Virus Research 92 (2003) 207 Á/212 www.elsevier.



Resistance mechanisms to plant viruses: an overview
Rob Goldbach *, Etienne Bucher, Marcel Prins
Laboratory of Virology, Wageningen University, Binnenhaven 11, PD-6709 Wageningen, The Netherlands Received 3 September 2002; received in revised form 3 December 2002; accepted 4 December 2002

Abstract To obtain virus-resistant host plants, a range of operational strategies can be followed nowadays. While for decades plant breeders have been able to introduce natural resistance genes in susceptible genotypes without knowing precisely what these resistance traits were, currently a growing number of (mostly) dominant resistance genes have been cloned and analyzed. This has led not only to a better understanding of the plant’s natural defence systems, but also opened the way to use these genes beyond species borders. Besides using natural resistance traits, also several novel, ‘‘engineered’’ forms of virus resistance have been developed over the past 15 years. The first successes were obtained embarking from the principle of pathogen-derived resistance (PDR) by transforming host plants with viral genes or sequences with the purpose to block a specific step during virus multiplication in the plant. As an unforeseen spin-off of these investments, the phenomenon of post-translational gene silencing (PTGS) was discovered, which to date is by far the most successful way to engineer resistance. It is generally believed that PTGS reflects a natural defence system of the plant, and part of the hypothesized components required for PTGS have been identified. As counteracting strategy, and confirming PTGS to be a natural phenomenon, a considerable number of viruses have acquired gene functions by which they can suppress PTGS. In addition to PDR and PTGS, further strategies for engineered virus resistance have been explored, including the use of pokeweed antiviral protein (PAP), 2?,5?-oligoadenylate synthetase and ‘‘plantibodies’’. This paper will give a brief overview of the major strategies that have become operational during the past 10 years. # 2003 Elsevier Science B.V. All rights reserved.
Keywords: Pathogen-derived resistance; Hypersensitive response; Post-transcriptional gene silencing

1. Introduction As in many years of the past, plant viruses are still forming a major problem in the cultivation of many vegetable and ornamental crops throughout the world. For long times, these pathogens have been controlled using conventional measures like crop rotation and other cultivation techniques, early detection, destruction of infected source plants, cross-protection, breeding for resistance, and chemical control of their vectors (Bos, 2000; Hull, 2002). Increased knowledge of both the molecular genetics of plant viruses and, more recently, also of their hosts’ natural defence systems have resulted in the development of a number of novel ways to control virus diseases in plants. This paper presents a brief overview of novel insights in the natural defence mechanisms of plants to viruses as
* Corresponding author. E-mail address: (R. Goldbach).

well as some technologies to control viruses by exploiting this knowledge. Special reference will be made throughout this paper to recent reviews in which these issues have been covered in a much more detailed way, and which are recommended to the reader for further reading.

2. Natural resistance to plant viruses Besides passive defence based on the presence of existing barriers like the rigid cell wall, plants exhibit active defence mechanisms upon recognition of pathogens such as viruses. The most common mechanism associated with active defence is the so-called hypersensitive response (HR), during which cells surrounding the primary infection site of the virus die due to a rapidly induced programmed cell death, which results in a visible necrotic local lesion. The induction of this response is preceded by a specific recognition of the

0168-1702/03/$ - see front matter # 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0168-1702(02)00353-2

