in Chlamydomonas reinhardtii Two Protein Phosphatases Are Involved in State Transitions. Plant Physiol. 2020, 183, 1749–1764. [Google Scholar] [CrossRef]
  140. Terentyev, V.V.; Shukshina, A.K.; Shitov, A.V. Carbonic anhydrase CAH3 supports the activity of photosystem II under increased pH. Biochim. Et Biophys. Acta (BBA) Bioenerg. 2019, 1860, 582–590. [Google Scholar] [CrossRef] [PubMed]
  141. Terentyev, V.V.; Shukshina, A.K.; Ashikhmin, A.A.; Tikhonov, K.G.; Shitov, A.V. The Main Structural and Functional Characteristics of Photosystem-II-Enriched Membranes Isolated from Wild Type and cia3 Mutant Chlamydomonas reinhardtii. Life 2020, 10, 63. [Google Scholar] [CrossRef] [PubMed]
  142. Reisman, S.; Ohad, I. Light-dependent degradation of the thylakoid 32 kDa QB protein in isolated chloroplast membranes of Chlamydomonas reinhardtii. Biochim. Et Biophys. Acta (BBA) Bioenerg. 1986, 849, 51–61. [Google Scholar] [CrossRef]
  143. Murata, N.; Nishiyama, Y. ATP is a driving force in the repair of photosystem II during photoinhibition. Plant Cell Environ. 2018, 41, 285–299. [Google Scholar] [CrossRef]
  144. Schuster, G.; Timberg, R.; Ohad, I. Turnover of thylakoid photosystem II proteins during photoinhibition of Chlamydomonas reinhardtii. Eur. J. Biochem. 1988, 177, 403–410. [Google Scholar] [CrossRef] [PubMed]
  145. Haussuhl, K.; Andersson, B.; Adamska, I. A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO J. 2001, 20, 713–722. [Google Scholar] [CrossRef] [PubMed]
  146. Huesgen, P.F.; Schuhmann, H.; Adamska, I. Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease. FEBS Lett. 2006, 580, 6929–6932. [Google Scholar] [CrossRef] [PubMed]
  147. Kapri-Pardes, E.; Naveh, L.; Adam, Z. The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. Plant Cell 2007, 19, 1039–1047. [Google Scholar] [CrossRef] [PubMed]
  148. Sun, X.; Peng, L.; Guo, J.; Chi, W.; Ma, J.; Lu, C.; Zhang, L. Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. Plant Cell 2007, 19, 1347–1361. [Google Scholar] [CrossRef] [PubMed]
  149. Barker, M.; de Vries, R.; Nield, J.; Komenda, J.; Nixon, P.J. The Deg Proteases Protect Synechocystis sp. PCC 6803 during Heat and Light Stresses but Are Not Essential for Removal of Damaged D1 Protein during the Photosystem Two Repair Cycle. J. Biol. Chem. 2006, 281, 30347–30355. [Google Scholar] [CrossRef]
  150. Malnoë, A.; Wang, F.; Girard-Bascou, J.; Wollman, F.-A.; de Vitry, C. Thylakoid FtsH Protease Contributes to Photosystem II and Cytochrome b 6 f Remodeling in Chlamydomonas reinhardtii under Stress Conditions. Plant Cell 2014, 26, 373–390. [Google Scholar] [CrossRef] [PubMed]
  151. Schroda, M.; de Vitry, C. Molecular chaperones, proteases, and unfolded protein responses. In The Chlamydomonas Sourcebook; Elsevier: Amsterdam, The Netherlands, 2023; pp. 647–689. [Google Scholar]
  152. Theis, J.; Lang, J.; Spaniol, B.; Ferté, S.; Niemeyer, J.; Sommer, F.; Zimmer, D.; Venn, B.; Mehr, S.F.; Mühlhaus, T.; et al. The Chlamydomonas deg1c Mutant Accumulates Proteins Involved in High Light Acclimation1 [OPEN]. Plant Physiol. 2019, 181, 1480–1497. [Google Scholar] [CrossRef] [PubMed]
  153. Theis, J.; Schroda, M. Revisiting the photosystem II repair cycle. Plant Signal. Behav. 2016, 11, e1218587. [Google Scholar] [CrossRef] [PubMed]
  154. Muranaka, L.S.; Rütgers, M.; Bujaldon, S.; Heublein, A.; Geimer, S.; Wollman, F.-A.; Schroda, M. TEF30 Interacts with Photosystem II Monomers and Is Involved in the Repair of Photodamaged Photosystem II in Chlamydomonas reinhardtii. Plant Physiol. 2015, 170, 821–840. [Google Scholar] [CrossRef] [PubMed]
  155. Park, S.; Khamai, P.; Garcia-Cerdan, J.G.; Melis, A. REP27, a Tetratricopeptide Repeat Nuclear-Encoded and Chloroplast-Localized Protein, Functions in D1/32-kD Reaction Center Protein Turnover and Photosystem II Repair from Photodamage. Plant Physiol. 2007, 143, 1547–1560. [Google Scholar] [CrossRef]
  156. Dewez, D.; Park, S.; García-Cerdán, J.G.; Lindberg, P.; Melis, A. Mechanism of REP27 Protein Action in the D1 Protein Turnover and Photosystem II Repair from Photodamage. Plant Physiol. 2009, 151, 88–99. [Google Scholar] [CrossRef]
Plants 13 00811 g001
Figure 1. An overview of PSII assembly and organization in Chlamydomonas. ① Nuclear-encoded PSII subunits, including PsbO, PsbP, and PsbQ, are translated in the cytosol and imported into the chloroplast using the TOC TIC system. ② These complexes are spatially aligned with the chloroplast translation zone near the pyrenoid. ③ PSII subunits assemble in an organized pathway from reaction center intermediates to mature dimers. ④ Active and phosphorylated PSII dimers are enriched in appressed domains of the thylakoid membranes. ⑤ PSII assembly and degradation occur in non-appressed domains of the thylakoid membranes. Additional details and references are provided in the text.
