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Psb27, a photosystem II assembly protein, enables quenching of excess light energy during its participation in the PSII lifecycle

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Virginia M. Johnson
Virginia M. Johnson
Virginia M. Johnson
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Sandeep Biswas at Washington University in St. Louis
Sandeep Biswas
Johnna L. Roose
Johnna L. Roose
Johnna L. Roose
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Himadri Pakrasi at Washington University in St. Louis
Himadri Pakrasi
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Abstract and Figures

Photosystem II (PSII), the enzyme responsible for oxidizing water into molecular oxygen, undergoes a complex lifecycle during which multiple assembly proteins transiently bind to and depart from PSII assembly intermediate complexes. Psb27 is one such protein. It associates with the CP43 chlorophyll-binding subunit of PSII to form a Psb27-PSII sub-complex that constitutes 7–10% of the total PSII pool. Psb27 remains bound to PSII assembly intermediates and dissociates prior to the formation of fully functional PSII. In this study, we compared a series of Psb27 mutant strains in the cyanobacterium Synechocystis sp. PCC 6803 with varied expression levels of Psb27: wild type (WT); psb27 genetic deletion (Del27), genetically complemented psb27 (Com27); and over-expressed Psb27 (OE27). The Del27 strain demonstrated decreased non-photochemical fluorescence quenching, while the OE27 strain showed increased non-photochemical quenching and tolerance to fluctuating light conditions. Multiple flashes and fluorescence decay analysis indicated that OE27 has the least affected maximum PSII quantum yield of the mutants. OE27 also displayed a minimal impact on the half-life of the fast component of QA– reoxidation over multiple flashes, indicating robust PSII function. We propose that the close association between Psb27 and CP43, and the absence of a fully functional manganese cluster in the Psb27-PSII complex create a PSII sub-population that dissipates excitation energy prior to its recruitment into the functional PSII pool. Efficient energy dissipation prevents damage to this pre-PSII pool and allows for efficient PSII repair and maturation. Participation of Psb27 in the PSII life cycle ensures high-quality PSII assembly.
OE27 growth outpaces WT Synechocystis 6803 in fluctuating light. A Growth under continuous light. This figure shows the growth curve of WT, Del27, Com27, OE27 under normal growth continuous light (30 μmol photons/m²s¹). B Growth under 1200 μmol photons/m²s¹, 30 min of on–off cycles
OE27 growth outpaces WT Synechocystis 6803 in fluctuating light. A Growth under continuous light. This figure shows the growth curve of WT, Del27, Com27, OE27 under normal growth continuous light (30 μmol photons/m²s¹). B Growth under 1200 μmol photons/m²s¹, 30 min of on–off cycles
… 
NPQ is increased in the Psb27 overexpression strain A NPQ traces from Fluorocam 800MF of four cell lines. Light and dark schemes are indicated with saturating pulses applied. Fm, Fd, and Fs are marked for WT trace. Deconvolution of the traces followed manufacturer’s protocol (Photo System Instruments, Brno, Czech Republic). B Plant vitality index Rfd (Fd/Fs) at intervals during light exposure. C Coefficient of quenching (Fm′−F)/(Fm′−Fo′). D NPQ ((Fm−Fm′)/Fm′). Data are representative of three replicates
NPQ is increased in the Psb27 overexpression strain A NPQ traces from Fluorocam 800MF of four cell lines. Light and dark schemes are indicated with saturating pulses applied. Fm, Fd, and Fs are marked for WT trace. Deconvolution of the traces followed manufacturer’s protocol (Photo System Instruments, Brno, Czech Republic). B Plant vitality index Rfd (Fd/Fs) at intervals during light exposure. C Coefficient of quenching (Fm′−F)/(Fm′−Fo′). D NPQ ((Fm−Fm′)/Fm′). Data are representative of three replicates
… 
OE27 is resilient to light adaptation over 1000 flashes. A Fluorescence induction (Kautsky effect), B Fluorescence decay over 500 ms for WT and OE27 strains after first (F) and last (L, 1000) flashes. CFm fluctuation over 1000 flashes. DFo fluctuation over 1000 flashes. EFv derived from (C) and (D). Fv value shows periodic change which is the opposite of flash-induced oxygen yield. Some studies use these values to derive S-state distribution analysis. FFv/Fm maximum quantum yield of PSII chemistry
