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.