Natural and Engineered Resistance to Plant Viruses: Part II

Natural and Engineered Resistance to Plant Viruses: Part II

by Elsevier Science

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Viruses are a huge threat to agriculture. In the past, viruses used to be controlled using conventional methods, such as crop rotation and destruction of the infected plants, but now there are more novel ways to control them. This volume focuses on topics that must be better understood in order to foster future developments in basic and applied plant virology. These range from virus epidemiology and virus/host co-evolution and the control of vector-mediated transmission through to systems biology investigations of virus-cell interactions. Other chapters cover the current status of signalling in natural resistance and the potential for a revival in the use of cross-protection, as well as future opportunities for the deployment of the under-utilized but highly effective crop protection strategy of pathogen-derived resistance.

  • Contributions from leading authorities
  • Informs and updates on all the latest developments in the field

Product Details

ISBN-13: 9780080923086
Publisher: Elsevier Science
Publication date: 06/16/2010
Series: ISSN , #76
Sold by: Barnes & Noble
Format: NOOK Book
Pages: 282
File size: 4 MB

About the Author

John P. Carr is at University of Cambridge, UK

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Volume 76 Natural and Engineered Resistance to Plant Viruses, Part II

Academic Press

Copyright © 2010 Elsevier Inc.
All right reserved.

ISBN: 978-0-08-092308-6

Chapter One

The Coevolution of Plants and Viruses: Resistance and Pathogenicity

Aurora Fraile and Fernando García-Arenal


I. Introduction 3 II. Virus Infection and Host Defenses Reciprocally Affect the Fitness of Host and Virus 4 III. The Outcome of Plant–Virus Interactions Depends on the Plant and Virus Genotypes Involved 6 IV. Genetic Variation of Resistance and Pathogenicity 13 A. Variability of resistance and pathogenicity under the gene-for-gene model 14 B. Variability of resistance and pathogenicity under the matching-allele model 18 V. Costs of Pathogenicity and Resistance Durability 20 VI. Concluding Remarks 23 Acknowledgments 24 References 24


Virus infection may damage the plant, and plant defenses are effective against viruses; thus, it is currently assumed that plants and viruses coevolve. However, and despite huge advances in understanding the mechanisms of pathogenicity and virulence in viruses and the mechanisms of virus resistance in plants, evidence in support of this hypothesis is surprisingly scant, and refers almost only to the virus partner. Most evidence for coevolution derives from the study of highly virulent viruses in agricultural systems, in which humans manipulate host genetic structure, what determines genetic changes in the virus population. Studies have focused on virus responses to qualitative resistance, either dominant or recessive but, even within this restricted scenario, population genetic analyses of pathogenicity and resistance factors are still scarce. Analyses of quantitative resistance or tolerance, which could be relevant for plant–virus coevolution, lag far behind. A major limitation is the lack of information on systems in which the host might evolve in response to virus infection, that is, wild hosts in natural ecosystems. It is presently unknown if, or under which circumstances, viruses do exert a selection pressure on wild plants, if qualitative resistance is a major defense strategy to viruses in nature, or even if characterized genes determining qualitative resistance to viruses did indeed evolve in response to virus infection. Here, we review evidence supporting plant–virus coevolution and point to areas in need of attention to understand the role of viruses in plant ecosystem dynamics, and the factors that determine virus emergence in crops.


BaMMV Barley mild mosaic virus

BaYMV Barley yellow mosaic virus

BCMV Bean common mosaic virus

BDMV Bean dwarf mosaic virus

BYDV Barley yellow dwarf virus

BYMV Bean yellow mosaic virus

CMV Cucumber mosaic virus

CYDV Cereal yellow dwarf virus

GRSV Groundnut ringspot virus

LMV Lettuce mosaic virus

MNSV Melon necrotic spot virus

PMMoV Pepper mild mottle virus

PSbMV Pea seed-borne mosaic virus

PVMV Pepper veinal mottle virus

PVX Potato virus X

PVY Potato virus Y

RRSV Raspberry ringspot virus

RYMV Rice yellow mottle virus

SMV Soybean mosaic virus

TCSV Tomato chlorotic spot virus

TCV Turnip crinkle virus

TEV Tobacco etch virus

TMV Tobacco mosaic virus

ToMV Tomato mosaic virus

TSWV Tomato spotted wilt virus

TuMV Turnip mosaic virus

ZYMV Zucchini yellow mosaic virus


Pathogens are able to infect a host and, as a result of infection, they cause damage to this host. The appropriate terminology for these two central properties of pathogens has lead to much discussion in the phytopathological literature since Vanderplank (1968) defined aggressiveness as the quantitative negative effect of a pathogen on its host and virulence as the capacity of a pathogen to infect a particular host genotype. However, in other areas of biology, including animal pathology and evolutionary biology, virulence is defined as the detrimental effect of parasite infection on host fitness (e.g., Read, 1994; Woolhouse et al., 2002), that is, virulence is related to the damage that parasite infection causes to the host, and the capacity to infect a host is named infectivity (Gandon et al., 2002; Tellier and Brown, 2007). In spite of other conventions in the phytopathological literature, the American Phytopathological Society defines pathogenicity as the ability of a pathogen to cause disease on a particular host (i.e., a qualitative property), and virulence as the degree of damage caused to the host (i.e., a quantitative property), assumed to be negatively correlated to host fitness (D'Arcy et al., 2001). These definitions are more in line with those used by other scientists interested in the biology of hosts and pathogens, and will be used in this review, except that for gene-for-gene (GFG) and matching-allele (MA) interactions we will retain the usual terminology of avirulence/virulence genes or factors.

