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Variability, Functions and Interactions of Plant Virus Movement Proteins: What Do We Know So Far?

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Variability, Functions and Interactions of Plant Virus Movement Proteins: What Do We Know So Far? microorganisms Review Variability, Functions and Interactions of Plant Virus Movement Proteins: What Do We Know So Far? Gaurav Kumar and Indranil Dasgupta * Department of Plant Molecular Biology, University of Delhi South Campus, New Delhi 110021, India; [email protected] * Correspondence: [email protected] Abstract: Of the various proteins encoded by plant viruses, one of the most interesting is the move- ment protein (MP). MPs are unique to plant viruses and show surprising structural and functional variability while maintaining their core function, which is to facilitate the intercellular transport of viruses or viral nucleoprotein complexes. MPs interact with components of the intercellular channels, the plasmodesmata (PD), modifying their size exclusion limits and thus allowing larger particles, including virions, to pass through. The interaction of MPs with the components of PD, the formation of transport complexes and the recruitment of host cellular components have all revealed different facets of their functions. Multitasking is an inherent property of most viral proteins, and MPs are no exception. Some MPs carry out multitasking, which includes gene silencing suppression, viral replication and modulation of host protein turnover machinery. This review brings together the current knowledge on MPs, focusing on their structural variability, various functions and interactions with host proteins. Citation: Kumar, G.; Dasgupta, I. Keywords: callose; coat protein; plasmodesmata; triple gene block; viral suppressor; virus movement; Variability, Functions and Interactions virus replication complex of Plant Virus Movement Proteins: What Do We Know So Far? Microorganisms 2021, 9, 695. https://doi.org/10.3390/ 1. Introduction microorganisms9040695 The process of infection of plants with viruses is broadly divided into two types; local and systemic. Local infection is often subliminal and is characterized by intracellular Academic Editor: Jesús confinement of virus within and nearby the site of infection, while the systemic infection Navas Castillo is progressive throughout the host and involves first, the short-distance movement of the virus from the infected cell to surrounding cells followed by long-distance movement using Received: 28 February 2021 the host vasculature preferably the phloem tissue [1]. However, some phloem-limited Accepted: 22 March 2021 Published: 27 March 2021 viruses often skip the first route and are directly injected into the phloem by their vector interested in the phloem sap. In general, the plant viruses show a “symplastic” life cycle, Publisher’s Note: MDPI stays neutral i.e., from entry into the host cell to it accumulates in multiple copies; all occur in the with regard to jurisdictional claims in cell symplast. The local intercellular virus spread in the host largely occurs through the published maps and institutional affil- symplastically connected cells via the plasmodesmata (PD, Figure1) until they encounter iations. the host vasculature for long-distance systemic infection [1,2]. The intercellular transport through PD depends upon its size exclusion limit (SEL), defined by the size of the largest molecule, which can pass through. Although solely dependent upon the hydrodynamic stokes radius [3], the PD SEL is highly dynamic and varies with cell-type, ambient light, temperature and developmental stages, being higher Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. in some newly formed mesophyll cells compared to the fully differentiated mature cells [4]. × This article is an open access article Not surprisingly, the size of most viruses, (e.g., tobacco mosaic virus, TMV = 300 18 nm) distributed under the terms and or their nucleic acids, whether in the free or folded state, exceeds the SEL of most PDs conditions of the Creative Commons (~60 nm) [5,6]. This indicates that the SEL of PD is modified during virus infection leading Attribution (CC BY) license (https:// to systemic movement of viral progenies. Most of the plant viruses, if not all, encode a creativecommons.org/licenses/by/ class of structurally diverse protein(s) known as movement protein (MP) that facilitates 4.0/). such intercellular adjustments for virus movements. These MPs have been reported to Microorganisms 2021, 9, 695. https://doi.org/10.3390/microorganisms9040695 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, 695 2 of 29 Microorganisms 2021, 9, 695 2 of 30 class of structurally diverse protein(s) known as movement protein (MP) that facilitates such intercellular adjustments for virus movements. These MPs have been reported to interactinteract with with various