OE27 is resilient to light adaptation over 1000 flashes. A Fluorescence induction (Kautsky effect), B Fluorescence decay over 500 ms for WT and OE27 strains after first (F) and last (L, 1000) flashes. CFm fluctuation over 1000 flashes. DFo fluctuation over 1000 flashes. EFv derived from (C) and (D). Fv value shows periodic change which is the opposite of flash-induced oxygen yield. Some studies use these values to derive S-state distribution analysis. FFv/Fm maximum quantum yield of PSII chemistry
… 
Schematic of the role of Psb27 NPQ. Psb27 is the determining factor in the pool size of Psb27-PSII from both the synthesis and repair pathways. A larger pool of the quenching species Psb27-PSII forms when more Psb27 is present in the cell, which enables higher NPQ
Schematic of the role of Psb27 NPQ. Psb27 is the determining factor in the pool size of Psb27-PSII from both the synthesis and repair pathways. A larger pool of the quenching species Psb27-PSII forms when more Psb27 is present in the cell, which enables higher NPQ
… 
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Vol.:(0123456789)
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Photosynthesis Research (2022) 152:297–304
https://doi.org/10.1007/s11120-021-00895-3
ORIGINAL ARTICLE
Psb27, aphotosystem II assembly protein, enables quenching
ofexcess light energy duringits participation inthePSII lifecycle
VirginiaM.Johnson1 · SandeepBiswas1 · JohnnaL.Roose2· HimadriB.Pakrasi1 · HaijunLiu1
Received: 4 October 2021 / Accepted: 27 December 2021 / Published online: 5 January 2022
© The Author(s), under exclusive licence to Springer Nature B.V. 2022
Abstract
Photosystem II (PSII), the enzyme responsible for oxidizing water into molecular oxygen, undergoes a complex lifecycle
during which multiple assembly proteins transiently bind to and depart from PSII assembly intermediate complexes. Psb27
is one such protein. It associates with the CP43 chlorophyll-binding subunit of PSII to form a Psb27-PSII sub-complex
that constitutes 7–10% of the total PSII pool. Psb27 remains bound to PSII assembly intermediates and dissociates prior
to the formation of fully functional PSII. In this study, we compared a series of Psb27 mutant strains in the cyanobacte-
rium Synechocystis sp. PCC 6803 with varied expression levels of Psb27: wild type (WT); psb27 genetic deletion (Del27),
genetically complemented psb27 (Com27); and over-expressed Psb27 (OE27). The Del27 strain demonstrated decreased
non-photochemical fluorescence quenching, while the OE27 strain showed increased non-photochemical quenching and
tolerance to fluctuating light conditions. Multiple flashes and fluorescence decay analysis indicated that OE27 has the least
affected maximum PSII quantum yield of the mutants. OE27 also displayed a minimal impact on the half-life of the fast
component of QA
– reoxidation over multiple flashes, indicating robust PSII function. We propose that the close association
between Psb27 and CP43, and the absence of a fully functional manganese cluster in the Psb27-PSII complex create a PSII
sub-population that dissipates excitation energy prior to its recruitment into the functional PSII pool. Efficient energy dis-
sipation prevents damage to this pre-PSII pool and allows for efficient PSII repair and maturation. Participation of Psb27 in
the PSII life cycle ensures high-quality PSII assembly.
Keywords Photosystem II· Photosynthesis· Non-photochemical quenching· Synechocystis 6803
Introduction
Photosystem II (PSII) is a unique enzyme in that it routinely
experiences damage caused by one of its substrates, light,
and its derivative reactive oxygen species. Additionally,
PSII is assembled modularly from chlorophyll-containing
subunits, which themselves are sensitive to damage by
absorption of light prior to complete PSII assembly. On the
organismal level, this photodamage is detrimental to fitness
unless a protective mechanism is adopted to dissipate excess
light energy, both during assembly and under photoactive
conditions. Cyanobacteria have several known mecha-
nisms of excitation energy quenching and redistribution,
collectively called non-photochemical quenching (NPQ).
These include quenching via the orange carotenoid protein
(OCP), which, in its light-induced active state, uncouples
the excitation energy transfer from phycobilisome antennas
to PSII, reducing its functional cross section (Wilson etal.
