5. What are the missing pieces in the lumen
thiol-disulfide regulation mechanism?
So far, we have discussed the redox regulation from the stroma to the
transmembrane region to the lumen and its photoprotective roles. The
molecular players in the redox regulation and relevant photoprotective
forms are summarized in Figure 5. In brief, reducing equivalents from
the stroma are transferred through CcdA and HCF164 to VDE and STN7.
These proteins are inactive in their reduced forms, as indicated by the
arrows pointing in the opposite direction (-). Another reducing
mediator, SOQ1, transfers reducing power to LCNP, which is inactivated
in its reduced form. The electron donors for KEA3-1, PsbO, and Deg1 are
still unknown, as indicated by the dashed arrows. The oxidizing system
appears to be mediated by LTO1. LTO pulls electrons from VDE, STN7, and
PsbO. The oxidizing mediators for KEA3-1, Deg1, and LCNP are not known.
All of the redox-regulated proteins in the lumen, including VDE (qE,
qZ), KEA3 (pmf partitioning into ∆ψ and ∆pH and effects on qE),
STN7 (qT), LNCP (qH), Deg1, and PsbO (qI), orchestrate photoprotective
mechanisms.
However, as seen in Figure 5, many of the pathways in lumenal redox
regulation are still hypothetical (so many dashed lines!). Certainly, we
have just begun to scratch the surface of this complex lumenal redox
regulation network. While there are many unanswered questions regarding
this complex redox network, there are two significant yet unresolved
questions we would like to focus on:
How do electrons get out of the lumen? Recall that LTO1 may be
involved in numerous oxidizing events but the final acceptor of LTO1
has not been identified (See Figure 5).
What keeps fine-tuning redox potentials and kinetics to achieve the
appropriate regulatory levels in the “acidic lumen?” As we discussed
in section 3.2, due to the ∆pH component of pmf , the lumen has
quite a unique redox environment, where the redox midpoint potentials
of the regulatory thiols substantially increase upon illumination (See
Figure 4).
One hypothetical model that could answer both of these questions is that
reactive oxygen species (ROS) act as a strong oxidant. It has been shown
that in the stroma, the 2CP-mediated oxidation system pulls electrons
from target enzymes and transfers them to the final acceptor hydrogen
peroxide (H2O2), which is then reduced
to water. In the hypothetical model for lumenal redox regulation, the
Trx-domain of LTO1 would pull electrons from target enzymes, and these
electrons would then be transferred to the VKOR domain of LTO1 in the
thylakoid membrane. From there, the electrons could be transferred to an
unknown oxidizing mediator (marked as ”?” in the figure), which could
further reduce H2O2. Another possibility
is that there is another oxidoreductase in the thylakoid membrane that
uses H2O2 as a final electron acceptor.
This hypothesis is supported by the results of state transition
experiments in the lto1 mutant, which showed that state
transitions were not completely abolished in this mutant (Wu et al
2021). This result strongly suggests that other factors are also
involved in keeping STN7 oxidized and active. The other possible strong
oxidants could be plastoquinone (PQ) pool. More research will be needed
to determine the exact mechanisms involved.