4.1 Cytoplasmic TRX: Regulating ROS and restricting viruses
Plant viruses have developed mechanisms to engage with and manipulate members of the TRX protein family to enhance their own replication and systemic dissemination (Table 1). The exploration of the roles of TRX proteins in plant-virus interactions has uncovered a common theme. In many instances, viruses can repress or counteract the functions of TRX, resulting in favorable conditions for viral cell-to-cell movement. In many cases, viruses can suppress or counteract TRX functions, creating favorable conditions for viral cell-to-cell movement (Fig. 1) . This suppression also leads to an increase in ROS levels. However, despite the well-established regulatory roles of ROS in PD permeability and intercellular trafficking, the outcome of virus-redox interactions depends on the organelle where ROS is produced. In some cases, viral control of TRX can help establish a microenvironment rich in ROS that facilitates viral accumulation and spread. In other cases, virus-mediated reduction of ROS hampers SA-related defenses, including those regulating PD permeability (Table 1) (Wu et al., 2018; Wang et al., 2021; Vu et al., 2022).
For example, NbTrxh1 hampers the movement of various viruses, including Barley stripe mosaic virus (BSMV), Lychnis ringspot virus, Beet black scorch virus, and Beet necrotic yellow virus (Jiang et al., 2022). However, the interaction between NbTrxh1 and the γb protein of BSMV leads to the reduction of NbTrxh1’s reductase activity. This decrease negatively impacts downstream SA-mediated gene expression, thus facilitating viral movement. The study concluded that type-h TRXs play a broad role in defending against both RNA and DNA viruses in plants (Jiang et al., 2022). The enhanced viral movement observed inNbTrxh1 -silenced Nicotiana benthamiana plants suggested an effect of NbTRXh1 on PD permeability although no direct analysis of PD function was made (Fig. 1) .
In a similar fashion to NbTRXh1 , pepper TRXh1 plays a crucial role in defending against Cucumber mosaic virus (CMV) and Euphorbia mosaic virus-Yucatan Peninsula (EuMV-YP). It is worth noting that inCaTRXh1 -silenced pepper (Capsicum annum ) plants, the accumulation of SA is higher, yet their susceptibility to EuMV-YP is greater compared to control plants (Luna-Rivero et al., 2016). These findings suggest that cytosolic TRXs negatively affect viral cell-to-cell movement, probably by controlling PD permeability via NPR1-mediated SA signaling.
Like cytosolic TRXs, chloroplast TRXs In N. benthamiana play roles in plant-virus interactions. The chloroplast NADPH-dependent thioredoxin C (NTRC) protein has a significant role in resistance against BSMV (Wang et al., 2021). Plants that constitutively expressed NTRC exhibited elevated levels of chloroplast ROS, contributing to their defense against BSMV. Notably, when genes encoding ROS scavengers, such as 2-Cys Prx which interacts with NTRC, were silenced, BSMV accumulated to higher levels than in control plants (Wang et al., 2021). This phenomenon was attributed to the BSMV-encoded γb protein’s capacity to interfere with and subvert NTRC-mediated chloroplast antioxidant defenses, leading to the creation of an oxidative chloroplast microenvironment necessary for BSMV infection. The γb protein was found to interact with NTRC and impair NTRC-2-Cys Prx interactions, thereby facilitating systemic infection. Notably, when the NTRC-γb interaction is disrupted by introducing a mutant γb (H85A), BSMVH85Afailed to spread systemically and exhibited lower accumulation levels in the inoculated leaves compared to wild-type BSMV (Wang et al., 2021, EMBO Journal). N. tabacum transgenic lines constitutively expressing the chloroplast-localized NtTRXh3 showed increased resistance to TMV and Cucumber mosaic virus (CMV), whereas silencing this gene led to suppressed defense responses, and increased accumulation of both viruses (Sun et al., 2010). There are other examples where viral proteins were reported to interact with differentTRX members, such as TGBp1 from Pepino mosaic virus with the tomato TRX SlTXND9 (Mathioudakis et al., 2018), and TRX-like proteins from whitefly with the coat proteins of two begomoviruses (Saurav et al., 2019). However, their exact roles in the context of host-virus interactions remain unexplored.
Recent research has unveiled that virus-derived small interfering RNA (vsiRNA) originating from the wheat yellow mosaic virus (WYMV) not only targets the WYMV genome but also the thioredoxin-like gene within the wheat chloroplast. TaAAED1 was identified as a key player with a negative regulatory role in ROS accumulation (Liu et al., 2021). WhenTaAAED1 was overexpressed in wheat protoplast, it promoted susceptibility to WYMV by reducing ROS levels. However, transgenic wheat expressing these vsiRNAs exhibited reduced levels of TaAAED1 and increased ROS levels, ultimately leading to resistance against various viruses. Nevertheless, it remains unexplored whether this defensive effect is confined to the cellular ROS level or influences the cell-to-cell movement of infecting viruses. Given the established negative impact of TRXs on ROS accumulation and, consequently, PD permeability, it is likely that TaAAED1 exerts similar effects on PD as observed in N. benthamiana plants.
While several TRX genes exhibit a common role in reducing ROS levels and governing antiviral resistance (Table 1), an exceptional TRXh variant, predominantly lacking canonical cysteines yet demonstrating chaperone-like attributes, has been unveiled. This distinct maize (Zea mays) ZmTRXh variant can suppress the accumulation of sugar cane mosaic virus (SCMV) RNA, thus contributing to resistance against SCMV (Liu et al., 2017). Remarkably, its mechanism of action appears distinct from the conventional SA or JA defense signaling pathways.