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.