Figure 1. An overview of PSII assembly and organization in Chlamydomonas. ① Nuclear-encoded PSII subunits, including PsbO, PsbP, and PsbQ, are translated in the cytosol and imported into the chloroplast using the TOC TIC system. ② These complexes are spatially aligned with the chloroplast translation zone near the pyrenoid. ③ PSII subunits assemble in an organized pathway from reaction center intermediates to mature dimers. ④ Active and phosphorylated PSII dimers are enriched in appressed domains of the thylakoid membranes. ⑤ PSII assembly and degradation occur in non-appressed domains of the thylakoid membranes. Additional details and references are provided in the text.
Plants 13 00811 g001
Plants 13 00811 g002
Figure 2. The PSII C2S2 complex from Chlamydomonas from (PDB ID 6KAC) [54]. Nuclear-encoded PSII subunits are shown in shades of purple.
Figure 2. The PSII C2S2 complex from Chlamydomonas from (PDB ID 6KAC) [54]. Nuclear-encoded PSII subunits are shown in shades of purple.
Plants 13 00811 g002
Plants 13 00811 g003
Figure 3. Discrete D1 fragments accumulate in Chlamydomonas in an FtsH mutant [150]. Note the appearance of ~23, 16–20 kDa, and 6–10 kDa fragments in the lower panels. (WT: wild type; LC: chloroplast translation inhibitors lincomycin and chloramphenicol added; ftsh1–1: mutant with defective FtsH protease due to a FtsH1−R420C mutation; OEE2: loading control probing PsbP). Reproduced with permission from Oxford University Press, Oxford, UK.
Figure 3. Discrete D1 fragments accumulate in Chlamydomonas in an FtsH mutant [150]. Note the appearance of ~23, 16–20 kDa, and 6–10 kDa fragments in the lower panels. (WT: wild type; LC: chloroplast translation inhibitors lincomycin and chloramphenicol added; ftsh1–1: mutant with defective FtsH protease due to a FtsH1−R420C mutation; OEE2: loading control probing PsbP). Reproduced with permission from Oxford University Press, Oxford, UK.
Plants 13 00811 g003
Table 1. Trans-regulatory elements of PSII subunit translation in Chlamydomonas.
Table 1. Trans-regulatory elements of PSII subunit translation in Chlamydomonas.
PSII Subunit
Affected		Translation FactorMechanismReferences
psbA (D1)RB47Binds to A-rich region in the psbA 5′ UTR; required for D1 synthesis[87,88,89]
RB60Protein disulfide isomerase that redox regulates RB47[87,90]
TBA1Oxidoreductase that facilitates binding of RB47 to psbA transcript[91]
RB55Observed to bind psbA mRNA but not characterized[92,93]
RBP63Binds to psbA 5′ UTR; essential for D1 synthesis; subunit of chloroplast pyruvate dehydrogenase complex that becomes a translational regulator upon acetylation[94,95,96]
CrHCF173Homolog of Arabidopsis HCF173; affects D1 accumulation[97]
psbD (D2)NAC1Promotes psbD translation at a step that is likely after initiation[98,99]
AC115
NAC2Promotes psbD stability by binding to its 5′ UTR[85,100]
RBP40 (RB38)Binds to U-rich region of psbD 5′ UTR; forms a complex with NAC2 to control psbD mRNA stability and initiation; also observed to bind psbA mRNA although this interaction may not be specific[92,101,102]
psbB (CP47)Mbb1Promotes psbB mRNA stability by interacting with its 5′ UTR; also affects psbH mRNA maturation[103,104]
psbC (CP43)TBC1Facilitates psbC translation by binding to its 5′ UTR[86,105,106]
TBC2
TBC3
MBCIStabilizes psbC mRNA[76]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Mehra, H.S.; Wang, X.; Russell, B.P.; Kulkarni, N.; Ferrari, N.; Larson, B.; Vinyard, D.J. Assembly and Repair of Photosystem II in Chlamydomonas reinhardtii. Plants 2024, 13, 811. https://doi.org/10.3390/plants13060811

AMA Style

Mehra HS, Wang X, Russell BP, Kulkarni N, Ferrari N, Larson B, Vinyard DJ. Assembly and Repair of Photosystem II in Chlamydomonas reinhardtii. Plants. 2024; 13(6):811. https://doi.org/10.3390/plants13060811

Chicago/Turabian Style

Mehra, Himanshu S., Xiaozhuo Wang, Brandon P. Russell, Nidhi Kulkarni, Nicholas Ferrari, Brent Larson, and David J. Vinyard. 2024. "Assembly and Repair of Photosystem II in Chlamydomonas reinhardtii" Plants 13, no. 6: 811. https://doi.org/10.3390/plants13060811

APA Style

Mehra, H. S., Wang, X., Russell, B. P., Kulkarni, N., Ferrari, N., Larson, B., & Vinyard, D. J. (2024). Assembly and Repair of Photosystem II in Chlamydomonas reinhardtii. Plants, 13(6), 811. https://doi.org/10.3390/plants13060811

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop