Cucumoviruses

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Abstract

Research on the molecular biology of cucumoviruses and their plant–virus interactions has been very extensive in the last decade. Cucumovirus genome structures have been analyzed, giving new insights into their genetic variability, evolution, and taxonomy. A new viral gene has been discovered, and its role in promoting virus infection has been delineated. The localization and various functions of each viral-encoded gene product have been established. The particle structures of Cucumber mosaic virus (CMV) and Tomato aspermy virus have been determined. Pathogenicity domains have been mapped, and barriers to virus infection have been localized. The movement pathways of the viruses in some hosts have been discerned, and viral mutants affecting the movement processes have been identified. Host responses to viral infection have been characterized, both temporally and spatially. Progress has been made in determining the mechanisms of replication, gene expression, and transmission of CMV. The pathogenicity determinants of various satellite RNAs have been characterized, and the importance of secondary structure in satellite RNA-mediated interactions has been recognized. Novel plant genes specifying resistance to infection by CMV have been identified. In some cases, these genes have been mapped, and one resistance gene to CMV has been isolated and characterized. Pathogen-derived resistance has been demonstrated against CMV using various segments of the CMV genome, and the mechanisms of some of these forms of resistances have been analyzed. Finally, the nature of synergistic interactions between CMV and other viruses has been characterized. This review highlights these various achievements in the context of the previous work on the biology of cucumoviruses and their interactions with plants.

Introduction

Considerable advances have been made in our understanding of the molecular biology and biochemistry of the cucumoviruses since they were last reviewed in detail (Edwardson and Christie, 1991). While most of the progress concerning gene functions and molecular mechanisms has been made with Cucumber mosaic virus (CMV), there have also been many advances made with Peanut stunt virus (PSV) and Tomato aspermy virus (TAV). The research results and conclusions include the following: (a) The nucleotide sequences of several strains of all three viruses have been obtained and their taxonomic relationships have been clarified, if not made simpler. (b) Hybrid viruses created within and between these viral species have enabled the delineation of the roles of gene products in various functions. (c) A new interspecies hybrid cucumovirus has been described. (d) Recombination was demonstrated to occur during cucumovirus evolution. (e) The role of recombination and pseudorecombination in CMV epidemiology has been examined. (f ) Defective RNAs and new subgenomic RNAs have been identified and characterized. (g) A new gene has been discovered in the genome of cucumoviruses, and some of its functions have been determined, including a role in suppressing gene silencing. (h) The roles of various viral gene products in replication and movement have been discerned. (i) The subcellular site of CMV replication has been determined. ( j) The subcellular location of the CMV movement protein has been delineated. (k) Promoter sequences for CMV replication have been mapped, as have promoter sequences for subgenomic RNA production. (l) Transgenic plants have been generated expressing various viral sequences used to engender resistance to virus infection. (m) Transgenic plants expressing viral genes have also been used for the complementation of viral gene functions or to determine viral gene functions. (n) Viral sequences involved in pathogenicity and host range have been identified and mapped. (o) The three-dimensional structures of the CMV and TAV particles have been resolved. (p) The topography of various epitopes on the surface of virions has been identified. (q) Sequences in the capsid protein important for the aphid transmission of CMV and various host interactions have been identified and mapped to the particle structure. (r) The interactions between CMV and other viruses in synergy have been characterized. (s) Progress has been made on identifying new genes for resistance to CMV and mapping such resistance genes, and one gene conferring resistance to CMV has been isolated and characterized. (t) The spatial and temporal dynamics of host enzyme activities during local virus infection has been analyzed. (u) Downregulation and upregulation of the expression of various host gene have been observed. (v) Secondary structures have been analyzed for three satellite RNAs of CMV. (w) Sequences and⧸or potential structures important in satellite-mediated pathogenicity have been identified.

This review describes and comments on these various discoveries and experimental observations. We will attempt to place this information into perspective, but will not again cover data reviewed previously in detail. We refer the reader to extensive reviews on the basic biology and physical properties of all three cucumoviruses (Edwardson 1991, Kaper 1981), as well as the biology and molecular biology of CMV (Palukaitis et al., 1992). We also refer the reader to a more extensive recent review on the functions and properties of CMV satellite RNAs (García-Arenal and Palukaitis, 1999). We will only cover such previously reviewed information here if it is essential for introduction or if earlier conclusions are no longer believed to be correct. It is hoped that readers with varying interests will find this review useful in itself, as well as a supplement to previous reviews.

