Abstract
Photosynthesis is the foundation of all life on Earth, providing oxygen
and energy. However, if not well regulated, it can also generate toxic
reactive oxygen species (ROS), which can cause photodamage. Regulation
of photosynthesis is highly dynamic, responding to both environmental
and metabolic cues, and occurs at many levels, from light capture to
energy storage and metabolic processes. One general mechanism of
regulation involves the reversible oxidation and reduction of protein
thiol groups, which can affect the activity of enzymes and the stability
of proteins. Such redox regulation has been well studied in stromal
enzymes, but more recently evidence has emerged of redox control of
thylakoid lumenal enzymes. This review/hypothesis paper summarizes the
latest research and discusses several open questions and challenges to
achieving effective redox control in the lumen, focusing on the distinct
environments and regulatory components of the thylakoid lumen, including
the need to transport electrons across the thylakoid membrane, the
effects of pH changes in the stromal and lumenal compartments, and the
observed differences in redox states. These constraints suggest that
activated oxygen species are likely to be major regulatory contributors
to lumenal thiol redox regulation, with key components and processes yet
to be discovered.
Keywords: Photosynthesis, redox regulation, thiol-disulfide redox
regulation, lumen, photoprotection, non-photochemical quenching (NPQ)
Introduction
Photosynthesis is a biological process that converts light energy into
chemical energy, which is then used to fix CO2 into
organic compounds. This process is essential for life on Earth, as it
provides the food and energy that all living things need. However, at
the same time, photosynthesis can be a dangerous process if it is not
finely tuned and regulated
(Kanazawa
et al. 2020; Kramer et al. 2004; Davis et al. 2017; Foyer 2018; Gururani
et al. 2015; Murata et al. 2007; Aro et al. 1993; Raven 2011). For
instance, the under stressful conditions, photosynthetic process can
generate reactive oxygen species (ROS) which can ultimately damage
numerous cellular components
(Asada
1996; Nishiyama, Allakhverdiev & Murata 2006; Nawrocki et al.2021b).
To avoid photodamage, photosynthetic organisms have evolved a
photoprotective mechanism, called non-photochemical quenching (NPQ)
(Demmig-Adams
& Adams 1996; Müller, Li & Niyogi 2001; Li et al. 2004). NPQ
itself is composed of several distinctive components. Each component is
defined by an underlying mechanism and rate of formation and relaxation
(Bellafiore,
Barneche, Peltier & Rochaix 2005). The most rapid responding form of
NPQ, is qE (energy-dependent of quenching) which is activated by
acidification of lumen (the ΔpH component of proton motive force
(pmf )) via protonation of photosystem II subunit S (PsbS)
(Liet al. 2004; Niyogi, Li, Rosenberg & Jung 2005) as well as
activation of violaxanthin de-epoxidase (VDE), which catalyzes the
conversion of violaxanthin (Vx) to antheraxanthin and then zeaxanthin
(Zx)
(Niyogi,
Grossman & Björkman 1998). There are additionally, more slowly
responding forms of NPQ, including sustained quenching (qH)
(Malnoëet al. 2018), photoinhibition (qI) which is related to the
photodamage of PSII centers and subsequent repair
(Andersson
& Aro 2004; Murata, Takahashi, Nishiyama & Allakhverdiev 2007;
Nawrocki, Liu, Raber, Hu & De Vitry 2021a), zeaxanthin-dependent
quenching (qZ) which involves the accumulation of Zx but not the PsbS
(Demmig-Adams
& Adams 1996; Müller et al. 2001; Li et al. 2004; Nilkenset al. 2010), and finally, qT, which involves antenna state
transitions (where LHCII migrates to PSI)
(Quick
& Stitt 1989). qZ, qH, qI and qT are likely to be too slow to respond
to rapid fluctuations in light but likely act as backup processes when
qE fails.
