Abstract
Autophagy is induced by viral infection and has antiviral functions in plants, but the underlying mechanism is poorly understood. We previously identified a viral small interfering RNA (vsiRNA) derived from rice stripe virus (RSV) RNA4 that contributes to the leaf-twisting and stunting symptoms caused by this virus by targeting the host eukaryotic translation initiation factor 4A (eIF4A) mRNA for silencing. In addition, autophagy plays antiviral roles by degrading RSV p3 protein, a suppressor of RNA silencing. Here, we demonstrate that eIF4A acts as a negative regulator of autophagy in Nicotiana benthamiana. Silencing of NbeIF4A activated autophagy and inhibited RSV infection by facilitating autophagic degradation of p3. Further analysis showed that NbeIF4A interacts with NbATG5 and interferes with its interaction with ATG12. Overexpression of NbeIF4A suppressed NbATG5-activated autophagy. Moreover, expression of vsiRNA-4A, which targets NbeIF4A mRNA for cleavage, induced autophagy by silencing NbeIF4A. Finally, we demonstrate that eIF4A from rice, the natural host of RSV, also interacts with OsATG5 and suppresses OsATG5-activated autophagy, pointing to the conserved function of eIF4A as a negative regulator of antiviral autophagy. Taken together, these results reveal that eIF4A negatively regulates antiviral autophagy by interacting with ATG5 and that its mRNA is recognized by a virus-derived siRNA, resulting in its silencing, which induces autophagy against viral infection.
Highlights
Eukaryotic initiation factor 4A, a member of the DEAD-box RNA helicase protein family, is thought to use the energy from ATP hydrolysis to unwind the mRNA structure and to prepare mRNA templates for ribosome recruitment during translation initiation, together with other components [1]
We demonstrate that Eukaryotic initiation factor 4A (eIF4A) is a negative regulator of autophagy in N. benthamiana and rice that acts by inhibiting the function
We previously determined that the mRNA of eIF4A from N. benthamiana (NbeIF4A) is targeted by a viral small interfering RNA produced from the genomic RNA4 fragment of rice stripe virus (RSV) by mRNA cleavage [4]
Summary
Eukaryotic initiation factor 4A (eIF4A), a member of the DEAD-box RNA helicase protein family, is thought to use the energy from ATP hydrolysis to unwind the mRNA structure and to prepare mRNA templates for ribosome recruitment during translation initiation, together with other components [1]. Eif4a1 mutants display slow growth, reduced lateral root formation, delayed flowering, and abnormal ovule development [2]. A T-DNA mutation of eIF4A confers dwarfing in Brachypodium distachyon in a dose-dependent manner [3]. EIF4A is essential for plant growth and development [2,3]. We previously determined that the mRNA of eIF4A from N. benthamiana (NbeIF4A) is targeted by a viral small interfering RNA (vsiRNA-4A) produced from the genomic RNA4 fragment of rice stripe virus (RSV) by mRNA cleavage [4]. Silencing of NbeIF4A caused dwarfing in plants, which is consistent with findings for B. distachyon [3,4]. The role of eIF4A in plant–virus interactions remains unclear
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