e. PVX. For a number of R genes. Engineered resistance to plant viruses 3. Audy et al. For a number of RNA viruses. which can only be overcome at extremely high inoculation pressure or inoculation with unencapsidated viral RNA. / Virus Research 92 (2003) 207 Á/212 virus. the tomato Sw -5 gene conferring resistance to a number of tospoviruses. 1996. 1993. This can either be a (putative) coiled-coil (CC) domain (CC-NB-LRR)..g. Baulcombe. Baulcombe. 1996). This concept was first launched by Sanford and Johnson (1985) as proposed broad application of pathogen-derived genes in generating specific host resistance. Goldbach et al. with homology to the intracellular signaling domains of the Drosophila Toll and the mammalian interleukin (IL)-1 receptors (TIR-NB-LRR). A pre-requisite for the use of PDR is of course that none of the approaches should interfere with essential host functions. it has been shown that host plants transgenically expressing their CP results in high levels of operational resistance (reviewed in a. including TMV.o. LRR domains have been shown to function in protein Á/protein binding. An additional feature of R genes appears to be that they are always a part of a gene cluster of homologues. Comparative analysis of the growing number of R genes indicate that these have evolved from ancient gene families by duplication. all R genes identified so far in a range of different model and crop species. under . a leucine zipper domain (LZ-NB-LRR) or a so-called TIR domain. Lomonossoff. a sub-division can be made on basis of the N-terminal domain. e. A few examples of R gene products are summarized in Table 1. and these have been proven excellent candidates for developing host resistance based on PDR. Kajava. Lapidot et al. they encode specific genes essential for these processes. Wilson. R genes) and the virus (avirulence genes). 1998). Strikingly. It is tempting to assume that the R gene products directly or indirectly interact with other (host or virus-encoded) factors. The availability of cloned R genes not only will lead to further unraveling of the working mechanisms of the natural defence systems in plants but also achieve their use across species borders. but this still needs to be demonstrated. Within the large class of NB-LRR resistance genes. it has been shown that it is functional in other host plants (Spassova et al. encode proteins which can be categorized into only five classes (for a recent review. 1995. 1994.1.208 R. The largest class of R genes encodes a so-called nucleotide-binding site plus leucine-rich repeat (NBLRR) type of protein. the significance of which being not yet understood. as they are all Table 1 Selected set of dominant resistance (R) genes against viruses and other pathogens R gene Prf Mi Rx HRT Sw -5 12c Bs2 Mla 1 N RPS4 Cf9 Plant Tomato Tomato Potato Arabidopsis Tomato Tomato Pepper Barley Tobacco Arabidopsis Tomato Pathogen P. and in many cases this is based on matching (dominant) gene products of the plant (produced from dominant resistance genes. 1994. 1992.. So far all R genes that have been isolated conferring resistance to viruses belong to this class. invading viruses. AlMV. Beachy. Pathogen-derived resistance As (plant) viruses have small genomes. The same holds for the NB domain. functional studies need to be done to understand how these R gene products act. see Dangl and Jones. 1994.. 1993. CMV and TRV. despite the wide range of pathogen taxa (varying from virus. syringae Meloidogyne incognita PVX TCV TSWV Fusarium oxysporum Xanthomonas campestris Blumeria graminis TMV P. peptide Á/ ligand binding or protein Á/carbohydrate interaction (Jones and Jones. Clearly. syringae Cladosporium fulvum Type LZ-NB-LRR LZ-NB-LRR LZ-NB-LRR LZ-NB-LRR LZ-NB-LRR NB-LRR NB-LRR CC-NB-LRR TIR-NB-LRR TIR-NB-LRR LRR-TM inter-related irrespective of which type of plant pathogen they act.. which suggests these R gene products to bind GTP or ATP. these pathogens are suitable targets for engineered resistance concepts based on the principle of pathogen-derived resistance (PDR). containing only a limited number of genes of which nowadays most functions during the viral replication cycle have been well elucidated. encapsidation of their genome. spread from the original infection site through the host and through the environment. Since viruses require replication of their genome and. 1997). Most successful and widely applied has been the exploitation of plant viral coat protein (CP) genes. and trigger an effective response to. the function of these related homologues having mostly remained unclear to date. In other types of protein. Other successful approaches for achieving PDR have been the transformation of host plants with cDNA copies of symptom-suppressing satellites and with mutagenized movement protein (MP) or replicase subunits (Anderson et al. To date a few dozen single dominant R resistance genes recognizing different categories of plant pathogens have been cloned and sequenced. 2001). thus achieving CP-mediated resistance. bacterium. fungi to nematode and insect pathogens). Palukaitis and Zaitlin. 2001). Although the various strategies have been shown to be successful. subsequent mutation and recombination.g. 3. The latter finding supported the idea that CP-mediated resistance is based on blocking the disassembly of the infecting virus due to the presence of transgenically expressed CP.

