Plastoquinone’s pivotal role in photosynthesis and redox sensing: a thylakoid redox hub for chloroplast and cyanobacterial signaling

1 Introduction

Earth is a 4.6-billion-year-old planet shaped by successive destructive and constructive geographical processes that established a stable ecological niche for biological colonization (Scheffers et al., 2015). These repetitive atmospheric and geological changes drove the diversification of flora and fauna (Taylor, 2004). However, the existence of different life forms has fundamentally restructured the Earth’s geochemistry through complex biochemical events. A primary example is the Great Oxidation Event (GOE), during which early cyanobacteria-like organism initiated oxygenic photosynthesis, transitioning the atmosphere from a reducing to an oxidizing state (Grettenberger and Sumner, 2024). This transition facilitated the formation of the stratospheric ozone layer, shielding the biosphere from harmful ultraviolet-C (UV-C; 100–280 nm) radiation (Cooke et al., 2022). Furthermore, as cyanobacteria established the foundation for oxygenic photosynthesis in algae and higher plants, it appears that fundamental mechanisms of this process have remained conserved throughout evolution (Sánchez-Baracaldo and Cardona, 2020).

Beyond its role in photosynthesis, light serves as a critical developmental cue for photosynthetic organisms. Diverse photoreceptors sense environmental light to elicit specific cellular responses via signaling cascades (Mullineaux, 2001; Kong and Okajima, 2016; Gupta et al., 2023; Tiwari et al., 2025), a process that can be defined as photon-triggered signal transduction. In contrast, photosystems function as energy-transforming units that convert solar energy into chemical energy intermediates such as reduced plastoquinone (PQH₂), adenosine triphosphate (ATP), and nicotinamide adenine dinucleotide phosphate (NADPH) (Sekar and Ramasamy, 2015). These molecules act as internal chemical sensors, providing feedback on the light environment without interrupting photosynthetic flux. This mechanism represents a chemical-triggered signal transduction system.

Among these metabolic sensors, the plastoquinone (PQ) pool is a well-characterized redox sensor that regulates gene expression under fluctuating light environment (Foyer and Hanke, 2022; Cheong et al., 2022; Calzadilla and Unrein, 2025; Johnson et al., 2026). PQ is a derivative of benzoquinone (BQ), which is the simplest parent compound containing a single quinone ring. Other parent quinone compounds, such as naphthoquinones (NQ) and anthraquinones (AQ) (Figure 1), contain double and triple quinone rings, respectively. Quinones are widely distributed across different taxa, where they maintain redox homeostasis, serve antioxidative functions, and participate in defense mechanisms (Wang et al., 2024). This review focuses on the functional role of PQ, as a mobile electron carrier within the photosynthetic electron transport chain (PETC).

The redox status of the PQ pool exerts both short- and long-term effects on photosynthetic efficiency. Fluctuations in light quality or intensity can lead to the accumulation of either reduced or oxidized PQ, which subsequently induces various physiological responses in plants, algae, and cyanobacteria. These responses include state transitions, chlorophyll and carotenoids biosynthesis, the assembly of photosystem subunits, and the scavenging of singlet oxygen (Liu and Lu, 2016; Murata, 2009; Longoni and Goldschmidt-Clermont, 2021; Yu et al., 2025; Havaux, 2020; Borisova-Mubarakshina et al., 2019; Borisova-Mubarakshina, 2025). PQ is also an essential precursor for the synthesis of carotenoids, ɑ-tetrapyrrole, and abscisic acid that collectively shield organisms from oxidative stress (Liu and Lu, 2016).

In cyanobacteria, PQ pool integrates into a more complex signaling network where its redox state regulates the circadian rhythm, spatial functioning of carboxysomes, and global metabolic reprogramming (Kim et al., 2012; Santos-Merino et al., 2025; Fan et al., 2021). A notable gap in the current literature is a comprehensive review of the diverse functions PQ performs in photoautotrophs in response to environmental signals. While the discovery of PQ’s antioxidative properties has led to greater emphasis on its chemical characteristics, a comprehensive analysis of its physiological roles across different oxygenic photoautotrophs remains absent. To address this gap, we examine the spectrum of physiological processes regulated by the PQ redox status, uncovering its distinct role in prokaryotic and eukaryotic oxygenic photoautotrophs. Elucidating these physiological roles offers a promising framework for engineering biological systems to enhance biomass production at a larger scale.

2 Structural classification and biological distribution of quinones

All quinones are derivatives of cyclohexa-2,5-diene-1,4-dione which is an efficient proton-coupled electron transferring molecule in the biological systems. Based on the numbers of hydrocarbon rings in their core structure, quinones are primarily categorized into three classes: benzoquinones (BQ), nephthoquinones (NQ), and anthraquinones (AQ) (Łazicka and Garstka, 2026). The derivatives of BQ and NQ have an evolutionary significance as some members of these classes are distributed among ancient bacterial groups that existed in Earth’s early reducing atmosphere (Glass et al., 2023; Stairs et al., 2018; Becker et al., 2018). Most NQ derivatives serve as electron carrier in the PSI electron transport chain of oxygenic photoautotrophs and the reaction centers of green sulfur bacteria (Yoshida et al., 2003; Kjær et al., 1998).

In contrast, BQ derivatives cover a broader taxonomic range, including anoxygenic purple sulfur bacteria, oxygenic photoautotrophs, aerobes, and anaerobes (Nowicka and Kruk, 2010). Consequently, it can be hypothesized that BQ constitutes a class of quinones that function as a mobile electron carrier within the type II reaction center lineage, whereas NQ serve as carriers within the type I lineage. Conversely, AQ lacks an evolutionary lineage as electron transport quinones, but maintain antioxidative and defensive properties in eukaryotes and some prokaryotes (Ek-Ramos et al., 2019; Chien et al., 2015; Fouillaud et al., 2016; Zhao and Zheng, 2023). While the polycyclic core defines the basic scaffold in parent compounds (BQ, AQ, and NQ) of quinone (Figure 1), the vast functional diversity of quinones arises from specific substituents and side-chain modifications attached to these rings (Łazicka and Garstka, 2026). The following sections detail the distribution and specialized physiological roles of quinone derivatives across various taxa.

2.1 Biological derivatives of benzoquinone (BQ)

BQ represents the simplest quinone scaffold yet serves as a critical electron carrier and redox signaling molecule in different biological systems (Nowicka and Kruk, 2010; Chen et al., 2024; Van Hellemond et al., 1995). BQs undergo sequential one-electron reductions, existing in three distinct redox states; the fully oxidized benzoquinone (BQ), the partially reduced radical semibenzoquinone (BQ^•—), and the fully reduced hydrobenzoquinone or benzoquinol (BQH₂) (Łazicka and Garstka, 2026). To navigate the hydrophobic environment of biological membranes, BQs possess an amphipathic structure analogous to fatty acids. Prominent biological examples of modified BQs include ubiquinone (UQ), plastoquinone (PQ), and rhodoquinone (RQ).