Because pathogen infection reduces their fitness, hosts have developed different defense strategies to avoid or limit infection and to compensate for its costs (Agnew et al., 2000). In plants, the two major defense mechanisms are resistance (defined as the ability of the host to limit parasite multiplication) and tolerance (defined as the ability of the host to reduce the damage caused by parasite infection) (Clarke, 1986). Host defenses may have a negative effect on parasite fitness. Hence, hosts and parasites may modulate the dynamics and genetic structure of each other's populations, and hosts and pathogens may coevolve, defining coevolution as the process of reciprocal, adaptive genetic change in two or more species (Woolhouse et al., 2002).

Woolhouse et al. (2002) point to three conditions that are required for host–pathogen coevolution: (1) reciprocal effects of the relevant traits of the interaction (e.g., defense and pathogenicity) on the fitness of the two species (i.e., pathogens and hosts), (2) dependence of the outcome of the host–pathogen interaction on the combinations of host and pathogen genotypes involved, and (3) genetic variation in the relevant host and pathogen traits. If these three conditions are met, demonstrating coevolution requires in addition to show changes in genotype frequencies in both the host and the pathogen populations in the field (Woolhouse et al., 2002). Although it is currently assumed that plants coevolve with their pathogens, this evidence is available for few plant–pathogen systems, and derives from analysis of the interaction of plants with bacteria, fungi, and oomycetes in their natural habitats (Burdon and Thrall, 2009; Salvaudon et al., 2008). To our knowledge, analyses of genotype changes of plants and their infecting viruses in natural populations have not been reported, and there is no specific demonstration of plant–virus coevolution. However, evidence consistent with coevolution of plants and pathogens has accumulated for more than 50 years (e.g., Flor, 1971; Salvaudon et al., 2008; Thompson and Burdon, 1992), deriving in a large part from agricultural systems, and this includes a considerable body of data from plant–virus interactions. In this review, we discuss the available evidence in support of coevolution in plant–virus systems; a major goal will be to pinpoint research areas in need of attention.


Selection for resistance in plants, and for pathogenicity in viruses, would occur only if pathogenicity and resistance would negatively affect the fitness of plants and viruses, respectively. It is widely assumed that pathogen infection decreases the fitness of the infected host, that is, that pathogens are virulent, and that resistance decreases the fitness of the pathogen. However, direct evidence of these two assumptions for plants and viruses is surprisingly scarce, probably due to a limited interest till recent times of plant virologists in virulence evolution, on the one hand, and to difficulties in estimating experimentally the fitness of any organisms and linking these estimates to its evolution in nature (Kawecki and Ebert, 2004).

For animal pathogens, the effect of infection on host fitness, that is, virulence, is usually estimated as increased host mortality (Frank, 1996). This assumes that a reduction in lifespan conveys a decrease in fecundity and, hence, in fitness. But this is not obvious in many plant species, particularly domesticates, which are semelparous, that is, reproduce only once during their lives. Also, most plant pathogens do not cause an immediate increase in host mortality and their effect on host fitness depends on the pathogen life history (Barrett et al., 2008). Hence, virulence on plants is most often estimated as the effect of pathogen infection on the plant's fecundity (i.e., viable seed production) or on one of its correlates, as plant size or biomass, or even symptom severity, the most commonly used correlate of virulence (Jarozs and Davelos, 1995). However, the relationship between fecundity and biomass or symptom severity may be nonlinear and depend on both genetic and environmental factors (e.g., Pagán et al., 2007; Schürch and Roy, 2004), and this relationship has been analyzed only seldom for plant viruses (Agudelo-Romero et al., 2008; Pagán et al., 2008). Thus, the assumption that plant viruses decrease the fitness of their hosts rests mostly on the severity of the symptoms induced by virus infection on crops, and on the effects of infection on crop productivity, what may not be relevant for plant–virus coevolution. Moreover, although several reports of experiments showing that virus infection can decrease the fitness of wild plants under controlled conditions (e.g., Friess and Maillet, 1996; Kelly, 1994; Pagán et al., 2007), there is little evidence that plant viruses have any effect on plant fitness in natural ecosystems, and it has been proposed that most often viruses would be mutualistic symbionts of plants (Roossinck, 2005; Wren et al., 2006). This hypothesis rests on the interesting observation that in wild hosts growing in nonagricultural ecosystems, virus infection most often does not cause any obvious symptom, at odds with what is known to occur in crops. But estimates of the effect of virus infection on wild plants fitness are presently scarce. The negative effect of virus infection on plant fitness in nature has been best documented for BYDV and CYDV on wild grasses in California (Malmstrom et al., 2006; Power and Mitchell, 2004). Interestingly, virus infection, in addition to direct fitness costs, has important indirect costs as it may reduce the competitive ability of the infected plants, a phenomenon (apparent competition) that may also occur among genotypes of the same species (Pagán et al., 2009). Virus infection has also been shown to increase mortality and to reduce fecundity in wild cabbage in southern England (Maskell et al., 1999), and to reduce lifespan of wild pepper in its natural habitats in Mexico (our unpublished results). Other reports suggest that the effect of virus infection on the population dynamics of wild plants will vary largely according to site or population (Pallett et al., 2002). On the other hand, virus infection may be beneficial for plants, as shown by an increase of tolerance to abiotic stress in virus-infected plants as compared with uninfected controls (Xu et al., 2008), or by a decreased herbivory on tymovirus-infected Kennedia rubicunda in Australia (Gibbs, 1980). Thus, it is obvious that the effects of virus infection on plant fitness in natural ecosystems may vary largely according to the specific virus–host interaction and, probably, according to the environment, a subject that requires further attention by virologists with an interest in ecology and evolution.

