Revision of The Nomenclature of The Differential Host-Pathogen Interactions of

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Revision of the Nomenclature of the Differential HostPathogen Interactions of Venturia inaequalis and Malus
Vincent G.M. Bus,1 Erik H.A. Rikkerink,2 Val rie Cafer,3 Charles-Eric Durel,4 e and Kim M. Plummer5
1 The Plant and Food Research Institute of New Zealand, Private Bag 1401, Havelock North 4157, New Zealand; email: Vincent.Bus@plantandfood.co.nz 2 The Plant and Food Research Institute of New Zealand, Private Bag 92169, Auckland 1142, New Zealand; email: Erik.Rikkerink@plantandfood.co.nz 3 INRA, UMR77 Pathologie V g tale PaV , INRA/ACO/UA, IFR QUASAV, BP 60057, e e e F-49071 Beaucouz , France; email: Valerie.Cafer@angers.inra.fr e 4 INRA, UMR 1259 Genetics and Horticulture GenHort, INRA/ACO/UA, IFR QUASAV, BP 60057, F-49071 Beaucouz , France; email: Charles-Eric.Durel@angers.inra.fr e 5 La Trobe University, Department of Botany, Bundoora, Vic. 3086, Australia; email: K.Plummer@latrobe.edu.au
Annu. Rev. Phytopathol. 2011.49:391-413. Downloaded from www.annualreviews.org by WIB6105 - Technische U. Muenchen on 04/22/12. For personal use only.
Annu. Rev. Phytopathol. 2011. 49:391413 The Annual Review of Phytopathology is online at phyto.annualreviews.org This articles 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 inaequalisMalus) pathosystem was one of the rst systems for which Flors concept of gene-for-gene (GfG) relationships between the host plant and the pathogen was demonstrated. There is a rich resource of host resistance genes present in Malus germplasm that could potentially be marshalled to confer durable resistance against this most important apple disease. A comprehensive understanding of the host-pathogen interactions occurring in this pathosystem is a prerequisite for effectively manipulating these host resistance factors. An accurate means of identication of specic resistance and consistent use of gene nomenclature is critical for this process. A set of universally available, differentially resistant hosts is described, which will be followed by a set of dened pathogen races at a later stage. We review pertinent aspects of the history of apple scab research, describe the current status and future directions of this research, and resolve some outstanding issues.
391
INTRODUCTION
Apple (Malus x domestica) is one of the major fruit crops produced in the world. At 72 million metric tons (MMT) (http://faostat.fao.org), apple is second only to banana (96 MMT) as a major fruit source for the worlds population. Much of the apple production (31 MMT) takes place in eastern and central China, away from the center of diversity of apple located in the western regions of China and parts of Central Asia (72). The species name and the presence of the x in the specic epithet reect the diverse ancestry of this species, with various hybridizations between Malus species giving rise to the domesticated apple (76). Nevertheless, it was recognized as one of the 33 primary Malus species in ve sections based on the classication by Wiersema (139). Generally, Malus species produce small fruit (<3 cm diameter), with the exception of Malus sieversii, which also includes accessions with fruit of the size expected of commercial apples today. M. sieversii has also been conrmed as the main progenitor of the domesticated apple and perhaps they should be regarded as a single species, Malus pumila (135), as argued previously (88). The haploid chromosome number of Malus is 17 and most species are diploid. The rst extensive genetic map of apple was published by Maliepaard et al. (90). It has become the reference map for over 20 apple and several pear maps, including one skeleton map based on an integrated consensus map (99) used here for the global mapping of the scab resistance genes discussed. Apple is host to a wide range of pests and diseases (139), a number of which need to be controlled for protable commercial production. Scab disease, caused by the ascomycete fungus Venturia inaequalis (Cke) Wint. (anamorph: Spilocaea pomi Fries), is one of the most damaging in economic terms, as most climates where apples are grown are conducive to scab (89). Orchard management techniques, such as leaf litter control, can reduce primary inoculum (89) but usually are not sufcient to control apple scab, and as many as 1825 fungicide applications per growing season may be required (139).
392 Bus et al.
Plant genetic resistance, when available, is widely regarded as the preferred method for controlling disease if the industry can afford to support a breeding program. A long-term driver for the development of resistant cultivars is the consumer antagonism to non-natural compounds in their food and the environment. This has led to increasingly stringent legislation. Using resistant cultivars helps to reduce socioeconomic and environmental impacts (139), but these gains will be realized in the long-term only if resistance is effective for at least one crop cycle, which is approximately 15 years for apple. Achieving such durable resistance through traditional breeding is a slow process but can be accelerated by adding resistance into existing high quality cultivars by marker-assisted fast breeding (138) or cisgenesis (116). Ultimately, an in-depth understanding of host-pathogen interactions, including the specic interactions of avirulence (Avr) genes in the pathogen with resistance (R) genes in the host, is required for these approaches to be successful. At the same time, other strategies (15)such as disease prevention through sanitary practices and fungicide application and spatial deployment of resistances (35, 113) should also be applied to enhance resistance durability. Fungal species of Venturia on Rosaceae appear to have coevolved with, and are limited to, their (fruit) tree hosts, e.g., Venturia pirina (pear), Venturia carpophila (peach), and Venturia cerasi (cherry) (115), as they are sufciently distinct species to prevent mating (15). The host range of V. inaequalis comprises species in the genera Malus, Crataegus, Sorbus, Pyracantha, Eriobotrya, Kageneckia, and Heteromeles (89, 110). However, isolates pathogenic on Pyracantha, Eriobotrya, and accessions of Kageneckia and Heteromeles could not infect Malus, therefore 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. pyracanthae on Pyracantha spp. and f.sp. pomi on Malus spp. Recent research indicated that V. inaequalis
populations from Malus, Pyracantha, and Eriobotrya belonged to the same phylogenetic species, but divergence has occurred between these populations, with those from Eriobotrya and Pyracantha being the most recently differentiated (52). In this review, we focus on scab resistance in Malus spp. associated with recognition of V. inaequalis races mediated by race-specic effectors. Approximately 20 scab R genes have been mapped to the apple genome and for most of them differential interactions have been demonstrated. We describe these gene-forgene (GfG) relationships and present an updated nomenclature system.
by epistatic interactions. The genetic basis of avirulence can be investigated readily using in vitro V. inaequalis crosses and tetrad dissection.
Gene-for-Gene Relationships
GfG relationships were rst proposed by Flor (44) to explain the ax (Linum usitatissimum)ax rust (Melampsora lini ) interaction as he postulated that for each gene that conditions resistance in the host, there is a corresponding gene that conditions pathogenicity in the parasite. Many specialist (hemi-)biotrophic parasites conform to this type of relationship (69). The V. inaequalis-Malus interaction was one of the rst examples for which GfG relationships were suggested based on the segregation of Avr genes in the fungus (13, 145). Today, the resistance relationship is commonly hypothesized to be a specic recognition event, either direct or indirect, between a host R gene product and a corresponding pathogen Avr gene product (69), the complexity of which is still not completely clear. Additionally, many major R gene loci in apple condition distinct phenotypic reactions, which have been assigned to resistance classes (Table 1; Supplemental Table 1, follow the Supplemental Material link from the Annual Reviews home page at http://www.annualreviews.org): hypersensitive response (HR) in Class 1; stellate necrosis (SN) in Class 2; and chlorosis (Chl) with limited sporulation in Class 3 (15, 119) (Figure 1). V. inaequalis populations are usually highly diverse genetically (53, 133, 134). The annual sexual phase followed by asexual multiplication during the growing season provides V. inaequalis opportunities for adaptive selection of new strains. In V. inaequalis populations in wild forests of Malus, selection is probably balanced by a high diversity of scab R genes. In monoculture orchards typical of modern horticulture, the narrow range of resistances present exert a high selection pressure on the pathogen population. The use of wellcharacterized single-spore reference isolates with known combinations of virulence and Avr alleles corresponding to known R genes
www.annualreviews.org Apple Scab Host/Race Nomenclature 393
THE VENTURIA INAEQUALISMALUS PATHOSYSTEM

