Christiane Gebhardt Jari P.T. Valkonenusers.aber.ac.uk/gwg/pdf/potres-arprev.pdfChristiane Gebhardt...

11 Jul 2001 14:55 AR AR138-05.tex AR138-05.SGM ARv2(2001/05/10)P1: GJB

Annu. Rev. Phytopathol. 2001. 39:79–102Copyright c© 2001 by Annual Reviews. All rights reserved

ORGANIZATION OF GENES CONTROLLING

DISEASE RESISTANCE IN THE POTATO GENOME

Christiane GebhardtMax-Planck Institute for Breeding Research, Carl von Linne Weg 10, D-50829 Cologne,Germany; e-mail: [email protected]

Jari P.T. ValkonenDepartment of Plant Biology, Swedish University of Agricultural Sciences (SLU), PO Box7080, S-750 07 Uppsala, Sweden, and Institute of Biotechnology, University of Helsinki;e-mail: [email protected]

Key Words Solanum tuberosumssp.tuberosum, quantitative trait loci (QTL),DNA markers, molecular map, candidate genes

■ Abstract Nineteen single dominant genes (R genes) for resistance to viruses,nematodes, and fungi have been positioned on the molecular map of potato using DNAmarkers. Fourteen of those genes are located in five “hotspots” for resistance in thepotato genome. Quantitative trait loci (QTL) for resistance to late blight caused bythe oomycetePhytophthora infestans, to tuber rot caused by the bacteriumErwiniacarotovorassp.atroseptica, and to root cyst nematodes have been identified on all12 potato chromosomes. Some QTL for resistance to different pathogens are linkedto each other and/or to resistance hotspots. Based on the genetic clustering withRgenes, we propose that some QTL for resistance have a molecular basis similar tosingle R genes. Mapping potato genes with sequence similarity to clonedR genesof other plants and other defense-related genes reveals linkage between candidategenes,Rgenes, and resistance QTL. To explain the molecular basis of polygenic resis-tance in potato we propose (a) genes having structural similarity with clonedR genesand (b) genes involved in the defense response. The “candidate gene approach” en-ables the identification of markers highly useful for marker-assisted selection in potatobreeding.

CONTENTS

INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80Short History of Resistance Breeding in Potato. . . . . . . . . . . . . . . . . . . . . . . . . . . . 80Inheritance of Disease Resistance in Potato. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81New Tools for Genetic Analysis of Disease Resistance in Potato. . . . . . . . . . . . . . 82

MAP POSITIONS OF POTATO GENES FOR RESISTANCE TONEMATODES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83

0066-4286/01/0901-0079$14.00 79


80 GEBHARDT ¥ VALKONEN

MAP POSITIONS OF POTATO GENES FOR RESISTANCE TOVIRUSES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86

MAP POSITIONS OF POTATO GENES FOR RESISTANCE TO FUNGI. . . . . . . . 87MAP POSITIONS OF POTATO GENES FOR RESISTANCE TOBACTERIA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88

CONCLUSIONS FROM THE LOCATION OF POTATO GENES FORRESISTANCE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89Clusters of R Genes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89Linkage Between QTL and R Gene Loci. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89Comparison of Function Maps for Resistance Between SolanaceousSpecies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

MOLECULAR BASIS FOR MONOGENIC AND POLYGENICRESISTANCE IN POTATO . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91R Genes Cloned from Potato. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91Linkage Between R Genes, Resistance QTL, and ResistanceGene-Like Loci in Potato. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92

Linkage Between Resistance QTL and Defense-Related Genes. . . . . . . . . . . . . . . 92Models to Explain the Outcome of R Gene–Mediated and QuantitativeResistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

CANDIDATE GENES FOR MARKER-ASSISTED RESISTANCEBREEDING . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

OUTLOOK . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95

INTRODUCTION

Short History of Resistance Breeding in Potato

Potato (Solanum tuberosumssp.tuberosumL.) is the fourth most important foodcrop worldwide after wheat, maize, and rice (44). Annual production is estimated asca. 300 million tons. However, potential production could exceed 400 million tonsif the diseases that reduce yield by approximately a quarter could be controlled (1).As a clonally propagated crop, potato is vulnerable to pests and diseases affectingleaves, stems, roots, and tubers. Also, after harvest the tuber crop is endangeredby fungal and bacterial pathogens, and by insects in hot climates. Infected seedtubers transmit pathogens to the next growing season, thereby causing progressivedegeneration of yield.

One of the most devastating famines in Europe, affecting millions of people,occurred in the 1840s. Late blight epidemics caused by the oomycetePhytoph-thora infestansalmost completely destroyed the potato crop (95). Late blight andthe various symptoms caused byPotato virus Y(PVY) still pose major diseaseproblems in potato production areas in temperate climates.

At the beginning of the twentieth century, shortly after the rediscovery ofMendel’s laws of inheritance, a tuber bearing wildSolanumspecies was discoveredto be a source of genetic resistance toPhytophthora infestans(94). Based on thisdiscovery, introgression of genes for resistance was initiated by crossing resistant


POTATO RESISTANCE GENE ORGANIZATION 81

wild potatoes with susceptible domestic potato varieties. From the 1920s onwards,numerous scientific expeditions to Mexico, Central, and South America, the cen-ters of origin and diversity of the potatoes, have led to the collection and taxonomicdescription of over 200 wild and 8 cultivated tuber-bearingSolanumspecies (re-viewed in 44). When tested with potato pathogens, resistant plants were identifiedamong the many accessions of wild and cultivated potatoes (44, 90). Comparedwith the huge natural genetic diversity available in the wild relatives of the potato,only a small number of these species have actually been used for introgression ofresistance traits into cultivars, because of the introduction of undesirable “wild”traits together with the resistance trait. Several generations of backcrossing andrecurrent selection are usually required before acceptable cultivars can be obtainedfrom such materials. Nevertheless, most genes for resistance to viruses, fungi, andnematodes present in modern potato varieties and breeding materials have beenintrogressed from closely related tuber-bearingSolanumspecies. For further de-tails on the history of resistance breeding in potato the reader is referred to Ross(90) and Hawkes (44).

