REMORIN proteins belong to a plant-specific multigene family that localise in plasma membrane nanodomains and in plasmodesmata. We previously showed that in Nicotiana benthamiana, group 1 StREM1.3 limits the cell-to-cell spread of a potexvirus without affecting viral replication. This prompted us to check whether an effect on viral propagation could apply to potyvirus species Turnip mosaic virus (TuMV) and Potato virus A (PVA). Our results show that StREM1.3 transient or stable overexpression in transgenic lines increases potyvirus propagation, while it is slowed down in transgenic lines underexpressing endogenous NbREMs, without affecting viral replication. TuMV and PVA infection do not alter the membranous localisation of StREM1.3. Furthermore, StREM1.3-membrane anchoring is necessary for its agonist effect on potyvirus propagation. StREM1.3 phosphocode seems to lead to distinct plant responses against potexvirus and potyvirus. We also showed that StREM1.3 interacts in yeast and in planta with the key potyviral movement protein CI (cylindrical inclusion) at the level of the plasma membrane but only partially at plasmodesmata pit fields. TuMV infection also counteracts StREM1.3-induced plasmodesmata callose accumulation at plasmodesmata. Altogether, these results showed that StREM1.3 plays an agonistic role in potyvirus cell-to-cell movement in N. benthamiana.

Summary: Lipid droplets (LDs), which are dedicated to storing neutral lipids (NLs), are dynamic organelles involved in numerous other functions, including membrane remodeling during abiotic stress. While the hijacking of LDs by animal viruses is well documented, their role(s) in plant virus infection remains largely unexplored. Similar to animal viruses, plant potyviruses reroute host proteins, intracellular membranes, and lipids to create an optimized microenvironment for their efficient viral replication compartment (VRC) assembly and movement. We therefore investigated whether potyviruses can also exploit the LD biogenesis machinery for their own benefit, akin to some animal viruses. Utilizing lipid analyses, confocal and transmission electron microscopy, and viral propagation surveys in plants impaired in LD biogenesis, we show that potyvirus turnip mosaic virus (TuMV) infection induces a significant accumulation of NLs and a proliferation of LDs in Nicotiana benthamiana or Arabidopsis thaliana ‐infected leaves, which are often located in close proximity to VRCs. This suggests that there is a spatial and functional relationship between LDs and TuMV. We demonstrate also that two protein families crucial for LD biogenesis, namely the lipid droplet‐associated proteins and SEIPINs, facilitate TuMV propagation in Arabidopsis thaliana . Taken together, our results indicate a pro‐viral function for LDs in potyvirus‐infected plants.

The dominant Pvr4 gene in pepper (Capsicum annuum) confers resistance to members of six potyvirus species, all of which belong to the Potato virus Y (PVY) phylogenetic group. The corresponding avirulence factor in the PVY genome is the NIb cistron (i.e., RNA-dependent RNA polymerase). Here, we describe a new source of potyvirus resistance in the Guatemalan accession C. annuum cv. PM949. PM949 is resistant to members of at least three potyvirus species, a subset of those controlled by Pvr4. The F₁ progeny between PM949 and the susceptible cultivar Yolo Wonder was susceptible to PVY, indicating that the resistance is recessive. The segregation ratio between resistant and susceptible plants observed in the F₂ progeny matched preferably with resistance being determined by two unlinked recessive genes independently conferring resistance to PVY. Inoculations by grafting resulted in the selection of PVY mutants breaking PM949 resistance and, less efficiently, Pvr4–mediated resistance. The codon substitution E₄₇₂K in the NIb cistron of PVY, which was shown previously to be sufficient to break Pvr4 resistance, was also sufficient to break PM949 resistance, a rare example of cross-pathogenicity effect. In contrast, the other selected NIb mutants showed specific infectivity in PM949 or Pvr4 plants. Comparison of Pvr4 and PM949 resistance, which share the same target in PVY, provides interesting insights into the determinants of resistance durability.