An intricate host-pathogen interaction structure has evolved in the V. inaequalisMalus pathosystem (89). Recent research supports the idea that the disease emerged in the center of origin of apple, Central Asia (53), with M. sieversii the likely original host of V. inaequalis (54). V. inaequalis spread with apple to all corners of the world as people migrated to new territories, and scab probably became more prevalent because clonal propagation of domesticated apple led to monoculture orchards (130). However, in some cases, e.g., several states in the United States, Japan, and Australia, V. inaequalis introductions have been relatively recent, much later than the introduction of apple (89). An important aspect of the life cycle of V. inaequalis is its annual sexual phase on leaf litter in winter. Pseudothecia are formed only from heterothallic mating, requiring two different mating types (73). Each pseudothecium contains many asci, each containing four pairs (tetrad) of ascospores resulting from a meiotic division followed by a mitotic division. Ascospore progeny thus carry different combinations of avirulence factors compared with their parents. Because ascospores give rise to haploid mycelium, the genotype at each locus, either avirulence (Avr) or virulence (avr), is expressed unless masked
Supplemental Material
Table 1 Nomenclature of the gene-for-gene relationships between Venturia inaequalis and Malus. The races are dened by the avirulence genes they are lacking, hence resulting in susceptibility on the complementary host Malus Differential host Number h(0) h(1) h(2) h(3) h(4) h(5) Accession Royal Gala Golden Delicious TSR34T15 Genevab TSR33T239 9-AR2T196 Priscilla Malus x oribunda 821b B45 K2 A7236b A7227 Hansens baccata #2b Durello di Forl` Dulmener Rosenapfelb GMAL2473 MIS op 93.051 G07098b Antonovka APF22b Phenotype susceptibility necrosis stellate necrosis stellate necrosis hypersensitive response hypersensitive response chlorosis hypersensitive response stellate necrosis stellate necrosis hypersensitive response stellate necrosis/chlorosis chlorosis stellate necrosis chlorosis hypersensitive response hypersensitive response chlorosis Vg Vh2 Vh3 Vh4 = Vx = Vr1 Vm Vf Vfh Vh8 Vdg Va Vbj Vb Vd Vdr1 Vr2 Vmis Va1 12 02 04 02 17 01 08 02 02 01c 02 12 10 06 02 03 01 Resistance locus Historical LGa New Rvi1 Rvi2 Rvi3 Rvi4 Rvi5 Rvi6 Rvi7 Rvi8 Rvi9 Rvi10 Rvi11 Rvi12 Rvi13 Rvi14 Rvi15 Rvi16 Rvi17 AvrRvi1 AvrRvi2 AvrRvi3d AvrRvi4d AvrRvi5 AvrRvi6 AvrRvi7 AvrRvi8 AvrRvi9 AvrRvi10d AvrRvi11d AvrRvi12d AvrRvi13d AvrRvi14d AvrRvi15d AvrRvi16d AvrRvi17d p-8 p-9 p-10 Venturia inaequalis Avirulence locus New Old Race (0) (1) (2) (3) (4) (5) (6) (7) (8) (9) (10) (11) (12) (13) (14) (15) (16) (17)
h(6) h(7) h(8) h(9) h(10) h(11) h(12) h(13) h(14) h(15) h(16) h(17)
LG = linkage group of apple. Temporary differential host until the host has been conrmed as being monogenic, or a monogenic progeny from this polygenic host has been selected. c Provisional placement based on the assumption that the resistance in sources PI 172623 and PI 172633 are identical. d Gene-for-gene relationship not conrmed to date.
a b
Major effect resistance gene: resistance gene that confers a high level of resistance, for example hypersensitive response, in incompatible interactions
in differential hosts will aid breeders in the preservation of known R genes and the identication of new ones. In the past, a number of isolates poorly dened on a low number of differential hosts have been used for genetic studies (Supplemental Table 2), which has led to uncertainty about specic interactions.
Denition of a Race
We dene a single-spore isolate of the pathogen as a race when it is able to overcome completely
Bus et al.
the resistance in a host. Determination of the race status is based on the premise that a mutation at the Avr locus in the pathogen leads to nonrecognition by the host, hence leading to complete susceptibility. The race spectrum is dened by the combination of R genes it can overcome. The effect of resistance genes covers a continuum from immunity for major effect genes to near-susceptibility for quantitative resistance loci (QRLs), depending on its genetic background, the pathogen, and the environment
394
1 cm
1 mm
1 cm
Figure 1
Characteristic scab resistance reactions on apple leaves. (a) Pin point pit, hypersensitive response conditioned by the Rvi4 gene, (b) stellate necrosis by the Rvi2 gene, and (c) chlorosis with limited sporulation conditioned by the Rvi6 gene under glasshouse conditions (15).
(109). The effect is independent of the spectrum of the resistance gene, as both narrow and broad spectrum resistance genes can condition a range of resistance reactions (17). The presence of lesions on differential hosts in the eld (see References 8, 112) does not necessarily mean the presence of a breaking race but instead can represent opportunistic infections by avirulent strains under conditions highly conducive to the disease. Follow-up research is therefore always required to conrm the virulence status of putative race isolates (see References 22, 23, 105).
Differential Interactions in the Venturia inaequalisMalus Pathosystem