2.1.1 Ubiquinone (UQ)

Ubiquinone (UQ), or coenzyme Q (CoQ), is structurally characterized by a BQ ring with two methoxy groups and a polyisoprenoid tail of varying length (Wang and Hekimi, 2019). Primarily, UQ functions as a mobile electron carrier within the aerobic respiratory electron transport chain (RETC) (Mitchell, 1976; Snyder et al., 1999; Jiang et al., 2011). The length of the isoprenoids tail is species-specific, leading to distinct homologs across different taxa. UQ₁₀ is predominantly found in the human, while rodents utilize both UQ₉ and UQ₁₀. In microorganisms, Saccharomyces cerevisiae and Escherichia coli utilize UQ₆ and UQ₈, respectively (Wang and Hekimi, 2019).

The RETC consists of membrane bound protein complexes I, II, III, IV, and V (Figure 2A). Complex I (NADH-UQ oxidoreductase) accepts electron from NADH and transfers them to UQ, reducing it to UQH₂. Complex II (succinate dehydrogenase) oxidizes succinate to fumarate and also transfer electrons to UQ. As a lipid-soluble mobile electron carrier, UQH₂ transfer these electrons to complex III (Cytochrome bc ₁ complex). Through Q-cycle, complex III sequentially transfer electrons to cytochrome c, which then transfers them to complex IV (cytochrome c oxidase). As the terminal electron acceptor of RETC, complex IV uses these electrons to reduce oxygen to water. The proton motive force generated across the mitochondrial membrane facilitates the synthesis of ATP via complex V (ATP Synthase) (Wang and Hekimi, 2019; Sun et al., 2018; Mitchell, 1976). Beyond its bioenergetic role, UQ serve as a potent antioxidant and a signaling molecule that mitigates oxidative stress (Jiang et al., 2011; Lapointe, 2014; Lankin et al., 2025).

2.1.2 Plastoquinone (PQ)

PQ serves as the primary mobile electron carrier within the PETC in all oxygenic photoautotrophs (Nowicka and Kruk, 2010). Based on the length of the isoprenoid chain, PQ is classified into several homologs, including PQ₃, PQ₄, PQ₈, and PQ₉ (Crane, 2010; Nowicka and Kruk, 2010). Of these homologs, PQ₉ (also termed PQ-A) is the most widely distributed and dominant form in oxygenic photoautotrophic organisms, whereas other homologs are restricted to specific plants species (Nowicka and Kruk, 2010). Beyond these homologs, structural variations in the side chain give rise to distinct PQ₉-derivatives (Havaux, 2020) Collectively, these PQs variants facilitate electron flux and provide critical photoprotection, safeguarding oxygenic photoautotrophs from light-induced oxidative damage (Havaux, 2020).

2.1.3 Rhodoquinone (RQ)

The chemical structure of rhodoquinone (RQ) is highly similar to that of UQ, with critical exception that an amino group replaces one methoxy group on the BQ ring. This minor structural modification lowers the redox potential of the molecule, enabling RQ to function as an electron carrier during anaerobic metabolism (Tan et al., 2020). RQ is distributed across specific prokaryotic and eukaryotic lineages. Among prokaryotes, it is found in photoautotrophic purple non-sulfur bacteria and certain aerobic chemotrophic beta-proteobacteria (Salinas et al., 2020; Van Hellemond et al., 1995). In eukaryotes, RQ is found in Euglena gracilis, Astasia longa, Pygsuia biforma, Nycotherus ovalis, parasitic helminthes, and various invertebrates, including oysters, snails, mussels, and lugworms (Salinas et al., 2020; Van Hellemond et al., 1995). The presence of RQ in these specific taxa facilitates an alternative bioenergetic pathway for ATP production.

Under anoxic or hypoxic conditions, RQ plays a vital role in generating reducing power to produce ATP by coupling reduction of fumarate to succinate (Salinas et al., 2020). While both RQ and UQ accept electrons from various dehydrogenases, their divergent redox potentials dictate different electron fates (Figure 2B). Instead of driving the standard RETC, RQ directs electrons toward complex II (fumarate reductase), where they are used to reduce fumarate (Tan et al., 2020; Salinas et al., 2020; Stairs et al., 2018). This potential movement of electrons via RQ maintains a proton gradient across the mitochondrial membrane, allowing for ATP synthesis in the absence of oxygen (Salinas et al., 2020; Stairs et al., 2018).

2.2 Biological derivatives of naphthoquinones (NQ)

Naphthoquinones (NQ) are aromatic compounds derived from naphthalene and characterized by two ketone groups typically situated at the 1 and 4 positions (Navarro-Tovar et al., 2023). Functionally, NQs are similar to BQs by serving as electron carriers and providing antioxidant function within biological systems (Kawamukai, 2018; Demir, 2020). While found across various taxa, NQ derivatives are most widely distributed and structurally diverse within the plant kingdom (Widhalm and Rhodes, 2016). This diversity, encompassing both natural and synthetic NQs, offers a broad spectrum of compounds with significant agricultural and pharmaceutical applications (Widhalm and Rhodes, 2016).

In plants, natural NQs such as lawsone, shikonin, and alkannin function as pigments, whereas compounds like juglone and plumbagin act as allelochemicals or defensive agents against biotic stress (Widhalm and Rhodes, 2016). Consequently, NQs represent both potent secondary metabolites and essential components of PETC. Given the vast array of NQs derivatives, this discussion focuses specifically on prenyl NQs, which include the critical biological electron carriers phylloquinone (PhQ; vitamin K1) and menaquinone (MK; vitamin K2) (Nowicka and Kruk, 2010).

2.2.1 Phylloquinone (vitamin K1, PhQ)

Phylloquinone (PhQ) is a phytyl-substituted NQ that is anchored to the lipid bilayer via its phytyl functional group (Reumann, 2013). As an essential component of the PETC, PhQ is exclusively synthesized in oxygenic photoautotrophs (Sakuragi et al., 2002; Hohmann-Marriott and Blankenship, 2011). In these organisms, PhQ functions as a vital electron carrier, facilitating electron transfer from PSI to final acceptors to drive the production of NADPH and ATP (Gross et al., 2006). Beyond its role in PSI, PhQ is involved in the assembly of PSII, while plasma membrane-localized PhQ serves as a ROS scavenger (Gross et al., 2006). In plants, PhQ is primarily sequestered within plastoglobules (detailed below), which act as a major reservoir for this molecule (Gu et al., 2021).

2.2.2 Menaquinone (vitamin K2, MK)

Menaquinone (MK) is considered the most evolutionary ancient isoprenyl quinone and serves as the primary electron carrier within the RETC of diverse prokaryotes (Nowicka and Kruk, 2010). Interestingly, certain MK derivatives, such as MK-4, replace PhQ in the PSI of red algae (Yoshida et al., 2003). Due to its lower redox potential, MK is a very good electron carrier for anaerobic RETC, facilitating electron transfer in Archaea, certain proteobacteria, Gram-positive bacteria, and green sulfur bacteria (Nowicka and Kruk, 2010). In addition to its role as an electron carrier, MK acts as a potent antioxidant, protecting cell membranes from lipid peroxidation and maintaining membrane integrity (Walther et al., 2013). Another derivative of MK, known as chlorobiumquinone, is found in green sulfur bacteria. In these organisms, chlorobiumquinone functions as a dedicated electron carrier within the RETC to drive ATP synthesis (Frigaard et al., 1997).