Inheritance of Disease Resistance in Potato

Among the first agronomically relevant traits investigated for mode of inheritancewas resistance of potatoes to the wart disease caused by the fungusSynchytriumendobioticum(96). The potato (Solanum tuberosumssp.tuberosum) is, however,a far from ideal species for genetic analysis: It is tetraploid (2n= 4x = 48)with tetrasomic inheritance and highly heterozygous owing to inbreeding depres-sion after repeated selfing. One to four different alleles are present per locus,resulting in one homozygous and four heterozygous genotypes: homozygousor quadruplex (A1A1A1A1), 4-times simplex (A1A2A3A4), duplex/simplex/simplex(A1A1A2A3), duplex/duplex (A1A1A2A2) and simplex/triplex (A1A2A2A2). Genotypesmay combine with each other in crosses resulting in 25 genetic models to be con-sidered in inheritance studies. The simplest genetic model for the inheritance ofdisease resistance is based on the monogenic inheritance of a dominant resistanceallele (R gene) present in a tetraploid plant in one of four allelic states, homozy-gous (RRRR) or heterozygousRRRr(triplex/simplex),RRrr (duplex/duplex) orRrrr (simplex/triplex). The Mendelian ratios expected in offspring of heterozy-gous resistant and homozygous susceptible plants (rrrr ) are then (assuming chro-mosome, not chromatide segregation) 1 : 0 resistant versus susceptible plants foraRRRrparent, 5 : 1 for aRRrrparent, and 1 : 1 for aRrrr parent. One of the mostcomprehensive studies on inheritance and linkage of single genes for resistance intetraploid potato was by Cockerham (16) on genes for resistance toPotato virus X(PVX) andPotato virus Y(PVY).

Flor’s gene-for-gene concept (31) states that for each host resistance (R) gene,there is a corresponding pathogen avirulence (Avr) gene. TheAvr gene produces,or results in the production of a ligand that is recognized by theR gene product(21). Recognition between these two products is required for elicitation of the



defense responses that are controlled by a wide variety of different genes. Thegene-for-gene concept is compatible with most of the single genes for resistancethat have been studied in potato species. The concept has been proven by classicalgenetic analysis, e.g., for the resistance geneH1 and the correspondingAvr geneof the root cyst nematodeGlobodera rostochiensis(50), and by molecular studiesthat have identified the PVX coat protein gene as theAvr gene corresponding tothe resistance geneRx, which is structurally similar to several otherRgenes clonedfrom plants (6).

The prominence of single gene resistance (“vertical”) in the scientific literaturehas resulted from its simple Mendelian inheritance rather than its prevalence innatural pathosystems. However, non-Mendelian, quantitative variation of resis-tance levels is frequently observed in wild and cultivated potatoes (11, 90). This“horizontal” or field resistance is assumed to be controlled by polygenes or minorgene complexes. The distinction made between two types of resistance, qualitativeand quantitative, vertical and horizontal, controlled by majorRgenes and by minorgenes or polygenes, is often not clear-cut at the phenotypic level. The relationshipbetween major genes and minor genes for resistance in plant-pathogen interactionsmay be compared to a few high and prominent mountain peaks standing out in avast landscape of rolling hills.

New Tools for Genetic Analysis of Disease Resistance in Potato

Two technical developments provided the enabling tools for genome-wide stud-ies on qualitative and quantitative disease resistance in potato: the manipulationof the ploidy level and the advent of DNA-based genetic markers. Ploidy reduc-tion from the tetraploid to the diploid level became possible either by pollina-tion of tetraploidSolanum tuberosumssp.tuberosumwith certain genotypes ofSolanum phureja(2n= 2x= 24), which induces the parthenogenetic develop-ment of diploid female gametes into plants (46, 47), or by regenerating diploidplants from male gametes of tetraploid plants via anther or microspore culture(22, 84). At the diploid level, the complexity of genetic analysis in potato isequivalent to human genetics: Partially heterozygous parents generate segre-gating offspring, with potato having the advantage that segregating F1 fami-lies with hundreds of sibs can be generated experimentally by crossing parentallines.

DNA-based genetic markers in eukaryotes were first described as restrictionfragment length polymorphism (RFLP) between genomic DNA of different strainsof yeast (81). The molecular basis of all DNA markers are the point mutations (sin-gle nucleotide polymorphism, SNP), insertions, deletions, or inversions of DNAfragments that differentiate the individual genomes of all members of a species.These DNA polymorphisms survived selection during species evolution becausethey had no negative effect on survival and reproduction. Mendelian inheritance,phenotypic neutrality, and unlimited availability made DNA-based markers impor-tant tools for genome analysis (9). Construction of linkage maps based on DNA



markers became feasible with a precision never achieved with classical morpho-logical or isozyme markers.

