Molecular crosstalk between plant translation initiation complexes influences the outcome of virus infection

Successful subversion of translation initiation factors 4E and 4G determines the infection success of potyviruses, the largest group of viruses affecting plants. In the natural variability of many plant species, resistance to potyvirus infection is provided by polymorphisms at4Eand4Gthat renders them inadequate for virus hijacking but still functional in translation initiation. In crops where such natural resistance alleles are limited, the genetic inactivation of4Ehas been proposed for the engineering of potyvirus resistance. However, recent findings indicate that knockout4Eand4Galleles may be deleterious for plant health and could jeopardize resistance efficiency in comparison to functional resistance proteins. Here, we explored the cause of these adverse effects by studying the role of theArabidopsis eIF4E1, whose inactivation was previously reported as conferring resistance to the potyvirus clover yellow vein virus (ClYVV) while also promoting susceptibility to another potyvirus called turnip mosaic virus (TuMV). We report thateIF4E1is required to maintain global plant translation and to restrict TuMV accumulation during infection, and its absence is associated with a favoured virus multiplication over host translation. Furthermore, our findings demonstrate that eIF4E1 plays a crucial role in inhibiting the TuMV-induced degradation of the translation initiation factor eIFiso4G1, thereby preventing the generation of a truncated protein. Finally, we demonstrate a role for eIFiso4G1 in TuMV accumulation and in supporting plant fitness during infection. These findings suggest that eIF4E1 counteracts the hijacking of the plant translational apparatus during TuMV infection and underscore the importance of preserving the functionality of translation initiation factors 4E and 4G when implementing potyvirus resistance strategies.Author summaryPlants are constantly under threat from viruses that can damage crops and reduce yield. Among these viruses, potyviruses are a major concern, and a small group of genes known aseIF4Eare key factors in making a plant susceptible to them. To combat these viruses, it is possible to either use naturally-selected variants ofeIF4Ethat provide resistance, or to disable the gene altogether. However, new research has shown that inactivatingeIF4Egenes may have unintended consequences for the plant’s development while compromise resistance to other potyviruses.To investigate this further, we focus in this work on the role of theArabidopsis eIF4E1whose inactivation confers resistance to one potyvirus, clover yellow vein virus (ClYVV). We looked why this same mutation ateIF4E1makes the plants more susceptible to another potyvirus, turnip mosaic virus (TuMV). Our study reveals that eIF4E1 acts in safeguarding the plant translational machinery during TuMV infection. By preventing the degradation of the translation initiation protein eIFiso4G1, eIF4E1 enables the plant to maintain its normal translation activity and ultimately prevents the accumulation of virus proteins.Our findings provide valuable insights into how potyviruses hijack the plant’s translation process, and emphasizes the need of preserving the functionality of translation initiation factors when developing potyvirus resistances.