Interestingly, the initial focus of genetic studies on the V. inaequalisMalus pathosystem was on avirulence in the pathogen rather than resistance in the host. Genetic analysis of over 23,000 asci resulted in the identication of 19 Avr genes, named pathogenicity ( p) genes (12, 13) (Supplemental Table 3). The rst alleles assigned were p-1 and p-1+ for the Avr and avr alleles, respectively, on the commonly grown cultivar McIntosh (13). Most Avr loci in V. inaequalis reported to date are inherited independently (7, 124, 145). Independent segregation of Avr loci provides the pathogen with a large potential to develop new pathotypes during the
sexual cycle (12). Nevertheless, some loci are linked, e.g., the p-8, p-9, and p-12 loci (145), and recently a further two clusters of four Avr genes were identied in a mapping study of V. inaequalis Avr genes (17). Many of the rst described interactions involved genes conferring resistance effective against a low proportion of the pathogen population, i.e., they were narrow spectrum (versus broad spectrum) genes (2, 3, 13). Similar results were found more recently with other susceptible cultivars, such as Boskoop, Bramley, Coxs Orange Pippin, Spartan, and Worcester (4, 123, 125), and the genes Vt57 (26), Vs/Vsv (17, 22), and Vd3 (127). The early V. inaequalis geneticists also realized that it was impractical to name all the races, as the isolates carrying the rst 19 avr ( p) alleles represented over half a million possible permutations of these alleles, hence as many potential races of V. inaequalis. Therefore, only those isolates that could overcome broad spectrum R genes with potential for resistance breeding were dened in the race nomenclature (89), comprising eight races that have been described to date (Supplemental Table 4). This old nomenclature system, however, was cumbersome as a single race number could involve several GfG relationships, e.g., race (2) isolate 356-2 could overcome the different resistances in Dolgo, Geneva, and certain segregates of Russian apple R12740-7A (121). A system where all compatible interactions can
www.annualreviews.org Apple Scab Host/Race Nomenclature
Quantitative resistance locus (QRL): resistance gene that confers partial resistance; also called minor effect resistance gene Narrow spectrum resistance gene: resistance gene that is effective against only a few isolates of the pathogen population Broad spectrum resistance gene: resistance gene that is effective against most if not all isolates of the pathogen population
395
be named separately is therefore required (25) as originally intended (145). This will allow the race status of existing isolates to change as they will invariably be shown to carry additional Avr alleles resulting in new host-pathogen interactions.
pathogen V. inaequalis to give the general locus prex Rvi. The proposed system is based on the following minimum criteria being imposed before a new Rvi-AvrVi interaction is added: 1. The R gene has been shown to segregate in a simple manner and is present in a genetic background from which a suitable reference host can be selected. 2. The R-Avr interaction has (sufciently) been shown to be novel either with the aid of a breaking race that has been screened against all other reference hosts to establish that the new Avr allele is different from existing alleles or preferably also by screening the R gene against all the established race reference isolates to demonstrate that none of them breaks the resistance. Novelty is also conrmed when a gene maps to a position where no known genes have been mapped previously, in the expectation that the genetics of the GfG relationships will be elucidated. 3. Plant material of the differential host and, where one is known to exist, also the corresponding reference race of the pathogen are available, so that the system can be readily utilized to build on current knowledge. Races lacking more than one Avr gene at different loci will be identied as race (k,l,m, . . .) and hosts carrying multiple R genes will be named host (k,l,m, . . .) or h(k,l,m, . . .). In cases where several candidate genes are identied from genome sequence data (e.g., for Rvi6; see below), we suggest that the functional paralog is named Rvik and the others Rvik.1, Rvik.2, . . . until differential interactions warrant naming them in their own right.
NOMENCLATURE OF VENTURIA INAEQUALIS RACES

The nomenclature system for the V. inaequalis avirulence genes and races commenced using a numerical system, but this was not followed through with the naming of the complementary scab resistance genes. The nomenclature for the latter was based on identifying them by their source of resistance, therefore the GfG relationships between the resistance genes in the host and the avirulence genes in the pathogen were not obvious. This anomaly will be corrected in the nomenclature system proposed here, which is based on the system rst proposed for Phytophthora infestans and potato (9) and is commonly used for other host-pathogen interactions.
The Nomenclature Model

In describing GfG relationships, where k represents the number of the specic interaction, each Rk-Avrk interaction can be represented by a differential host carrying only the Rk gene and an isolate of the pathogen having altered or lost only the complementary allele, identied as avrk, at the Avrk locus. Once the individual Rk-Avrk interaction has been dened, isolates lacking multiple avirulences can then be identied by their formula based on the combination of the individual virulences. It accommodates complex loci as well as QRLs for which differential host-pathogen interactions are demonstrated. Simultaneously with the revision of these GfG relationships, we align the nomenclature of apple scab R genes with the international standard of gene nomenclature for Arabidopsis (97). The names of major R genes start with R and contain an abbreviation of the
396 Bus et al.
Venturia inaequalisMalus Gene-for-Gene Relationships

