annurev-phyto-072910-095339

PY49CH19-Bus ARI 15 July 2011 17:26

Revision of the Nomenclatureof the Differential Host-Pathogen Interactions ofVenturia inaequalis and MalusVincent G.M. Bus,1 Erik H.A. Rikkerink,2

Valerie Caffier,3 Charles-Eric Durel,4

and Kim M. Plummer5

1The Plant and Food Research Institute of New Zealand, Private Bag 1401, Havelock North4157, New Zealand; email: [email protected] Plant and Food Research Institute of New Zealand, Private Bag 92169, Auckland1142, New Zealand; email: [email protected], UMR77 Pathologie Vegetale – PaVe, INRA/ACO/UA, IFR QUASAV, BP 60057,F-49071 Beaucouze, France; email: [email protected], UMR 1259 Genetics and Horticulture – GenHort, INRA/ACO/UA, IFRQUASAV, BP 60057, F-49071 Beaucouze, France; email: [email protected] Trobe University, Department of Botany, Bundoora, Vic. 3086, Australia;email: [email protected]

Annu. Rev. Phytopathol. 2011. 49:391–413

The Annual Review of Phytopathology is online atphyto.annualreviews.org

This article’s doi:10.1146/annurev-phyto-072910-095339

Copyright c© 2011 by Annual Reviews.All rights reserved

0066-4286/11/0908/0391$20.00

Keywords

apple scab, race isolate, resistance gene, avirulence gene,gene-for-gene relationship

Abstract

The apple scab (Venturia inaequalis–Malus) pathosystem was one of thefirst systems for which Flor’s concept of gene-for-gene (GfG) relation-ships between the host plant and the pathogen was demonstrated. Thereis a rich resource of host resistance genes present in Malus germplasmthat could potentially be marshalled to confer durable resistance againstthis most important apple disease. A comprehensive understanding ofthe host-pathogen interactions occurring in this pathosystem is a pre-requisite for effectively manipulating these host resistance factors. Anaccurate means of identification of specific resistance and consistentuse of gene nomenclature is critical for this process. A set of univer-sally available, differentially resistant hosts is described, which will befollowed by a set of defined pathogen races at a later stage. We reviewpertinent aspects of the history of apple scab research, describe thecurrent status and future directions of this research, and resolve someoutstanding issues.

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INTRODUCTION

Apple (Malus x domestica) is one of the majorfruit crops produced in the world. At 72 millionmetric tons (MMT) (http://faostat.fao.org),apple is second only to banana (96 MMT) asa major fruit source for the world’s population.Much of the apple production (31 MMT) takesplace in eastern and central China, away fromthe center of diversity of apple located in thewestern regions of China and parts of CentralAsia (72). The species name and the presenceof the x in the specific epithet reflect the di-verse ancestry of this species, with various hy-bridizations between Malus species giving riseto the domesticated apple (76). Nevertheless, itwas recognized as one of the 33 primary Malusspecies in five sections based on the classifi-cation by Wiersema (139). Generally, Malusspecies produce small fruit (<3 cm diameter),with the exception of Malus sieversii, which alsoincludes accessions with fruit of the size ex-pected of commercial apples today. M. sieversiihas also been confirmed as the main progeni-tor of the domesticated apple and perhaps theyshould be regarded as a single species, Maluspumila (135), as argued previously (88). Thehaploid chromosome number of Malus is 17 andmost species are diploid. The first extensive ge-netic map of apple was published by Maliepaardet al. (90). It has become the reference map forover 20 apple and several pear maps, includingone skeleton map based on an integrated con-sensus map (99) used here for the global map-ping of the scab resistance genes discussed.

Apple is host to a wide range of pests and dis-eases (139), a number of which need to be con-trolled for profitable commercial production.Scab disease, caused by the ascomycete fungusVenturia inaequalis (Cke) Wint. (anamorph: Spi-locaea pomi Fries), is one of the most damagingin economic terms, as most climates where ap-ples are grown are conducive to scab (89). Or-chard management techniques, such as leaf lit-ter control, can reduce primary inoculum (89)but usually are not sufficient to control applescab, and as many as 18–25 fungicide applica-tions per growing season may be required (139).

Plant genetic resistance, when available, iswidely regarded as the preferred method forcontrolling disease if the industry can affordto support a breeding program. A long-termdriver for the development of resistant culti-vars is the consumer antagonism to non-naturalcompounds in their food and the environment.This has led to increasingly stringent legis-lation. Using resistant cultivars helps to re-duce socioeconomic and environmental im-pacts (139), but these gains will be realized inthe long-term only if resistance is effective forat least one crop cycle, which is approximately15 years for apple. Achieving such durable re-sistance through traditional breeding is a slowprocess but can be accelerated by adding re-sistance into existing high quality cultivars bymarker-assisted fast breeding (138) or cisgene-sis (116). Ultimately, an in-depth understand-ing of host-pathogen interactions, including thespecific interactions of avirulence (Avr) genesin the pathogen with resistance (R) genes inthe host, is required for these approaches tobe successful. At the same time, other strate-gies (15)—such as disease prevention throughsanitary practices and fungicide application andspatial deployment of resistances (35, 113)—should also be applied to enhance resistancedurability.

Fungal species of Venturia on Rosaceaeappear to have coevolved with, and are limitedto, their (fruit) tree hosts, e.g., Venturia pirina(pear), Venturia carpophila (peach), and Venturiacerasi (cherry) (115), as they are sufficientlydistinct species to prevent mating (15). Thehost range of V. inaequalis comprises species inthe genera Malus, Crataegus, Sorbus, Pyracantha,Eriobotrya, Kageneckia, and Heteromeles (89,110). However, isolates pathogenic on Pyra-cantha, Eriobotrya, and accessions of Kageneckiaand Heteromeles could not infect Malus, there-fore were proposed to be of another species,Spilocaea pyracanthae (110). Le Cam et al. (80)suggested that, based on their ability to mate,they remain the same species, i.e., V. inaequalis,but separate formae speciales, f.sp. pyracanthaeon Pyracantha spp. and f.sp. pomi on Malus spp.Recent research indicated that V. inaequalis

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http://faostat.fao.org


populations from Malus, Pyracantha, andEriobotrya belonged to the same phylogeneticspecies, but divergence has occurred betweenthese populations, with those from Eriobotryaand Pyracantha being the most recentlydifferentiated (52).

In this review, we focus on scab resistancein Malus spp. associated with recognition ofV. inaequalis races mediated by race-specific ef-fectors. Approximately 20 scab R genes havebeen mapped to the apple genome and formost of them differential interactions have beendemonstrated. We describe these gene-for-gene (GfG) relationships and present an up-dated nomenclature system.

THE VENTURIAINAEQUALIS–MALUSPATHOSYSTEM

An intricate host-pathogen interaction struc-ture has evolved in the V. inaequalis–Maluspathosystem (89). Recent research supports theidea that the disease emerged in the center oforigin of apple, Central Asia (53), with M. siev-ersii the likely original host of V. inaequalis (54).V. inaequalis spread with apple to all corners ofthe world as people migrated to new territories,and scab probably became more prevalent be-cause clonal propagation of domesticated appleled to monoculture orchards (130). However,in some cases, e.g., several states in the UnitedStates, Japan, and Australia, V. inaequalis intro-ductions have been relatively recent, much laterthan the introduction of apple (89).

An important aspect of the life cycle of V. in-aequalis is its annual sexual phase on leaf litter inwinter. Pseudothecia are formed only from het-erothallic mating, requiring two different mat-ing types (73). Each pseudothecium containsmany asci, each containing four pairs (tetrad) ofascospores resulting from a meiotic division fol-lowed by a mitotic division. Ascospore progenythus carry different combinations of avirulencefactors compared with their parents. Becauseascospores give rise to haploid mycelium, thegenotype at each locus, either avirulence (Avr)or virulence (avr), is expressed unless masked

by epistatic interactions. The genetic basis ofavirulence can be investigated readily using invitro V. inaequalis crosses and tetrad dissection.