RFLP markers, in particular, allowed comparative mapping of genomes of sex-ually incompatible species for the first time. This was possible because the DNA ofrelated species may share high sequence similarity and the RFLP assay is based onnucleic acid hybridization between a labeled marker probe and a membrane-boundgenomic target sequence. Hence, depending on the experimental conditions used,cross hybridization is detected between DNA sequences that are not identical butsimilar, and RFLP markers originating from one species can be used to constructlinkage maps in related species. Conserved linkage between loci identified by thesame markers in different species indicates not only similarity of DNA sequencebut also similarity of genome structure (synteny). A first molecular linkage mapof potato was constructed with tomato RFLP markers mapped to the 12 linkagegroups of tomato. The study demonstrated for the first time extensive genome col-inearity between two closely related plant species (8). Over the past one and a halfdecades, several linkage maps have been constructed for potato based on RFLP,AFLP (Amplified Fragment Length Polymorphism, 114), SSR (Simple SequenceRepeat), and other PCR-based markers (8, 14, 35–37, 48, 73, 103, 113). Some ofthose maps can be aligned with the molecular maps of tomato (103) and pepper(65), based on common RFLP markers.

Molecular linkage maps provide the framework for the location of loci forpathogen resistance in the potato genome. Using those maps, genes controllingmonogenic and polygenic resistance to various pathogens have been located onthe 12 potato chromosomes over the past ten years. Mapping experiments carriedout in different laboratories have used different, generally diploid, potato geno-types. Independent maps can be aligned provided some common potato or tomatoRFLP markers are used for their construction. RFLP anchor markers (Table 1)allow positional information to be integrated into a single potato function map forresistance (Figure 1). This map is an interpretation of various mapping experimentsand summarizes our current knowledge of the organization of genes for resistancein the potato genome. Using anchor markers, the potato function map for resistancecan also be linked to syntenic regions in the related genomes of tomato, tobacco,and pepper.

MAP POSITIONS OF POTATO GENESFOR RESISTANCE TO NEMATODES

The nematode species most damaging to the cultivated potato are the root cystnematodesGlobodera rostochiensisandGlobodera pallida, followed by root knotnematode species of the genusMeloidogyne(82). Since 1948 (26), genes forresistance toG. rostochiensisandG. pallida have been discovered in a range ofwild potato species. A few genes have been introgressed in breeding lines andcultivars (reviewed in 82, 90).



TABLE 1 R genes and QTL mapped in potato

AnchorChromosome Gene markers Pathogen Reference

I Eca QTL CP108, St3.3.13(d ) E. carotovora ssp. 119atroseptica

Pi QTL CP11 P. infestans 78

II Eca QTL GP23 E. carotovora ssp. 119atroseptica

Pi QTL GP23 P. infestans 78Pi QTL GP26 P. infestans 78

III Eca QTL St1.2.1(b) E. carotovora ssp. 119atroseptica

Pi QTL GP1(a), GP25, CP6 P. infestans 61, 78Pi QTL TG135 P. infestans 30Gro1.4 QTL Ssp8 G. rostochiensis 58Pi QTL GP276 P. infestans 78Pi QTL 4CL P. infestans 61, 106

IV Pi QTL GP180, MBF, TG62 P. infestans 61, 78Eca QTL St1.2.4(e) E. carotovora ssp. 119

atrosepticaGpa4 QTL Stm3016 G. pallida 10Pi QTL Stm3016 P. infestans 73R2 — P. infestans 64

V Pi QTL Gp21, GP179 P. infestans 61, 78R1 GP21, GP179 P. infestans 60Rx2 GP21 Potato Virus X 87Nb GP21 Potato Virus X 20Gpa QTL Ssp72 G. pallida 57Gpa5 QTL GP21, GP179 G. pallida 92Grp1 QTL GP21, GP179 G. pallida, 91

G. rostochiensisPi QTL CP113 P. infestans 78H1 CP113, CD78 G. rostochiensis 34, 83GroV1 TG69 G. rostochiensis 49

VI Pi QTL GP79 P. infestans 78Eca QTL St3.3.13(c) E. carotovora ssp. 119

atrosepticaPi QTL GP76 P. infestans 61, 78

VII Eca QTL GP219 E. carotovora ssp. 119atroseptica

Gro1 CP56, St3.3.2 G. rostochiensis 4, 59

VIII Pi QTL GbssI(wx), Osm P. infestans 78, 106Eca QTL GbssI E. carotovora ssp. 119

atroseptica



TABLE 1 (Continued)

AnchorChromosome Gene markers Pathogen Reference

Eca QTL — E. carotovorassp. 119atroseptica

Rblc CP53 P. infestans 76

IX Pi QTL Prp1, PAL(a,c) P. infestans 61, 78Eca QTL GP129 E. carotovorassp. 119

atrosepticaNxphu TG424, CT220 Potato Virus X 104Gpa6QTL CT220 G. pallida 92

X Eca QTL — E. carotovorassp. 119atroseptica

Rber TG63 P. infestans 30Gro1.2 QTL TG63 G. rostochiensis 56

XI Ryadg CP58, GP125 Potato Virus Y 42Rysto CP58, TG523 Potato Virus Y 12Naadg TG523 Potato Virus A 40RMc1 TG523 M. chitwodii 13Pi QTL GP125 P. infestans 61, 78Eca QTL GP125, St3.3.13(a) E. carotovorassp. 119

atrosepticaSen1 CP58, GP125 S. endobioticum 45Gro1.3 QTL Ssp75, TG30 G. rostochiensis 56R3 TG105(a), GP185, P. infestans 23

GP250R6 GP185, GP250 P. infestans 25R7 GP185, GP250 P. infestans 25Pi QTL GP185, GP250 P. infestans 78Eca QTL GP185, St1.2.1(a) E. carotovorassp. 119

atroseptica

XII Eca QTL — E. carotovorassp. 119atroseptica

Pi QTL — P. infestans 38Pi QTL GP34, CP60 P. infestans 78Rx1 GP34, CP60 Potato Virus X 87Gpa2 GP34 G. pallida 93

The positions of loci for nematode resistance identified to date in potato areshown on the function map for resistance (Figure 1, Table 1). The first nematode-resistance gene mapped to the potato molecular map using RFLP markers wasthe monogenic dominantGro1 gene for resistance toG. rostochiensis, which islocated on chromosome VII (4). This gene originated from an interspecific hybrid



(2n= 2x= 24) betweenS. tuberosumand the wild potato speciesS. spegazziniiand conferred resistance to allG. rostochiensispathotypes tested.Gro1 may beidentical to theFb gene that was identified by Ross (89) inS. spegazzinii(syn.S. famatinae).