Below we describe the 17 GfG relationships dened to date and add relationship (0) involving host (0) that does not carry any resistance genes to correct the erroneous use of
race (1) to date. We identify the knowledge gaps and conrm the genetics of resistance and (a)virulence in different accessions and races. In the development of the new numerical nomenclature system, we aimed to maintain as much of the existing system as possible by making use of current associations of race numbers with genes. The accessions representing the differential hosts for races (2) to (7) remain largely the same, although there is some rationalization by assigning host status, where possible, to Malus accessions carrying a single R allele (Table 1). Some of the well-characterized genes with temporary working names that are used in breeding will be assigned Rvi-AvrRvi relationship numbers for inclusion in the nomenclature system. We also recognize that some of the resistances have long played an important role in apple breeding, but GfG relationships have not been conrmed and/or differential hosts have not been selected. In all of these cases, research is in progress to rectify the situation, as is the determination of a set of reference isolates of V. inaequalis representing corresponding races, which will be reported at a later stage. Relationship (0). Host (0) can be dened as the host that does not carry any R genes and hence is susceptible to all isolates of V. inaequalis. Today, Gala, or more often its sports, is the commonly used universally susceptible host in many scab experiments, and it is also a widely grown cultivar and an important parent in many breeding programs worldwide. Although V. inaequalis showed a lower rate of disease development on this cultivar, attributed to two QRLs (128), than on Golden Delicious (103), it is generally highly susceptible. It therefore has been selected to represent h(0) (Table 1). On the pathogen side, the common race (121, 145) of V. inaequalis was originally dened as race (1), which is inconsistent with the race names in other pathosystems. We therefore rename it race (0) and dene it as the race that is avirulent to all hosts carrying R genes and hence induces lesions only on hosts not carrying any known scab R genes. We recognize that, as new
relationships are added, this will actually become a theoretical denition because no reference candidates exhibiting a complete avirulence pattern will be available. Relationship (1). An exception to the premise that narrow spectrum R genes should be excluded from the nomenclature is made for the Rvi1 (Vg) gene from Golden Delicious. Although this gene is overcome by an estimated 87% of the pathogen population in Europe (103), both host (1) and race (1) have been extensively characterized, which makes this an important model system to advance our understanding of the basis of ephemeral, versus durable, R genes. The inclusion of relationship (1) also reduces the degree of confusion between races (0) and (1), as isolates described as race (1) in the old nomenclature before the discovery of Rvi1 generally can overcome it, hence they remain race (1) in the new nomenclature. Differential interactions of isolates with Golden Delicious (119) suggested the presence of a resistance factor. The monogenetic nature of this resistance was rst demonstrated with avirulent isolate 101 (84) and conrmed with isolate 1066 (7). Rvi1 (Vg) maps to the very distal end of linkage group (LG) 12 of Prima (40) (Figure 2), which has Golden Delicious as one of its grandparents. The Rvi1 gene conditions necrotic resistance reactions (84, 100), which may show weak sporulation (31). The segregation of the complementary Avr gene in this GfG relationship was demonstrated in a cross between the virulent V. inaequalis isolate 104 (79, 104) and avirulent isolate 147 (61). These ndings were conrmed in a 301 (virulent) x 1066 (avirulent) progeny set (7) that was used in the attempt to clone AvrRvi1 (18). Relationship (2). Early genetic studies on Russian apple R12740-7A, whose resistance reactions ranged from Class 0 (no macroscopic symptoms) to Class 2 (necrosis), depending on the inoculum used (119), showed that it contained at least two (34), if not three, scab resistance genes (122): Vr was assigned to the putatively race-nonspecic gene effective against all
LG1
CH03g12a
LG2
Rvi15 CH02c02a Rvi4
LG3
LG4
LG6
CH03e03
CH04e02 Rvi14 HB09 CH1d03y CH03d07
AG11 Rvi10 Rvi6 CH-Vf1 Rvi17 CH05g08 Aco-1 CH03g07 Hi03d06 Rvi11 CH05e03 Rvi9 Rvi2 Rvi8 CH03d01
CH05d02 CH03d12 Rvi3 Hi08e04
Rvi16 AU223657
CH0202b CH03c01
CH03g12y
LG8
Rvi7
LG10
CH05h12 CH02b07 Rvi13
LG12
LG17
CH04c06
CH05d04
CH01e12 CH01c06
CH04f03
CH02g04 CH01g12 CH01f02 Rvi12 CH04f08
CH03d11 CH05a02y
CH01h10 Hi15h11
Hi07f01 GD100 CH01d03z Rvi1 NZ17e06
was known to condition Class 2 resistance reactions (121), which recently were specied as SN (26). Nevertheless, Vr became associated with the SN phenotype (1), but this error was corrected when Vr in Russian apple (59) and Vh2 in TSR15T34 (26) were shown to be the same. Rvi2 has been mapped to the lower end of LG2 in h(2) accession TSR34T15, an F2 selection of Russian apple (Figure 3), and Vr is now putatively associated with a Class 3 chlorotic phenotype also described by Aldwinckle et al. (1), but whose mapping position remains elusive. Host (2) has mistakenly been reported as being accession TSR34T132 (104, 105), an error perpetuated in other papers (e.g., 50, 89, 112). However, the correct identication numbers are TSR34T15 (correspondence E.B. Williams to Y. Lespinasse, 20 February 1984) and PRI 384-1 (26). In the same correspondence TSR34T15 is also identied as OR42T173 (145), but this has been disputed based on genetic marker research (95). The original race (2) isolate 356-2 is no longer available, and its replacement, 1770-3, identied in the Purdue-Rutgers-Illinois (PRI) program and distributed as race (2), more recently was found to be unable to infect h(2) (20). Isolate 1639 has been shown to overcome the Rvi2 gene (26), but AvrRvi2 in this isolate segregated 3:1 rather than 1:1, and it is also linked to other AvrRvi genes, which indicates that this relationship may be more complicated than a simple GfG one (17). Relationship (3). Geneva is a red-leafed, open-pollinated selection of M. pumila (68), which was regarded as resistant to scab until 1951 when it was reported as infected in Nova Scotia (120). Although the resistance symptoms can range from HR to Chl (71), avirulent isolates predominantly induce SN reactions but were able to sporulate under extended moisture conditions in lesions described as 2 4 (121). In fact, Geneva was shown to carry two resistance genes, and the authors interpretation was that the p-10 locus induced Class 2 resistance reactions with one R gene and the independently segregating p-11 locus the 2 4
Rvi5 Hi07h02
Figure 2 Global positions on the apple genome of the 17 Rvi scab resistance genes named to date. The skeleton genetic map is based on the integrated consensus map by NDiaye et al. (99).
known races of V. inaequalis at that time (32), and the Russian apple derivatives Si and Si were the differential hosts for races (2) and (4), respectively (82, 100). Host (2), rst shown to be overcome by the South Dakota isolate 356-2,
398 Bus et al.
phenotype with another gene (Supplemental Table 5). However, a Chl-conditioning gene was also observed in Geneva (145), which suggests that it carries three genes; hence, Nova Scotia isolate 651 used in the study would lack all three complementary Avr alleles. To date, two linked genes, temporarily named Vh3.1 and Vh3.2, were mapped to LG4 in progenies of Geneva crossed with Elstar and Braeburn (V.G.M. Bus et al., unpublished data) (Figure 2). Research is in progress to determine which gene has the broader spectrum and therefore should be assigned Rvi3. This will most likely not be Vh3.2 because isolate 1639 was the only one out of six isolates that could not infect Geneva x Braeburn accession Q49 carrying the gene (V.G.M. Bus, unpublished data). Its complementary gene in the pathogen has been mapped as AvrVh3.2 to an Avr gene cluster in isolate 1639 (17). Until further elucidation, Geneva will remain h(3) and the U.S. isolate 1774-1 reference race (3). Relationship (4). Although derivatives of Russian apple R12740-7A were long known to condition HR (121), it is only recently that the Rvi4 gene in the F2 derivative TSR33T239 of Russian apple (Figure 3) was denitely associated with this resistance phenotype (26). Several names have been assigned to the gene. First, the temporary name Vx (29) was assigned to indicate that its genetic relationship to known genes needed further elucidation, following the identication of linked markers (59). Initial positioning to LG6 of the White Angel map (60), equivalent to LG10 on the European apple map (85, 90), was inconclusive until it was mapped denitively to LG2 of TSR33T239 (26) (Figure 2). Using the cultivar Regia, it was also named Vr1 to differentiate it from other Russian apple genes in genetic studies performed in Germany (14). The reporting of V. inaequalis race (4) has persistently been attributed to Shay et al. (122) in other reports (89, 141, 144); however, they merely stated that Russian apple is known to contain at least 3 gene pairs, only one of which is resistant to all known races. Several isolates
Host (2)
TSR34T15 (PRI 384-1; OR42T173) McIntosh R7T81 (PRI 45-39) Russian apple R12740-7A Delicious
Host (4)
TSR33T239 (PRI 478-33; W7AR44T20)
Dg. R13T43 (PRI 27-330) Delicious
Wealthy Russian apple R12740-7A
Host (5)
9-AR2T196 (PRI 643) McIntosh R14T102 (PRI 76-29) McIntosh R16T52 (PRI 69-118) Wolf River M. micromalus 245-38 Wolf River M. x atrosanguinea 804
OR45T132 (PRI 333-9)
Host (6)
Priscilla (PRI 1659-1)
Starking Delicious PRI 610-2
McIntosh PRI 14-266
Golden Delicious 26829-2-2
Host (8)
B45 N23
Sciearly M. sieversii GMAL4302-X8 Sciros M. sieversii GMAL4026-X435 Elstar Dolgo M. baccata M. prunifolia
Host (9)
K2
M. x robusta Open-pollinated
Host (10)
A723-6
Worcester Pearmain PI 172623 (B VIII 33,25) McIntosh PRI 703-1 (9-AR6T136) PI 172633 (B VIII 34,6) Jonared
PRI 1841-11 (CCR3T11)
Host (11)
A722-7
Starking M. baccata jackii
Figure 3 The pedigrees of Malus differential hosts for apple scab derived from mostly polygenic accessions.
of V. inaequalis have been identied as race (4) in both the United States and France (Supplemental Table 2); however, none of these was completely compatible with hosts carrying the Rvi4 gene (Figure 4) (20).
Relationship (5). Malus micromalus 245-38 and Malus x atrosanguinea 804 were identied early in the PRI breeding program (63) as highly resistant sources conditioning HR, visible within three days after inoculation (119,
which is incompatible with Rvi1 hosts (61, 84). A fraction of three proteins with elicitor activity from isolate MNH120 (146) may include the AvrRvi5 effector. Relationship (6). The genetics of the resistance from Malus x oribunda 821, the source of Rvi6 (Vf ) resistance (64) and progenitor of most scab-resistant apple cultivars to date, has been extensively reviewed (50, 89). Many allelic sources of Rvi6 have been identied (33, 142, 143), some of which have been suggested to also carry the gene based on the specic linkage of the CH-Vf1-159 bp allele with Rvi6 (137). Sequencing of the locus revealed that it contains four paralogs (136, 148), which we propose to rename Rvi6 for HcrVf2/Vfa2 (5, 102) and Rvi6.1 to Rvi6.3 for the other three paralogs. The Rvi6.1 (HcrVf1/Vfa1) paralog may also be renamed if its functionality (92) is conrmed as having sufciently broad utility. Rvi6-associated resistance is variable in both segregation ratios and resistance levels (30), and a range of explanations for this has been proposed, e.g., inuence of QRLs (39, 50, 89, 111, 144) and variation in incubation conditions and inocula applied (74, 78). Ratios lower than the expected R:S = 1:1 have also been attributed to (sub)lethal genes linked to Rvi6 (48). A simpler explanation, however, is that some plants presented a phenotypic reaction with chlorosis and high sporulation, i.e., Class 3B (30), and were assumed as not carrying the gene (89, 129), whereas genetic markers could conrm Rvi6 being present in most seedlings in this class (49). In early backcross generations, the M. x oribunda 821 resistance clearly segregated as a single major gene (64) (Supplemental Table 7), but differential interactions among F2 descendants of M. x oribunda 821 (104) suggested the presence of a second gene (7), Rvi7 (see below). Race (6) of V. inaequalis is dened by its compatibility with hosts carrying Rvi6 only (83), but to date many of the commonly used h(6) accessions (e.g., Prima and Florina), were found to also carry Rvi1. Because Priscilla does not (7), we propose it as h(6). The initial race (6) studies