Gene-for-Gene Relationships

GfG relationships were first proposed by Flor(44) to explain the flax (Linum usitatissimum)-flax rust (Melampsora lini ) interaction as he pos-tulated that “for each gene that conditions re-sistance in the host, there is a correspondinggene that conditions pathogenicity in the par-asite.” Many specialist (hemi-)biotrophic para-sites conform to this type of relationship (69).The V. inaequalis-Malus interaction was one ofthe first examples for which GfG relationshipswere suggested based on the segregation of Avrgenes in the fungus (13, 145). Today, the resis-tance relationship is commonly hypothesizedto be a specific recognition event, either di-rect or indirect, between a host R gene prod-uct and a corresponding pathogen Avr geneproduct (69), the complexity of which is stillnot completely clear. Additionally, many ma-jor R gene loci in apple condition distinct phe-notypic reactions, which have been assignedto resistance classes (Table 1; Supplemen-tal Table 1, follow the Supplemental Mate-rial link from the Annual Reviews home pageat http://www.annualreviews.org): hypersen-sitive response (HR) in Class 1; stellate necrosis(SN) in Class 2; and chlorosis (Chl) with limitedsporulation in Class 3 (15, 119) (Figure 1).

V. inaequalis populations are usually highlydiverse genetically (53, 133, 134). The annualsexual phase followed by asexual multipli-cation during the growing season providesV. inaequalis opportunities for adaptive selec-tion of new strains. In V. inaequalis populationsin wild forests of Malus, selection is probablybalanced by a high diversity of scab R genes.In monoculture orchards typical of modernhorticulture, the narrow range of resistancespresent exert a high selection pressure onthe pathogen population. The use of well-characterized single-spore reference isolateswith known combinations of virulence andAvr alleles corresponding to known R genes

www.annualreviews.org • Apple Scab Host/Race Nomenclature 393

Supplemental Material

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Table 1 Nomenclature of the gene-for-gene relationships between Venturia inaequalis and Malus. The races are defined bythe avirulence genes they are lacking, hence resulting in susceptibility on the complementary host

Malus Venturia inaequalis

Differential host Resistance locusAvirulence

locus

Number Accession Phenotype Historical LGa New New Old Raceh(0) Royal Gala susceptibility – – (0)h(1) Golden Delicious necrosis Vg 12 Rvi1 AvrRvi1 (1)h(2) TSR34T15 stellate necrosis Vh2 02 Rvi2 AvrRvi2 p-9 (2)h(3) Genevab stellate necrosis Vh3 04 Rvi3 AvrRvi3d p-10 (3)h(4) TSR33T239 hypersensitive response Vh4 = Vx = Vr1 02 Rvi4 AvrRvi4d (4)h(5) 9-AR2T196 hypersensitive response Vm 17 Rvi5 AvrRvi5 (5)h(6) Priscilla chlorosis Vf 01 Rvi6 AvrRvi6 (6)h(7) Malus x floribunda

821bhypersensitive response Vfh 08 Rvi7 AvrRvi7 (7)

h(8) B45 stellate necrosis Vh8 02 Rvi8 AvrRvi8 (8)h(9) K2 stellate necrosis Vdg 02 Rvi9 AvrRvi9 p-8 (9)h(10) A723–6b hypersensitive response Va 01c Rvi10 AvrRvi10d (10)h(11) A722–7 stellate necrosis/chlorosis Vbj 02 Rvi11 AvrRvi11d (11)h(12) Hansen’s baccata

#2bchlorosis Vb 12 Rvi12 AvrRvi12d (12)

h(13) Durello di Forlı stellate necrosis Vd 10 Rvi13 AvrRvi13d (13)h(14) Dulmener

Rosenapfelbchlorosis Vdr1 06 Rvi14 AvrRvi14d (14)

h(15) GMAL2473 hypersensitive response Vr2 02 Rvi15 AvrRvi15d (15)h(16) MIS op 93.051

G07–098bhypersensitive response Vmis 03 Rvi16 AvrRvi16d (16)

h(17) AntonovkaAPF22b

chlorosis Va1 01 Rvi17 AvrRvi17d (17)

aLG = linkage group of apple.bTemporary differential host until the host has been confirmed as being monogenic, or a monogenic progeny from this polygenic host has been selected.cProvisional placement based on the assumption that the resistance in sources PI 172623 and PI 172633 are identical.dGene-for-gene relationship not confirmed to date.

Major effectresistance gene:resistance gene thatconfers a high level ofresistance, for examplehypersensitiveresponse, inincompatibleinteractions

in differential hosts will aid breeders in thepreservation of known R genes and the iden-tification of new ones. In the past, a numberof isolates poorly defined on a low number ofdifferential hosts have been used for geneticstudies (Supplemental Table 2), which hasled to uncertainty about specific interactions.

Definition of a Race

We define a single-spore isolate of the pathogenas a race when it is able to overcome completely

the resistance in a host. Determination of therace status is based on the premise that a mu-tation at the Avr locus in the pathogen leadsto nonrecognition by the host, hence leadingto complete susceptibility. The race spectrumis defined by the combination of R genes it canovercome.

The effect of resistance genes covers a con-tinuum from immunity for major effect genesto near-susceptibility for quantitative resistanceloci (QRLs), depending on its genetic back-ground, the pathogen, and the environment

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1 cm 1 mm 1 cm

a b c

Figure 1Characteristic scab resistance reactions on apple leaves. (a) Pin point pit, hypersensitive responseconditioned by the Rvi4 gene, (b) stellate necrosis by the Rvi2 gene, and (c) chlorosis with limited sporulationconditioned by the Rvi6 gene under glasshouse conditions (15).

Quantitativeresistance locus(QRL): resistancegene that conferspartial resistance; alsocalled minor effectresistance gene

Narrow spectrumresistance gene:resistance gene that iseffective against only afew isolates of thepathogen population

Broad spectrumresistance gene:resistance gene that iseffective against mostif not all isolates of thepathogen population

(109). The effect is independent of the spec-trum of the resistance gene, as both narrow andbroad spectrum resistance genes can conditiona range of resistance reactions (17).

The presence of lesions on differential hostsin the field (see References 8, 112) does notnecessarily mean the presence of a breakingrace but instead can represent opportunistic in-fections by avirulent strains under conditionshighly conducive to the disease. Follow-up re-search is therefore always required to confirmthe virulence status of putative race isolates (seeReferences 22, 23, 105).

Differential Interactions in theVenturia inaequalis–MalusPathosystem

Interestingly, the initial focus of genetic stud-ies on the V. inaequalis–Malus pathosystem wason avirulence in the pathogen rather than re-sistance in the host. Genetic analysis of over23,000 asci resulted in the identification of 19Avr genes, named pathogenicity ( p) genes (12,13) (Supplemental Table 3). The first allelesassigned were p-1 and p-1+ for the Avr and avralleles, respectively, on the commonly growncultivar McIntosh (13). Most Avr loci in V. in-aequalis reported to date are inherited indepen-dently (7, 124, 145). Independent segregationof Avr loci provides the pathogen with a largepotential to develop new pathotypes during the

sexual cycle (12). Nevertheless, some loci arelinked, e.g., the p-8, p-9, and p-12 loci (145),and recently a further two clusters of four Avrgenes were identified in a mapping study ofV. inaequalis Avr genes (17).

