Roles for host factors in plant viral pathogenicity

https://doi.org/10.1016/j.pbi.2004.04.006Get rights and content

Abstract

The simple, obligate nature of viruses requires them to usurp or divert cellular resources, including host factors, away from their normal functions. The characterization of host proteins, membranes, and nucleic acids that are implicated in viral infection cycles, together with other recent discoveries, is providing fundamental clues about the molecular bases of viral susceptibility. As viruses invade susceptible plants, they create conditions that favor systemic infections by suppressing multiple layers of innate host defenses. When viruses meddle in these defense mechanisms, which are interlinked with basic cellular functions, phenotypic changes can result that contribute to disease symptoms.

Introduction

As obligate intracellular parasites, viruses are intimately associated with and completely dependent on the host cellular milieu. This dependency requires viral proteins and nucleic acids to divert resources, including host factors, away from their normal functions. Typical plant viruses encode 4–10 gene products that coordinate the complex biochemistry and intermolecular interactions required for infection cycles, which involve the steps of replication, cell–cell movement, and systemic movement [1]. A challenge for plant virologists has been to identify specific cellular factors that contribute to susceptibility and disease symptoms.

Host proteins, membranes, and nucleic acids that are involved in infection cycles and their explicit roles in viral pathogenicity are being revealed through the development and use of model host systems, host genetics, and functional genomics, in combination with other molecular-genetic, biochemical, and cell-biological methods. The discovery of each new host factor provides clues about the molecular bases of susceptibility and/or symptomatology. An emerging theme is that the cellular events within each step and between steps in an infection cycle are highly orchestrated and interlinked. Some factors are required for basic compatibility, whereas others appear to modulate infections by being involved in competition for resources, by degrading viral RNA (i.e. by RNA interference [RNAi]), or by shutting-off host translation or a hypersensitive response mediated by resistance genes. RNAi and shut-off of host translation are prevented through the direct action of viral proteins 2., 3.••, whereas resistance genes may be overcome through passive means such as spontaneous mutation or genetic diversity. The ‘collateral damage’ inflicted on hosts as viruses invade rapidly growing tissues is reflected in characteristic changes in plant phenotype (i.e. the symptoms). Molecular events that may be associated with symptoms include changes in the spatial and temporal patterns of host gene expression at various stages of infection 4.•, 5., 6., 7., 8., 9., 10., 11., 12., as well as the suppression of RNAi mechanisms that control growth and development 13.••, 14..

In this review, we highlight recent advances that have provided functional evidence for the involvement of specific host factors in one or more aspects of viral pathogenicity (summarized in Table 1). For recent in-depth reviews on the steps of viral infection cycles, readers are referred to 15.•, 16.•, 17., 18., 19..

Section snippets

Virus translation and replication

A paradoxical problem for (+)-stranded RNA viruses is that their genomes are templates for both translation and replication. Balanced control of these seemingly inextricable processes is achieved through cis- and trans-acting signals and factors. For some viruses, this conflict might be resolved by the base-pairing of specific RNA sequences that are embedded in their RNA genomes 20., 21.. It is not yet known whether intramolecular interactions such as base-pairing are sufficient to maintain a

Virus movement

Cell–cell and systemic trafficking of viral genomes involves the host cytoskeleton and membranes 17., 18.. Here, we focus on the recent identification of other host factors that are potentially involved in the movement of TMV and potato virus X (PVX). The 30K MP of TMV is responsible for gating plasmodesmata and translocating viral genomes to new cells. A cell periphery ER-membrane protein NtNCAPP (Nicotiana tabacum NON-CELL-AUTONOMOUS PATHWAY PROTEIN) selectively controls the translocation of

Viral pathogenesis/host responses

Understanding the molecular mechanisms that underlie the onset of disease symptoms has remained an elusive goal of plant virologists, but these mechanisms are now being associated with ways in which host functions are being subverted. The fact that both viruses and viroids induce diseases demonstrates that nucleic acids themselves, as well as proteins, are sufficient to cause symptoms. Interestingly, the severity of symptoms is not necessarily linked to pathogen titer, indicating that disease

Conclusions

Major advances in identifying host factors that are involved in viral pathogenicity are being aided by the use of model systems, host genetics, advances in cell biology, and yeast two-hybrid interaction cloning combined with functional genomics. These host factors are either directly involved in the steps of viral infection or are targeted to create conditions that are optimal for sustained systemic infections, often resulting directly in the onset of symptoms. There is much more to learn, as