1990... Hence. 2000. Indeed.. Sobemovirus Complete 1999) TBSV (Voinnet et al. while this is also true in case of an RNA virus infection where dsRNA is formed as replication intermediates. The model also accommodates data generated by genetic screens of Arabidopsis by which some factors involved in RNA silencing have been identified (Mourrain et al. 2001). Canto et al. In addition. a Dicer-like dsRNAse. 1994). 1. Next it was proposed by Lindbo et al.. 2002) CMV (Brigneti et al. instead. 21 Á/23 nt long RNA fragments are formed. The dsRNA produced in either way form a trigger to recruit further components required for sequence-specific breakdown of the transgenic RNA. Moreover. in which only low levels of transgenic viral RNA accumulated.. while genetic screens in Arabidopsis confirmed a crucial involvement in PTGS (in case of single copy sense transgenes). it was frequently found in control experiments using untranslatable versions of viral genes (initially included to serve as negative controls) that similar levels Table 2 Known silencing suppressing plant viruses Virus ACMV (Voinnet et al.. 1994. At least in plants. a desired high level of transgenic expression of viral genes. suppress this silencing. revealed that indeed in the resistant plant lines the transgenic RNA was rapidly broken down in a sequence-specific manner. Dalmay et al. To date transgenic resistance against virtually all major plant viruses.2. Transgenically expressed ssRNA is first copied into short dsRNA during a surveillance/amplication process in which a host-encoded RNA-dependent RNA polymerase (RdRP) is involved.R. 2001). while. Hence. exhibited the highest levels of resistance. A very strong argument pointing toward the natural role of RNA silencing in antiviral defence is the presence of plant viral gene products that. and more recently in some animal species. it has been shown that recombination may occur between transgenically expressed viral RNA transcripts and infecting viral genomes (Greene and Allison. i. it was frequently observed that transgenic plant lines. Further studies. it can be activated in the plant against virtually any virus species.e. the mechanism of a natural resistance gene was found to be based on RNA silencing (Covey et al.. also known as RNA silencing refers to related processes of post-transcriptional control of gene expression found in plants and fungi. transgenes with no sequence homology to the host’s genome can trigger RNA silencing and may do so in a very efficient way. Indeed under laboratory conditions. Such RdRPs have indeed been identified in various plant species (Schiebel et al. 1998) Potyvirus Complete RHBV (Bucher et al. These small interfering (si)RNAs probably also play a role in the systemic signal which is spread . 3. PTGS was first discovered in transgenic petunia plants in which introduced gene copies of the chalcon synthetase gene together with the endogenous gene copy were co-ordinately (co-)suppressed (Van der Krol et al.e. evidence has accumulated that PTGS in plants in fact acts as a natural antiviral defence system by surveying for aberrant RNAs such as double-stranded viral replication intermediates.. A success story worthwhile mentioning has been the control of papaya ringspot virus on Hawaii by the use of transgenic papaya (Ferreira et al. 2003) Tenuivirus Complete RYMV (Voinnet et al. in turn... has been reported. while ssRNA targets are broken down by the so-called RISC-like nuclease complexes. (1993) and Dougherty et al. so far transgenic crop plants expressing (parts of) functional genes or genome parts of plant viruses have not been widely introduced due to legislation problems related to biosafety issues. has been overcome by introducing transgenic virus resistance based on ‘‘co-suppression’’ or post-transcriptional gene silencing (PTGS). as a product of PTGS typically small. i. in different systems.. 2002) Pecluvirus Complete PVX (Voinnet et al. i.. Goldbach et al. without the involvement of an RdRP. (1994) as mechanism to explain a number of unexpected outcomes of experiments where virus resistance based on PDR was originally aimed. 1998). Transgenes with inverted repeats may directly produce dsRNA. 2000.e.. plant lines with high accumulating levels of transgenic RNA were poor performers. 1999) Tombusvirus Complete TSWV (Bucher et al. 2002). The PTGS defence system acts remarkably efficient and works very broad. 2002) BWYV (Pfeffer et al. antiviral defence system. / Virus Research 92 (2003) 207 Á/212 209 greenhouse and field conditions. 2000) Potexvirus Partial/systemic PVY (Brigneti et al. and involving suppression of foreign genetic elements such as viruses and transposons through a specific RNA breakdown mechanism. PTGS serves as an adaptive. Although originally found in transgenic plants producing foreign or aberrant RNA.. 2003) Tospovirus Complete of transgenic resistance could be obtained. 1990). Napoli et al.. which also serve as sequence-specific targeting complexes due to the incorporation of 21 Á/23 nt short interfering RNAs (siRNAs).. indiscriminate of the nature of their genome (RNA or DNA). PTGS. 1998) Genus Begomovirus Hordeivirus Polerovirus Cucumovirus Suppression Protein AC2 gb P0 2b ? P15 P25 HcPro NS3 P1 P19 NSs Complete Complete Complete Partial/systemic CPMV (Voinnet et al.. 1999) BSMV (Yelina et al.. Post-transcriptional gene silencing as mean to achieve virus resistance One of the major drawbacks of true PDR. 1999) Comovirus Partial PCV (Dunoyer et al. A simplified model to explain how PTGS results in virus resistance and how it can be enhanced by transgene expression is presented in Fig...