Many of the first described interactionsinvolved genes conferring resistance effectiveagainst a low proportion of the pathogen pop-ulation, i.e., they were narrow spectrum (versusbroad spectrum) genes (2, 3, 13). Similar re-sults were found more recently with other sus-ceptible cultivars, such as Boskoop, Bramley,Cox’s Orange Pippin, Spartan, and Worcester(4, 123, 125), and the genes Vt57 (26), Vs/Vsv(17, 22), and Vd3 (127). The early V. inaequalisgeneticists also realized that it was impracticalto name all the races, as the isolates carryingthe first 19 avr ( p) alleles represented over halfa million possible permutations of these alleles,hence as many potential races of V. inaequalis.Therefore, only those isolates that could over-come broad spectrum R genes with potentialfor resistance breeding were defined in the racenomenclature (89), comprising eight races thathave been described to date (SupplementalTable 4). This old nomenclature system, how-ever, was cumbersome as a single race numbercould involve several GfG relationships, e.g.,race (2) isolate 356-2 could overcome the dif-ferent resistances in Dolgo, Geneva, and certainsegregates of Russian apple R12740-7A (121).A system where all compatible interactions can



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be named separately is therefore required (25)as originally intended (145). This will allowthe race status of existing isolates to change asthey will invariably be shown to carry additionalAvr alleles resulting in new host-pathogeninteractions.

NOMENCLATURE OF VENTURIAINAEQUALIS RACES

The nomenclature system for the V. inaequalisavirulence genes and races commenced usinga numerical system, but this was not followedthrough with the naming of the complemen-tary scab resistance genes. The nomenclaturefor the latter was based on identifying them bytheir source of resistance, therefore the GfG re-lationships between the resistance genes in thehost and the avirulence genes in the pathogenwere not obvious. This anomaly will be cor-rected in the nomenclature system proposedhere, which is based on the system first pro-posed for Phytophthora infestans and potato (9)and is commonly used for other host-pathogeninteractions.

The Nomenclature Model

In describing GfG relationships, where k rep-resents the number of the specific interaction,each Rk-Avrk interaction can be represented bya differential host carrying only the Rk geneand an isolate of the pathogen having alteredor lost only the complementary allele, identi-fied as avrk, at the Avrk locus. Once the in-dividual Rk-Avrk interaction has been defined,isolates lacking multiple avirulences can thenbe identified by their formula based on thecombination of the individual virulences. It ac-commodates complex loci as well as QRLs forwhich differential host-pathogen interactionsare demonstrated. Simultaneously with the re-vision of these GfG relationships, we align thenomenclature of apple scab R genes with the in-ternational standard of gene nomenclature forArabidopsis (97). The names of major R genesstart with R and contain an abbreviation of the

pathogen V. inaequalis to give the general locusprefix Rvi.

The proposed system is based on the fol-lowing minimum criteria being imposed beforea new Rvi-AvrVi interaction is added:

1. The R gene has been shown to segregatein a simple manner and is present in agenetic background from which a suitablereference host can be selected.

2. The R-Avr interaction has (sufficiently)been shown to be novel either with the aidof a breaking race that has been screenedagainst all other reference hosts to estab-lish that the new Avr allele is differentfrom existing alleles or preferably also byscreening the R gene against all the estab-lished race reference isolates to demon-strate that none of them breaks the resis-tance. Novelty is also confirmed when agene maps to a position where no knowngenes have been mapped previously, inthe expectation that the genetics of theGfG relationships will be elucidated.

3. Plant material of the differential hostand, where one is known to exist, alsothe corresponding reference race of thepathogen are available, so that the systemcan be readily utilized to build on currentknowledge.

Races lacking more than one Avr gene at dif-ferent loci will be identified as race (k,l,m, . . .)and hosts carrying multiple R genes will benamed host (k,l,m, . . .) or h(k,l,m, . . .). In caseswhere several candidate genes are identifiedfrom genome sequence data (e.g., for Rvi6; seebelow), we suggest that the functional paralogis named Rvik and the others Rvik.1, Rvik.2, . . .until differential interactions warrant namingthem in their own right.

Venturia inaequalis–MalusGene-for-Gene Relationships

Below we describe the 17 GfG relationshipsdefined to date and add relationship (0) in-volving host (0) that does not carry any resis-tance genes to correct the erroneous use of

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race (1) to date. We identify the knowledgegaps and confirm the genetics of resistance and(a)virulence in different accessions and races. Inthe development of the new numerical nomen-clature system, we aimed to maintain as muchof the existing system as possible by making useof current associations of race numbers withgenes. The accessions representing the differ-ential hosts for races (2) to (7) remain largelythe same, although there is some rationaliza-tion by assigning host status, where possible,to Malus accessions carrying a single R allele(Table 1). Some of the well-characterizedgenes with temporary working names that areused in breeding will be assigned Rvi-AvrRvi re-lationship numbers for inclusion in the nomen-clature system. We also recognize that someof the resistances have long played an impor-tant role in apple breeding, but GfG relation-ships have not been confirmed and/or differen-tial hosts have not been selected. In all of thesecases, research is in progress to rectify the sit-uation, as is the determination of a set of refer-ence isolates of V. inaequalis representing cor-responding races, which will be reported at alater stage.

Relationship (0). Host (0) can be defined asthe host that does not carry any R genes andhence is susceptible to all isolates of V. inae-qualis. Today, Gala, or more often its sports, isthe commonly used universally susceptible hostin many scab experiments, and it is also a widelygrown cultivar and an important parent in manybreeding programs worldwide. Although V. in-aequalis showed a lower rate of disease develop-ment on this cultivar, attributed to two QRLs(128), than on Golden Delicious (103), it is gen-erally highly susceptible. It therefore has beenselected to represent h(0) (Table 1). On thepathogen side, the common race (121, 145) ofV. inaequalis was originally defined as race (1),which is inconsistent with the race names inother pathosystems. We therefore rename itrace (0) and define it as the race that is avir-ulent to all hosts carrying R genes and henceinduces lesions only on hosts not carrying anyknown scab R genes. We recognize that, as new

relationships are added, this will actually be-come a theoretical definition because no ref-erence candidates exhibiting a complete aviru-lence pattern will be available.

Relationship (1). An exception to the premisethat narrow spectrum R genes should be ex-cluded from the nomenclature is made for theRvi1 (Vg) gene from Golden Delicious. Al-though this gene is overcome by an estimated87% of the pathogen population in Europe(103), both host (1) and race (1) have been ex-tensively characterized, which makes this animportant model system to advance our un-derstanding of the basis of ephemeral, versusdurable, R genes. The inclusion of relationship(1) also reduces the degree of confusion be-tween races (0) and (1), as isolates described asrace (1) in the old nomenclature before the dis-covery of Rvi1 generally can overcome it, hencethey remain race (1) in the new nomenclature.

Differential interactions of isolates withGolden Delicious (119) suggested the presenceof a resistance factor. The monogenetic natureof this resistance was first demonstrated withavirulent isolate 101 (84) and confirmed withisolate 1066 (7). Rvi1 (Vg) maps to the very dis-tal end of linkage group (LG) 12 of Prima (40)(Figure 2), which has Golden Delicious as oneof its grandparents. The Rvi1 gene conditionsnecrotic resistance reactions (84, 100), whichmay show weak sporulation (31).

The segregation of the complementary Avrgene in this GfG relationship was demonstratedin a cross between the virulent V. inaequalis iso-late 104 (79, 104) and avirulent isolate 147 (61).These findings were confirmed in a 301 (viru-lent) x 1066 (avirulent) progeny set (7) that wasused in the attempt to clone AvrRvi1 (18).