H1, a dominant gene that confers durable resistance to pathotype Ro1 ofG. rostochiensis, was discovered nearly 50 years ago in the cultivated potato speciesS. tuberosumssp.andigena(27, 105) and was most widely used in potato breed-ing for nematode resistance. TheH1 locus has been mapped with RFLP markersto the same genomic segment of potato chromosome V in two different diploidpopulations (34, 83).GroV1 for resistance toG. rostochiensisoriginating fromthe wild potato speciesS. verneiis closely linked to theH1 locus (49). Based onpedigree information, accession CPC 1673 ofS. tuberosumssp.andigenawas thesource not only of theH1 gene but also ofGpa2, a major gene for resistance toG. pallida. TheGpa2gene was localized with AFLP and RFLP markers on potatochromosome XII (93).

Only one resistance locus againstMeloidogynespecies has been identified so farin the potato genome. The geneRMc1for resistance toM. chitwoodiwas introgressedinto cultivated potato from the wild potato speciesS. bulbocastanumby somatichybridization and is located on chromosome XI (13).

A number of factors for quantitative resistance (Quantitative Trait Loci, QTL)to root cyst nematodes have also been identified and mapped. QTLGro1.2, Gro1.3,andGro1.4 for resistance toG. rostochiensiswere localized with RFLP markerson potato chromosomes X, XI, and III, respectively. The source of resistance wasS. spegazzinii(56, 58). The sameS. spegazziniiparent also carried quantitativeresistance toG. pallida. QTL mapping of this resistance resulted in one majorQTL Gpaon chromosome V (57). Two further QTL for resistance toG. pallida,Gpa5 and Gpa6, mapped to chromosomes V and IX, respectively (92).Gpa5is tightly linked toGpa. Grp1, a QTL for broad-spectrum resistance to both cystnematode speciesG. rostochiensisandG. pallida, was independently mapped to thesame segment on chromosome V as QTLsGpaandGpa5(91, 92).Grp1, Gpa, andGpa5originate from different genetic backgrounds involving several wild potatospecies. QTL mapping of resistance toG. pallida in a tetraploid cross using AFLPand SSR markers allocated a QTL (Gpa4) to chromosome IV, which was possiblevia the linkage ofGpa4to SSR markerStm3016with a known map position (10).

In contrast to quantitative resistance againstPhytophthora infestansor Erwiniacarotovorassp.atroseptica, which are controlled by factors on every potato chro-mosome (see below), quantitative resistance to nematodes seems to be controlledmainly by few QTL with large effects.

MAP POSITIONS OF POTATO GENESFOR RESISTANCE TO VIRUSES

At least 40 viruses are known to infect potatoes in the field (51). The most importantviruses for potato cultivation arePotato leaf roll virus(PLRV) andPotato virus Y(PVY) (90), followed byPotato virus X(PVX), A (PVA), M (PVM), S(PVS) (19),



andPotato mop-top virus(PMTV) (99). Most potato viruses are transmitted byaphids, except PMTV, which is transmitted by the zoospores of the powdery scabpathogenSpongospora subterranea(a protist) and PVX, which has no vector butis contact-transmitted. Viruses cannot be chemically controlled in the field, and thecontrol of virus vectors with pesticides does not efficiently control the spread ofviruses in the field in most cases. Therefore, virus-free seed potatoes and resistantcultivars form the basis for virus control in potato.

Single dominant genes for resistance to viruses have been discovered and ge-netically characterized in wild and cultivated potato species since the middle of theprevious century (5, 16, 90, 102). The common types of single gene resistance toviruses in potato are extreme resistance (ER) and hypersensitive resistance (HR).The genes for ER confer high levels of resistance to all or most virus strains. Ex-tremely low amounts of virus are detected in inoculated plants and no symptomsare observed (3, 16, 90). The genes for hypersensitive resistance (HR) are usuallyvirus strain group specific. Their phenotypic expression is characterized by devel-opment of necrotic symptoms in the virus-infected tissues (16, 52), whereas suchsymptoms are very limited and usually absent in plants expressing ER (3, 42, 90).The nomenclature of virus resistance genes in potato has been reviewed (109).

The positions of loci for virus resistance known to date in potato are shownon the function map for resistance (Figure 1) (Table 1). GenesRx1andRx2conferER to Potato virus X(PVX) in S. tuberosumssp.andigena(16) andS. acaule(102), respectively.Rx1andRx2have been introgressed into potato breeding linesand mapped to chromosomes XII and V, respectively (87). The geneNbconferringHR to PVX has been mapped to the same region on chromosome V asRx2(20).Nxphu controls HR to PVX inS. phureja, a diploid cultivated species, and resideson the south arm of chromosome IX (104).

On chromosome XI, the same region contains genesRyadg andRysto for ERto Potato virus Y(PVY) (12, 41, 42) andNaadg for HR to Potato virus A(PVA)(40).Ryadg andNaadg (40–42) originate from an accession ofS. tuberosumsubsp.andigena(75, 111), whereasRysto is thought to be derived fromS. stoloniferum(12), although pedigree information might not be reliable in this case. Genes forER or HR to PVY, PVA, andPotato virus Vwith a probable common origin inS.stoloniferumcosegregate, which suggests that all these genes might reside on chro-mosome XI (3, 108). This suggestion remains to be tested with molecular markers.

