Susceptibility factor StEXA1 interacts with StnCBP to facilitate potato virus Y accumulation through the stress granule-dependent RNA regulatory pathway in potato

Abstract

Plant viruses recruit multiple host factors for translation, replication, and movement in the infection process. The loss-of-function mutation of the susceptibility genes will lead to the loss of susceptibility to viruses, which is referred to as “recessive resistance”. Essential for potexvirus Accumulation 1 (EXA1) has been identified as a susceptibility gene required for potexvirus, lolavirus, and bacterial and oomycete pathogens. In this study, EXA1 knockdown in potato (StEXA1) was found to confer novel resistance to potato virus Y (PVY, potyvirus) in a strain-specific manner. It significantly compromised PVYO accumulation but not PVYN:O and PVYNTN. Further analysis revealed that StEXA1 is associated with the HC-Pro of PVY through a member of eIF4Es (StnCBP). HC-ProO and HC-ProN, two HC-Pro proteins from PVYO and PVYN, exhibited strong and weak interactions with StnCBP, respectively, due to their different spatial conformation. Moreover, the accumulation of PVYO was mainly dependent on the stress granules (SGs) induced by StEXA1 and StnCBP, whereas PVYN:O and PVYNTN could induce SGs by HC-ProN independently through an unknown mechanism. These results could explain why StEXA1 or StnCBP knockdown conferred resistance to PVYO but not to PVYN:O and PVYNTN. In summary, our results for the first time demonstrate that EXA1 can act as a susceptibility gene for PVY infection. Finally, a hypothetical model was proposed for understanding the mechanism by which StEXA1 interacts with StnCBP to facilitate PVY accumulation in potato through the SG-dependent RNA regulatory pathway.

Plant eIF4E isoforms as factors of susceptibility and resistance to potyviruses

“…In potato, eIF4E1 inactivation reduced PVY multiplication (Lucioli et al, 2022). Notably, the suppression of nCBP in potato cells has a similar effect to one PVY strain (Chen et al, 2022a). Although these data strongly suggest that at least some PVY strain could unexpectedly use multiple and leastsimilar eIF4E isoforms in potato, the inactivation of a single eIF4E isoform would likely disturb some regulatory mechanism between different eIF4E isoforms.…”

“…Zlobin and Taranov 10.3389/fpls.2023.1041868 Frontiers in Plant Science frontiersin.org Igreja, 2021). In potatoes, nCBP knockdown causes deformation of young leaves (Chen et al, 2022a). Additional eIF4E factors have been discovered in different plants (Figure 1) (Patrick and Browning, 2012;Patrick et al, 2014).…”

“…Reducing the concentration of eIF4E in plant cells will lead to a lower efficiency of its use by the virus, whereas its increase will have the opposite effect. In fact, increased eIF4E levels promote potyviral accumulation (Schaad et al, 2000;Nicaise et al, 2003;Hafreń et al, 2013), whereas eIF4E silencing results in resistance or at least significantly suppressed potyviral accumulation in plant tissues (Hwang et al, 2009;Eskelin et al, 2011;Mazier et al, 2011;Takakura et al, 2018;Chen et al, 2022a). Artificial silencing rarely results in complete gene repression; however, the decrease in eIF4E concentration was sufficient to achieve resistance.…”

Repression of mRNA translation initiation by GIGYF1 via blocking the eIF3-eIF4G1 interaction

“…It is interesting to note that this function of the GIGYF family appears to be evolutionarily conserved. The depletion of SMY2-type ILE-GYF domain-containing protein 1 (EXA1), the plant homolog of GIGYF1, has also been identified as a susceptibility gene for viral infections (Chen et al, 2022; Wu et al, 2017; Yusa et al, 2019).…”

Plant virology in the 21st century in China: Recent advances and future directions

“…Other host factors, such as TaPDIL5‐1 in wheat and RabGDIα in maize, were identified as recessive resistance genes against WYMV and RBSDV infection, respectively (Liu et al, 2020b; Kan et al, 2022). EXA1 and nCBP in potatoes have been identified as recessive resistance genes against PVY (Chen et al, 2022). WPRb and the chloroplast phosphoglycerate kinase gene chl‐PGK are recessive resistance genes against CGMMV and BaMV, respectively (Cheng et al, 2013; Cai et al, 2023).…”