CMV, PSV, and TAV are the three viruses presently admitted as species of the genus Cucumovirus, in the family Bromoviridae (van Regenmortel et al., 2000). Although superfamilies have no official status in the taxonomy of plant viruses, the family Bromoviridae is often referred to as being in the alphavirus-like or Sindbis virus-like superfamily. Other putative members of the genus Cucumovirus listed in the literature include Cowpea banding mosaic virus (Sharma and Varma, 1975), Cowpea ringspot virus (Phatak 1974, Phatak 1976), and Bean distortion mosaic virus (White et al., 1995a). Because the first two of these viruses have not been characterized molecularly and there do not appear to be any reports concerning these viruses since they were last reviewed (Edwardson and Christie, 1991), we will not mention them further here. The last virus is a natural pseudorecombinant between CMV and TAV (see Section VII,B). Thus, this review is confined to CMV, PSV, and TAV, with most of the data coming from CMV.

Section snippets

Particle Structure

Cucumoviruses have icosahedral particles with a T = 3 quasisymmetry (Finch 1967, Francki 1966). Particles are 29 nm in diameter, have 180 capsid protein subunits, and consist of about 18% RNA (Finch 1967, Francki 1980, Habili 1974a, Kaper 1974). Particles of CMV and TAV (Habili and Francki, 1974a), or of all three cucumoviruses (Tolin, 1977), are indistinguishable morphologically and have a similar physical and chemical composition. CMV and TAV particles differ in their stability after exposure

Protein Functions

The five proteins encoded by CMV have been analyzed for various functions. Most of this work has been at the genetic level, but some of the studies have been done using purified proteins.

Replicase Composition, Architecture, and Localization

The CMV replicase is membrane bound (Jaspars et al., 1985) and contains viral-encoded as well as host-encoded components (Hayes and Buck, 1990). There are at least three components, and probably more. These include the CMV 1a and 2a proteins, as well as a host protein of 50 kDa (Hayes and Buck, 1990). In addition, proteins of 100, kDa 50, and 32 kDa were found to bind to the 3′-terminal sequences of (−) stand RNA of CMV (Hayes et al., 1994a). The roles of the various host proteins in the

Virus Movement

Although many aspects of the basis of movement have been ascertained, there are many complexities still to unravel. These include what host factors are involved in cell-to-cell and long-distance movement, as well as the nature of the barriers to these processes. There are also a number of inconsistencies that have been observed in studies on cucumovirus movement, which will be mentioned, as they exemplify the complexity of the processes involved in virus movement.

Host-Derived Resistance

Resistance to infection by CMV and PSV has been described for a number of plants species (reviewed by Edwardson 1991, Fraser 1986, Fraser 1990). In many cases, the resistance was multigenic, and recessive, but usually was not characterized further (e.g., Caranta 2002, Chaim 2001, Grube 2000). In other cases, the phenotype was better characterized, but virtually nothing is known about the genetics of resistance (Celebi 1998, Dufour 1989, Gal-On 2000, Kobori 2000, Lakshman 1985, Roossinck 1991,

Genetic Diversity and Taxonomy

Data on host range, symptomatology, immunology, and molecular analysis of the genomic RNAs demonstrate that isolates of CMV are extremely heterogeneous. This led to the early classification of CMV strains into two subgroups based on different criteria (reviewed in Palukaitis et al., 1992), now named subgroup I and subgroup II according to molecular analyses of the genomic RNAs (Owen and Palukaitis, 1988). The percentage identity in the nucleotide sequence between pairs of isolates belonging to

Support Specificity, Sequences, and Structure

Cucumoviruses are helper viruses of small, linear, single-stranded satellite RNAs that depend on the helper viruses for their replication, encapsidation, and transmission. Satellite RNAs have been found in association with isolates of CMV and PSV. Neither CMV–satellite RNAs nor PSV–satellite RNAs can be maintained by the heterologous helper viruses. No satellite RNAs have been found in association with TAV isolates; however, TAV can be a helper virus for CMV–satellite RNAs, but not

Synergy with Other Viruses

Synergy is the interaction between two viruses resulting in a worse disease than caused by infection with either virus alone. In a synergistic interaction, there is usually an increase in the accumulation of one of the interacting viruses. Cucumoviruses have been shown to be involved in various forms of synergy. In some cases, such as in cowpea stunt disease and in a severe mosaic disease of radish, CMV and a potyvirus [Blackeye cowpea mosaic virus (BICMV) and Turnip mosaic virus (TuMV),

Future Prospects

A perusal of this review makes it quite apparent where the bulk of progress has been made in the last decade. Areas still in need of considerable research include, but are not limited to, the mechanisms of seed and aphid transmission, the nature of host components involved in various interactions leading to infection, resistance or pathogenicity, and the mechanisms of cell-to-cell movement and resistance breakage. New sources of resistance to virus infection, disease, or the vector will

Acknowledgements

This review is dedicated to Robert H. Symons for his many contributions to plant virology and, in particular, for his pioneering work on the molecular biology and biochemistry of CMV. We thank Aurora Fraile for preparing Table I, Table IV and Fig. 2. We also thank various colleagues for their unpublished data referred to here. Unpublished work in the laboratory of FGA was supported by Grant BIO99-1121-C02-02, Ministerio de Ciencia y Tecnología, Spain. Unpublished work in the laboratory of PP

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