The geneNsfor resistance toPotato virus S(PVS) was tagged by RAPD markersof unknown position in the potato genome (67). No genes for resistance to thePot-ato leaf roll virus, Potato virus M, andPotato mop-top virushave been mapped todate. No QTL mapping for quantitative virus resistance has been reported in potato.

MAP POSITIONS OF POTATO GENESFOR RESISTANCE TO FUNGI

Late blight, the most important so-called fungal disease of potato (53, 107), iscaused by the oomyceteous fungusPhytophthora infestans, which is, in fact, moreclosely related to brown algae than to higher fungi (107). Intentional breeding for



resistance to late blight began nearly 100 years ago with the introgression of resis-tance fromS. demissum, a wild potato species indigenous to Mexico (see 116 forreview). On one hand, resistance to late blight is determined by dominantRgenesinducing an HR response upon infection with specific races ofP. infestans. Ele-ven suchRgenes have been described (66). On the other hand, quantitative, race-nonspecific resistance controlled by an unknown number of genes is also known.

TheR1locus for resistance to late blight was identified on potato chromosomeV by RFLP mapping (60). The genesR3, R6, andR7with different pathogen racespecificities have been located on chromosome XI in the same genome segment(23, 24).R2has been mapped with AFLP markers to chromosome IV (64). All theseRgenes originate from the wild potato speciesS. demissum. Recently, late blight-resistance genesRber of S. berthaultiiandRblc of S. bulbocastanumwere identifiedand mapped to chromosomes X and VIII, respectively (30, 76). These genes conferresistance to contemporaryP. infestansraces carrying multiple virulence factors.

Genetic dissection of quantitative resistance toP. infestansusing DNA-basedmarkers has been done in several diploid mapping populations (17, 30, 38, 61, 78,97) and in one tetraploid mapping population (69). Factors controlling quantitativeresistance toP. infestanshave been found on almost every potato chromosome(Figure 1) (Table 1), confirming the truly polygenic nature of this trait. Linkage toanchor markers uncovered some QTL in similar regions of the potato genome indifferent mapping populations. In this respect, the most promising QTL for marker-assisted breeding are those on chromosomes III (30, 61, 78), IV (61, 72, 78, 97), V(61, 78, 97), and VI (17, 61, 78). The most significant and most reproducible QTLfor foliage and tuber resistance toP. infestansis located on chromosome V close tothe anchor markerGP179. This QTL and a second one linked to the markerGP76on chromosome VI (Figure 1) are particularly interesting because both are linkedwith QTL for plant maturity (17, 78). Breeding for field resistance to late blightunder long day conditions (e.g., in Central and Northern Europe) usually resultsin late-maturing cultivars (116). The same correlation is observed at the two QTLon chromosomes V and VI: Plants having alleles that increase resistance maturelater and vice versa. Therefore, resistance to late blight and delayed plant maturitymay be pleiotropic effects of the same gene(s).

Only one gene for resistance to a fungus other thanP. infestanshas been iden-tified and mapped in potato. TheSen1gene of unknown origin has been located onpotato chromosome XI (Figure 1) and confers resistance to potato wart, a quaran-tine disease caused bySynchytrium endobioticumthat destroys the tubers (45).

MAP POSITIONS OF POTATO GENESFOR RESISTANCE TO BACTERIA

The two most important bacterial diseases of cultivated potato, blackleg of stemsand tuber soft rot, are caused byErwinia species. No source of monogenic resis-tance is known (29). Quantitative trait loci for tuber and foliar resistance toErwiniacarotovorassp.atroseptica(Eca) have been mapped in diploid hybrids originating



from intercrossingS. tuberosumwith the wild potato speciesS. chacoenseandS. yungasense(119). For one F1 hybrid population, a linkage map was constructedbased on AFLP and RFLP markers, including three resistance gene-like markers(see below). The QTL analysis revealed complex inheritance of resistance toEca.Loci for genetic factors affecting resistance toEca were found on all 12 potatochromosomes. Most QTL can be incorporated in the potato function map for resis-tance (Figure 1) using RFLP anchor markers. The QTL with the largest and mostreproducible effect on tuber resistance mapped to chromosome I.

CONCLUSIONS FROM THE LOCATIONOF POTATO GENES FOR RESISTANCE

As known from classical genetic studies in plants, single genes conferring resis-tance to specific races of a pathogen may be tightly linked, either because they aremultiple alleles of one gene or because several related genes with similar functionare located next to each other in the same narrow genome segment (85). Suchclustered gene families evolve from common ancestors by local gene duplicationsfollowed by structural and functional diversification. Several clusters of this typehave now been analyzed at the molecular level in plants, e.g. in flax (2), tomato(80), or lettuce (70).

Clusters of R Genes

In potato, DNA markers made possible the identification of complex loci havingseveralR genes. At least threeR genes (R3, R6, R7) for race-specific resistanceto P. infestansare organized in a cluster in the distal segment of chromosomeXI anchored by the marker locusTG105(a) (Figure 1). At least two genes (H1,GroV1) for resistance to the cyst nematodeG. rostochiensisin two different potatospecies identify another cluster on chromosome V.

More surprisingly, genes for resistance to different pathogens also form clus-ters. This was first observed in the potato genome when theR1gene for resistanceto P. infestansand theRx2gene for resistance to PVX were found to be closelylinked to the same RFLP anchor markerGP21on chromosome V (60, 87). Later,Nbcontrolling HR to PVX was mapped to the sameRgene cluster (20). Two addi-tional clusters ofRgenes with different pathogen specificities are known (Figure 1):GenesRyadg, Naadg(both virus-resistance genes),RMc1 (nematode-resistance gene)andSen1(resistance to the wart fungus) form a cluster on chromosome XI, an-chored by markerCP58. GenesRx1(virus-resistance gene) andGpa2(nematode-resistance gene) are clustered on chromosome XII close to anchor markerGP34(Figure 1) (Table 1).

