A Family of Plasmodesmal Proteins with Receptor-Like Properties for Plant Viral Movement Proteins

Khalid Amari,Andrew J Maule,Lourdes Fernandez-Calvino,Corinne Schmitt-Keichinger,Yves Mély,Christina Hofmann,Jérome Mutterer,Pascal Didier,Manfred Heinlein,Emmanuel Boutant,Christophe Ritzenthaler,Carole L Thomas,Alexander Lerich

doi:10.1371/journal.ppat.1001119

Abstract

Plasmodesmata (PD) are essential but poorly understood structures in plant cell walls that provide symplastic continuity and intercellular communication pathways between adjacent cells and thus play fundamental roles in development and pathogenesis. Viruses encode movement proteins (MPs) that modify these tightly regulated pores to facilitate their spread from cell to cell. The most striking of these modifications is observed for groups of viruses whose MPs form tubules that assemble in PDs and through which virions are transported to neighbouring cells. The nature of the molecular interactions between viral MPs and PD components and their role in viral movement has remained essentially unknown. Here, we show that the family of PD-located proteins (PDLPs) promotes the movement of viruses that use tubule-guided movement by interacting redundantly with tubule-forming MPs within PDs. Genetic disruption of this interaction leads to reduced tubule formation, delayed infection and attenuated symptoms. Our results implicate PDLPs as PD proteins with receptor-like properties involved the assembly of viral MPs into tubules to promote viral movement.

Highlights

Propagation of viruses in higher organisms depends upon cycles of virus uptake and egress
We show that a family of plasmodesmata-located proteins, called PD-located proteins (PDLPs), which are conserved amongst higher plants, mediate this process
This class of movement proteins (MPs) occurs for a diverse range of plant virus genera and we show that representatives of these viruses have MPs that bind PDLPs

Summary

Introduction

Propagation of viruses in higher organisms depends upon cycles of virus uptake and egress. Since PDs are tightly regulated, viruses encode movement proteins (MPs) to extend structurally and functionally the restrictions on molecular flux through the PD channel [7,8,9]. Some MPs, assemble into tubules that profoundly alter PD structure by displacing the desmotubule inside the PD, preserving only the integrity of the plasma membrane [13,14,15]. These tubules aid the transport of virus particles or viral ribo-nuclear complexes [16] into neighbouring cells (for review, see [13,14]). Members of the Caulimoviridae, Badnaviridae, Tospoviridae, Ilarviridae and Bromoviridae families are representatives of this latter group

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