General model for gene silencing in plants induced by viruses and transgenes. Goldbach et al. 2002). 1993). Voinnet et al. The mechanism by which the antibody conferred resistance remained unanswered. Plantibodies The use of full size antibodies or antibody fragments can be an attractive addition to the palette of virus resistance strategies.o. and this might have been due to a few bottlenecks intrinsic to the approach. PTGS has been reported in animals.3..3. it is not at all a surprise that these viruses can encode a counteracting activity. Already in 1993. elegans ) and flies (Drosophila ). Other strategies 3. nor does it lead to the presence of transgenic RNA. and which may act stronger or weaker on specific parts of the pathway.210 R. Baulcombe. fungi. Indeed PTGS-based resistance does not involve the transgenic production of functional viral genes or proteins. 3.. As already mentioned above. 1998. the finding that plant viruses encode such suppressors is consistent with the idea that RNA silencing operates as an innate antiviral defence mechanism. high expression . nematodes and insects. 1999. First of all. 1998. a. Dunoyer et al. in nematodes (C. 2002).. 1998. 2002). i. Cartoons of known and putatively involved genes are presented in the box with their homologues in plants.e. More recently. Suppressors of silencing are often identified in silencing reversal assays. using silenced GFP transgenic plants (Brigneti et al. see Voinnet. 1996.1. but where a possible antiviral role still needs to be substantiated (Fire et al. rather than being a mechanism to control host gene expression (for recent reviews. Table 2 gives an overview of viruses that have been shown to produce such a suppressor protein. Since 1993. As PTGS results in well-fragmented RNA. which might become engaged in RNA recombination events. One of the best studied suppressors of RNA silencing is the helper componentprotease (HCPro) encoded by potyviruses (see also the contribution of V. it has been demonstrated that transgenic expression of a singlechain (scFv) antibody against the CP of Artichoke mottle crinkle virus results in reduced susceptibility to the virus (Tavladoraki et al. a ‘‘suppressor of gene silencing’’. as high levels of expressed antibodies form a pre-requisite for success. it might be argued that transgenic resistance against viruses based on this mechanism fulfils more easily the current high demands with respect to biosafety. 2000). Vance in this issue). Schillberg et al. only limited progress appears to have been made (Fecker et al. 1.. As plant-infecting viruses have to deal with PTGSbased defence mechanisms. Distinct viruses may specify suppressors which target distinct steps in the silencing reaction. Kennerdell and Carthew. through the plant.. 2001.. Plasterk.. / Virus Research 92 (2003) 207 Á/212 Fig. where it has been shown to be involved in genome defence against transposable elements. often referred to as ‘‘plantibody’’ technology. but since this first publication different research groups have tried to optimize this approach.

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