Linkage Between QTL and R Gene Loci

QTL are positioned on the molecular map with less precision than single genesbecause individual recombinants between a QTL and a linked Mendelian marker



cannot be identified. The effects of quantitative trait alleles can be detected withmarkers that span a genetic distance of a few centimorgans up to a whole linkagegroup that may be tens of centimorgans. The phenotypic effect detectable witha marker decreases with increasing genetic distance between the marker and theQTL. The genetic distance covered by a QTL correlates with the size of the effect,not with the number of genes causing the effect. A single gene with a large effectis still detectable by relatively distant markers, whereas a gene or a group of geneswith small effects is detectable only by the most closely linked markers. Inde-pendent QTL maps can be compared using as anchors single markers or markerintervals with the most significant trait effects. Integration of QTL for resistance toP. infestans, cyst nematodes, andErwinia carotovorassp.atrosepticain the potatofunction map for resistance reveals several examples of linkage between QTL andRgenes. This was first observed when the RFLP markersGP21andGP179flankingtheR1gene within a 3-cM interval also detected the largest effects on quantitativeresistance toP. infestanson chromosome V (61). The most conspicuous genetichotspots containing multiple genes forR gene resistance and quantitative resis-tance to different pathogens are located on chromosomes V, XI, and XII of potato(Figure 1).

Comparison of Function Maps for ResistanceBetween Solanaceous Species

The potato function map for resistance can be anchored with markers to colinearsegments of the related genomes of tomato, tobacco, and pepper, revealing syn-teny between resistance loci of these species. However, structural synteny doesnot necessarily implicate functional synteny. Only four selected and particularlyinteresting cases of synteny between resistance loci are mentioned here. For moredetailed comparisons among Solanaceae genomes the reader is referred to Leisteret al (59) and Grube et al (39).

1. A map segment on the short arm of potato chromosome VI (marked byGP79;Figure 1) having QTL for resistance to bothP. infestansandEca (78, 119)is syntenic with a resistance hotspot on tomato chromosome 6, includinggenes for resistance to a nematode (Mi), an aphid (Meu1), a virus (Ty1), andfungi (Cf2, Cf5, Ol-1) (59).

2. GeneHero for resistance to the nematodeG. rostochiensismaps to a similarposition on tomato chromosome 4 (33) as QTL for resistance toP. infestans(61, 78) andG. pallida (10) on the collinear potato chromosome IV.

3. MarkerCP58anchors the resistance hotspot to viruses (Ryadg, Naadg), a ne-matode (RMc1), and a fungus (Sen1) on the North arm of potato chromosomeXI to the geneN for resistance toTobacco mosaic virus(TMV) in tobacco(45).

4. The resistance gene cluster on the South arm of potato chromosome XI islinked by markersTG105andTG36 to I2 for resistance to theFusarium



oxysporumin tomato (98) andL for resistance to TMV in pepper (62),respectively.

Clustering of genes controlling monogenic and polygenic resistance to diversepathogens, as observed in the potato genome, may occur by chance alone or maybe a consequence of reduced recombination fractions due to proximity of thecentromere. Alternatively, the clustering suggests an underlying principle similarto the one known for clustered genes for resistance to specific races of a singlepathogen. The first implication of this principle is that monogenic resistance toviruses, nematodes, and fungi may be encoded by alleles of a single gene orby paralogous members of the same gene family. The latter option is now wellsupported by molecular data (see next section). The second implication is thatsome QTL for quantitative resistance may be structurally related toRgenes actingagainst the same or a different pathogen. The third implication is that linked QTLfor resistance to different pathogens, such asP. infestans, Eca, and cyst nematodes,may be similar at the molecular level.

MOLECULAR BASIS FOR MONOGENIC ANDPOLYGENIC RESISTANCE IN POTATO

R Genes Cloned from Potato

Only during the past decade have plant genes controlling monogenic resistancebeen cloned and characterized (reviewed in 28, 43, 118).R genes of unrelatedplant species that confer a gene-for-gene type of resistance to viruses, bacteria,fungi, or nematodes possess structural similarities, allowing their classificationin four major structural groups regardless of pathogen specificity. Most of theRgenes characterized to date belong to a superfamily of genes sharing a putativenucleotide binding site (NBS) or CheY domain (receiver domain common to manyproteins of His-Asp phosphotransfer pathways) (86) and a leucine-rich repeat(LRR) domain (NBS/CheY-LRR genes). The second group are resistance genesthat have only an LRR domain (LRR genes) in common. Members of the thirdgroup share an LRR and a protein kinase domain (PK-LRR genes), and membersof the fourth group are protein kinases without a LRR domain (PK-type genes).Proteins with such domains may function as receptors or downstream componentsof signal transduction pathways leading to the transcriptional activation of a batteryof “signal response” genes (68). In the case ofR genes, the responding genes arethose required for various defense reactions that eventually prevent advancementof pathogen infection.

ThreeRgenes have been cloned from potato. Two of these genes, namelyRx1andGpa2(6, 112), reside in the resistance hotspot on chromosome XII (Figure 1).Rx2from the resistance hotspot on chromosome V was cloned based on sequencesimilarity with Rx1 (7). The three genes are members of the NBS/CheY-LRRsuperfamily (see DC Baulcombe, this volume), similar to the tobacco geneN



(117) and the genesI2 (79, 100) andMi (74) of tomato. As mentioned above, themap positions of theseRgenes of tobacco and tomato are syntenic with resistancegene clusters on potato chromosomes XI and VI (Figure 1).