Relationship (2). Early genetic studies onRussian apple R12740-7A, whose resistance re-actions ranged from Class 0 (no macroscopicsymptoms) to Class 2 (necrosis), depending onthe inoculum used (119), showed that it con-tained at least two (34), if not three, scab resis-tance genes (122): Vr was assigned to the puta-tively race-nonspecific gene effective against all


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LG1

Rvi10

Rvi6

Rvi17

AG11

CH05g08

CH-Vf1

Rvi15

Rvi4CH02c02a

Rvi16

CH03e03

CH03g07

Hi03d06

AU223657

Rvi3Hi08e04

Rvi14

CH03d12

CH03c01

CH03d07

HB09

CH0202b

CH05d02

CH1d03y

CH04e02

CH03g12y

CH03g12a

Rvi11

Rvi9Rvi2Rvi8

Aco-1

CH03d01

CH05e03

LG2 LG3 LG4 LG6

LG8

Rvi7

Rvi13

CH02b07

CH05h12

CH04f03

CH03d11

GD100

Rvi1

Rvi12

CH01d03z

Hi07f01

CH01f02

CH01g12

CH05d04

Rvi5Hi07h02

NZ17e06

CH04c06

CH02g04

CH04f08

CH01e12

CH01c06

CH05a02y

CH01h10

Hi15h11

LG10 LG12 LG17

Figure 2Global positions on the apple genome of the 17 Rvi scab resistance genesnamed to date. The skeleton genetic map is based on the integrated consensusmap by N’Diaye et al. (99).

known races of V. inaequalis at that time (32),and the Russian apple derivatives Si and S’i werethe differential hosts for races (2) and (4), re-spectively (82, 100). Host (2), first shown to beovercome by the South Dakota isolate 356-2,

was known to condition Class 2 resistance reac-tions (121), which recently were specified as SN(26). Nevertheless, Vr became associated withthe SN phenotype (1), but this error was cor-rected when Vr in Russian apple (59) and Vh2in TSR15T34 (26) were shown to be the same.Rvi2 has been mapped to the lower end of LG2in h(2) accession TSR34T15, an F2 selection ofRussian apple (Figure 3), and Vr is now puta-tively associated with a Class 3 chlorotic phe-notype also described by Aldwinckle et al. (1),but whose mapping position remains elusive.

Host (2) has mistakenly been reported asbeing accession TSR34T132 (104, 105), anerror perpetuated in other papers (e.g., 50,89, 112). However, the correct identifica-tion numbers are TSR34T15 (correspondenceE.B. Williams to Y. Lespinasse, 20 February1984) and PRI 384-1 (26). In the same cor-respondence TSR34T15 is also identified asOR42T173 (145), but this has been disputedbased on genetic marker research (95).

The original race (2) isolate 356-2 is nolonger available, and its replacement, 1770-3,identified in the Purdue-Rutgers-Illinois (PRI)program and distributed as race (2), more re-cently was found to be unable to infect h(2) (20).Isolate 1639 has been shown to overcome theRvi2 gene (26), but AvrRvi2 in this isolate seg-regated 3:1 rather than 1:1, and it is also linkedto other AvrRvi genes, which indicates that thisrelationship may be more complicated than asimple GfG one (17).

Relationship (3). Geneva is a red-leafed,open-pollinated selection of M. pumila (68),which was regarded as resistant to scab until1951 when it was reported as infected in NovaScotia (120). Although the resistance symptomscan range from HR to Chl (71), avirulent iso-lates predominantly induce SN reactions butwere able to sporulate under extended mois-ture conditions in lesions described as 2 → 4(121). In fact, Geneva was shown to carry tworesistance genes, and the authors’ interpreta-tion was that the p-10 locus induced Class 2resistance reactions with one R gene and the in-dependently segregating p-11 locus the 2 → 4

398 Bus et al.

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phenotype with another gene (SupplementalTable 5). However, a Chl-conditioning genewas also observed in Geneva (145), which sug-gests that it carries three genes; hence, NovaScotia isolate 651 used in the study would lackall three complementary Avr alleles. To date,two linked genes, temporarily named Vh3.1and Vh3.2, were mapped to LG4 in proge-nies of Geneva crossed with Elstar and Brae-burn (V.G.M. Bus et al., unpublished data)(Figure 2). Research is in progress to deter-mine which gene has the broader spectrum andtherefore should be assigned Rvi3. This willmost likely not be Vh3.2 because isolate 1639was the only one out of six isolates that couldnot infect Geneva x Braeburn accession Q49carrying the gene (V.G.M. Bus, unpublisheddata). Its complementary gene in the pathogenhas been mapped as AvrVh3.2 to an Avr genecluster in isolate 1639 (17). Until further elu-cidation, Geneva will remain h(3) and the U.S.isolate 1774-1 reference race (3).

Relationship (4). Although derivatives ofRussian apple R12740-7A were long known tocondition HR (121), it is only recently that theRvi4 gene in the F2 derivative TSR33T239 ofRussian apple (Figure 3) was definitely associ-ated with this resistance phenotype (26). Severalnames have been assigned to the gene. First,the temporary name Vx (29) was assigned toindicate that its genetic relationship to knowngenes needed further elucidation, following theidentification of linked markers (59). Initial po-sitioning to LG6 of the White Angel map (60),equivalent to LG10 on the European apple map(85, 90), was inconclusive until it was mappeddefinitively to LG2 of TSR33T239 (26)(Figure 2). Using the cultivar Regia, it wasalso named Vr1 to differentiate it from otherRussian apple genes in genetic studies per-formed in Germany (14).

The reporting of V. inaequalis race (4) haspersistently been attributed to Shay et al. (122)in other reports (89, 141, 144); however, theymerely stated that Russian apple “is known tocontain at least 3 gene pairs, only one of whichis resistant to all known races.” Several isolates

TSR34T15 (PRI 384-1; OR42T173)

Host (2)McIntosh

Russian apple R12740-7AR7T81 (PRI 45-39)

Delicious

Host (4) WealthyDg. R13T43 (PRI 27-330)

TSR33T239 (PRI 478-33; W7AR44T20) Russian apple R12740-7ADelicious

Host (5)McIntosh

9-AR2T196 (PRI 643) Wolf RiverR14T102 (PRI 76-29)

M. micromalus 245-38

McIntoshOR45T132 (PRI 333-9) Wolf River

R16T52 (PRI 69-118)M. x atrosanguinea 804

Host (6)Starking Delicious

Priscilla (PRI 1659-1) McIntoshPRI 610-2 Golden Delicious

PRI 14-26626829-2-2

Host (8)Sciearly

B45M. sieversii GMAL4302-X8

ScirosN23

M. sieversii GMAL4026-X435

Host (9)Elstar M. baccata

K2 M. x robustaDolgo M. prunifolia

Open-pollinated

Host (10)Worcester Pearmain

A723-6PI 172623 (B VIII 33,25)

McIntoshPRI 1841-11 (CCR3T11) PI 172633 (B VIII 34,6)

PRI 703-1 (9-AR6T136)Jonared

Host (11) Starking

A722-7M. baccata jackii

Figure 3The pedigrees of Malus differential hosts for apple scab derived from mostlypolygenic accessions.

of V. inaequalis have been identified as race (4)in both the United States and France (Supple-mental Table 2); however, none of these wascompletely compatible with hosts carrying theRvi4 gene (Figure 4) (20).

Relationship (5). Malus micromalus 245-38and Malus x atrosanguinea 804 were identifiedearly in the PRI breeding program (63) ashighly resistant sources conditioning HR, vis-ible within three days after inoculation (119,



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a

EU-NL19 EU-NL19 EU-B05

1638 1638 1638

b c

Figure 4Partial differential interactions of Venturia inaequalis isolates on seedlings (a)E035 and (b) E053 of a Royal Gala x TSR33T239 family; and (c) F002 of anA19R03T127 x TSR33T239 family carrying the scab resistance gene Rvi4 fromhost (4). Race (4) isolate 1638 first induced a hypersensitive response on theseseedlings, which was followed by different levels of sporulation, ranging from(a) very limited and (c) dense to moderate. Each top-bottom pair of symptomsis the result of simultaneous inoculation of a pair of isolates on the same leaf.