2.3 Biological derivatives of anthraquinones (AQs)

Anthraquinones (AQs) are tricyclic aromatic compounds derived from anthracene, characterized by ketone substitutions at the 9 and 10 positions (Malik and Müller, 2016). Substitutions particularly at the 1 and 8 positions on the outer rings primarily dictate the solubility, color intensity, and bioactivity of AQs (Chien et al., 2015; Fouillaud et al., 2016; Zhao and Zheng, 2023). Unlike the primary electron-carrying quinones, AQs function predominantly as secondary metabolites with potent antioxidant, anti-inflammatory, and antimicrobial properties (Wang et al., 2024; Sydiskis et al., 1991). AQs are widely distributed across diverse taxa, including bacteria, fungi, algae, lichen, plants, and insects (Wang et al., 2024). In fungi, these compounds are localized in conidia, spores and mycelia, where they contribute to pigmentation, chemical defence, and interspecific interactions (Fouillaud et al., 2016; Masi and Evidente, 2020; Wang et al., 2025).

Within plants, AQs accumulate in various tissues, including roots, rhizomes, bark, fruits, leaves, and flowers. While they do not participate directly in photosynthetic electron transport, AQs provide essential photoprotection against UV radiation and mediate ecological interactions by deterring herbivores and inhibiting pathogen invasion (Nagaoka et al., 2011; DeLiberto and Werner, 2016). Common natural AQs such as emodin, physcion, alizarin, chrysophanol, rhein, quinizarin, and purpurin, exhibit distinct bioactivities based on their specific hydroxylation and methylation patterns (Mueller et al., 1999).

3 Evolution and experimental analogs of quinones

The redox potential of quinones is a variable factor determined by both their chemical structure and biological environment. Consequently, structural variation in quinones derivatives along with interactions with proteins, solvents, membrane lipids, hydrogen bonding, and electrostatic environments can substantially alter their redox potential (Prince et al., 2022; Kato and Noguchi, 2021). As mentioned above, the distribution of quinones across different taxonomic groups reflects evolutionary hierarchies and selection pressure driven by the reducing and oxidizing environmental conditions of primitive and present-day Earth, respectively (Figure 3). Because photosynthesis and respiration, the fundamental processes of biological systems, are redox reactions, the selection pressure for redox-active molecules drove the evolution of BQ and NQ (Elling et al., 2025; Chobert et al., 2025).

MK serves as a common electron carrier that functions not only in anaerobic RETC but also as a central electron carrier in the photochemical reaction centers of heliobacteria (Sattley et al., 2008; Kondo et al., 2015). Therefore, MK may represent a key evolutionary bridge between these two fundamental bioenergetics processes. It is plausible that Earth’s highly reducing primitive environment favored low-potential electron carriers such as MK, which is exclusively found in the low-potential terminal respiratory system (anaerobic RETC) of numerous bacteria (Figure 3). In contrast, the scattered distribution of RQ across eukaryotes and prokaryotes, which does not follow a strict evolutionary trend, suggests a cellular survival strategy and lineage-specific adaptation to low redox-potential environments.

Conversely, the oxygenation of Earth due to the GOE created a bioenergetic niche for high-potential electron acceptors such as oxygen (Elling et al., 2025; Chobert et al., 2025). It can also be hypothesized that the GOE favored the loss of function in RQ biosynthesis, leaving UQ as the primary electron carrier of the RETC, given that RQ is synthesized from UQ in the Rhodospirillum rubrum (Brajcich et al., 2010). Therefore, change in Earth’s redox environment might have triggered a selection pressure on cells to phase out low-potential electron carriers. The high redox potential of UQ enables efficient oxygen reduction, leading to the evolution of aerobic RET and modern aerobes (Elling et al., 2025). Similarly, the evolution of oxygenic photosynthesis favored PQ as a mobile electron carrier between PSII and the cytochrome b ₆ f (Cyt b _*6* f) complex, and PhQ, a NQ, as a tightly bound electron carrier in the PSI reaction center, highlighting an evolutionary adaptation.

Overall, irrespective of BQ and NQ, the prevailing redox status of Earth acted as a selection pressure that drove the diversification of quinones. Thus, the specific redox potential of BQs and NQs is a combined effect of the cell’s external and internal environment. Despite such chemical diversifications, protein architectures remain remarkably flexible, capable of binding various structural analogs. Synthetic compounds such as 2,5-dibromo-3-methyl-6-isopropylbenzoquinone (DBMIB) and the dinitrophenyl ether of iodonitrothymol (DNP-INT) have been widely used to probe quinone/quinol oxidation at the Q_p site of Cyt b _*6* f complex (Roberts and Kramer, 2001; Vilyanen et al., 2022). Meanwhile, dichlorophenolindophenol (DCPIP) is commonly used as an artificial electron acceptor in spectrophotometric assays of complex I in the RETC and PSII in PETC (Weinrich et al., 2019; Chernev et al., 2020).

4 Regulation of PQ redox poise via thylakoid electron transport

PQ serves as a primary and central electron acceptor for all redox reactions within the thylakoid membrane. Therefore, the redox poise of PQ is dynamically regulated under light and dark conditions via photochemical and non-photochemical processes (Kodru et al., 2021; Munekage et al., 2002; Satoh et al., 2025; Peltier and Cournac, 2002; Bennoun, 1982; Dijkman and Kroon, 2002). This suggests that first line of defense mechanism protecting the photosynthetic machinery against environmental stress is governed by electronic shuffling via oxidation and reduction of PQ pool (Figure 4). Here, the thylakoid membrane acts as a functional hub for protein complexes that maintain efficient photochemistry through linear electron flow (LEF, or the Z-scheme) and cyclic electron flow (CEF) (Heldt et al., 1973; Myers, 1974; Tiwari et al., 2025), as well as respiration and chlororespiration (Peltier and Cournac, 2002; Bennoun, 1982; Dijkman and Kroon, 2002; Hart et al., 2005; Molitor and Peschek, 1986).

4.1 Linear electron flow (LEF) and cyclic electron flow (CEF)

In the context of the Z-scheme and cyclic electron transport (CET), the PQ-pool functions as a dynamic electron reservoir, accepting electrons from photosystem II (PSII) and PSI, respectively (Alric, 2015; Tiwari et al., 2025). In LEF, four major complexes (PSII, Cyt b _*6* f complex, PSI, and ATP synthase) work in series (Figure 4). Upon excitation, PSII transfer electrons to the Cyt b _*6* f complex via the PQ-pool, which acts as a mobile and stable redox mediator. The f subunit of Cyt b _*6* f complex facilitates electron transfer to plastocyanin (Pc) or cytochrome c _*6* (Cyt c _*6*, cyanobacteria and some algal species), while the b _*6* subunit participates in the Q-cycle, recirculating electrons back to the PQ-pool. Pc/Cyt c _*6* then transfer electrons to PSI, which further transfer electrons to ferredoxin (Fd) and ultimately used by ferredoxin-dependent NADP⁺ reductase (FNR) enzyme to reduce NADP⁺. The concomitant oxidation of water and transmembrane electron flux create a proton motive force that drives ATP synthesis by the activity of ATP synthase (Amesz, 1973; Mitchell, 1976; Hill and Bendall, 1960; Torrado et al., 2019; Tiwari et al., 2025).

