Selective Interaction of Sugarcane eIF4E with VPgs from Sugarcane Mosaic Pathogens

Abstract

Eukaryotic translation initiation factor 4E (eIF4E) plays a key role in the infection of potyviruses in susceptible plants by interacting with viral genome-linked protein (VPg). Sugarcane (Saccharum spp.) production is threatened by mosaic disease caused by Sugarcane mosaic virus (SCMV), Sorghum mosaic virus (SrMV), and Sugarcane streak mosaic virus (SCSMV). In this study, two eIF4Es and their isoform eIF(iso)4E and 4E-binding protein coding genes were cloned from sugarcane cultivar ROC22 and designated SceIF4Ea, SceIF4Eb, SceIF(iso)4E, and ScnCBP, respectively. Real-time quantitative PCR analysis showed different expression profiles of these four genes upon SCMV challenge. A subcellular localization assay showed that SceIF4Ea, SceIF4Eb, SceIF(iso)4E, and ScnCBP were distributed in the nucleus and cytoplasm. Yeast two-hybrid (Y2H) and bimolecular fluorescence complementation (BiFC) assays showed that SceIF4Ea/b and SceIF(iso)4E were selectively employed by different sugarcane mosaic pathogens, i.e., SCMV-VPg interacted with SceIF4Ea/b and SceIF(iso)4E, SrMV-VPg interacted with both SceIF4Eb and SceIF(iso)4E, and SCSMV-VPg interacted only with SceIF(iso)4E. Intriguingly, the BiFC assays, but not the Y2H assays, showed that ScnCBP interacted with the VPgs of SCMV, SrMV, and SCSMV. Competitive interaction assays showed that SCMV-VPg, SrMV-VPg, and SCMV-VPg did not compete with each other to interact with SceIF(iso)4E, and SceIF(iso)4E competed with SceIF4Eb to interact with SrMV-VPg but not SCMV-VPg. This study sheds light on the molecular mechanism of sugarcane mosaic pathogen infection of sugarcane plants and benefits sugarcane breeding against the sugarcane mosaic disease.

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

“…These results indicate a link between EXA1 and viral translation depending on eIF4Es. Several studies in various plants have suggested that the interactions between eIF4Es and VPgs are responsible for eIF4E -mediated resistance [ 76 – 79 ]. However, the interaction between eIF4Es and VPg/NIa alone cannot fully elucidate the role of eIF4Es in the infection cycle of potyviruses.…”

“…S8b ). In a recent study of sugarcane, the interactions between ScnCBP and VPgs of several sugarcane mosaic pathogens were detected only in bimolecular fluorescence complementation (BiFC), but not in Y2H assay [ 79 ]. Thus, we cannot exclude the possibility that the VPg or some other proteins of PVY may also be involved in the resistance mediated by StEXA1 and StnCBP.…”

Eukaryotic translation initiation factor 4E family member nCBP facilitates the accumulation of TGB-encoding viruses by recognizing the viral coat protein in potato and tobacco

“…Recessive resistance genes have become a very important resource in plant breeding for virus resistance ( Truniger and Aranda, 2009 ). eIF4Es are the most extensively studied recessive resistance genes involved in the infection of various viruses ( Hashimoto et al, 2016 ; Xu et al, 2017 ; Yang et al, 2021 ). This study for the first time reports that StnCBP , a member of the eIF4E family in potato, is involved in PVS infection as a recessive resistance gene.…”

“…They are also the most extensively studied susceptibility genes ( Lellis et al, 2002 ), and particular research attention has been paid to the relationship between eIF4E/eIF(iso)4E and potyvirus infection. For instance, mutation in eIF4E/eIF(iso)4E resulted in loss of susceptibility to potyviruses in multiple hosts, such as Arabidopsis, tomato, pepper, lettuce, pea, peanut, and sugarcane ( Ruffel et al, 2002 , 2005 ; Nicaise et al, 2003 ; Gao et al, 2004 ; Xu et al, 2017 ; Yang et al, 2021 ). In most cases, the interaction between eIF4E/eIF(iso)4E and the viral genome-linked proteins (VPgs) of potyviruses is required for virus infection ( Léonard et al, 2000 ; Charron et al, 2008 ; Tavert-Roudet et al, 2017 ; Yang et al, 2021 ).…”

“…For instance, mutation in eIF4E/eIF(iso)4E resulted in loss of susceptibility to potyviruses in multiple hosts, such as Arabidopsis, tomato, pepper, lettuce, pea, peanut, and sugarcane ( Ruffel et al, 2002 , 2005 ; Nicaise et al, 2003 ; Gao et al, 2004 ; Xu et al, 2017 ; Yang et al, 2021 ). In most cases, the interaction between eIF4E/eIF(iso)4E and the viral genome-linked proteins (VPgs) of potyviruses is required for virus infection ( Léonard et al, 2000 ; Charron et al, 2008 ; Tavert-Roudet et al, 2017 ; Yang et al, 2021 ). Moreover, eIF4E/eIF(iso)4E was also found to mediate recessive resistance to other viruses.…”