2006; Wilson etal. 2008). Another mechanism is via IsiA,
a chlorophyll-containing homolog of CP43, which forms
oligomeric ring structures under stress conditions (Chen
etal. 2018; Ihalainen etal. 2005). These rings are thought
to absorb and dissipate excess light energy as a means of
photoprotection. Additionally, during assembly, the reac-
tion center proteins of PSII are associated with carotenoid-
containing quenching proteins known as HLIPS for protec-
tion prior to their assembly into active PSII (Knoppova etal.
2014; Niedzwiedzki etal. 2016). This mechanism relies on
carotenoids’ ability to quench both triplet chlorophyll and
singlet oxygen. Cyanobacteria have two other mechanisms
* Himadri B. Pakrasi
pakrasi@wustl.edu
1 Department ofBiology, Washington University inSt. Louis,
St.Louis, USA
2 Division ofBiochemistry andMolecular Biology,
Department ofBiological Sciences, Louisiana State
University, BatonRouge, LA, USA
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... This study shows that the iron-deficiency generated IsiA maintains direct spatial contact with membrane intrinsic PSII. In other works, it has been proposed that the PSII that coexists with IsiA in cyanobacterial membrane also participates in regulatory energy dissipation along with its routine light-harvesting function (Sandström et al. 2001;Horton et al. 1996;Huang et al. 2021;Johnson et al. 2022). However, direct support for such a proposition with the aid of electronic structures and excited state dynamics of PSII is lacking so far. ...
... Here in this study, we set out to carry systematic and comprehensive analyses of the F and SF spectra (of IsiA membrane) to achieve the aforementioned goals. Under extreme environmental stress, the PSII pools present in the cyanobacterial membrane are suggested to be conformationally distorted, and hence largely energy dissipative (Huang et al. 2021;Johnson et al. 2022;Zabret et al. 2021). To shed some more light on this hypothesis, we carried out SF investigation on the iron-deficient cyanobacterial membrane, as SF spectroscopy was found to be very efficient in characterizing the functional state of various native and artificially aggregated photosynthetic pigment-protein complexes (Wahadoszamen et al. 2012(Wahadoszamen et al. , 2014a(Wahadoszamen et al. , b, 2020Ara et al. 2021). ...
... The conformational distortion, if taken place, can lead to tangible rearrangements on the available photoactive cofactors (such as Chls and carotenoids) which in turn can greatly increase the mixing between the permissible excitonic and CT states, hence making PSII more energy dissipative through the interplay of the CT state (Wahadoszamen et al. 2014a, b). It has been reported that PSII of cyanobacteria takes part in regulative energy dissipation through the direct intervention of a small membrane extrinsic miniature protein, Psb27 (Huang et al. 2021;Johnson et al. 2022;Zabret et al. 2021). During environmental stress, the auxiliary protein Psb27 binds available inactive PSII to form a larger population of transient Psb27-PSII pool. ...
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In this work, we applied Stark fluorescence spectroscopy to an iron-stressed cyanobacterial membrane to reveal key insights about the electronic structures and excited state dynamics of the two important pigment-protein complexes, IsiA and PSII, both of which prevail simultaneously within the membrane during iron deficiency and whose fluorescence spectra are highly overlapped and hence often hardly resolved by conventional fluorescence spectroscopy. Thanks to the ability of Stark fluorescence spectroscopy, the fluorescence signatures of the two complexes could be plausibly recognized and disentangled. The systematic analysis of the SF spectra, carried out by employing standard Liptay formalism with a realistic spectral deconvolution protocol, revealed that the IsiA in an intact membrane retains almost identical excited state electronic structures and dynamics as compared to the isolated IsiA we reported in our earlier study. Moreover, the analysis uncovered that the excited state of the PSII subunit of the intact membrane possesses a significantly large CT character. The observed notably large magnitude of the excited state CT character may signify the supplementary role of PSII in regulative energy dissipation during iron deficiency.
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... PCC6803 or Arabidopsis thaliana not being affected under optimal light conditions, the PSII activity and growth were dramatically decreased under high light stress or fluctuating light (Be ckov a et al., 2017;Chen et al., 2006;Hou et al., 2015). Psb27 has been demonstrated to participate in the repair cycle of PSII by interacting with the CP43 subunit of PSII core (Johnson et al., 2022;Liu et al., 2011). By contrast, the psb29 mutants of Synechocystis and Arabidopsis had compromised growth compared to wild type under normal light conditions. ...