Conversely, CEF involves only PSI, the Cyt b _*6* f complex, and ATP synthase (Myers, 1974; Cleland and Bendall, 1992; Tiwari et al., 2025). In plants and algae, electrons from PSI are transferred to Ferredoxin (Fd) and recycled back to the Cyt b _*6* f complex via two distinct pathways designated as CET1 and CET2 (Zhang et al., 2023; Malone et al., 2021). CET1 represents PGR5/PGRL1-dependent CEF, whereas CET2 is driven by NDH-1 (in streptophytes) or Nda2 (in most green algae), both of which divert electrons from Fd to reduce the PQ pool (Figure 4A). In cyanobacteria (Figure 4B), either NDH-1 or PGR-5/PGRL1-like proteins similarly capture electrons from Fd and transfer them to the Cyt b _*6* f complex via PQ pool reduction rather than utilizing them for NADP⁺ reduction (Ohnishi et al., 2023; Myers, 1974; Cleland and Bendall, 1992; Shikanai et al., 2025; Tiwari et al., 2025; Maekawa et al., 2024; Milrad et al., 2024). However, despite the fact that PGR5 reduces the PQ pool, direct evidence for this mechanism remains an open question. As a vital photoprotective mechanism, CET is employed by all oxygenic photoautotrophs under environmental stress conditions to regulate the redox poise of the PQ pool and prevent the generation of reactive oxygen species (ROS) (Khan et al., 2025). Notably, PQ and Pc serve as mobile carriers shared between linear and cyclic pathways, playing a pivotal role in balancing the ATP/NADPH ratio required for downstream metabolic processes (Kodru et al., 2021; Munekage et al., 2002; Satoh et al., 2025).

4.2 Respiration/chlororespiration in cyanobacteria/plants

Since the cyanobacterial thylakoid membrane is a shared site for both respiration and photosynthesis, the redox state of the PQ pool can become oxidized or reduced (Figure 4B). In the dark, the succinate dehydrogenase (SDH) oxidizes succinate to fumarate and leads to reduction of PQ. Reduced PQ (PQH₂) diffuses through the thylakoid membrane to transfer electron to the Cyt b ₆ f complex. From there, electrons are passed via Pc or cytochrome c _*6* to terminal oxidases, cytochrome c oxidase (Cox), to reduce O₂ (Hart et al., 2005; Molitor and Peschek, 1986). Alternatively, cytochrome bd quinol oxidase (Cyd) accepts electrons directly from the PQ pool, completely bypassing the Cyt b ₆ f complex and soluble luminal carriers and donate electrons to O₂ (Wey et al., 2026). Similarly, in the chloroplast of higher plants and algae, the chlororespiration maintain PQ redox status under dark and electronic stress. However, the chloroplast possesses plastid terminal oxidase (PTOX) instead of cox and cyd to reduce oxygen (Figure 4A). Mechanistically, the NDH-1 or Nda-2 transfer electron to PQ, a central pool transferring electron to PTOX and produce water via reducing O₂ (Peltier and Cournac, 2002; Bennoun, 1982; Dijkman and Kroon, 2002; Nawrocki et al., 2015). If PTOX is absent or inactive, PQH₂ naturally feeds into the Cyt b ₆ f complex. Additionally, PTOX is a structural and evolutionary homolog (di-iron carboxylate protein) of the mitochondrial alternative oxidase (AOX), whereas cyd represents a non-homologous bacterial quinol oxidase containing distinct heme cofactors (Wang et al., 2021; Friedrich et al., 2022).

5 Structural and functional involvement of Cyt b _*6* f in PETC

The Rieske/cytochrome b type complexes are a class of enzymes that belongs to “Rieske proteins” superfamily broadly distributed in RETC and PETC of eukaryotes and prokaryotes (Schmidt and Shaw, 2001). The members of this class contain an iron-sulfur protein (ISP) that coordinates 2Fe-2S cluster via two histidine and two cysteine residues located within a conserved sequences known as the Rieske motif (Schmidt and Shaw, 2001). Also, the enzymes of this class function as proton-translocating quinol oxidases that facilitate ATP generation via Q-cycle. The Cyt bc ₁/Cyt bc complex and the Cyt b ₆ f complex are the most extensively studied enzymes in this class. The Cyt bc ₁ complex and Cyt bc complex confined to RETC of eukaryotes and anoxygenic purple bacteria, respectively, while Cyt b ₆ f is limited to PETC in oxygenic photoautotrophs (Schmidt and Shaw, 2001; Xiong and Bauer, 2002; Schütz et al., 2000; Baymann et al., 2012).

The Cyt b _*6* f is a ∼220 KDa dimeric complex; monomer contain four major subunits: Cyt f (Pet A), Cyt b _*6* (Pet B), Rieske iron-sulfur protein (Pet C), and subunit IV (Pet D), along with four minor subunits (Pet G, L, M, N). The Cyt b _*6* core contain cofactors directly involved in the Q-cycle, binding b-type hemes (b _p and b _n) as well as c-type heme (c _n). Both Cyt f and iron-sulfur protein of Cyt b _*6* f complex project into the thylakoid lumen (p-side). Similar to Cyt bc _*1*, Cyt f binds c-type heme (heme f), whereas the iron-sulfur protein binds a 2Fe-2S cluster. Cyt f and Cyt c ₁ are analogs, serving as a classic example of a convergent evolution. Additionally, subunit IV of cyt b ₆ f contains chlorophyll a and 9-cis beta-carotene molecule (Malone et al., 2021), the specific functions of which remain unclear.

Figure 5 illustrates the sequential oxidation of PQH₂ within the Cyt b ₆ f complex via the Q-cycle. The Cyt b ₆ f complex contains two sites: Q_p on the luminal side and Q_n on the stromal side of the thylakoid membrane. These distantly located sites are functionally bridged by redox cofactors organized into two distinct pathways: a low-potential chain comprising hemes (b _p, b _n, and c _n), and a high-potential chain comprising a 2Fe-2S cluster and the c-type heme cyt f (Malone et al., 2021). The Q_p site serves as a branch point connecting these two pathways, linking to Q_n through the low-potential chain and to Pc via high potential chain. Oxidation of PQH₂ at Q_p site, transfers one electron to Pc by way of 2Fe-2S cluster and Cyt f, and a second electron to PQ at Q_n site using b_p and b_n/c_n heme pair (Figure 5). Through this bifurcation reaction the oxidation of a PQH₂ molecule transfers single electron to PQ at Q_n site, maximizing proton translocation into the lumen (Tikhonov, 2014; Cape et al., 2006; Pintscher et al., 2024; Malone et al., 2021).

The acidic pH of thylakoid lumen disables PQH₂ oxidation at Cyt b _*6* f which is a rate-limiting step of the PETC, also known as “photosynthetic control” (Tikhonov and Vershubskii, 2014; Tikhonov, 2014; Rumberg and Siggel, 1969; Tikhonov, 2013; Vilyanen et al., 2022). Therefore, PQ/PQH₂ ratio strongly regulates both LEF and CEF, and state transitions in cyanobacteria and planta (Ivanov et al., 2008; Zito et al., 1999; Laisk et al., 2005). Furthermore, the PQ-pool is a critical determinant of PSII stability; by facilitating the oxidation of reduced PQ, i.e., PQH₂, it alleviates excitation pressure on PSII, preventing over-reduction and subsequent photodamage (Ivanov et al., 2008). Therefore, the Cyt b _*6* f complex serve as a redox sensing hub controlling various physiological processes across plants, algae, and cyanobacteria.

