A Begomovirus Nuclear Shuttle Protein-Interacting Immune Hub: Hijacking Host Transport Activities and Suppressing Incompatible Functions

Abstract

Begomoviruses (Geminiviridae family) represent a severe constraint to agriculture worldwide. As ssDNA viruses that replicate in the nuclei of infected cells, the nascent viral DNA has to move to the cytoplasm and then to the adjacent cell to cause disease. The begomovirus nuclear shuttle protein (NSP) assists the intracellular transport of viral DNA from the nucleus to the cytoplasm and cooperates with the movement protein (MP) for the cell-to-cell translocation of viral DNA to uninfected cells. As a facilitator of intraand intercellular transport of viral DNA, NSP is predicted to associate with host proteins from the nuclear export machinery, the intracytoplasmic active transport system, and the cell-to-cell transport complex. Furthermore, NSP functions as a virulence factor that suppresses antiviral immunity against begomoviruses. In this review, we focus on the protein-protein network that converges on NSP with a high degree of centrality and forms an immune hub against begomoviruses. We also describe the compatible host functions hijacked by NSP to promote the nucleocytoplasmic and intracytoplasmic movement of viral DNA. Finally, we discuss the NSP virulence function as a suppressor of the recently described NSP-interacting kinase 1 (NIK1)-mediated antiviral immunity. Understanding the NSP-host protein-protein interaction (PPI) network will probably pave the way for strategies to generate more durable resistance against begomoviruses.

Geminivirus Resistance: A Minireview

“…This same T474 when changed to phosphomimetic aspartate constitutively activates antiviral response genes, circumvents interference by NSP, and confers tolerance to begomovirus infection (Brustolini et al, 2015). Furthermore, a GTPase that interacts with NSP can also be conceived as a target to develop resistance against geminiviruses (Martins et al, 2020). These responses exemplify that understanding and changing genetic interactions can provide new solutions for disease management.…”

“…MP is responsible primarily for the intercellular spread of viral DNA ( Noueiry et al, 1994 ) by increasing the size exclusion limit of plasmodesmata ( Rojas et al, 2001 ). For excellent reviews in these subjects please see Hanley-Bowdoin et al, 2013 ; Czosnek et al, 2017 ; Rojas et al, 2018 , and Martins et al, 2020 .…”

Geminiviral Triggers and Suppressors of Plant Antiviral Immunity

“…Adapted from [1] The B component of bipartite geminiviruses encodes BC1 and BV1. BV1 is a nuclear shuttling protein (NSP) that facilitates the intracellular transport of viral DNA from the nucleus to the cell periphery and assists BV1, the classic movement protein (MP), to move the viral DNA to the adjacent, uninfected cell via plasmodesmata [20]. Some geminiviruses are often associated with DNA satellites, designated beta-and alphasatellites, which affect geminiviral pathogenicity and symptom development [21,22] (Figure 1).…”

Plant-virus-insect tritrophic interactions: insights into the functions of geminivirus virion-sense strand genes

“…The interaction of CP-coated viral DNA with the importin α or karyopherin α1 facilitates its entry into the nucleus [58,59]. The non-specific DNA binding ability supports the CP to sequester viral DNAs from the replication pool for viral packaging and transport to the neighbouring cells [57,60,61]. The bipartite begomovirus-encoded nuclear shuttle protein (NSP) recruits an acetyl transferase to acetylate viral DNA-wrapped CP to reduce its DNA binding affinity and favours the binding of NSP with the viral DNA to assist in nuclear export [60,61].…”