... In the recent decade, great advances have been made in our understanding of the biogenesis and assembly of PSII in photosynthetic organisms under steady-state conditions (Fadeeva et al., 2023;Li et al., 2020;Pollastri et al., 2019;Zhu et al., 2022), and a suite of auxiliary protein factors have been identified to regulate this intricate but ordered process (Johnson et al., 2022;Keren et al., 2005;Knoppov a et al., 2022;Pl€ ochinger et al., 2016). However, some of the key steps in the maintenance of PSII remain unclear. ...
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Enhancing the efficiency of photosynthesis represents a promising strategy to improve crop yields, with keeping the steady state of PSII being key to determining the photosynthetic performance. However, the mechanisms whereby the stability of PSII is maintained in oxygenic organisms remain to be explored. Here, we report that the Psb28 protein functions in regulating the homeostasis of PSII under different light conditions in Arabidopsis thaliana. The psb28 mutant is much smaller than the wild‐type plants under normal growth light, which is due to its significantly reduced PSII activity. Similar defects were seen under low light and became more pronounced under photoinhibitory light. Notably, the amounts of PSII core complexes and core subunits are specifically decreased in psb28, whereas the abundance of other representative components of photosynthetic complexes remains largely unaltered. Although the PSII activity of psb28 was severely reduced when subjected to high light, its recovery from photoinactivation was not affected. By contrast, the degradation of PSII core protein subunits is dramatically accelerated in the presence of lincomycin. These results indicate that psb28 is defective in the photoprotection of PSII, which is consistent with the observation that the overall NPQ is much lower in psb28 compared to the wild type. Moreover, the Psb28 protein is associated with PSII core complexes and interacts mainly with the CP47 subunit of PSII core. Taken together, these findings reveal an important role for Psb28 in the protection and stabilization of PSII core in response to changes in light environments.
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... Previous studies have shown that PsaD is located on the stromal side of the thylakoids and that it assembles in vitro into the membranes in its precursor (pre-PsaD) and also in its mature (PsaD) form [42]. In addition, PsaE plays a role in O 2 reduction in photosystem I and protects photosystem II against photoinhibition [43]; PsaF is involved in the docking of the electron donor proteins plastocyanin and cytochrome c 6 in eukaryotic photosynthetic organisms [44]; PsaK has two transmembrane alpha-helices [45]; PsaL functions as a light-driven plastocyanin-ferredoxin oxidoreductase in the thylakoid membranes of cyanobacteria and higher plants [46]; PsaO is involved in the balance of the excitation energy between photosystems I and II; PetH controls the rate of the interaction with PetF [47]; Psb27 enables the quenching of excess light energy during its participation in the PSII lifecycle [48]; PsbR is a missing link in the assembly of the oxygen-evolving complex of PSII [49]; the PsbW protein stabilizes the supramolecular organization of photosystem II [50]; F-type ATPase delta produces ATP in cells. We found that the quality of the light affects the gene expressions of the PsaD, PsaE, PsaF, PsaK, PsaL, PsaO, PetH, Psb27, PsbR, PsbW, and delta proteins and finally impacts F 0 and Pn. ...
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Redesigning photosynthesis to sustainably meet global food and bioenergy demand
Article
  • Jun 2015
  • P NATL ACAD SCI USA
The world's crop productivity is stagnating whereas population growth, rising affluence, and mandates for biofuels put increasing demands on agriculture. Meanwhile, demand for increasing cropland competes with equally crucial global sustainability and environmental protection needs. Addressing this looming agricultural crisis will be one of our greatest scientific challenges in the coming decades, and success will require substantial improvements at many levels. We assert that increasing the efficiency and productivity of photosynthesis in crop plants will be essential if this grand challenge is to be met. Here, we explore an array of prospective redesigns of plant systems at various scales, all aimed at increasing crop yields through improved photosynthetic efficiency and performance. Prospects range from straightforward alterations, already supported by preliminary evidence of feasibility, to substantial redesigns that are currently only conceptual, but that may be enabled by new developments in synthetic biology. Although some proposed redesigns are certain to face obstacles that will require alternate routes, the efforts should lead to new discoveries and technical advances with important impacts on the global problem of crop productivity and bioenergy production.
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