The Potyviral P3 Protein Targets Eukaryotic Elongation Factor 1A to Promote the Unfolded Protein Response and Viral Pathogenesis

Abstract

The biochemical function of the potyviral P3 protein is not known, although it is known to regulate virus replication, movement, and pathogenesis. We show that P3, the putative virulence determinant of soybean mosaic virus (SMV), targets a component of the translation elongation complex in soybean. Eukaryotic elongation factor 1A (eEF1A), a well-known host factor in viral pathogenesis, is essential for SMV virulence and the associated unfolded protein response (UPR). Silencing GmEF1A inhibits accumulation of SMV and another ER-associated virus in soybean. Conversely, endoplasmic reticulum (ER) stress-inducing chemicals promote SMV accumulation in wild-type, but not GmEF1A-knockdown, plants. Knockdown of genes encoding the eEF1B isoform, which is important for eEF1A function in translation elongation, has similar effects on UPR and SMV resistance, suggesting a link to translation elongation. P3 and GmEF1A promote each other's nuclear localization, similar to the nuclearcytoplasmic transport of eEF1A by the Human immunodeficiency virus 1 Nef protein. Our results suggest that P3 targets host elongation factors resulting in UPR, which in turn facilitates SMV replication and place eEF1A upstream of BiP in the ER stress response during pathogen infection.

Soybean mosaic virus: a successful potyvirus with a wide distribution but restricted natural host range

“…Although SMV may activate and be partially limited by basal defences, it induces changes in cellular physiology that favour virus accumulation. The SMV P3 protein interacts with eukaryotic elongation factor 1A (eEF1A), a guanosine diphosphate:guanosine triphosphate (GDP:GTP)‐binding protein that delivers aminoacylated tRNAs to ribosomes (Luan et al ., ). The guanine nucleotide exchange factor eEF1B recycles eEF1A to the active GTP‐bound form.…”

“…The guanine nucleotide exchange factor eEF1B recycles eEF1A to the active GTP‐bound form. VIGS of both eEF1A and eEF1B reduces SMV virulence, suggesting that these proteins are essential for virulence (Luan et al ., ). In addition, VIGS of these genes prevents an endoplasmic reticulum stress response to SMV.…”

Cross-Talk in Viral Defense Signaling in Plants

“…Notably, most such recessive R genes have been analyzed in potyviruses and encode translation initiation factors of the 4E or 4G family (eIF4E/eIF4G) (Kang et al, 2005; Truniger and Aranda, 2009). Interestingly, EF1A is required for Soybean Mosaic virus (SMV)-induced endoplasmic reticulum (ER) stress and, therefore, replication of SMV (Luan et al, 2016). Consequently, silencing of EF1A inhibits SMV replication and confers resistance against SMV.…”

The Current Status of the Soybean-Soybean Mosaic Virus (SMV) Pathosystem

“…Eukaryotic elongation factor 1A (eEF1A) is a well-known host factor in viral pathogenesis. Recently, Luan et al (2016) showed that silencing GmeEF1A inhibits accumulation of SMV and P3 protein of SMV interacts with GmeEF1A to facilitate its nuclear localization and therefore, promotes SMV pathogenicity.…”