6 Plastoquinone as a redox sensor of light stress

The conserved function of PQ in the PETC of oxygenic photoautotrophs suggests its ancient existence in ancestral cyanobacterial cells that drove the GOE. Furthermore, the retention of PQ exclusively in oxygenic photoautotrophs highlights the physiological integration of LEF and CEF in these organisms. In addition to standard PETC electron carriers, cyanobacteria, algae, and plants utilize alternative redox-active molecules such as Cox, Cyd, and PTOX, as mentioned above, to regulate the redox status of the PQ pool under various stress conditions (Peltier and Cournac, 2002; Bennoun, 1982; Dijkman and Kroon, 2002; Nawrocki et al., 2015; Wey et al., 2026). Because cyanobacteria are the evolutionary ancestors of chloroplasts (Stadnichuk and Kusnetsov, 2021), the physiological responses to changes in the redox status of the PQ pool are comparable between the two systems. However, the structural and functional regulation of these responses is considerably more complex in higher plants and algae than in cyanobacteria.

Unlike cyanobacteria and glaucophytes, the PSII and PSI of planta, except red algae are spatially distributed in stacked (grana) and unstacked (stromal lamellae and grana margin) region of thylakoid membrane, respectively. The stacking of thylakoid membrane avoids spillover of excitation energy between PSII and PSI in higher plants and algae (Kirchhoff et al., 2004). This placement tightly regulates the sublocalization of Cytb ₆ f complex (Kirchhoff et al., 2017; Anderson, 1992; Milrad et al., 2024). The functional role of Cyt b ₆ f complex and its interaction with photosystems is highly dependent on its sublocalization in the thylakoid membrane (Kirchhoff et al., 2017; Anderson, 1992). The processes like CEF and state transitions are largely dependent on the diffusion of the Cyt b ₆ f complex. This dependence is due to the fact that mobile electron carrier PQ diffuses only within a restricted range, while Pc mobility is physically hindered by the luminal protrusion of thylakoid-embedded protein complexes (Höhner et al., 2020; Kirchhoff et al., 2017).

The granal regions contain fewer Cyt b ₆ f complexes, accompanied by a narrow stromal space between the grana membranes (Mohamed et al., 2026). This spatial restriction can hinder the mobility of Cyt b _*6* f complex, which is crucial for balancing excitation energy distribution between PSII and PSI, given that the redox status of the complex governs LHCII phosphorylation (Kirchhoff et al., 2017; Longoni and Goldschmidt-Clermont, 2021). Conversely, phycobilisomes-containing organisms exhibit a homogenous distribution of the Cyt b ₆ f complex (Milrad et al., 2024; Perez-Boerema et al., 2024), thereby diminishing the complexity of short-term regulatory responses.

In photoautotrophs, light becomes a major source of ROS when excitation exceeds the capacity of the photosynthetic machinery during photochemistry. Under these conditions, the redox state of PQ-pool shifts toward an over-reduced or over-oxidized state, effectively serving as a central redox sensor for environmental light levels (Ritter et al., 2020). The redox status of the PQ-pool acts as a primary sensor for fluctuating light conditions, a function critical for the survival of plants, algae and cyanobacteria in unstable light environment. The dynamic shifts between oxidized (PQ) and reduced (PQH₂) states trigger a hierarchical regulatory network, encompassing short-term and long-term physiological responses in plants and cyanobacteria. Below, we first review the physiological roles of PQ in cyanobacteria followed by its function under dynamic light conditions.

6.1 PQ signaling in cyanobacteria

In a cyanobacterial cell, light-harvesting is uniquely governed by a specialized group of proteins, including orange carotenoids protein (OCP), iron-starvation induced protein A (IsiA), high-light inducible proteins (HliPs), and β-carotene. These proteins mediate non-photochemical quenching and structural reorganization that ensure the efficient operation of photosystems under fluctuating light. These structural proteins ensure the photoprotection of photosystems from high irradiance (Tiwari et al., 2025 and references therein). In addition to these photoprotective modulators, various membrane-bound proteins regulate the electronic pressure of PQH₂ pool to prevent irreversible photodamage to PSII (Tiwari et al., 2025).

An over-reduced PQ-pool in cyanobacteria serves as a primary sensor for high-light stress, triggering the upregulation of carotenoids biosynthesis (Yu et al., 2025). Since cyanobacteria integrate all cellular processes, including respiration and photosynthesis, within a single prokaryotic cell, they conserve a significant amount of energy during signal transduction and accelerate cellular responses to fluctuating light environments. Consequently, in the fluctuating light conditions typical of large-scale industrial cultivation, cyanobacteria may exhibit superior resilience and efficiency compared to algae. The following section outlines the role of PQ in cyanobacteria, focusing on photoacclimation and the regulation of core cellular processes. We first discuss the responses that acclimatize the PETC to changing light regimes, followed by other functions of PQ beyond photosynthesis.

6.1.1 Short-term and long-term responses

The primary light-harvesting antenna complexes of PSII in cyanobacteria are phycobilisomes attached on thylakoid surface. The prolonged exposure of cyanobacteria to qualitative or quantitative light stress alters the redox potential of thylakoid membrane, triggering both short-term and long-term acclimatization responses (Ritter et al., 2020). Under dynamic light environment, changes in the redox status of the PQ pool dictate the movement and functional association of phycobilisomes with either PSII or PSI (Figure 6B), a process known as state transition (Murata, 2009). Several models have been proposed for cyanobacterial state transition under low-light conditions (Calzadilla and Kirilovsky, 2020; Tiwari et al., 2025).

The preferential absorption of red light by PBS and the subsequent excitation of PSII lead to the over-reduction of the PQ pool. To restore redox balance, PBSs functionally detach from PSII and associate with PSI to reallocate excitation energy (state 2 transition) (Murata, 2009). Conversely, blue light preferentially excite PSI, due to the presence of plant- and algae-like chlorophyll a and carotenoids-rich light-harvesting complex, leading to the oxidation of the PQ pool. This redox cue signals PBSs to migrate back from PSI to PSII (state 1 transition). In addition to light-driven excitation, the non-photochemical reduction of the PQ pool by RET in the dark can also induce a state 2 transition (Calzadilla and Kirilovsky, 2020; van Stokkum et al., 2025; Tiwari et al., 2025).

Global stress-responsive sensor kinases, such as Hik33 and Nbls, respond to redox state of PQ and play critical role in the long-term acclimation of cyanobacteria. Hik33 in Synechocystis sp. PCC 6803 and NblS in Synechococcus elongatus PCC 7942 regulate the expression of high-light responsive genes, including hliA, hliB, rpoD3, and nblA (Rachedi et al., 2020). Hik33 dynamically controls the expression of photosynthesis-related genes by modulating the phosphorylation state of its response regulator, RpaB, under varying light conditions (Wilde and Hihara, 2016; Kadowaki et al., 2016; Rachedi et al., 2020).

Qualitative light stress triggers long-term responses involving change in photosystems stoichiometry and phycobilisome attachment. For example, in blue-light acclimated cells, preferential excitation of PSI leads to PQ pool oxidation. Oxidized PQ pool acts as a signal to upregulate PSII stoichiometry in Synechocystis sp. PCC 6803 (Luimstra et al., 2018; Luimstra et al., 2020). Similarly, in S. elongatus PCC 7942, prolonged exposure to blue light and the consequent oxidized PQ state is associated with thylakoid stacking, increased lipid content, and decoupling of phycobilisomes (Maurya et al., 2023).

