4. Roles of redox in virus cell-to-cell movement
Viruses are obligate intercellular pathogens and in plant cells they are restricted to the symplast form by PD connecting host cells. Most plant viruses typically use the phloem for systemic transport, except for a few that can enter the xylem (Kappagantu et al., 2020, Sun et al., 2022). Plant viruses can modulate ROS production and scavenging by targeting enzymes crucial for maintaining redox balance, such as TRXs. TRXs belong to a family of small, highly conserved proteins found in plants and other organisms. Serving as thiol-disulfide oxidoreductases, they play a significant role in plants’ antioxidant defense system, contributing to protection against oxidative stress. Typically, they have a positive role in reducing ROS and maintaining cellular redox balance (Sevilla et al., 2015; Mata-Perez and Spoel, 2019). Since most studies report on the roles of TRX in ROS/redox processes related to infection, TRXs will be the focus of this discussion.
Specific members of Trx possess the ability to move from cell to cell and regulate PD permeability. For example, the rice thioredoxin h protein, RPP13-1, can translocate from the initially injected cell into surrounding cells, resulting in an increase in the plasmodesmal permeability (Ishiwatari et al., 1998). In Arabidopsis, when AtTrxh9 is controlled by the tissue-specific promoter SCARECROW (pSCR), which specifically directs downstream gene expression in the single endodermal cell layer of the root, AtTRXh9 migrated from its initial expression site in endodermal cells to other cell layers of the root (Meng et al., 2009). These observations suggests a potential role in regulating PD permeability. It implies that Trx proteins can function as signaling molecules, enhancing intercellular communication by modifying PD-mediated intercellular trafficking.
Certain TRXs are actively involved in plant defense mechanisms against pathogens. They have the capacity to influence the activation of defense genes and the production of antimicrobial compounds in response to pathogen attacks (Mata-Perez and Spoel, 2019). In Arabidopsis, the cytosolic TRXhs AtTRXh3 and AtTRXh5 play critical roles in the salicylic acid (SA)-dependent defense pathway. Their roles revolve around the reduction of disulfide bonds in the NPR1 oligomer complex, thereby generating monomeric NPR1 proteins. These monomeric NPR1 proteins are subsequently translocated to the nucleus, where they function as transcription factors to activate SA-related defense genes [Fig. 1; (Tada et al., 2008; Liu et al., 2020)). A separate study has proposed an SA-independent role for NPR1 in which it exerts a negative influence on the activation of the adaptive unfolded protein response (UPR). This was observed when npr1 mutants displayed a significant increase in UPR marker genes (Lai et al., 2018). Additionally, it is worth noting that a reduction in roGFP2 activity, a cytosolic ROS sensor, was observed in the cytosol under ER stress conditions. This observation supports the idea that ER stress can lead to a reduction in cytosolic redox potential, akin to the effects of SA accumulation, a condition that is known to induce the nuclear translocation of NPR1 (Lai et al., 2018).