146). Both accessions also carried a Chl-conditioning gene for scab resistance that ap-pears allelic to Rvi6 (Vf ) (33, 143).

The HR-conditioning gene (Rvi5) in M. mi-cromalus 245-38 segregated as a single gene inprogeny of F1 accession PRI 76-27 (118) andwas later confirmed in related progenies (24,62) (Supplemental Table 6). Segregating in-dependently from other major gene loci (32),the name Vm was assigned to the allelic genein both original sources (33). By that stage, arace of V. inaequalis had been identified amongisolates collected from M. micromalus trees inEngland (141), and in France in 1968 certainRvi5 progeny of M. micromalus 245-38 becameinfected (84). The commonly used M. microma-lus derivative 9-AR2T196 (Figure 3) has beenselected as the reference h(5). Genetic markersfor Rvi5 were identified in M. x atrosanguinea804 derivatives NY748828-12 and OR45T132(Figure 3) (29) before it was mapped to LG17of Murray (108) (Figure 2).

A number of race (5) isolates have been iso-lated from Rvi5 hosts, including isolate 147,

which is incompatible with Rvi1 hosts (61, 84).A fraction of three proteins with elicitor activ-ity from isolate MNH120 (146) may include theAvrRvi5 effector.

Relationship (6). The genetics of the resis-tance from Malus x floribunda 821, the sourceof Rvi6 (Vf ) resistance (64) and progenitor ofmost scab-resistant apple cultivars to date, hasbeen extensively reviewed (50, 89). Many al-lelic sources of Rvi6 have been identified (33,142, 143), some of which have been suggested toalso carry the gene based on the specific linkageof the CH-Vf1-159 bp allele with Rvi6 (137).Sequencing of the locus revealed that it con-tains four paralogs (136, 148), which we pro-pose to rename Rvi6 for HcrVf2/Vfa2 (5, 102)and Rvi6.1 to Rvi6.3 for the other three par-alogs. The Rvi6.1 (HcrVf1/Vfa1) paralog mayalso be renamed if its functionality (92) is con-firmed as having sufficiently broad utility.

Rvi6-associated resistance is variable in bothsegregation ratios and resistance levels (30), anda range of explanations for this has been pro-posed, e.g., influence of QRLs (39, 50, 89, 111,144) and variation in incubation conditions andinocula applied (74, 78). Ratios lower than theexpected R:S = 1:1 have also been attributedto (sub)lethal genes linked to Rvi6 (48). A sim-pler explanation, however, is that some plantspresented a phenotypic reaction with chloro-sis and high sporulation, i.e., Class 3B (30),and were assumed as not carrying the gene (89,129), whereas genetic markers could confirmRvi6 being present in most seedlings in thisclass (49). In early backcross generations, theM. x floribunda 821 resistance clearly segregatedas a single major gene (64) (SupplementalTable 7), but differential interactions amongF2 descendants of M. x floribunda 821 (104) sug-gested the presence of a second gene (7), Rvi7(see below).

Race (6) of V. inaequalis is defined by its com-patibility with hosts carrying Rvi6 only (83), butto date many of the commonly used h(6) acces-sions (e.g., Prima and Florina), were found toalso carry Rvi1. Because Priscilla does not (7),we propose it as h(6). The initial race (6) studies

400 Bus et al.


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were mostly performed with isolate 302 (7, 104)collected from a Prima derivative in Germanyin 1988 (105). Recently, isolate EU-D42 fromthe European core collection has been used asthe reference isolate for race (6; for examples,see References 26, 79, 103, 127, 128).

Relationship (7). Studies with isolate 1066 ledto the identification of the HR-conditioningRvi7 (Vfh) gene in M. x floribunda 821. It seg-regates independently from Rvi6 (7) and wastentatively mapped to LG8 (38) (Figure 2).Research to identify a single gene referenceh(7) from an M. x floribunda 821 progeny is inprogress.

A GfG relationship for Rvi7 was most clearlydemonstrated through the differential interac-tions of the incompatible isolates 104, 301, 302,and 1093, and the compatible isolate 1066 oncertain progeny of a Golden Delicious x M. xfloribunda family (7) (Supplemental Table 8).A more recent virulent isolate is EU-NL05from the European core collection (103).

Relationship (8). A GfG relationship wasdemonstrated for the Rvi8 (Vh8) gene from M.sieversii host (8) accession GMAL3631-W193Bfrom the Tarbagatai mountain range in Kaza-khstan, and the AvrRvi8 gene segregating inprogenies of race (8) isolates NZ188B.2 (22)and 1639 (17). The Rvi8 gene conditions SNthat is indistinguishable from that conditionedby Rvi2 and both genes map to the lower end ofLG2 (22, 26). Rvi8 and Rvi2 are closely linked,if not allelic, but are clearly separate genes be-cause isolate NZ188B.2 cannot infect h(2). Sim-ilarly, the Avr loci showed genetic interaction,but its nature is not clear (17). The differen-tial interaction of race (8) isolate NZ188B.2was clearly demonstrated in a range of M. siev-ersii hosts (22), suggesting that Rvi8 is preva-lent in the Kazakh accessions sampled. Twomore differential hosts have been selected fromthis germplasm: B45 derived from accessionGMAL4302-X8 and N23 from GMAL4026-X435 (Figure 3) (V.G.M. Bus, unpublisheddata), of which B45 is the reference h(8).

Relationship (9). The presence of a majorgene in the crabapple Dolgo (Figure 3) hasbeen demonstrated in three independent stud-ies (Supplemental Table 9) (3, 118; V.G.M.Bus, unpublished data). From the fact that Rvi2-and Rvi9-conditioning SN resistance reactionsare indistinguishable from each other and thatthe South Dakota scab isolate 356-2 could over-come both genes (96), one could have con-cluded that the genes were the same. How-ever, studies with a 356-2 x 651 progeny clearlydemonstrated separate GfG relationships forRvi2 and Rvi9, and genetic dissociation of theirrespective complementary Avr loci, originallynamed p-9 and p-8, in the fungus (Supplemen-tal Table 5) (121). Interestingly, both Rvi9 andRvi2 map close together on LG2 (Figure 2),and their complementary Avr genes are alsolinked in the pathogen (17, 145). Furthermore,AvrRvi9, like AvrRvi2, shows a 3:1 segregationpattern toward avirulence, with two progeny ofthe EU-B04 x 1639 cross carrying only Avr-Rvi9 (17) and therefore being reference race (9)candidates.

Progeny K2 of an Elstar x Dolgo(Figure 3) has been selected to replaceDolgo as h(9) because the contrasting in-teractions of the EU-B04 and 1639 parentsconfirmed the presence of the previouslysurmised second scab gene in Dolgo (145),which is identified by only a few isolates. AGfG relationship was demonstrated for thisVdg2 gene in the Elstar x Dolgo progeny K108(17) but is not included in the nomenclaturesystem because it is a narrow spectrum gene.

Relationship (10). The Rvi10 (Va) gene wasoriginally identified in the Antonovka accessionPI 172623 (32) but has also been attributed to PI172633 (82), PI 172612 (144), Freedom (152),and as Va2 to Antonovka APF22 (37). However,the resistance reactions on neither the Freedomnor Antonovka APF22 progenies showed thedistinct HR associated with Rvi10 (32), hencerequiring further investigation.

Because all three PI accessions are con-firmed selections from the same B VIII familyderived from open-pollinated Antonovka (114),


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Monogenicresistance: theresistance in a host isconditioned by a singlegene; the gene can be amajor or minor effectresistance gene

Polygenic resistance:the resistance in a hostis conditioned by morethan one gene

all of them indeed may carry Rvi10. However,being derived from the original Rvi10 source PI172623 (32), A723-6 (Figure 3) is the preferredh(10) (50), and research is in progress to con-firm its resistance being monogenic given thatdifferential interactions, compared with puta-tive Rvi10 accession PRI 1841-11 (CCR3T11),with race (6) isolates 302 and 305 (104) suggestits parent PI 172623 carries two R genes.