EU-NL19
EU-NL19
EU-B05
1638
1638
1638
Figure 4 Partial differential interactions of Venturia inaequalis isolates on seedlings (a) E035 and (b) E053 of a Royal Gala x TSR33T239 family; and (c) F002 of an A19R03T127 x TSR33T239 family carrying the scab resistance gene Rvi4 from host (4). Race (4) isolate 1638 rst induced a hypersensitive response on these seedlings, which was followed by different levels of sporulation, ranging from (a) very limited and (c) dense to moderate. Each top-bottom pair of symptoms is the result of simultaneous inoculation of a pair of isolates on the same leaf.
146). Both accessions also carried a Chlconditioning gene for scab resistance that appears allelic to Rvi6 (Vf ) (33, 143). The HR-conditioning gene (Rvi5) in M. micromalus 245-38 segregated as a single gene in progeny of F1 accession PRI 76-27 (118) and was later conrmed in related progenies (24, 62) (Supplemental Table 6). Segregating independently from other major gene loci (32), the name Vm was assigned to the allelic gene in both original sources (33). By that stage, a race of V. inaequalis had been identied among isolates collected from M. micromalus trees in England (141), and in France in 1968 certain Rvi5 progeny of M. micromalus 245-38 became infected (84). The commonly used M. micromalus derivative 9-AR2T196 (Figure 3) has been selected as the reference h(5). Genetic markers for Rvi5 were identied in M. x atrosanguinea 804 derivatives NY748828-12 and OR45T132 (Figure 3) (29) before it was mapped to LG17 of Murray (108) (Figure 2). A number of race (5) isolates have been isolated from Rvi5 hosts, including isolate 147,
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were mostly performed with isolate 302 (7, 104) collected from a Prima derivative in Germany in 1988 (105). Recently, isolate EU-D42 from the European core collection has been used as the reference isolate for race (6; for examples, see References 26, 79, 103, 127, 128). Relationship (7). Studies with isolate 1066 led to the identication of the HR-conditioning Rvi7 (Vfh) gene in M. x oribunda 821. It segregates independently from Rvi6 (7) and was tentatively mapped to LG8 (38) (Figure 2). Research to identify a single gene reference h(7) from an M. x oribunda 821 progeny is in progress. A GfG relationship for Rvi7 was most clearly demonstrated through the differential interactions of the incompatible isolates 104, 301, 302, and 1093, and the compatible isolate 1066 on certain progeny of a Golden Delicious x M. x oribunda family (7) (Supplemental Table 8). A more recent virulent isolate is EU-NL05 from the European core collection (103). Relationship (8). A GfG relationship was demonstrated for the Rvi8 (Vh8) gene from M. sieversii host (8) accession GMAL3631-W193B from the Tarbagatai mountain range in Kazakhstan, and the AvrRvi8 gene segregating in progenies of race (8) isolates NZ188B.2 (22) and 1639 (17). The Rvi8 gene conditions SN that is indistinguishable from that conditioned by Rvi2 and both genes map to the lower end of LG2 (22, 26). Rvi8 and Rvi2 are closely linked, if not allelic, but are clearly separate genes because isolate NZ188B.2 cannot infect h(2). Similarly, the Avr loci showed genetic interaction, but its nature is not clear (17). The differential interaction of race (8) isolate NZ188B.2 was clearly demonstrated in a range of M. sieversii hosts (22), suggesting that Rvi8 is prevalent in the Kazakh accessions sampled. Two more differential hosts have been selected from this germplasm: B45 derived from accession GMAL4302-X8 and N23 from GMAL4026X435 (Figure 3) (V.G.M. Bus, unpublished data), of which B45 is the reference h(8).
Relationship (9). The presence of a major gene in the crabapple Dolgo (Figure 3) has been demonstrated in three independent studies (Supplemental Table 9) (3, 118; V.G.M. Bus, unpublished data). From the fact that Rvi2and Rvi9-conditioning SN resistance reactions are indistinguishable from each other and that the South Dakota scab isolate 356-2 could overcome both genes (96), one could have concluded that the genes were the same. However, studies with a 356-2 x 651 progeny clearly demonstrated separate GfG relationships for Rvi2 and Rvi9, and genetic dissociation of their respective complementary Avr loci, originally named p-9 and p-8, in the fungus (Supplemental Table 5) (121). Interestingly, both Rvi9 and Rvi2 map close together on LG2 (Figure 2), and their complementary Avr genes are also linked in the pathogen (17, 145). Furthermore, AvrRvi9, like AvrRvi2, shows a 3:1 segregation pattern toward avirulence, with two progeny of the EU-B04 x 1639 cross carrying only AvrRvi9 (17) and therefore being reference race (9) candidates. Progeny K2 of an Elstar x Dolgo (Figure 3) has been selected to replace Dolgo as h(9) because the contrasting interactions of the EU-B04 and 1639 parents conrmed the presence of the previously surmised second scab gene in Dolgo (145), which is identied by only a few isolates. A GfG relationship was demonstrated for this Vdg2 gene in the Elstar x Dolgo progeny K108 (17) but is not included in the nomenclature system because it is a narrow spectrum gene. Relationship (10). The Rvi10 (Va) gene was originally identied in the Antonovka accession PI 172623 (32) but has also been attributed to PI 172633 (82), PI 172612 (144), Freedom (152), and as Va2 to Antonovka APF22 (37). However, the resistance reactions on neither the Freedom nor Antonovka APF22 progenies showed the distinct HR associated with Rvi10 (32), hence requiring further investigation. Because all three PI accessions are conrmed selections from the same B VIII family derived from open-pollinated Antonovka (114),
Monogenic resistance: the resistance in a host is conditioned by a single gene; the gene can be a major or minor effect resistance gene Polygenic resistance: the resistance in a host is conditioned by more than one gene
all of them indeed may carry Rvi10. However, being derived from the original Rvi10 source PI 172623 (32), A723-6 (Figure 3) is the preferred h(10) (50), and research is in progress to conrm its resistance being monogenic given that differential interactions, compared with putative Rvi10 accession PRI 1841-11 (CCR3T11), with race (6) isolates 302 and 305 (104) suggest its parent PI 172623 carries two R genes. Assuming that PRI 1841-11 derived from PI 172633 (Figure 3) carries the gene, Rvi10 has been mapped about 24 cM above the Rvi6 region on LG1 (58) (Figure 2). This conrmed earlier ndings that the phosphoglucomutase (PGM-1) marker (90, 93) is linked to both genes but contradicts the reported independent segregation of Rvi6 and Rvi10 (32). We note, however, that the number of testcrosses used by these authors was too small to be conclusive. Also, a better understanding of the polygenic Antonovka scab resistance needs to be developed before a reference race (10) can be identied [see relationship (17) below]. Relationship (11). Malus baccata jackii was recognized early in the PRI backcross program to carry Rvi11 (Vbj) (32). Rvi11 maps as a distinct R locus near simple sequence repeat (SSR) marker CH05e03, just below the middle of LG2 (57) (Figure 2). A722-7 from an M. baccata jackii cross with Starking (Figure 3) is designated as h(11), provided the resistance of A722-7 is conrmed as being monogenic since M. baccata jackii carries at least one additional narrow spectrum R gene (V.G.M. Bus, unpublished data). To date, no race (11) isolates have been reported. Relationship (12). Rvi12 (Vb) from Hansens baccata #2 is another gene that was recognized early as an independently segregating gene (32). Although it was initially mapped on LG1 (58), Rvi12 was later denitively mapped to LG12 (41) at a considerable distance from Rvi1 (Figure 2). The gene predominantly conditions Chl, in some cases with sporulation, whereas a few progeny show necrotic reactions (32, 41). With Hansens baccata #2 carrying
more than one gene, research is in progress to select an h(12) carrying the single gene Rvi12 resistance. No differential interactions with Rvi12 have been reported to date. Relationship (13). The old Italian cultivar Durello di Forl` containing the major gene Rvi13 (Vd ) (131) has been designated h(13). The gene maps to the proximal end of LG10 of this host near SSR marker CH02b07 (Figure 2). The resistance reactions range from typical SN when the host is inoculated with individual V. inaequalis isolates, such as EUD42, to sporulating Chl reactions when inoculated with a mixture of isolates (131). Although Durello di Forl` appears to carry broad spec trum resistance to apple scab that may involve more than one R gene or QRL (50), certain isolates, such as 1066 and EU-NL05, are able to overcome Rvi13 (79, 103). Relationship (14). The potential of Dulmener Rosenapfel, a scab-resistant cultivar raised from open-pollinated Gravenstein, in resistance breeding was conrmed as it demonstrated broad spectrum resistance (79). The resistance complex includes the Chlconditioning gene Rvi14, previously known under the working name Vdr1 (38), which is the rst scab resistance gene to have been reported under the new nomenclature system presented here and also is the rst R gene that maps to LG6, toward the top near SSR marker HB09 (128) (Figure 2). The resistance is overcome by V. inaequalis isolates 301, EU-D42, and EU-B04, all of which are being characterized for their suitability as reference isolates. Relationship (15). The gene Rvi15 (Vr2) was originally thought to be the third scab R gene from Russian apple (50). However, once it was established that its source accession GMAL 2473 was not related to Russian apple, the gene was recognized as a new source of resistance (106). Although the gene has been shown to induce a range of resistance reactions from no symptoms to Chl in progeny of a cross with Idared (106), it conditioned only necrotic
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reactions in a cross with Golden Delicious (50). Detailed observations determined that the phenotype is HR (45), very similar to those conditioned by Rvi4, to which it appears to be closely linked on LG2 (46, 106) (Figure 2). The locus contains three TIR-NBS-LRR analogs (47) and if, by analogy to the Rvi6 locus, one of them proves to be Rvi15, the other two will be named Rvi15.1 and Rvi15.2 if they are not functional. No V. inaequalis isolate virulent on Rvi15 hosts has been identied to date.
ify the identity of new genes. Some genes, such as Vc and Vj from Cathay and Jonsib, respectively (32, 75), display differential interactions (104), but there is insufcient data on the genetics of these resistances to warrant inclusion at this time. With 992 NBS-LRR and 575 LRRkinase candidate resistance genes identied in the apple genome (135) and approximately 20 scab resistance genes phenotypically mapped onto genetic maps, it is clear that many more genes remain to be revealed through functional testing.
Relationship (16). The Rvi16 gene, with the working name Vmis, was identied in the openpollinated mildew immune selection (MIS) progeny 93.051 G07-098 (21). The gene conditioned a range of resistance reactions from predominantly no visible symptoms with singlespore isolate J222 to Chl reactions with a mixture of V. inaequalis isolates. The resistance was mapped to the lower end of LG3, near SSR marker AU223657 (Figure 2). Recent observations with an extended range of monospore isolates on an open-pollinated MIS progeny suggest that it also carries a narrow spectrum gene (V.G.M. Bus, unpublished data), hence a monogenic h(16) will need to be selected. Relationship (17). Recently, two genes were mapped in an Antonovka APF22 progeny, one of which is Va2 and possibly the same as Rvi10 (see above), whereas the other is Va1, now assigned Rvi17 (37). The gene was identied in a progeny screened in the eld and conrmed on a 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 is not overcome by race (6) isolates and has a specic CH-Vf1 marker allele of 138 bp linked to it (37) [159 bp for Rvi6 (137)]. A suitable differential host is being selected for the determination of differential interactions with V. inaequalis.
Complex Races and Hosts