Linkage Between R Genes, Resistance QTL,and Resistance Gene-Like Loci in Potato

Some short sequence motifs are highly conserved betweenR genes of the NBS/CheY-LRR class. Primers designed to such motifs have been used to obtain, bythe polymerase chain reaction (PCR), potato gene fragments that, as expected,have DNA sequence similarity with knownRgenes (59). RFLP mapping of theseresistance gene-like (RGL) markers identifies at least 20 RGL loci on the potatomolecular map. Most potato RGL probes detect complex gene families with somemembers tightly linked and others mapping to different loci (59, 119; C Gebhardt,unpublished results). Assuming 20 RGL loci, each having between five and tencopies of NBS/CheY-LRR genes, it is estimated that the potato genome containsat least 100–200 genes of this class. InArabidopsis, NBS/CheY-LRR genes makeup 1% of the genome (71). Moreover, gene families homologous to the tomatoCf genes for resistance to the fungusCladosporium fulvum(LRR genes) and thetomatoPto gene (a protein kinase) have been mapped to syntenic segments ofthe potato genome (59). Therefore, the RGL loci discovered so far in the potatogenome may represent just the tip of the iceberg. Integrating RGL loci into thepotato function map for resistance reveals tight linkage between RGL loci and locicontrolling monogenic and/or polygenic disease resistance (Figure 1) (59, 119).Molecular characterization of theGro1 and R1 loci (C Gebhardt, unpublisheddata) and theRy locus (J Valkonen, unpublished data; DC Baulcombe, personalcommunication) has revealed clusters of genes with sequence similarity to knownRgenes.

Based on current molecular evidence, we expect that most, if not all, of thesingle dominant genes for resistance that populate the potato function map areprimarily encoded by NBS/CheY-LRR genes or one of the other major classes ofresistance genes, irrespective of their pathogen specificity. We propose that not onlymonogenic resistance but also genetic factors controlling quantitative resistanceare encoded by the same classes of genes (61, 78, 91, 119).

Linkage Between Resistance QTL and Defense-Related Genes

Genes involved in defense reactions against pathogens (55) were identified, char-acterized, and cloned long before the firstR genes. In potato, many of them areorganized in clustered gene families (C Gebhardt, unpublished data). Defensegenes have been mapped or tested for linkage with QTL for resistance in potato(37, 61, 106). Integrating defense-related loci in the potato function map revealslinkage with QTL for resistance toP. infestansand/orEca (Figure 1). Genes in-volved in defense responses are candidates, therefore, for controlling quantitativeresistance. The most conspicuous candidates based on map position are:



1. Genes encoding phenylalanine ammonia lyase (PAL, linkage groups III, IX,X) and 4-coumarate:CoA ligase (4CL, linkage group III), both of which arekey enzymes in the phenylpropanoid metabolism leading to the productionof phytoalexins (32).

2. Pathogenesis-related (PR) genes encoding glutathione-S transferases (prp1,linkage group IX), acidic and basic glucanases (GluA, GluB, linkage groupI), lipoxygenases (Lox, linkage group VIII), proteinase inhibitors (Pin, PinI,linkage groups III and IX), osmotins (Osm, linkage group VIII), and locidetected by tobacco RFLP probes for PR-1a and PR-5 (115) (NtPR-1a,NtPR-5, linkage groups X and XII).

Models to Explain the Outcome of R Gene–Mediatedand Quantitative Resistance

How could quantitative resistance to pathogens be explained based on genes thathave a receptor-like structure similar toR genes or that are members of defensegene families?

A major QTL such asGrp1 that is located in the resistance hotspot on potatochromosome V and explains 45% to 77% of the phenotypic variance (91, 92)might be, in fact, a single gene. The Mendelian segregation might just be difficultto score precisely because of the effects of environmental factors on the phenotype.Environmental effects on resistance expression have been widely documented inplants, including potato (88, 90).

Only the extremes of multiple alleles at a resistance locus may express fullresistance or full susceptibility, whereas other alleles may have an intermedi-ate effect on resistance. At the molecular level, allelic variation incis-regulatoryregions for transcription or translation of anR gene or a defense gene couldmodulate the cellular concentration of the protein in different tissues at differ-ent developmental stages, thereby quantitatively affecting the kinetics of signaltransduction and defense response. For example, the same defense genes are ac-tivated in potato irrespective of whether or not the interaction withP. infestansleads to resistance or susceptibility. The difference between the outcome of theinteraction is the induction kinetics of the defense response (32). Quantitativeeffects may also result from allelic variation in the structural part of a gene,which may modify in a nondisruptive way the binding affinities for interactingmolecules such as an Avr gene product or proteins of the signal transductionpathway.

The biologically active plant receptor that interacts with the avirulence factormay be a dimeric protein or a protein complex of even higher order. Hence, bindingspecificity for the avirulence factor, efficiency, and kinetics of signal transductionand defense reaction would then be the result of interaction of two or severaldifferent NBS/CheY-LRR subunits. As all plants seem to have numerous genesof this type, countless possibilities are available for genotype-dependent quan-titative variation of resistance phenotype. Monogenic resistance would then be



nothing but the outcome of a perfect match between the product of a recognizedgene for resistance and the products of other members of this ubiquitous genefamily.