Note added in proof

Dunoyer et al. [75] recently performed a comparative analysis of the functions of five distinct viral suppressors of RNA silencing. Particularly relevant to this review was their observation that the three silencing suppressors that caused noticeable developmental defects when expressed in Arabidopsis also prevented the cleavage and degradation of endogenous miRNAs. In contrast, all five suppressors were able to block the silencing of a chalcone synthase gene whose silencing is mediated by

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • of special interest

  • ••

    of outstanding interest

Acknowledgements

We thank Barbara Baker for helpful discussion and reading the manuscript. This work was supported by Hatch Act and State of Iowa Funds, the US Department of Agriculture — National Research Initiative (02-35319-12566), the Iowa Soybean Promotion Board, and the Iowa State University Plant Sciences Institute.

References (75)

  • R Anandalakshmi et al.

    A viral suppressor of gene silencing in plants

    Proc Natl Acad Sci USA

    (1998)
  • R Anandalakshmi et al.

    A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants

    Science

    (2000)
  • S Boutet et al.

    Arabidopsis HEN1: a genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance

    Curr Biol

    (2003)
  • T.G Lee et al.

    The 58,000-dalton cellular inhibitor of the interferon-induced double-stranded RNA−activated protein kinase (PKR) is a member of the tetratricopeptide repeat family of proteins

    Mol Cell Biol

    (1994)
  • M Gale et al.

    Regulation of interferon-induced protein kinase PKR: modulation of P58IPK inhibitory function by a novel protein, P52rIPK

    Mol Cell Biol

    (1998)
  • L Hao et al.

    Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase

    Plant Cell

    (2003)
  • Hull R: Matthews’ Plant Virology, edn 4. London: Academic Press;...
  • A Maule et al.

    The dialogue between viruses and hosts in compatible interactions

    Curr Opin Plant Biol

    (2002)
  • M.A Aranda et al.

    Induction of HSP70 and polyubiquitin expression associated with plant virus replication

    Proc Natl Acad Sci USA

    (1996)
  • C Geri et al.

    Altered patterns of gene expression in Arabidopsis elicited by cauliflower mosaic virus (CaMV) infection and by a CaMV gene VI transgene

    Mol Plant Microbe Interact

    (1999)
  • M Escaler et al.

    Pea embryonic tissues show common responses to the replication of a wide range of viruses

    Virology

    (2000)
  • Z Havelda et al.

    Complex spatial responses to cucumber mosaic virus infection in susceptible Cucurbita pepo cotyledons

    Plant Cell

    (2000)
  • S.A Whitham et al.

    Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants

    Plant J

    (2003)
  • S Golem et al.

    Tobacco mosaic virus induced alterations in the gene expression profile of Arabidopsis thaliana

    Mol Plant Microbe Interact

    (2003)
  • K.D Kasschau et al.

    P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction

    Dev Cell

    (2003)
  • J.C Carrington et al.

    Role of microRNAs in plant and animal development

    Science

    (2003)
  • P Ahlquist et al.

    Host factors in positive-strand RNA virus genome replication

    J Virol

    (2003)
  • S.Y Morozov et al.

    Triple gene block: modular design of a multifunctional machine for plant virus movement

    J Gen Virol

    (2003)
  • M Heinlein

    The spread of tobacco mosaic virus infection: insights into the cellular mechanism of RNA transport

    Cell Mol Life Sci

    (2002)
  • S.G Lazarowitz et al.

    Viral movement proteins as probes for intracellular and intercellular trafficking in plants

    Plant Cell

    (1999)
  • J.K Barry et al.

    A-1 ribosomal frameshift element that requires base pairing across four kilobases suggests a mechanism of regulating ribosome and replicase traffic on a viral RNA

    Proc Natl Acad Sci USA

    (2002)
  • J Pogany et al.

    A replication silencer element in a plus-strand RNA virus

    EMBO J

    (2003)
  • A.O Noueiry et al.

    Yeast Lsm1p-7p/Pat1p deadenylation-dependent mRNA-decapping factors are required for brome mosaic virus genomic RNA translation

    Mol Cell Biol

    (2003)
  • D.R Gallie

    Translational control of cellular and viral mRNAs

    Plant Mol Biol

    (1996)
  • D.R Gallie

    The 5′-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F

    Nucleic Acids Res

    (2002)
  • A Duprat et al.

    The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses

    Plant J

    (2002)
  • A.D Lellis et al.

    Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection

    Curr Biol

    (2002)
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