As outlined above, isolates uniquely lacking the Avr locus complementary to the R gene in each host will be hard to nd. For example, reference race candidate for relationship (1) EU-B04 can overcome Rvi14 besides Rvi1, hence it is identied as race (1,14), and is able to overcome many narrow spectrum genes that are not taken into account in the nomenclature (17). Availability of phenotyped V. inaequalis progenies will facilitate the selection of reference isolates. For example, two progeny from race (1,2,8,9) isolate 1639 crossed with EU-B04 have been identied that can only overcome Rvi9 and Rvi1, and therefore are race (1,9), whereas isolate NZ188B.2 (22) is race (1,8). Linkage between Avr loci, however, may prevent the selection of simple reference isolates, such as race (1,2) in the EU-B04 x 1639 cross. Other examples of complex races are 1066, which is race (6,7,13), and EU-NL24, which is race (1,3,6,7). Given that the latter is known to overcome Antonovka genes, its status is sure to change. Complementary to the race nomenclature, hosts carrying multiple R genes can be identied accordingly, e.g., M. x oribunda is host (6,7), Prima is host (1,6), and Russian apple is host (2,4). Further research is required to complete the table on the host-pathogen interactions of the current reference isolates or their replacement isolates, including reevaluation of several interactions, as some tests have been contradictory and/or inconclusive. Additional reference isolates need to be identied and characterized on
Potential Additional Differential Hosts

