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Breeding Virus Resistant Potatoes (Solanum Tuberosum): a Review of Traditional and Molecular Approaches

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Breeding Virus Resistant Potatoes (Solanum Tuberosum): a Review of Traditional and Molecular Approaches Heredity 86 (2001) 17±35 Received 22 December 1999, accepted 20 September 2000 Breeding virus resistant potatoes (Solanum tuberosum): a review of traditional and molecular approaches RUTH M. SOLOMON-BLACKBURN* & HUGH BARKER Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, Scotland, U.K. Tetraploid cultivated potato (Solanum tuberosum) is the World's fourth most important crop and has been subjected to much breeding eort, including the incorporation of resistance to viruses. Several new approaches, ideas and technologies have emerged recently that could aect the future direction of virus resistance breeding. Thus, there are new opportunities to harness molecular techniques in the form of linked molecular markers to speed up and simplify selection of host resistance genes. The practical application of pathogen-derived transgenic resistance has arrived with the ®rst release of GM potatoes engineered for virus resistance in the USA. Recently, a cloned host virus resistance gene from potato has been shown to be eective when inserted into a potato cultivar lacking the gene. These and other developments oer great opportunities for improving virus resistance, and it is timely to consider these advances and consider the future direction of resistance breeding in potato. We review the sources of available resistance, conventional breeding methods, marker-assisted selection, somaclonal variation, pathogen-derived and other transgenic resistance, and transformation with cloned host genes. The relative merits of the dierent methods are discussed, and the likely direction of future developments is considered. Keywords: breeding, host gene, potato virus, resistance, review, transgenic. The viruses whether the infection is primary (current season infec- tion) or secondary (tuber-borne). The potato viruses discussed in this paper (and their PLRV is probably the most damaging and widespread abbreviations) are listed in Table 1. For a more com- virus of potato and is found wherever potato crops are prehensive list, including symptoms, see Jeries (1998). grown. PVY is next in importance and although it tends Most of these viruses cause yield losses, which vary to cause less damage than PLRV in some cultivars, it can between cultivars. Some also cause tuber defects, which cause severe damage in others (Beemster & Rozendaal, can render the tubers unsaleable, including: spraing 1972), and isolates of the PVYNTN subgroup cause severe (necrotic arcs or rings in or on the tubers) resulting from symptoms. PVY is also widespread, and in some parts of TRV or PMTV; potato tuber necrotic ringspot disease Europe it is more common than PLRV. The viruses PVA resulting from PVYNTN; net necrosis resulting from and PVV are related to PVY, but are less commonly PLRV in a few cultivars and deformed tubers resulting reported. PVA occurs worldwide (except for the Andes) from PSTVd. Symptom severity also depends on and causes symptoms that range from very mild to fairly severe. PVV is relatively restricted in its distribution, and *Correspondence. E-mail: [email protected] tends to cause few symptoms. PVX occurs worldwide and is also important, although its symptoms tend to be Abbreviations: AFLP, ampli®ed fragment length polymorphism; [a/s], mild. However, mixed infections with PVX and other antisense; cDNA, complementary DNA; CP, coat protein; CPMR, viruses are very damaging. Other viruses that we shall coat protein-mediated resistance; CSIRO, Commonwealth Scienti®c and Industrial Research Organization, Australia; dsRNA, double- consider, such as PVS, PVM, TRV and PMTV, tend to stranded RNA; ELISA, enzyme-linked immuno-sorbent assay; ER, be locally important. For example, PMTV seems to be extreme resistance; GM, genetically modi®ed; HC-Pro, helper compo- restricted to areas with cooler climates such as the nent proteinase; HR, hypersensitive resistance; ORF, open reading Andean region of South America, Canada, China, Japan frame; PAP, pokeweed antiviral protein; PTGS, post-transcriptional and Northern Europe. TRV is prevalent in light sandy gene silencing; QTL, quantitative trait locus; [s], sense; SSR, simple soils that favour the trichodorid nematode vectors. sequence repeat; TGB, triple gene block; wt, wild type. Ó 2001 The Genetics Society of Great Britain. 