Assuming that PRI 1841-11 derived from PI172633 (Figure 3) carries the gene, Rvi10 hasbeen mapped about 24 cM above the Rvi6 re-gion on LG1 (58) (Figure 2). This confirmedearlier findings that the phosphoglucomutase(PGM-1) marker (90, 93) is linked to both genesbut contradicts the reported independent seg-regation of Rvi6 and Rvi10 (32). We note, how-ever, that the number of testcrosses used bythese authors was too small to be conclusive.Also, a better understanding of the polygenicAntonovka scab resistance needs to be devel-oped before a reference race (10) can be identi-fied [see relationship (17) below].

Relationship (11). Malus baccata jackii was rec-ognized early in the PRI backcross program tocarry Rvi11 (Vbj) (32). Rvi11 maps as a distinct Rlocus near simple sequence repeat (SSR) markerCH05e03, just below the middle of LG2 (57)(Figure 2). A722-7 from an M. baccata jackiicross with Starking (Figure 3) is designatedas h(11), provided the resistance of A722-7 isconfirmed as being monogenic since M. baccatajackii carries at least one additional narrow spec-trum R gene (V.G.M. Bus, unpublished data).To date, no race (11) isolates have been re-ported.

Relationship (12). Rvi12 (Vb) from Hansen’sbaccata #2 is another gene that was recognizedearly as an independently segregating gene(32). Although it was initially mapped on LG1(58), Rvi12 was later definitively mapped toLG12 (41) at a considerable distance from Rvi1(Figure 2). The gene predominantly condi-tions Chl, in some cases with sporulation,whereas a few progeny show necrotic reactions(32, 41). With Hansen’s baccata #2 carrying

more than one gene, research is in progressto select an h(12) carrying the single geneRvi12 resistance. No differential interactionswith Rvi12 have been reported to date.

Relationship (13). The old Italian cultivarDurello di Forlı containing the major geneRvi13 (Vd ) (131) has been designated h(13).The gene maps to the proximal end of LG10of this host near SSR marker CH02b07(Figure 2). The resistance reactions range fromtypical SN when the host is inoculated withindividual V. inaequalis isolates, such as EU-D42, to sporulating Chl reactions when inocu-lated with a mixture of isolates (131). AlthoughDurello di Forlı appears to carry broad spec-trum resistance to apple scab that may involvemore than one R gene or QRL (50), certain iso-lates, such as 1066 and EU-NL05, are able toovercome Rvi13 (79, 103).

Relationship (14). The potential ofDulmener Rosenapfel, a scab-resistant cultivarraised from open-pollinated Gravenstein,in resistance breeding was confirmed as itdemonstrated broad spectrum resistance (79).The resistance complex includes the Chl-conditioning gene Rvi14, previously knownunder the working name Vdr1 (38), which is thefirst scab resistance gene to have been reportedunder the new nomenclature system presentedhere and also is the first R gene that maps toLG6, toward the top near SSR marker HB09(128) (Figure 2). The resistance is overcomeby V. inaequalis isolates 301, EU-D42, andEU-B04, all of which are being characterizedfor their suitability as reference isolates.

Relationship (15). The gene Rvi15 (Vr2) wasoriginally thought to be the third scab R genefrom Russian apple (50). However, once it wasestablished that its source accession GMAL2473 was not related to Russian apple, the genewas recognized as a new source of resistance(106). Although the gene has been shown toinduce a range of resistance reactions fromno symptoms to Chl in progeny of a crosswith Idared (106), it conditioned only necrotic

402 Bus et al.

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reactions in a cross with Golden Delicious (50).Detailed observations determined that the phe-notype is HR (45), very similar to those condi-tioned by Rvi4, to which it appears to be closelylinked on LG2 (46, 106) (Figure 2). The lo-cus contains three TIR-NBS-LRR analogs (47)and if, by analogy to the Rvi6 locus, one of themproves to be Rvi15, the other two will be namedRvi15.1 and Rvi15.2 if they are not functional.No V. inaequalis isolate virulent on Rvi15 hostshas been identified to date.

Relationship (16). The Rvi16 gene, with theworking name Vmis, was identified in the open-pollinated mildew immune selection (MIS)progeny 93.051 G07-098 (21). The gene condi-tioned a range of resistance reactions from pre-dominantly no visible symptoms with single-spore isolate J222 to Chl reactions with a mix-ture of V. inaequalis isolates. The resistance wasmapped to the lower end of LG3, near SSRmarker AU223657 (Figure 2). Recent observa-tions with an extended range of monospore iso-lates on an open-pollinated MIS progeny sug-gest that it also carries a narrow spectrum gene(V.G.M. Bus, unpublished data), hence a mono-genic h(16) will need to be selected.

Relationship (17). Recently, two genes weremapped in an Antonovka APF22 progeny, oneof which is Va2 and possibly the same as Rvi10(see above), whereas the other is Va1, now as-signed Rvi17 (37). The gene was identified in aprogeny screened in the field and confirmed ona subset of plants inoculated in the glasshouse.Rvi17 maps within 1 cM of Rvi6 on LG1(Figure 2), but is different from Rvi6 since it isnot overcome by race (6) isolates and has a spe-cific CH-Vf1 marker allele of 138 bp linked to it(37) [159 bp for Rvi6 (137)]. A suitable differen-tial host is being selected for the determinationof differential interactions with V. inaequalis.

Potential Additional Differential Hosts

The revised nomenclature for the V. inaequalis–Malus pathosystem is proposed to facilitatework with existing genetic resources and to clar-

ify the identity of new genes. Some genes, suchas Vc and Vj from Cathay and Jonsib, respec-tively (32, 75), display differential interactions(104), but there is insufficient data on the genet-ics of these resistances to warrant inclusion atthis time. With 992 NBS-LRR and 575 LRR-kinase candidate resistance genes identified inthe apple genome (135) and approximately 20scab resistance genes phenotypically mappedonto genetic maps, it is clear that many moregenes remain to be revealed through functionaltesting.

Complex Races and Hosts

As outlined above, isolates uniquely lacking theAvr locus complementary to the R gene in eachhost will be hard to find. For example, referencerace candidate for relationship (1) EU-B04 canovercome Rvi14 besides Rvi1, hence it is identi-fied as race (1,14), and is able to overcome manynarrow spectrum genes that are not taken intoaccount in the nomenclature (17). Availabilityof phenotyped V. inaequalis progenies will fa-cilitate the selection of reference isolates. Forexample, two progeny from race (1,2,8,9) iso-late 1639 crossed with EU-B04 have been iden-tified that can only overcome Rvi9 and Rvi1,and therefore are race (1,9), whereas isolateNZ188B.2 (22) is race (1,8). Linkage betweenAvr loci, however, may prevent the selection ofsimple reference isolates, such as race (1,2) inthe EU-B04 x 1639 cross. Other examples ofcomplex races are 1066, which is race (6,7,13),and EU-NL24, which is race (1,3,6,7). Giventhat the latter is known to overcome Antonovkagenes, its status is sure to change. Complemen-tary to the race nomenclature, hosts carryingmultiple R genes can be identified accordingly,e.g., M. x floribunda is host (6,7), Prima is host(1,6), and Russian apple is host (2,4).

Further research is required to complete thetable on the host-pathogen interactions of thecurrent reference isolates or their replacementisolates, including reevaluation of several inter-actions, as some tests have been contradictoryand/or inconclusive. Additional reference iso-lates need to be identified and characterized on


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the differential hosts for the scab R genes, forwhich no reference race isolates have been iden-tified to date (assuming they exist).