For parasites, fitness is also best estimated as fecundity, that is, production of new infections per unit time (Anderson and May, 1982). However, for plant viruses, fitness is usually estimated as within-host multiplication rates (e.g., Sacristán et al., 2005) or, when different genotypes are compared, as competitive ability (e.g., Carrasco et al., 2006; Elena et al., 2006; Fraile et al., 2010). Because resistance results in a decrease of within-host virus multiplication, it is assumed that resistance decreases virus fitness. This assumption implicitly considers that rates of between-host transmission positively correlate with rates of within-host multiplication. Indeed, for viruses transmitted by aphids, both nonpersistently and persistently, it has been shown that transmission efficiency is positively correlated with virus accumulation in source tissues (Barker and Harrison, 1986; Escriu et al., 2000; Foxe and Rochow, 1975; Jiménez-Martínez and Bosque-Pérez, 2004; Pirone and Megahed, 1966). Whether or not this correlation holds for other mechanisms of horizontal transmission, or for seed transmission, remains to be analyzed.

In summary, although direct evidence is far less common than might be expected, it supports that in the case of virulent virus–plant interactions traits related to pathogenicity have a negative effect on the plant's fitness, and traits related to defense have a negative effect on the virus fitness.


For the last 50 years, different theoretical analyses aimed at understanding and modeling host–pathogen coevolution have been published. All these analyses assume that the outcome of the host–pathogen interaction is determined by the combination of host and pathogen genotypes involved. Two major models of host–parasite interaction determining the success of infection have been proposed: the GFG and the MA models, which have been applied mostly to plant and animal systems, respectively. Genetic and molecular genetic evidence support both these models to explain plant–virus interactions (Kang et al., 2005a; Maule et al., 2007; Sacristán and García-Arenal, 2007).

In plant–pathogen systems, pathogenicity has been most often related and analyzed as conforming to GFG interactions, first described in the flax–flax rust system (Flor, 1955). According to this model, the interaction of specific products of the plant and pathogen genotypes determines an incompatible interaction (Fig. 1), that is, host defenses are triggered and infection is limited. Plant proteins encoded by resistance genes (R proteins) recognize corresponding proteins of the pathogen, encoded by avirulence genes (AVR). Recognition can be either through a direct R–AVR interaction or, more often, via multiprotein interactions, including AVR–host protein complexes, modified/unmodified host targets of AVR, and/or adapter proteins that mediate binding, stabilize, or localize R (Friedman and Baker, 2007; Jones and Dangl, 2006; McDowell and Simon, 2006; Moffett, 2009). The recognition of AVR by the host triggers defense responses leading to limitation of multiplication and spread of the pathogen which remains localized at the infection site, and the resistance response is often associated to a hypersensitive response (HR), often involving localized host cell death. In the absence of the AVR allele in the pathogen or of the R allele in the host, the parasite is not recognized by the host, resistance is not triggered, and the host is infected, resulting in a compatible interaction. Accordingly, a key feature of the GFG model is that universal pathogenicity occurs, that is, there are pathogen genotypes able to infect all host genotypes (Agrawal and Lively, 2002).


Excerpted from Advances in VIRUS RESEARCH Copyright © 2010 by Elsevier Inc. . Excerpted by permission of Academic Press. All rights reserved. No part of this excerpt may be reproduced or reprinted without permission in writing from the publisher.
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Table of Contents

1. The Co-evolution of plants and viruses: Resistance and pathogenicity

Fernando García-Arenal and Aurora Fraile

2. Assessment of the benefits and risks for engineered virus resistance

Mark Tepfer and Jeremy R. Thompson

3. Signaling in Induced Resistance

John Carr, Mathew G. Lewsey and Peter Palukaitis

4. Global genomics and proteomics approaches to identify host factors as targets to induce resistance against Tomato bushy stunt virus

Peter Nagy and Judit Pogany

5. Resistance to Aphid Vectors of Virus Disease

Jack Westwood and Mark Stevens

6. Cross-protection: A century of mystery

Heiko Ziebell and John Peter Carr

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