It is important to note that the processes listed above are involved in
balancing the tradeoffs between photoprotection and photosynthetic
efficiency
(Krameret al. 2004; Zhu, Long & Ort 2010; Kromdijk et al. 2016;
Davis et al. 2017; Kanazawa et al. 2020). For instance,
slow onset of photoprotection causes photodamage when light intensity
rapidly increases
(Krameret al. 2004; Davis et al. 2017; Kanazawa et al.2020), whereas slow recovery leads to losses of photosynthetic
efficiency when light intensity suddenly decreases
(Krameret al. 2004; Zhu et al. 2010; Kromdijk et al. 2016;
Davis et al. 2017; Kanazawa et al. 2020). Understanding
such “fine-tuning” mechanisms that are involved in maintaining energy
balance when plants are subjected to constantly changing environmental
conditions will be required if one wants to achieve more robust and
resilient photosynthesis, and thus, improve overall crop productivity.
So how do plants adjust to their constantly changing environmental
conditions such as light availability and quality? One approach involves
the regulation and/or fine-tuning of protein function using a
thiol-disulfide redox mechanism
(Buchanan
& Balmer 2005; Waszczak et al. 2015). In this approach, we can
exploit the fact that, under physiological conditions, pairs of the
amino acid cysteine (Cys), exist in two forms: when reduced, the Cys
residues will be in their (thiol, SH) forms, whereas when oxidized, may
form a disulfide (S-S) form, linked by a covalent bond
(Cremers
& Jakob 2013). In the chloroplast, thiol-disulfide reactions are
involved in numerous functions such as, in protein folding, in
regulating the activity of countless enzymes, and in ROS detoxification
(Buchanan
and Balmer 2005; Kieselbach 2013; Balsera and Buchanan 2019; Yoshida and
Hisabori 2016; Montrichard et al. 2009). These processes are mediated
by a complex network of redox-sensing and redox-regulated enzymes. The
reductive and oxidative activities of this intricate system are
essential for achieving regulatory redox balance.
While many questions still remain, this general scheme for stromal redox
control appears to explain much of the known data on regulation of
stromal enzymes as illustrated in Figure 1. In the light, electron flow
from photochemistry reduces regulatory thiols through the
ferredoxin/thioredoxin and NADPH-dependent thioredoxin reductase C
(NTRC) systems in the stroma. This activation or deactivation of key
enzymes is mediated by the redox state of the thiol groups. Meanwhile,
H2O2 reoxidizes the regulatory thiol
pools both in the light and dark
(Cejudo,
Ojeda, Delgado-Requerey, González & Pérez-Ruiz 2019).]
Recently, it has been recognized that reactions at the thylakoid
membrane and within the lumen are also redox-regulated. However, the
roles and mechanisms of these reactions are not well understood.
Several key proteins involved in photoprotection (e.g., violaxanthin
de-epoxidase (VDE)), partitioning of pmf into Δψ and ΔpH (the
H+/K+ antiporter KEA3), PSII
stability and repair (Deg1 and PsbO), state transition (STN7) have
redox-active thiol groups that are exposed to the thylakoid lumen
(Ströher
& Dietz 2008; Hall et al. 2010; Kieselbach 2013; Yu, Lu, Du,
Peng & Wang 2014; Simionato et al. 2015; Hallin, Guo & Åkerlund
2015; Wang et al. 2017a; Wu et al. 2021). These thiol
groups can undergo redox transitions, meaning that they can be oxidized
or reduced. Interestingly, while the reduction of regulatory thiols in
the stroma tends to activate enzymes involved in photosynthesis, the
opposite seems to be true for lumenal proteins (e.g., VDE)
(Yuet al. 2014; Simionato et al. 2015; Hallin et al.2015). This suggests that oxidative reactions may be critical for
adjusting the activities of lumenal proteins and preventing the buildup
of damaged PSII centers.
This review will discuss the possible important role(s) of redox
regulation in photoprotection in preventing plants from photodamage,
focusing on redox-regulated proteins in the thylakoid lumen, which is a
unique environment with different properties than the stroma. Also, we
will discuss the challenges of achieving redox regulation in the lumen
and point out that it involves a distinct mode of regulation that links
redox changes, reactive oxygen species generation, and stress responses.