6.1.2 PQ inhibits synthesis of chlorophyll under high light

Under high irradiance, excited chlorophyll molecules act as a potent electron donor to both the PQ-pool and molecular oxygen (Krieger-Liszkay and Shimakawa, 2022; Kozuleva and Ivanov, 2023). Failure to dissipate the excitation energy leads to the formation of ROS, including singlet oxygen (¹O₂), superoxide (O₂ ^¯), and peroxide (O₂ ^2¯), which cause excessive photodamage to the thylakoid membrane and compromise photosystem integrity (Krieger-Liszkay and Shimakawa, 2022; Kozuleva and Ivanov, 2023). To mitigate this, photoautotrophs utilize transcription factors that regulate chlorophyll biosynthesis to reduce the photodamage to photosystem (Moustaka and Moustakas, 2025).

While these regulatory circuits are well-characterized in plants, recent research has begun to bridge the knowledge gap in cyanobacteria (Yu et al., 2025; Yu et al., 2026). A key mediator identified in this process is RppA (regulator of photosynthesis and photopigment-related gene expression A), a response regulator within the OmpR subfamily (Li and Sherman, 2000). The transcription factor RppA, part of a conserved two-component signaling system, senses the redox poise of the PQ-pool to modulate the synthesis of photosynthetic pigments (Figure 6A), including phycobiliproteins, chlorophyll, and carotenoids, during high-light stress and dark-to-light transitions (Calzadilla and Unrein, 2025; Li and Sherman, 2000; Yu et al., 2025).

Specifically, RppA regulates the expression of chlorophyll synthase gene (chlG) and the magnesium chelatase H subunit (chlH). Under high-light conditions, RppA inhibits the transcription of chlG and chlH genes to stall chlorophyll production, preventing the accumulation of free chlorophyll molecules that could otherwise generate harmful ROS. Concurrently, RppA upregulates genes associated with PSI to enhance electron sink capacity (Yu et al., 2025). This coordinated response ensures a tight coupling between pigment biosynthesis and photosystem assembly, prioritizing photoprotection over maximum light absorption during environmental fluctuation.

6.1.3 Circadian rhythm in cyanobacteria: The PQ-pool as a redox environment signal

The circadian clock or biological clock is an endogenous ∼24 h biological oscillator that governs physiological processes, ensuring they persist even in the absence of external environmental cues (Cohen and Golden, 2015; Fang et al., 2025). This internal timing system allows organisms to anticipate daily environmental shifts and optimize cellular processes by triggering specific biological processes at the appropriate time. A functional circadian system comprises three integrated nodes: input pathways (entrainment), a central oscillator (timekeeping), and output signaling (Fang et al., 2023; Fang et al., 2025).

In cyanobacteria, the entrainment process synchronizes the internal rhythm with the external environment through specialized input proteins. The heart of this system is the central oscillator, which in cyanobacteria consists of three core proteins: KaiA, KaiB, and KaiC (Kondo et al., 1993; Cohen and Golden, 2015; Ishiura et al., 1998). For comprehensive structural and temporal details of the KaiABC oscillator, we refer readers to earlier work (Cohen and Golden, 2015; Fang et al., 2025). Timekeeping is maintained by the rhythmic phosphorylation and deposphorylation of KaiC. Specifically, the sequential binding of KaiA facilitates KaiC phosphorylation, while KaiB binding promote deposphorylation of Kai C (Johnson et al., 2008; Fang et al., 2025). This autonomous cycle of phosphorylation and dephosphorylation occurs with an endogenous periodicity of approximately 24 h. To align this internal phase of oscillation with the solar day, the clock must be reset or entrained by external signals. In cyanobacteria, the redox status of the PQ-pool serves as a primary input signal for this entrainment. By sensing the metabolic and energetic state of the cell, which fluctuates with light availability, the PQ-pool modulates the activity of input proteins such as CikA (circadian input kinase A) and KaiA to advance or delay the KaiABC oscillator (Johnson et al., 2008; Fang et al., 2025). This effectively reset the biological clock to match the prevailing light environment.

While eukaryotic circadian rhythms are primarily governed by transcription-translational feedback loop (TTFL), prokaryotes like cyanobacteria utilize a combination of a post translational oscillator (PTO) and a TTFL (Hurley et al., 2016). Although it was once hypothesized that the rapid division rates of prokaryotes precluded circadian rhythms, the discovery of a robust clock in cyanobacterium S. elongatus PCC 7942 established it as the premier prokaryotic model to study circadian rhythm (Johnson et al., 1996). In cyanobacteria, the entrainment and phase-shifting of this clock are strictly aligned with the cellular energy status, specifically the redox state of the PQ-pool and the ATP/ADP ratio (Kim et al., 2020a). The circadian signaling architecture is divided into two major sensory systems: one system detects external environmental signal (PQ and ATP/ADP ratio) to adjust the oscillator’s phase, while the second system translates the oscillator’s internal phase into global physiological outputs via a two-component relay system (Fang et al., 2023).

During dusk, the levels of oxidized PQ increase. Both KaiA and CikA possess pseudo-receiver domains that bind to oxidized PQ in the thylakoid membrane, triggering phase advances or delays, respectively (Figure 6C), to reset the endogenous oscillator (Kim et al., 2020b). Concurrently, a high ATP/ADP ratio drives the autokinase activity of KaiC, leading to phosphorylation at its threonine and serine residues. This process is further accelerated when KaiA binds to the A-loop of KaiC (Nishiwaki-Ohkawa et al., 2014; Swan et al., 2018). KaiC essentially function as a molecular machine with intrinsic kinase, phosphatase, and ATPase activities that fluctuate throughout the 24-h cycle (Egli, 2014).

The temporal state of KaiABC oscillator is communicated to the SasA (Synechococcus adaptive sensor A) histidine kinase and its cognate response regulator, RpaA (regulator of phycobilisomes association A) (Cohen and Golden, 2015; Fang et al., 2025). SasA interacts with KaiC via an N-terminal KaiB-like domain, phosphorylating RpaA to drive the rhythmic expression of genes involved in carbohydrate metabolism (Cohen and Golden, 2015; Markson et al., 2013). In the dark, the metamorphic protein KaiB undergoes a structural transition, allowing it to compete with SasA for the B-loop region of Kai C (Chang et al., 2015). This binding sequesters KaiA away from A-loop of Kai C, facilitating KaiC dephosphorylation throughout the night (Egli, 2014).

Simultaneously, CikA associates with the KaiBC complex, acting as a phosphatase to dephosphorylate the RpaA, altering its ability to control gene expression (Figure 6C) (Sancar and Golden, 2025). During the onset of day, the accumulation of reduced PQ inhibits KaiA binding, causing disassembly of the nighttime KaiABC complex (Fang et al., 2024). Recent findings indicate that this coordination between the PQ-pool and RpaA is also essential for the structural and functional regulation of carboxysome (Santos-Merino et al., 2025), linking the circadian clock directly to the efficiency of carbon fixation.