Genetic and Genomic Tractabilityof Host and Pathogen

Genetics and genomics of both the host andpathogen in the Malus–V. inaequalis interac-tion have advanced dramatically in the past twodecades. In terms of the host, comprehensivegenetic maps exist, and a version of the genomesequence has just been published (135). Applebehaves in most aspects as a genetic diploiddespite the polyploidization event in the his-tory of the Rosaceae subfamily to which it be-longs. Candidates for both major R gene lociand important resistance QRLs can now bemined and empirically tested by using genomesequence, aided by next-generation sequenc-ing skim reads from selected hosts carrying al-leles of interest. Other genomic aids, such astransformation (67, 91, 151) and gene knock-down using RNAi (51) are also practical in thehost and will aid in identifying functional al-leles. In terms of the pathogen V. inaequalis,the first genetic maps have been developed(17, 149), and genome sequencing (28a; M.Templeton, personal communication; B. LeCam, personal communication) and in plantatranscriptomics (M. Templeton, personal com-munication) will further facilitate the identi-fication of specific Avr genes. Asexually pro-duced conidia of V. inaequalis allow each geno-type to be fixed through clonal multiplicationin vitro for use in phytopathological and ge-nomic studies. In addition, transformation sys-tems are available that enable complementationand RNAi-based knockdown of genes (42, 43)to validate fungal effector function as candidatesare identified (16, 77). Heterologous expressionin apple or yeast, combined with purification ofindividual V. inaequalis avirulence proteins, mayalso allow elucidation of specific GfG interac-tions. Thus, both host and pathogen systemsare now eminently tractable and the pace of ad-vances in Malus–V. inaequalis research can beexpected to accelerate in the next decade.

CONCLUSION

A thorough understanding of host-pathogeninteractions is required if we are to achievedurable resistance, particularly in perennialcrops such as apple. The identification of dif-ferential hosts with monogenic resistances willassist in the monitoring of pathogen popula-tions to determine the potential of specific Rgenes, currently the main sources of resistancein apple breeding. It is clear that not all R genesare equivalent when it comes to durability. De-veloping durable strategies will require signifi-cant knowledge advances in several areas: iden-tification of the armory of pathogen effectorsthat manipulate host-preformed and inducedbarriers to infection; how pathogen moleculestrigger defense in hosts; how host factors re-late to quantitative resistances; and how non-host resistance operates. Moreover, durabilityof a combination of R genes can be somewhatdifferent from the simple addition of intrinsicdurability, if measurable, of each gene involved.Current strategies to create durable scab resis-tance in apple involve gene pyramiding withboth R genes and available quantitative resis-tances (28, 39, 86, 128), which has proved ef-fective in other crops (see References 19, 101),or transgenics involving antifungal proteins(11).

Apple breeders have a broad range of Rgenes and QRLs available to them for creat-ing polygenic resistances. Currently in tradi-tional breeding, marker-assisted selection, mosteffectively with functional markers, plays an es-sential role in efficiently developing new cul-tivars (117) with the desired R gene combina-tions effective against scab and other pests anddiseases. Unless breeders have detailed knowl-edge of the most effective R gene and/or QRLcombinations, genes will continue to be pyra-mided at random, until research shows that cer-tain R genes/QRLs may be superior in termsof their individual durability. This is conceiv-able as some of the resistance proteins are likelyto recognize effector proteins significant to thepathogen infection process and/or have a dif-ferent mode of action.

404 Bus et al.

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Although many natural scab resistance pyra-mids of major R genes have been identified ingermplasm, this does not necessarily translateinto durable resistance. Combinations presentin, for example, Russian apple R12740–7A andM. micromalus have not been deployed exten-sively in temporal or spatial terms to confirmtheir durability, and the development of race(6,7) on M. x floribunda (7), at first glance,suggests that pyramiding is no guarantee fordurable resistance. This race may have acquiredthe virulences in sequential order, which, if thisis the case, accentuates the need for only releas-ing cultivars with at least two, if not three ormore, resistance genes. It has been suggestedthat four to six genes may provide long-termresistance or even immunity (98). Gene pyra-miding will be more effective if it is aimed at themost essential effector genes from the pathogen(140), i.e., the effectors that evoke the maximumfitness cost when lost or compromised (81).

A glasshouse simulation study with race (5)isolates of V. inaequalis indeed suggested thatsome, but not all, isolates had a lower fit-ness leading to their disappearance from thepathogen population (61). Similarly, isolatesof race (6) were shown to exhibit a lower fit-ness when compared with isolates of race (1)(27). It is anticipated that sequential losses ofthe pathogenicity factors (effectors) that arecommonly encoded by Avr loci will increas-ingly reduce the fitness of the pathogen untilthe combined losses become insurmountable,which would lead to stabilizing selection (132).

The efficacy of gene combinations will bepartly determined by the geographical distribu-tion of cognate races. V. inaequalis populationsare highly diverse genetically, both within or-chards and regions as well as in different partsof the world (53, 133, 134, 150), and differ intheir virulence in different geographical regions(see Reference 87). The next major challenge isto determine the race distribution of V. inae-qualis in apple production regions and to de-velop a strategy for the durable deployment ofR genes, and to prevent it from being undonethrough human activity (56). To this effect, apathogen population monitoring program has

been initiated involving the establishment ofa network of trap orchards around the worldcomprising a range of well-characterized differ-ential hosts (107). Breeders and researchers canregister to participate in this project at the web-site http://www.vinquest.ch and will receivebudwood of the differential host set. Newlyconfirmed GfG relationships can be reportedthrough the same website for inclusion in therevised nomenclature system.

Race monitoring will be aided by the iden-tification of Avr/effector proteins, which will inturn facilitate R gene identification and deploy-ment. To date, no Avr genes have been cloned;however, the identification of SSR markers inV. inaequalis (55, 134) and mapping of aviru-lence loci (17) have been the first step towardthe mapping and cloning of the first Avr gene,AvrRvi1, in this pathogen (18).

Research on host-pathogen interactions atthe molecular level and understanding the rolethat proteins, such as NBS-LRR, play in therecognition and signaling pathways (6) is oneof the major research topics in plant sciencetoday. Knowledge of plant defenses that arevulnerable to pathogen attack and cell deathsuppressors that negate the programmed celldeath of HR in the presence of R-Avr interac-tions (e.g., 94) has thrown new light on GfGrelationships. In the arms race, the host evolvesnew resistance specificities through intragenicrecombination (65) and sometimes only smallchanges are required to change specificity (seeReferences 36, 70). As some R genes carry sig-nificant fitness costs, a wide array of allelesare maintained in wild populations through arapid process of birth and death. Pathogenshave complementary birth and death systemsin place that can evolve rapidly (147). Follow-ing research on host-pathogen interactions inmajor agricultural crops, molecular research onthe host-pathogen interaction of scab in ap-ple is progressing in both the host, e.g., Rgene cloning, which has advanced to the proof-of-function stage for the Rvi6 gene (5, 92,102, 126, 136, 148), and the pathogen, e.g.,identification of candidate effector genes andproteins (16, 43, 146). R gene transformation


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may range from transferring genes within thegenus through cisgenesis (116), to artificiallyconstructed genes effective against a range ofpathogens (66). A major advantage of transfor-mation systems in the host is that gene cassettescan be inserted into one cultivar specifically de-signed to resist the regional V. inaequalis pop-ulations, based on the near-isogenic lines con-cept, but still be marketed as a single cultivar.Going a step further, trees with different genecassettes could be planted in the same orchardin order to achieve genetic diversity for scabresistance to help reduce the rate of pathogenadaptation (10, 35, 113).