The oligomer receptor model combined with allelic variability atR loci and atloci involved in signal transduction and defense responses is particularly attractivebecause it provides a plausible, although not exclusive, explanation for severalreported phenomena:

1. The influence of the genetic background on resistance phenotype. Modifi-cation or even suppression of the resistance phenotype is observed in theoffspring, depending on which susceptible parent the resistance source iscrossed with (15, 25, 40, 90, 110).R gene specificities different from thosepresent in the parents may appear in hybrid progeny (25, 94). In offspringsegregating for quantitative resistance, resistance levels higher or lower thanthose present in the parents may be expressed (transgressive segregation)(60, 90).

2. Epistatic interactions between resistance QTL (30, 63, 92).

3. Difficulty of proving a physical interaction between anR gene product andanAvr gene product (28).

CANDIDATE GENES FOR MARKER-ASSISTEDRESISTANCE BREEDING

The “Know Where” ofR genes, QTL, and hotspots for resistance on the potatomolecular maps provides the “Know How” for marker-assisted combination ofvarious genes for resistance. The positional information also gives access to nu-merous, potentially useful DNA markers (14, 37, 73, 103) beyond those developedwithin a particular mapping experiment. Crossing programs have been started us-ing as parents the same genotypes that were the source of resistance in mappingexperiments. Tightly linked DNA markers (54, 77; C Gebhardt, unpublished data)are being used to select plants at the seedling stage that have combinations ofgenes for resistance to cyst nematodes, PVY, PVX, and potato wart (C Gebhardt &J Valkonen, unpublished data). In this case, the marker genotype predicts the resis-tance phenotype because we do know which marker allele (e.g., a PCR product ofspecific size) is linked in coupling phase with the resistance gene (known markerphase) and is, therefore, coinherited with the resistance gene, except when recom-bination has occurred (linkage disequilibrium between DNA marker and resistancetrait).

Breeding potato cultivars is, however, based on intercrossing hundreds of geno-types of various pedigrees. In such a wide gene pool, prediction of resistancephenotype based on marker genotype is not straightforward because, owing tomultiple generations of meiotic recombination separating the individuals in sucha gene pool, linkage equilibrium may have been reached between a specific gene



for resistance and an even closely linked marker (unknown marker phase); in otherwords, a singular marker allele known to be coinherited with resistance in a singlecross may not be coinherited with that same resistance in a wide gene pool (77).Only when the marker resides within the resistance gene itself, or is physicallyclose to the resistance gene, is recombination between marker allele and resistanceabsent or rare even after many generations of meiotic recombination. In this case,linkage disequilibrium between marker allele and resistance gene is still strong,even in wide gene pools (18). Markers based on DNA polymorphism of the genescontrolling monogenic or quantitative resistance will be, therefore, the ultimatediagnostic tools for marker-assisted resistance breeding.

Markers have been found that are diagnostic for the presence of theRyadg

gene for resistance to PVY in a wide potato gene pool (54, 101). These markersare based on a resistance gene-like sequence that maps to the resistance hotspotincludingRyon potato chromosome XI (59). Moreover, markers from within theresistance hotspot on chromosome V that includes theR1gene are associated withQTL for late blight resistance and plant maturity when scored in more than 400potato cultivars (C Gebhardt, unpublished data). Thus, candidate gene markersare excellent tools when searching for “universal” markers for marker assistedselection by linkage disequilibrium mapping in wide gene pools. On the otherhand, the finding of linkage disequilibrium between a candidate gene marker andanRgene or QTL for resistance provides excellent support for the hypothesis thatthe candidate gene is indeed the resistance gene or at least is located physicallyvery close to the resistance gene.

OUTLOOK

The challenge for the future is the molecular identification of those genes that areimportant for controlling quantitative disease resistance. Quantitative resistance isdifficult to manipulate by phenotypic selection in breeding programs. Significantprogress may be achieved when we learn how to improve field resistance to diseaseby combining superior alleles of known genes for quantitative resistance. Thepotato function map for resistance in combination with candidate gene maps, theanalysis of sequence variation present in candidate gene loci, and the associationof such variation with resistance phenotype in wide gene pools are considered tobe promising approaches to reach that goal in tetraploid potato.

ACKNOWLEDGMENTS

Financial support for the authors’ studies on molecular genetics of disease resis-tance in potato was provided by the Max-Planck Society, the German Ministry forResearch and Technology, and the European Union (C Gebhardt); and the Uni-versity of Helsinki, The Academy of Finland, SLU, the Forestry and AgriculturalResearch Council of Sweden, and Carl Tryggers Stiftelse (J Valkonen).



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P1: FQP/LQD P2: FQP

July 11, 2001 14:38 Annual Reviews AR138-05-COLOR

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P1: FQP/LQD P2: FQP

July 11, 2001 14:38 Annual Reviews AR138-05-COLOR

Figure 1 (from previous page) Potato function map for pathogen resistance. Twelve link-age groups corresponding to the 12 potato chromosomes are shown schematically withapproximate genetic distances. Relative positions of potato/tomato anchor markers are in-dicated in black to the left of the linkage groups. MappedRgenes and QTL for resistance todifferent pathogens of potato (solid letters) or tomato, tobacco and pepper (outlined letters)are shown at their approximate map positions relative to anchor markers. Different colorsindicate the pathogen type. Green: genes for resistance to fungi. Red: genes for resistanceto nematodes and aphids. Blue: genes for resistance to viruses. Map segments having QTLfor resistance toP. infestansandE. carotovorassp.atrosepticaare marked as green andviolet rectangles, respectively. Loci mapped with resistance gene-like markers of potato (StandRGL loci) are indicated in purple to the right of the linkage groups. Loci detected bypathogenesis related and defense gene markers of potato or tobacco (Nt loci) are shown inblue to the right. Small letters in parenthesis indicate that the same marker probe identifiesmore than one locus. For further details the reader is referred to Table 1 and References 37,59, 78, 119, 106.

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