The revised nomenclature for the V. inaequalis Malus pathosystem is proposed to facilitate work with existing genetic resources and to clar-
the differential hosts for the scab R genes, for which no reference race isolates have been identied to date (assuming they exist).
CONCLUSION
A thorough understanding of host-pathogen interactions is required if we are to achieve durable resistance, particularly in perennial crops such as apple. The identication of differential hosts with monogenic resistances will assist in the monitoring of pathogen populations to determine the potential of specic R genes, currently the main sources of resistance in apple breeding. It is clear that not all R genes are equivalent when it comes to durability. Developing durable strategies will require signicant knowledge advances in several areas: identication of the armory of pathogen effectors that manipulate host-preformed and induced barriers to infection; how pathogen molecules trigger defense in hosts; how host factors relate to quantitative resistances; and how nonhost resistance operates. Moreover, durability of a combination of R genes can be somewhat different from the simple addition of intrinsic durability, if measurable, of each gene involved. Current strategies to create durable scab resistance in apple involve gene pyramiding with both R genes and available quantitative resistances (28, 39, 86, 128), which has proved effective in other crops (see References 19, 101), or transgenics involving antifungal proteins (11). Apple breeders have a broad range of R genes and QRLs available to them for creating polygenic resistances. Currently in traditional breeding, marker-assisted selection, most effectively with functional markers, plays an essential role in efciently developing new cultivars (117) with the desired R gene combinations effective against scab and other pests and diseases. Unless breeders have detailed knowledge of the most effective R gene and/or QRL combinations, genes will continue to be pyramided at random, until research shows that certain R genes/QRLs may be superior in terms of their individual durability. This is conceivable as some of the resistance proteins are likely to recognize effector proteins signicant to the pathogen infection process and/or have a different mode of action.
Genetic and Genomic Tractability of Host and Pathogen