6.2 Functional role of PQ in higher plants and algae

Unlike cyanobacteria and algae, land plants are sessile and cannot employ phototactic movement to escape unfavorable light conditions. Therefore, plants have acquired sophisticated acclimation mechanisms to mitigate the effect of dynamic light environments. These responses are either triggered directly by photosensor proteins (Yadukrishnan and Datta, 2021) or by metabolic signaling triggered by ROS (Kozuleva and Ivanov, 2023; Vetoshkina et al., 2024). Similar to its function in cyanobacteria, the potential roles of PQ in plants and algae are primarily associated with state transitions and adjustments of photosystems stoichiometry via chloroplast genome under dynamic light conditions. In addition, PQ also regulate light-harvesting complex of PSII (LHCII) through retrograde signaling in plants. However, more recent findings demonstrate that PQ also acts as a potent scavenger of singlet oxygen, protecting PSII functionality and preventing lipid peroxidation in the thylakoid membrane (Vetoshkina et al., 2024). Consequently, expanding the PQ pool size to enhance the photooxidative tolerance in plants became a major focus of photosynthetic research. In following sections, we review the physiological functions regulated by PQ in planta.

6.2.1 Short-term response

Unlike cyanobacteria, state transitions in plants are more complex because the light harvesting complex of PSII, i.e., LHCII, is embedded within the chloroplast thylakoid membrane (Longoni and Goldschmidt-Clermont, 2021). The PSII of higher plants contains monomeric light-harvesting chlorophyll a/b-binding proteins (Lhcb4, Lhcb5, and Lhcb6), and trimeric LHCII complexes composed of Lhcb1, Lhcb2, and Lhcb3 subunits, which reside in the grana stacks to capture light (Kouřil et al., 2012). In contrast, PSI consists of four monomeric subunits Lhca1-Lhca4 localized in the peripheral grana and stroma lamellae (Mazor et al., 2015; Busch and Hippler, 2011).

In the model green alga Chlamydomonas reinhardtii, the LHCII trimers comprise of eight distinct subunits (LHCBM1-LHCBM9, with LHCBM2 and LHCBM7 sharing an identical amino acid sequence) and LHCII monomers composed of only two monomeric subunits LHCB4 and LHCB5 (Minagawa and Takahashi, 2004). Furthermore, the algal PSI core associated with 10 LHCA subunits, including two LHCA1 subunits and single subunits of LHCA2-LHCA9 (Kubota-Kawai et al., 2019). Compared to higher plants, state transition in green algae involves detachment of both trimeric and monomeric LHCII subunits, making the transition more rigorous than in higher plants, where loosely bound LHCII migrates to form the PSI-LHCI-LHCII supercomplex (Delosme et al., 1996; Depège et al., 2003; Kargul et al., 2005).

Light conditions that preferentially excite PSII relative to PSI lead to greater reduction of the PQ pool. The resulting PQH₂ oxidation at the Q_o or Q_p site of the Cyt b _*6* f complex activates chloroplast thylakoid protein kinases (Figure 7A), specifically State Transition 7 kinase (STN7) in plants and its ortholog STT7 in green algae (Vener et al., 1997; Dumas et al., 2017; Shapiguzov et al., 2016; Longoni et al., 2019; Lemeille et al., 2010). The kinase activity of STN7/STT7 phosphorylates the LHCII of the PSII, promoting the redistribution of LHCII trimers from PSII to PSI. Meanwhile, State Transition 8 (STN8), a paralog of STN7 in plants, phosphorylates PSII core proteins to facilitate acclimation to rapid light variations. Green algae also possess a STN8-related kinase termed STT7-like 1 (STL1), although its precise functional role is not completely understood. Ultimately, displaced LHCII binds to PSI to form the PSI-LHCI-LHCII supercomplex (Longoni et al., 2015; Wu et al., 2023; Longoni and Goldschmidt-Clermont, 2021).

Conversely, the light conditions that favor PSI excitation lead to an oxidized PQ pool. Under these conditions, the phosphatase activity of Protein Phosphatase1/Thylakoid-Associated Phosphatase38 (PPH1/TAP38) and Photosystem II core Phosphatase (PBCP) dephosphorylate LHCII, and results in its detachment from PSI (Samol et al., 2012; Pribil et al., 2010; Shapiguzov et al., 2010). In C. reinhardtii, homologs of PPH1/TAP38, and PBCP play a crucial role in dephosphorylation of LHCII and detachment from PSI-LHCI-LHCII supercomplex (Cariti et al., 2020).

6.2.2 Mid-term response

Chloroplast contains its own genome, which encodes key proteins involved in the PETC. The regulation of chloroplast genes expression is classified as a mid-term response due to its rapid onset and sustained nature (Borisova-Mubarakshina et al., 2019). An example of this acclimation is the adjustment of photosystem stoichiometry, the relative ratio of PSII to PSI, in response to sustained alterations in the PQ/PQH₂ ratio (Pfannschmidt et al., 1999; Borisova-Mubarakshina et al., 2019). This stoichiometric tuning is mediated by chloroplast Sensor Kinase (CSK), a conserved redox sensor and bacterial-type two-component signaling protein that responds to changes in PQ redox status (Puthiyaveetil et al., 2008). In higher plants and eukaryotic algae, CSK phosphorylates Plastid Transcriptional Kinase (PTK), a eukaryotic serine/threonine kinase, and Chloroplast Sigma Factor 1 (SIG1) to regulate the expression of PSII and PSI reaction center genes (Figure 7B). For example, prolonged exposure to PSI-favored light oxidizes PQ pool, inducing phosphorylation of SIG1 and the subsequent repression of the genes coding for PSI reaction center proteins PsaA/PsaB (Shimizu et al., 2010; Macadlo et al., 2020; Puthiyaveetil et al., 2012; Baginsky et al., 1999).

6.2.3 Long-term response

Long-term exposure of plants and algae to high-light conditions induce adjustment of PSII antennae size via retrograde signaling (Figure 7). The first evidence of PQ-mediated chloroplast-to-nucleus retrograde signaling was observed in Dunaliella tertiolacta, where oxidation of the PQ pool upregulated the expression of nuclear gene Lhcb, whereas a reduced PQ pool repressed its expression (Escoubas et al., 1995). Despite such early finding, the actual mediator carrying signal from the chloroplast to the nucleus remained elusive until hydrogen peroxide (H₂O₂) was identified as a key signaling molecule (Borisova-Mubarakshina et al., 2015). Under high light conditions, a highly reduced PQ pool quench electron from singlet oxygen and convert it into H₂O₂. This H₂O₂ then diffuses out of the chloroplast into the nucleus (Figure 7), where it modulates the expression of Lhcb genes (Borisova-Mubarakshina, 2025; Borisova-Mubarakshina et al., 2015).

Additionally, PQ-mediated redox signaling can alter thylakoid membrane fluidity through retrograde signaling. In the marine diatom Phaeodactylum tricornutum, PQ-mediated retrograde signaling facilitates a unique photoprotective mechanism involving thylakoid remodeling. Under low-light conditions, signaling favors a decrease in lipid saturation, increasing membrane fluidity to facilitate rapid electron diffusion. Conversely, high-light stress induces an increase in lipid saturation, which restricts the mobility of electrons carriers (Cheong et al., 2022). This PQ-based change in fluidity reduces electronic load on the photosystems, providing an additional layer of protection against photo-oxidative damage in fluctuating marine light environments. Beyond its core function in PETC redox homeostasis, PQ also plays a vital antioxidative role as a scavenger of reactive oxygen species. This additional role of PQ is detailed in a subsequent section.