17 18 R. M. SOLOMON-BLACKBURN & H. BARKER Table 1 The potato viruses mentioned in this paper Virus Abbreviation Genus Means of transmission Potato leafroll virus PLRV Polerovirus aphid ± persistent Potato virus Y PVY Potyvirus aphid ± nonpersistent Potato virus X PVX Potexvirus contact Potato virus A PVA Potyvirus aphid ± nonpersistent Potato virus V PVV Potyvirus aphid ± nonpersistent Potato virus S PVS Carlavirus contact (aphid ± nonpersistent*) Potato virus M PVM Carlavirus aphid ± nonpersistent (contact ) Tobacco rattle virus TRV Tobravirus Trichodorid nematodes Potato mop-top virus PMTV Pomovirus Spongospora subterranea Potato spindle-tuber viroid PSTVd Pospiviroid contact (aphidà) * Some isolates of PVS are transmitted by aphids. Some isolates are transmitted by contact. à PSTVd can be transmitted by aphids if encapsidated by PLRV (Querci et al., 1997). Note: PVY, PVA and PVV can also be transmitted by contact, but much less readily than PVX and PVS. (Adams et al., 1998) PSTVd occurs in North and South America, China and tions, concern about environmental eects of pesticides, parts of Eastern Europe but is considered to be non- and consumer concern about pesticide residues in food. indigenous in most of Western Europe. The potential bene®ts of virus resistance are therefore great, because resistant cultivars are the most economic and environmentally acceptable way of controlling virus The need for resistance diseases of potato. Potato is the world's fourth major food crop. Viruses are a serious problem, not only because of eects caused Nomenclature of virus resistance genes by primary infection, but also because the crop is vegetatively propagated and they are transmitted This paper follows the conventions described in Solomon- through the tubers to subsequent vegetative generations. Blackburn & Barker (2001) for resistance gene nomen- Crop yield losses resulting from PLRV, PVY and PVX clature, indicating the type and origin of resistance and in the UK were estimated, using 1982 prices, at £30±50 the virus or strain resisted. million during a year of average infection (Hull, 1984). The potential net gain from using cultivars resistant to Types of resistance these three viruses has been estimated at 22% in Mexico (where only a quarter of ware hectarage uses certi®ed The nomenclature for the responses of plants to virus seed) (Quaim, 1998). Yield losses attributable to PLRV infection was reviewed by Cooper & Jones (1983), and worldwide have been estimated at 20 million tonnes per the types of host resistance in potato by Valkonen year (Kojima & Lapierre, 1988). Losses can take the (1994) and Valkonen et al. (1996). The following are form of reduced yield, downgrading of seed crops, and/ descriptions of dierent types of responses that occur in or tuber blemishes (described above) but, in most resistant potato plants. Most can be applied to host countries, the true cost has also to be seen in terms of gene-mediated and transgenic resistance. expensive control measures. These include seed potato Extreme resistance (ER) and hypersensitive resistance production/certi®cation schemes (with the attendant (HR) are described in Solomon-Blackburn & Barker costs of roguing, crop inspections and diagnostics (2001). Host gene-mediated ER prevents virus multipli- including the increasing use of postharvest tuber test- cation at an early stage of infection and is not normally ing); the use of pesticides to kill vector aphids (for associated with cell death (HaÈ maÈ laÈ inen et al., 1997; PLRV control) or nematodes (for TRV control) and Gilbert et al., 1998). HR is well studied and can be other measures such as mineral oil sprays to prevent considered as a rapid defence response that results in nonpersistent aphid transmission of PVY. Control of death of a few cells (necrosis) at the site of infection aphids and nematodes by pesticides is expensive, and which prevents the infection from spreading further likely to become more dicult with increasing insecti- (Dixon et al., 1994). cide resistance in aphid populations, any long-term Resistance to infection can be de®ned as when the climatic changes leading to changes in vector popula- likelihood of infection by natural means (i.e. from vector Ó The Genetics Society of Great Britain, Heredity, 86, 17±35. REVIEW OF POTATO VIRUS RESISTANCE BREEDING 19 inoculation) is reduced in resistant plants. Such resist- 2HaÈ maÈ laÈ inen et al., 1998) and there are, no doubt, many ance was called `®eld resistance' by Cooper & Jones others as yet undiscovered. (1983). Infection resistance can also be manifested in plants that are resistant or unattractive to the vector Introduction of potato to Europe and its early decline in (e.g. aphids) itself (Flanders et al., 1992). vigour. The history of the potato crop has been reviewed Plants with resistance to virus accumulation are by Bradshaw & Mackay (1994) and Glendinning (1983), infectible but the virus reaches only a relatively low and by Davidson (1980) with respect to virus problems. concentration in the plant. The term `moderate resist- The modern Tuberosum potato (S. tuberosum ssp. ance', adopted by Valkonen et al. (1996) for this type of tuberosum) was derived from (probably two) introduc- resistance, is not used
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