4.4 TRX’s Impact on Plasmodesmata: Dependent on or Independent
of SA
The effects of cytosolic TRX on increasing NPR1 monomerization, thereby
bolstering the SA-mediated antiviral defenses, are potentially
intertwined with the established roles of SA in reducing PD
permeability. However, it is worth noting that regardless of their
subcellular locations, impairing or silencing most of the TRXs leads to
increased PD-mediated intercellular trafficking. This is likely due to
the disruption of the redox balance and an increase in ROS, suggesting
that the TRX-mediated rise in SA levels and the expression of SA-related
genes might not signify heightened resistance to viral threats. Instead,
it appears to be a consequence of the fine-tuned equilibrium between
cellular defense mechanisms and intracellular mobility via PD (Fig. 1).
The established role of SA in regulating callose deposition at PD, which
in turn reduces PD permeability (Wang et al., 2013; Huang et al., 2020),
along with ROS’s function in reducing intercellular trafficking by
limiting PD permeability (Rutschow et al., 2011), highlights a crucial
point. It is interesting to note that ROS-induced decreases in PD
permeability remain consistent, irrespective of the subcellular origin
of the ROS (plasma membrane, cytoplasm, or chloroplasts). This
collective evidence suggests that the influence of ROS on PD
permeability can in some cases be distinguished from that of the SA
pathway. This is in harmony with the findings of Cui and Lee, where
exogenous application of H2O2 decreased
PD permeability in SA-mutants and independent of the SA-regulated PDLP5,
indicating that there are pathways in which ROS can induce callose at PD
independent of SA (Cui and Lee, 2016). Nevertheless, the outcome of
virus-redox interactions cannot be generalized and depends on the
organelles where a virus influences ROS production to create an
environment favoring accumulation and spread (Table 1).
Resistant soybean plants demonstrated a robust upregulation of
photosynthesis-related genes in response to soybean mosaic virus (SMV)
infection. Upon close examination of two specific genes, namely, the
photosystem I (PSI) subunit PSaC and the ATP synthase subunit α
(ATPsyn-α ), it was observed that their overexpression within the
SMV genome in a susceptible soybean cultivar resulted in a reduction in
SMV accumulation in the inoculated leaves. This was coupled with an
increase in the expression of genes associated with the antiviral RNA
silencing pathway and defense hormone signaling pathways such as SA and
ABA (Bwalya et al., 2022). Interestingly, the C-termini of these two
proteins physically interacted with NIb and NIa-Pro proteins encoded in
the SMV genome. When SMV chimeras expressing these C-termini infected
susceptible soybean plants, the ability of SMV to accumulate locally and
spread systemically was diminished (Bwalya et al., 2023). Importantly,
the overexpression of these two genes did not lead to an increase in ROS
production in soybean leaves. However, given the documented roles of ABA
and SA in controlling PD permeability (Alazem, 2017), it can be inferred
that the elevated expression of these photosynthesis genes, as well as
the ABA and SA genes, impeded aspects of cell-to-cell movement, likely
contributing to the limited accumulation of SMV in the inoculated
leaves.
Conclusions
Recent years have heralded important advances in understanding the roles
of ROS and redox signaling in regulating intercellular trafficking via
PD. Yet, many crucial unknowns still exist. How organelle redox state is
‘communicated’ to PD remains an open question. Current data suggests
that other signals besides ROS may be involved and so the role of TRX
and other redox systems should be examined. Further, how light affects
PD and intercellular trafficking remains mysterious. Given the critical
importance of light quantity, quality, and duration to plant
development, one can expect that plants would integrate these parameters
to optimize not only PD function in trafficking metabolites and signals
but also the formation and structure of the PD themselves. The
interference of viruses with the mechanisms controlling PD permeability
such as ROS and redox remains a complex area. Beyond the TRXs discussed
here, other ROS and redox regulators are also implicated in viral
infection, although there is room for more exploration. Therefore, using
viruses as a tool to understand factors and mechanisms that control PD
function could unveil crucial insights into unexplored facets of PD
biology, and can help shed the light on the molecular dynamics governing
viral spread within plants.