6.2.4 PQ as an antioxidant

High irradiance increases electronic load on the PETC, and hence, alternative electron transport pathways help to alleviate this electronic excitation pressure in plants (Havaux, 2020; Borisova-Mubarakshina et al., 2019). In addition to its role in PETC, PQ is a scavenger of singlet oxygen, and therefore, overproducing PQ can protect plants against photooxidative stress (Borisova-Mubarakshina et al., 2019; Vetoshkina et al., 2024). In higher plants and algae, the PQ-pool is not restricted to the thylakoid membranes; it also occupies extra-thylakoidal storage sites within the chloroplast envelope and plastoglobules (Figure 7), a lipoprotein particle surrounded by a membrane lipid monolayer (Havaux, 2020; van Wijk et al., 2017). Accordingly, cellular PQ can be distinguished into photoreducible (active in electron transport) and non-photoreducible (sequestered) fractions (Havaux, 2020). These extra-thylakoidal reservoirs are vital for managing photo-oxidative stress and functioning of PSII under high irradiance (Ksas et al., 2022). For comprehensive overview of PG-mediated pathways, including biosynthesis of tocopherol, carotenoids, abscisic acid, jasmonic acid, and gibberellic acid, we refer to van Wijk and Kessler (2017).

Overexpression of PQ-synthesizing gene SOLANESYL DIPHOSPHATE SYNTHASE1 (SPS1) improves plant fitness by increasing tolerance to photooxidative stress, decreasing lipid peroxidation, and mitigation of PSII photoinhibition under high light (Ksas et al., 2018). However, to replenish the reduced thylakoidal PQ pool, the ongoing transfer of oxidized PQ is essential to protect PSII from photodamage. Therefore, plastoglobule-localized kinases, specifically Activity of BC1 Complex kinase (ABC1K1) and ABC1K3 (Figure 7), facilitate this thylakoidal PQ redox homeostasis (Zhao et al., 2026; Pralon et al., 2020; Ksas et al., 2022). However, PQ redox homeostasis within plastoglobules is maintained by other prenyl groups, such as tocopherol and plastochromonol-8, synthesized by Vitamin E cyclase enzymes VTE3 and VTE1, respectively. Additionally, NADPH-dependent quinone oxidoreductase C1 (NDC-1) is required to maintain the overall size of the PQ pool (Eugeni Piller et al., 2011; Ksas et al., 2018; Podgórska et al., 2020).

The PQ redox homeostasis is also regulated by PTOX under different environmental stresses. PTOX is evolutionary and functionally related to mitochondrial AOX as both share common ancestry originating near the root of the eukaryotic photosynthetic lineage (McDonald and Vanlerberghe, 2006). PTOX is a non-heme di-iron quinol oxidase found in all oxygenic photoautotrophs. It was first identified in the IMMUTANS mutant of Arabidopsis and the GHOST mutant of tomato, both of which exhibit mottled phenotype (Carol et al., 1999; Barr et al., 2004). PTOX provide widespread photoprotection against oxidative stress in diverse plants and algae, including extremophiles. For example, under salt stress, the halophyte Eutrema salsugineum transfers up to 30% of its total PSII electron flux to O₂ via PTOX, whereas in the halotolerant alga Dunaliella salina, alternative oxidase helps in maintaining PQ redox poise under hyper saline conditions (Hüner et al., 2022; Calzadilla et al., 2024; Messant et al., 2021; Naydov et al., 2024; Bolte et al., 2020). Furthermore, in the psychrophilic alga Chlamydomonas priscuii, PTOX aids in reducing ROS accumulation under high irradiance (Hüner et al., 2022). Overall, PQ redox status is dynamically modulated not only under high light, but also during salt, temperature, and drought stress, highlighting its regulation by multiple electron transport components across the thylakoid membrane.

7 Biotechnological implications and future outlook

This comparative study of biological quinones reveals that despite structural variations, the fundamental role of these molecules, i.e., maintaining redox homeostasis, is strictly conserved across life forms. This conservation underscores their diverse applications, ranging from pharmaceutical development to industrial-scale bioenergy. In the context of photoautotrophs, the photoprotective role of PQ is a universal priority. Regardless of the physiological complexity found in land plants and algae, PQ acts as the primary safeguard for the thylakoid membrane, ensuring productive photosynthesis. In cyanobacteria, PQ emerges as a master regulator controlling global gene expression through the KaiABC post-translational oscillator. The elegance of this system, using only three core proteins and the redox state of the PQ-pool, demonstrates the evolutionary efficiency of prokaryotic cells in aligning their internal metabolic rhythms with the environmental clock. This targeted and rapid entrainment mechanism highlights the PQ-pool not just as a chemical intermediate, but as the essential pulse of the photosynthetic cell.

The redox state of the PQ-pool regulates both the circadian control of glycolysis (when oxidized) and carboxysome functionality (when reduced). This dual role suggests that precise light management can maximize glycogen accumulation to provide ideal substrates for biofuel production (Kim et al., 2012; Santos-Merino et al., 2025; Fan et al., 2021). Because KaiC phosphorylation is ATP-dependent, leveraging the relationship between light intensity and ATP synthesis can effectively shorten the cell’s perceived dark period. Minimizing dark period reduces the mobilization of stored carbon via glycolysis, thereby increasing total cellular carbon reserves. Also, truncating CEF under low-light conditions could theoretically extend the day length, prolonging glycogen synthesis while mitigating photo-oxidative damage and reducing nocturnal energy expenditure on photosynthetic repair. However, the systemic implications of these modifications on overall organismal fitness require further evaluation. While engineering circadian genes may be redundant in controlled indoor bioreactors that lack natural dawn/dusk cycles, such modifications could prove transformative for large-scale outdoor cultivation systems where natural light fluctuations typically compromise productivity.

The role of PQ as a stable electron acceptor and central metabolic sensor offers significant potential for enhancing sustainable energy and biomass production. By leveraging the redox properties of PQ-pool, next-generation biophotovoltaic (BPV) and optimized cultivation strategies could be developed. BPV technology has emerged as a promising sustainable approach for direct electricity generation. In BPV systems, power is produced through the interaction between photosynthetic microorganisms and external electron quenchers (Yuan et al., 2025). Currently, the photocurrent efficiency of BPV systems is approximately 1% which is considerably lower than conventional photovoltaics. However, performance could be significantly enhanced by pairing photosynthetic organisms with high PSII activity with efficient quenchers that specifically target the oxidation of PQH₂ (Yuan et al., 2025). Current research is focused on identifying quenchers capable of extracting electrons without compromising the organism’s photosynthetic efficiency or carbon storage capacity.

Generative AI statement

The author(s) declared that generative AI was not used in the creation of this manuscript.

Any alternative text (alt text) provided alongside figures in this article has been generated by Frontiers with the support of artificial intelligence and reasonable efforts have been made to ensure accuracy, including review by the authors wherever possible. If you identify any issues, please contact us.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Footnotes

Edited by: Francesco Francia, University of Bologna, Italy

Reviewed by: Maciej Z Garstka, University of Warsaw, Poland

Yuval Milrad, University of Münster, Germany