The combination of the different resistancemechanisms present in the plant determinesits ability to withstand infection by particular

pathogens. In this review, the focus has been onthe differential interactions involving GfG re-lationships in the V. inaequalis–Malus pathosys-tem. Host-specific resistance has an importantrole to play in this pathosystem provided somemeasure of predicting the durability of resis-tance strategies is developed. Nonhost resis-tance also deserves some attention in the fu-ture as an area that has considerable promisefor generating lasting resistance. Understand-ing of the molecular basis of fungal effectorfunction and their influence on host physiologyvia interactions with host molecules, includingresistance proteins, will provide the conceptualcontext required to achieve durable resistanceto V. inaequalis as well as other pathogens inapple.

SUMMARY POINTS

1. The existing nomenclature system for apple scab races suffered from significant problemsand was in need of updating.

2. A comprehensive new nomenclature system and a set of rules for defining new GfGrelationships in the V. inaequalis–Malus pathosystem is presented.

3. Information on the first 17 relationships is provided with a focus on identifying differentialMalus hosts carrying single resistance genes.

4. The nomenclature system is well-suited to describe complex races of V. inaequalis as wellas resistance sources carrying pyramided resistances.

FUTURE ISSUES

1. A project to develop a reference set of V. inaequalis isolates for the validation of newlyidentified GfG relationships is in progress.

2. Another project to monitor V. inaequalis populations for their pathotypes to determinethe effectiveness of scab resistance genes by geographic region has been initiated. Theinformation generated should enable association mapping of avirulence genes in thepathogen to eventually replace pathogenicity tests for virulence confirmation.

3. The pathotyping information will be used to identify virulence patterns that may improveour understanding on fitness penalties in the pathogen and translate this into breedingstrategies for durable resistance. This will be supported by molecular research on effectorgenes and their protein products and host targets.

4. It is the intention to cast the research net wider by investigating additional strategies forscab control involving alternative resistances based on race-nonspecific genes, nonhostresistance, and manipulation of the specificity of resistance genes.

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5. The ultimate goal is to integrate various resistance and disease management strategiesto achieve resistance that is durable in the field.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

We thank our colleagues of the scab resistance research and breeding community for their con-tributions to a preliminary proposal and support to update the scab race nomenclature (25): HerbAldwinckle, Susan Gardiner, Cesare Gessler, Remmelt Groenwold, Francois Laurens, Bruno LeCam, Jim Luby, Bert Meulenbroek, Markus Kellerhals, Luciana Parisi, Andrea Patocchi, HenkSchouten, Stefano Tartarini, and Eric van de Weg. The research is supported by the New ZealandFoundation for Science, Research and Technology (contracts C06X0810 and C06X0812).

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PY49-FrontMatter ARI 8 July 2011 9:55

Annual Review ofPhytopathology

Volume 49, 2011Contents

Not As They SeemGeorge Bruening � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Norman Borlaug: The Man I Worked With and KnewSanjaya Rajaram � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �17

Chris Lamb: A Visionary Leader in Plant ScienceRichard A. Dixon � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �31

A Coevolutionary Framework for Managing Disease-Suppressive SoilsLinda L. Kinkel, Matthew G. Bakker, and Daniel C. Schlatter � � � � � � � � � � � � � � � � � � � � � � � � � � �47

A Successful Bacterial Coup d’Etat: How Rhodococcus fascians RedirectsPlant DevelopmentElisabeth Stes, Olivier M. Vandeputte, Mondher El Jaziri, Marcelle Holsters,

and Danny Vereecke � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �69

Application of High-Throughput DNA Sequencing in PhytopathologyDavid J. Studholme, Rachel H. Glover, and Neil Boonham � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �87

Aspergillus flavusSaori Amaike and Nancy P. Keller � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 107

Cuticle Surface Coat of Plant-Parasitic NematodesKeith G. Davies and Rosane H.C. Curtis � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 135

Detection of Diseased Plants by Analysis of Volatile OrganicCompound EmissionR.M.C. Jansen, J. Wildt, I.F. Kappers, H.J. Bouwmeester, J.W. Hofstee,

and E.J. van Henten � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 157

Diverse Targets of Phytoplasma Effectors: From Plant Developmentto Defense Against InsectsAkiko Sugio, Allyson M. MacLean, Heather N. Kingdom, Victoria M. Grieve,

R. Manimekalai, and Saskia A. Hogenhout � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 175

Diversity of Puccinia striiformis on Cereals and GrassesMogens S. Hovmøller, Chris K. Sørensen, Stephanie Walter,

and Annemarie F. Justesen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 197

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Emerging Virus Diseases Transmitted by WhitefliesJesus Navas-Castillo, Elvira Fiallo-Olive, and Sonia Sanchez-Campos � � � � � � � � � � � � � � � � � 219

Evolution and Population Genetics of Exotic and Re-EmergingPathogens: Novel Tools and ApproachesNiklaus J. Grunwald and Erica M. Goss � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 249

Evolution of Plant Pathogenesis in Pseudomonas syringae:A Genomics PerspectiveHeath E. O’Brien, Shalabh Thakur, and David S. Guttman � � � � � � � � � � � � � � � � � � � � � � � � � � � 269

Hidden Fungi, Emergent Properties: Endophytes and MicrobiomesAndrea Porras-Alfaro and Paul Bayman � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 291

Hormone Crosstalk in Plant Disease and Defense: More Than JustJASMONATE-SALICYLATE AntagonismAlexandre Robert-Seilaniantz, Murray Grant, and Jonathan D.G. Jones � � � � � � � � � � � � � 317

Plant-Parasite Coevolution: Bridging the Gap between Geneticsand EcologyJames K.M. Brown and Aurelien Tellier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 345

Reactive Oxygen Species in Phytopathogenic Fungi: Signaling,Development, and DiseaseJens Heller and Paul Tudzynski � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 369

Revision of the Nomenclature of the Differential Host-PathogenInteractions of Venturia inaequalis and MalusVincent G.M. Bus, Erik H.A. Rikkerink, Valerie Caffier, Charles-Eric Durel,

and Kim M. Plummer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 391

RNA-RNA Recombination in Plant Virus Replication and EvolutionJoanna Sztuba-Solinska, Anna Urbanowicz, Marek Figlerowicz,

and Jozef J. Bujarski � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 415

The Clavibacter michiganensis Subspecies: Molecular Investigationof Gram-Positive Bacterial Plant PathogensRudolf Eichenlaub and Karl-Heinz Gartemann � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 445

The Emergence of Ug99 Races of the Stem Rust Fungus is a Threatto World Wheat ProductionRavi P. Singh, David P. Hodson, Julio Huerta-Espino, Yue Jin, Sridhar Bhavani,

Peter Njau, Sybil Herrera-Foessel, Pawan K. Singh, Sukhwinder Singh,and Velu Govindan � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 465

The Pathogen-Actin Connection: A Platform for DefenseSignaling in PlantsBrad Day, Jessica L. Henty, Katie J. Porter, and Christopher J. Staiger � � � � � � � � � � � � � � � 483

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Understanding and Exploiting Late Blight Resistance in the Ageof EffectorsVivianne G.A.A. Vleeshouwers, Sylvain Raffaele, Jack H. Vossen, Nicolas Champouret,

Ricardo Oliva, Maria E. Segretin, Hendrik Rietman, Liliana M. Cano,Anoma Lokossou, Geert Kessel, Mathieu A. Pel, and Sophien Kamoun � � � � � � � � � � � � � � � 507

Water Relations in the Interaction of Foliar Bacterial Pathogenswith PlantsGwyn A. Beattie � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 533

What Can Plant Autophagy Do for an Innate Immune Response?Andrew P. Hayward and S.P. Dinesh-Kumar � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 557

Errata

An online log of corrections to Annual Review of Phytopathology articles may be found athttp://phyto.annualreviews.org/

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Documents

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