Critical Reviews in Plant Sciences, 23(3):195–250 (2004) Copyright C Taylor and Francis Inc. ISSN: 0735-2689 print / 1549-7836 online DOI: 10.1080/07352680490452807 The Ins and Outs of Nondestructive Cell-to-Cell and Systemic Movement of Plant Viruses Elisabeth Waigmann Max F. Perutz Laboratories, University Departments at the Vienna Biocenter, Institute of Medical Biochemistry, Medical University of Vienna, Dr. Bohrgasse 9 A-1030, Vienna, Austria Shoko Ueki Department of Biochemistry and Cell Biology, State University of New York, Stony Brook, NY 11794-5215 Kateryna Trutnyeva Max F. Perutz Laboratories, University Departments at the Vienna Biocenter, Institute of Medical Biochemistry, Medical University of Vienna, Dr. Bohrgasse 9 A-1030, Vienna, Austria Vitaly Citovsky∗ Department of Biochemistry and Cell Biology, State University of New York, Stony Brook, NY 11794-5215 Referee: Dr. Ernest Hiebert, Professor, Department of Plant Pathology, University of Florida/IFAS, P.O. Box 110680, 1541 Fifield Hall, Gainesville, FL 32611-0680, USA. Table of Contents 1. Introduction ..........................................................................................................................................................196 2. Structure and Composition of Plasmodesmata, the Intercellular Conduits for Viral Movement ..............................198 3. Cell-to-Cell Transport of Plant Viruses: Have Movement Protein, Will Travel ........................................................200 3.1. MP Structure: Are Common Functions Supported by Common Structures? ...........................................................200 3.2. Movement Complexes as Cell-to-Cell Transport Intermediates .............................................................................202 3.3. Viral MPs Gate Plasmodesmata and Themselves Move Between Cells ..................................................................205 3.4. Subcellular Localization of Viral MPs ................................................................................................................207 3.4.1. Localization to the Cell Wall and Plasmodesmata ......................................................................................207 3.4.2. Association with Microtubules .................................................................................................................210 3.4.3. Association with the ER ..........................................................................................................................212 3.4.4. Association with the Nucleus, Plasma Membrane and Other Cellular Structures ...................................................................................................................213 3.4.5. Subcellular Localization Patterns of MPs: A Doorway to Function? ...........................................................................................................................................215 3.5. Partners-in-Movement: Host Proteins that Interact with MP .................................................................................216 3.6. Regulation of MP Functions by Phosphorylation .................................................................................................219 3.7. Multiple Roles of TMV MP in the Viral Life Cycle: A Host Factor-Based Model ...................................................221 4. Systemic Transport of Plant Viruses: Long-Distance Runners ................................................................................224 4.1. Viral Factors Involved in Systemic Movement .....................................................................................................224 4.1.1. Tobamoviruses .......................................................................................................................................227 4.1.1.1. TMV CP .................................................................................................................................227 4.1.1.2. The 126 kDa Protein of TMV ....................................................................................................228 4.1.2. Potyviruses ............................................................................................................................................229 ∗Corresponding author. E-mail: [email protected] 195 196 E. WAIGMANN ET AL. 4.1.2.1. CP ..........................................................................................................................................229 4.1.2.2. HC-Pro ...................................................................................................................................230 4.1.2.3. VPg ........................................................................................................................................230 4.1.3. Umbraviruses .........................................................................................................................................231 4.2. Host Factors Involved in Systemic Movement .....................................................................................................231 4.2.1. Cellular Factors that Facilitate Viral Systemic Movement .............................................................................................................................................231 4.2.2. Cellular Factors that Restrict Viral Systemic Movement .............................................................................232 4.2.2.1. RTM Genes .............................................................................................................................232 4.2.2.2. Cell-Wall Components: cdiGRP, Callose, and β-1,3-Glucanase ....................................................232 4.3. Cellular Routes for Systemic Movement .............................................................................................................233 4.3.1. Invasion of Vasculature Through the BS-VP Cell Boundary ...............................................................................................................................................234 4.3.2. Entry into the CC/SE Complex Through the VP-CC Boundary ...............................................................................................................................................234 4.3.3. Viruses Move Differently Through Internal and External Phloem ...............................................................................................................................234 4.3.4. Virus Unloading from Phloem into Systemic Organs .................................................................................235 4.3.5. Restricted Phloem Unloading and Its Alleviation by Coinoculation with Unrelated Viruses ..................................................................................................236 5. ARABIDOPSIS THALIANA as a Model Plant to Study Virus Movement ................................................................236 6. Concluding Remarks .............................................................................................................................................237 References ..................................................................................................................................................................238 special emphasis is placed on host factors and cellular structures Propagation of viral infection in host plants comprises two dis- involved in viral transport. tinct and sequential stages: viral transport from the initially in- fected cell into adjacent neighboring cells, a process termed local or Keywords coat protein, host factors, intercellular transport, move- cell-to-cell movement, and a chain of events collectively referred to ment protein, phloem transport, plasmodesmata as systemic movement that consists of entry into the vascular tissue, systemic distribution with the phloem stream, and unloading of the virus into noninfected tissues. To achieve intercellular transport, Moveo ergo sum. viruses exploit plasmodesmata, complex cytoplasmic bridges in- —From musings of a Descartesvirus terconnecting plant cells. Viral transport through plasmodesmata is aided by virus-encoded proteins, the movement proteins (MPs), which function by two distinct mechanisms: MPs either bind vi- ral nucleic acids and mediate passage of the resulting movement 1. INTRODUCTION complexes (M-complexes) between cells, or MPs become a part of pathogenic tubules that penetrate through host cell walls and serve Studies of tobacco plants infected with Tobacco mosaic virus as conduits for transport of viral particles. In the first mechanism, (TMV) led to the recognition of viruses as plant pathogens more M-complexes pass into neighboring cells without destroying or ir- than a century ago (Beijerinck, 1898), laying the foundation for reversibly altering plasmodesmata, whereas in the second mecha- the modern science of virology. Since then, a huge variety of nism plasmodesmata are replaced or significantly modified by the plant viruses have been isolated and characterized from a mul- tubules. Here we summarize the current knowledge on both local and systemic movement of viruses that progress from cell to cell titude of agronomically important plant species. Although ge- as M-complexes in a nondestructive fashion. For local movement, nomic structures and sequences of individual plant viruses are we focus mainly on movement functions of the 30 K superfamily very diverse, the essential principles of the infection