4.4 PSII stability and repair of PSII, qI
Under stress conditions, such as high light intensity or extreme
temperature, PSII is highly susceptible to photodamage of its core
proteins, specifically the D1 protein. This photodamage can lead to the
irreversible damage of PSII, which requires repair
(Andersson
& Aro 2004; Murata et al. 2007; Nawrocki et al. 2021a).
However, PSII function can be maintained through an intricate mechanism
involving the turnover and replacement of damaged D1 protein using an
elaborate PSII repair cycle
(Tikkanen,
Mekala & Aro 2014). Accordingly, when the rate of damage of D1 exceeds
the rate of repair of D1, this unbalance can ultimately lead to
photoinhibition.
Briefly, the PSII repair cycle begins with the monomerization and
detachment of the light-harvesting complex (LHCII) from the PSII core by
phosphorylation through STN8 (STN7) kinase. The monomerized PSII core
then migrates to the unstacked region of the thylakoid membrane, where
it is dephosphorylated by the phosphatase, PBCP. The damaged D1 subunit
is then degraded by the proteases Deg and FtsH. Once the damaged D1
subunit has been degraded, a new D1 subunit is synthesized and inserted
into the PSII core
(Kirchhoff
2014). Coincidently, the key proteases, Deg and FtsH, that are involved
in D1 protein turnover are reported to be redox-regulated during this
process.
By dynamic thiol-disulfide redox proteomics, Deg1 and Deg2 were found to
be redox regulated
(Ströher
& Dietz 2008). Deg1 is peripherally attached to the thylakoid lumenal
side
(Chassin,
Kapri-Pardes, Sinvany, Arad & Adam 2002) and is subsequently regulated
by both the proton gradient (∆pH) and redox state of the thylakoid
membrane
(Ströher
& Dietz 2008; Knopf & Adam 2018). The formation of Deg1 homo-hexamers
is dependent on ∆pH
(Knopf
& Adam 2018). Further, Deg1 showed maximal activity under reducing
conditions and less activity under mild oxidative stress conditions
(Ströher
& Dietz 2008). Although Deg1 has only one Cys residue in its mature
form (Table 1), the fact that it forms homo-hexamers and changes its
activity depending on oxidizing/reducing condition suggests that is
regulated by redox regulation upon formation of homo-hexamers, however
this possible unique regulation needs to be studied further. Conversely,
Deg2 is located in the stroma and has an opposite redox-dependent
mechanism, showing higher proteolytic activity under oxidizing
conditions
(Haussühl,
Andersson & Adamska 2001). Other interacting factors of Deg protease,
such as electron donors, and oxidizers have not yet been determined.
FtsH is an ATP-dependent zinc metalloprotease that exists as two types
of subunits: A (FtsH1 and FtsH5) and B (FtsH2 and FtsH8)
(Zaltsman,
Ori & Adam 2005; Kato & Sakamoto 2018). Both types have a similar
structure, with a C-terminal extension orientated towards the stroma and
an N-terminal transmembrane domain
(Lindahlet al. 1996). The C-terminal domain has ATP hydrolysis activity
and conserved cysteines
(Sauer
& Baker 2011; Wang et al. 2017b). FtsH cooperates with Deg
proteases to degrade the D1 protein in the PSII repair cycle. It has
been suggested that FtsH degrades D1 after it has been cleaved by
Deg-mediated proteolysis
(Nishimura,
Kato & Sakamoto 2016; Kato & Sakamoto 2018). FtsH is active under
reducing conditions, and it has been proposed that the possible electron
donors for FtsH are members of the stromal Trx family
(Wanget al. 2017b). However, the oxidant for FtsH remains unknown.
Given that photoinhibition decreases the efficiency of photosynthesis
and redox regulation directly affects protease activity and rate of
repair, further research will be needed to fully understand the role
that redox regulation has on these proteases.
Finally, besides proteases, PsbO, a subunit of the oxygen-evolving
complex (OEC), is also associated with PSII stability and repair. The
redox state of two cysteine residues in PsbO is the key determinant of
its stability
(Hallet al. 2010; Kieselbach 2013). The oxidized form of PsbO is
stable, while the reduced form is unstable and becomes a target for
proteolysis, leading to increased accessibility of PSII core proteins
for degradation. For example, when D1 in PSII is damaged, PsbO in its
stable oxidized form is less accessible to degradation, which further
inhibits the repair cycle. Therefore, the redox state of PsbO must be
tightly regulated. It has been shown that LTO1 oxidizes PsbO
(Karamokoet al. 2011), but the reducing pathway for PsbO remains to be
determined. PsbO was found to be a potential target of Trx
(Leeet al. 2004; Marchand, Le Maréchal, Meyer & Decottignies 2006;
Hall et al. 2010), but given the location of Trx and PsbO in the
stroma and lumen respectively, a mediator such as CcdA and HCF164 or
another unknown factor may be involved in the transfer of electrons to
PsbO (Fig. 4).