various host host factors factors to to ensure ensure successful successful virus virus movement movement across across cells cells [5]. [In5]. general,In general, the theMPs MPs perform perform the function the function of interacting of interacting with withthe viral the genome, viral genome, targeting targeting them tothem PDs toand PDs modifying and modifying the SEL theof PD, SEL a process of PD, aoften process termed often as “ termedgating” as. The “gating”. idea of syn- The chronousidea of synchronous coupling of couplingvirus replication of virus replicationand intercellular and intercellular movement movementof viral genomes of viral throughgenomes MP through-assisted MP-assisted PD-gating has PD-gating further divided has further the movement divided the into movement sub-stages into involv- sub- ingstages post involving replication post interactions, replication movement interactions, of an movement infection ofunit an from infection the replication unit from site the toreplication the gated sitePDs to and the the gated actual PDs intercellular and the actual transport. intercellular This has transport. further expanded This has furtherthe list ofexpanded MP interacting the list partners of MP interacting [1,2,5,6]. partners [1,2,5,6]. FigureFigure 1. 1. TheThe symplastic symplastic and and apoplastic apoplastic pathways pathways between between adjacent adjacent plant plant cells cells and and the the model model illustrating illustrating plasmodesmata plasmodesmata ((PD)PD) structure structure with with-associated-associated cytoskeletal cytoskeletal components components and and proteins proteins governing governing PD PD permeability. permeability. Abbreviations: Abbreviations: CalS CalS—— callosecallose synthases; synthases; NCAPP NCAPP—non-cell-autonomous—non-cell-autonomous pathway pathway proteins; proteins; PAPK PAPK—plasmodesmal-associated—plasmodesmal-associated protein protein kinase; kinase; PDCBPDCB—plasmodesmata-associated—plasmodesmata-associated callose callose-binding-binding proteins; proteins; PDLP PDLP—plasmodesmata-located—plasmodesmata-located proteins; proteins; RGP RGP—reversibly—reversibly glycosylatedglycosylated polypeptide; polypeptide; Syta Syta—synaptotagmin—synaptotagmin A. DespiteDespite sharing sharing a a common common function function,, there there exists exists a a large large variation among among MPs MPs and and theirtheir mechanisms mechanisms of of action. action. In In recent recent years, years, a a number number of of functions functions-associated-associated with with MPs, MPs, namelynamely the the mechanisms mechanisms of of modifying modifying the the PD PD SEL, SEL, formation formation of of a a viral viral transport transport complex, complex, interactioninteraction with with host host com componentsponents and and suppression suppression of of RNA RNA silencing silencing,, have have been been revealed. revealed. InIn addition, addition, there there are are other other viral viral proteins proteins that that mimic mimic the the functionality functionality of ofMPs. MPs. In this In thisre- viewreview,, we we have have chosen chosen to to bring bring together together recent recent findings findings on on MPs, MPs, interactions interactions that that they they shareshare and and the the div divisionision of of labor labor that that they they show show with with other other ancillary ancillary proteins proteins required required for for thethe intercellular intercellular movement movement of of plant plant viruses. viruses. Several Several other other previous previous in-depth in-depth reviews reviews pre- sentpresent an exhaustive an exhaustive discussion discussion on onvarious various aspects aspects governing governing the the intra intra-,-, and and intercellular intercellular movememovementnt of viruses and thethe readerreader isis guidedguided to to these these for for a a more more holistic holistic understanding understanding of ofthis this topic topic [7 –[714–14]]. Additionally,. Additionally, we we request request readers readers to to go go through through the the reviews reviews [5 ,[5,1515–18–]18] to get an overview of the historical perspective and earlier findings, specifically on MPs and their interactions. Microorganisms 2021, 9, 695 3 of 30 2. PD and PD Associated Proteins (PDAPs): The Facilitators of Virus Movement PDs (Figure1) are membrane-lined interconnected channels formed primarily upon entrapment of components of the endoplasmic reticulum (ER) in the course of phrag- moplast formation during cytokinesis. PDs are centrally occupied by the appressed ER (desmotubule; DT), which brings about cytoplasmic continuity at the interface of adjacent cells. Surrounding the DT is a continuous channel of variable size called cytoplasmic sleeve, which is delimited by the plasma membrane (PM) [19] and is available for intercellular trafficking.
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