Genetics and genomics of both the host and pathogen in the MalusV. inaequalis interaction have advanced dramatically in the past two decades. In terms of the host, comprehensive genetic maps exist, and a version of the genome sequence has just been published (135). Apple behaves in most aspects as a genetic diploid despite the polyploidization event in the history of the Rosaceae subfamily to which it belongs. Candidates for both major R gene loci and important resistance QRLs can now be mined and empirically tested by using genome sequence, aided by next-generation sequencing skim reads from selected hosts carrying alleles of interest. Other genomic aids, such as transformation (67, 91, 151) and gene knockdown using RNAi (51) are also practical in the host and will aid in identifying functional alleles. In terms of the pathogen V. inaequalis, the rst genetic maps have been developed (17, 149), and genome sequencing (28a; M. Templeton, personal communication; B. Le Cam, personal communication) and in planta transcriptomics (M. Templeton, personal communication) will further facilitate the identication of specic Avr genes. Asexually produced conidia of V. inaequalis allow each genotype to be xed through clonal multiplication in vitro for use in phytopathological and genomic studies. In addition, transformation systems are available that enable complementation and RNAi-based knockdown of genes (42, 43) to validate fungal effector function as candidates are identied (16, 77). Heterologous expression in apple or yeast, combined with purication of individual V. inaequalis avirulence proteins, may also allow elucidation of specic GfG interactions. Thus, both host and pathogen systems are now eminently tractable and the pace of advances in MalusV. inaequalis research can be expected to accelerate in the next decade.
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Although many natural scab resistance pyramids of major R genes have been identied in germplasm, this does not necessarily translate into durable resistance. Combinations present in, for example, Russian apple R127407A and M. micromalus have not been deployed extensively in temporal or spatial terms to conrm their durability, and the development of race (6,7) on M. x oribunda (7), at rst glance, suggests that pyramiding is no guarantee for durable resistance. This race may have acquired the virulences in sequential order, which, if this is the case, accentuates the need for only releasing cultivars with at least two, if not three or more, resistance genes. It has been suggested that four to six genes may provide long-term resistance or even immunity (98). Gene pyramiding will be more effective if it is aimed at the most essential effector genes from the pathogen (140), i.e., the effectors that evoke the maximum tness cost when lost or compromised (81). A glasshouse simulation study with race (5) isolates of V. inaequalis indeed suggested that some, but not all, isolates had a lower tness leading to their disappearance from the pathogen population (61). Similarly, isolates of race (6) were shown to exhibit a lower tness when compared with isolates of race (1) (27). It is anticipated that sequential losses of the pathogenicity factors (effectors) that are commonly encoded by Avr loci will increasingly reduce the tness of the pathogen until the combined losses become insurmountable, which would lead to stabilizing selection (132). The efcacy of gene combinations will be partly determined by the geographical distribution of cognate races. V. inaequalis populations are highly diverse genetically, both within orchards and regions as well as in different parts of the world (53, 133, 134, 150), and differ in their virulence in different geographical regions (see Reference 87). The next major challenge is to determine the race distribution of V. inaequalis in apple production regions and to develop a strategy for the durable deployment of R genes, and to prevent it from being undone through human activity (56). To this effect, a pathogen population monitoring program has
been initiated involving the establishment of a network of trap orchards around the world comprising a range of well-characterized differential hosts (107). Breeders and researchers can register to participate in this project at the website http://www.vinquest.ch and will receive budwood of the differential host set. Newly conrmed GfG relationships can be reported through the same website for inclusion in the revised nomenclature system. Race monitoring will be aided by the identication of Avr/effector proteins, which will in turn facilitate R gene identication and deployment. To date, no Avr genes have been cloned; however, the identication of SSR markers in V. inaequalis (55, 134) and mapping of avirulence loci (17) have been the rst step toward the mapping and cloning of the rst Avr gene, AvrRvi1, in this pathogen (18). Research on host-pathogen interactions at the molecular level and understanding the role that proteins, such as NBS-LRR, play in the recognition and signaling pathways (6) is one of the major research topics in plant science today. Knowledge of plant defenses that are vulnerable to pathogen attack and cell death suppressors that negate the programmed cell death of HR in the presence of R-Avr interactions (e.g., 94) has thrown new light on GfG relationships. In the arms race, the host evolves new resistance specicities through intragenic recombination (65) and sometimes only small changes are required to change specicity (see References 36, 70). As some R genes carry signicant tness costs, a wide array of alleles are maintained in wild populations through a rapid process of birth and death. Pathogens have complementary birth and death systems in place that can evolve rapidly (147). Following research on host-pathogen interactions in major agricultural crops, molecular research on the host-pathogen interaction of scab in apple is progressing in both the host, e.g., R gene cloning, which has advanced to the proofof-function stage for the Rvi6 gene (5, 92, 102, 126, 136, 148), and the pathogen, e.g., identication of candidate effector genes and proteins (16, 43, 146). R gene transformation
may range from transferring genes within the genus through cisgenesis (116), to articially constructed genes effective against a range of pathogens (66). A major advantage of transformation systems in the host is that gene cassettes can be inserted into one cultivar specically designed to resist the regional V. inaequalis populations, based on the near-isogenic lines concept, but still be marketed as a single cultivar. Going a step further, trees with different gene cassettes could be planted in the same orchard in order to achieve genetic diversity for scab resistance to help reduce the rate of pathogen adaptation (10, 35, 113). The combination of the different resistance mechanisms present in the plant determines its ability to withstand infection by particular
pathogens. In this review, the focus has been on the differential interactions involving GfG relationships in the V. inaequalisMalus pathosystem. Host-specic resistance has an important role to play in this pathosystem provided some measure of predicting the durability of resistance strategies is developed. Nonhost resistance also deserves some attention in the future as an area that has considerable promise for generating lasting resistance. Understanding of the molecular basis of fungal effector function and their inuence on host physiology via interactions with host molecules, including resistance proteins, will provide the conceptual context required to achieve durable resistance to V. inaequalis as well as other pathogens in apple.
SUMMARY POINTS 1. The existing nomenclature system for apple scab races suffered from signicant problems and was in need of updating. 2. A comprehensive new nomenclature system and a set of rules for dening new GfG relationships in the V. inaequalisMalus pathosystem is presented. 3. Information on the rst 17 relationships is provided with a focus on identifying differential Malus hosts carrying single resistance genes. 4. The nomenclature system is well-suited to describe complex races of V. inaequalis as well as resistance sources carrying pyramided resistances.
FUTURE ISSUES 1. A project to develop a reference set of V. inaequalis isolates for the validation of newly identied GfG relationships is in progress. 2. Another project to monitor V. inaequalis populations for their pathotypes to determine the effectiveness of scab resistance genes by geographic region has been initiated. The information generated should enable association mapping of avirulence genes in the pathogen to eventually replace pathogenicity tests for virulence conrmation. 3. The pathotyping information will be used to identify virulence patterns that may improve our understanding on tness penalties in the pathogen and translate this into breeding strategies for durable resistance. This will be supported by molecular research on effector genes and their protein products and host targets. 4. It is the intention to cast the research net wider by investigating additional strategies for scab control involving alternative resistances based on race-nonspecic genes, nonhost resistance, and manipulation of the specicity of resistance genes.
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5. The ultimate goal is to integrate various resistance and disease management strategies to achieve resistance that is durable in the eld.
DISCLOSURE STATEMENT
The authors are not aware of any afliations, memberships, funding, or nancial holdings that might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
We thank our colleagues of the scab resistance research and breeding community for their contributions to a preliminary proposal and support to update the scab race nomenclature (25): Herb Aldwinckle, Susan Gardiner, Cesare Gessler, Remmelt Groenwold, Francois Laurens, Bruno Le Cam, Jim Luby, Bert Meulenbroek, Markus Kellerhals, Luciana Parisi, Andrea Patocchi, Henk Schouten, Stefano Tartarini, and Eric van de Weg. The research is supported by the New Zealand Foundation for Science, Research and Technology (contracts C06X0810 and C06X0812). LITERATURE CITED
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Not As They Seem George Bruening p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1 Norman Borlaug: The Man I Worked With and Knew Sanjaya Rajaram p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p17 Chris Lamb: A Visionary Leader in Plant Science Richard A. Dixon p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p31 A Coevolutionary Framework for Managing Disease-Suppressive Soils Linda L. Kinkel, Matthew G. Bakker, and Daniel C. Schlatter p p p p p p p p p p p p p p p p p p p p p p p p p p p47 A Successful Bacterial Coup dEtat: How Rhodococcus fascians Redirects Plant Development Elisabeth Stes, Olivier M. Vandeputte, Mondher El Jaziri, Marcelle Holsters, and Danny Vereecke p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p69 Application of High-Throughput DNA Sequencing in Phytopathology David J. Studholme, Rachel H. Glover, and Neil Boonham p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p87 Aspergillus avus Saori Amaike and Nancy P. Keller p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 107 Cuticle Surface Coat of Plant-Parasitic Nematodes Keith G. Davies and Rosane H.C. Curtis p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 135 Detection of Diseased Plants by Analysis of Volatile Organic Compound Emission R.M.C. Jansen, J. Wildt, I.F. Kappers, H.J. Bouwmeester, J.W. Hofstee, and E.J. van Henten p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 157 Diverse Targets of Phytoplasma Effectors: From Plant Development to Defense Against Insects Akiko Sugio, Allyson M. MacLean, Heather N. Kingdom, Victoria M. Grieve, R. Manimekalai, and Saskia A. Hogenhout p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 175 Diversity of Puccinia striiformis on Cereals and Grasses Mogens S. Hovmller, Chris K. Srensen, Stephanie Walter, and Annemarie F. Justesen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 197
Volume 49, 2011
Emerging Virus Diseases Transmitted by Whiteies Jesus Navas-Castillo, Elvira Fiallo-Oliv , and Sonia S nchez-Campos p p p p p p p p p p p p p p p p p 219 e a Evolution and Population Genetics of Exotic and Re-Emerging Pathogens: Novel Tools and Approaches Niklaus J. Grunwald and Erica M. Goss p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 249 Evolution of Plant Pathogenesis in Pseudomonas syringae: A Genomics Perspective Heath E. OBrien, Shalabh Thakur, and David S. Guttman p p p p p p p p p p p p p p p p p p p p p p p p p p p 269 Hidden Fungi, Emergent Properties: Endophytes and Microbiomes Andrea Porras-Alfaro and Paul Bayman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 291
Hormone Crosstalk in Plant Disease and Defense: More Than Just JASMONATE-SALICYLATE Antagonism Alexandre Robert-Seilaniantz, Murray Grant, and Jonathan D.G. Jones p p p p p p p p p p p p p 317 Plant-Parasite Coevolution: Bridging the Gap between Genetics and Ecology James K.M. Brown and Aur lien Tellier p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 345 e Reactive Oxygen Species in Phytopathogenic Fungi: Signaling, Development, and Disease Jens Heller and Paul Tudzynski p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 369 Revision of the Nomenclature of the Differential Host-Pathogen Interactions of Venturia inaequalis and Malus Vincent G.M. Bus, Erik H.A. Rikkerink, Val rie Cafer, Charles-Eric Durel, e and Kim M. Plummer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 391 RNA-RNA Recombination in Plant Virus Replication and Evolution Joanna Sztuba-Solinska, Anna Urbanowicz, Marek Figlerowicz, and Jozef J. Bujarski p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 415 The Clavibacter michiganensis Subspecies: Molecular Investigation of Gram-Positive Bacterial Plant Pathogens Rudolf Eichenlaub and Karl-Heinz Gartemann p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 445 The Emergence of Ug99 Races of the Stem Rust Fungus is a Threat to World Wheat Production Ravi 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 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 465 The Pathogen-Actin Connection: A Platform for Defense Signaling in Plants Brad Day, Jessica L. Henty, Katie J. Porter, and Christopher J. Staiger p p p p p p p p p p p p p p p 483
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Understanding and Exploiting Late Blight Resistance in the Age of Effectors Vivianne 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 p p p p p p p p p p p p p p p 507 Water Relations in the Interaction of Foliar Bacterial Pathogens with Plants Gwyn A. Beattie p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 533 What Can Plant Autophagy Do for an Innate Immune Response? Andrew P. Hayward and S.P. Dinesh-Kumar p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 557
Errata An online log of corrections to Annual Review of Phytopathology articles may be found at http://phyto.annualreviews.org/
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ANNUAL REVIEWS

THE VENTURIA INAEQUALISMALUS PATHOSYSTEM

Differential Interactions in the Venturia inaequalisMalus Pathosystem

NOMENCLATURE OF VENTURIA INAEQUALIS RACES

The Nomenclature Model

Venturia inaequalisMalus Gene-for-Gene Relationships

CH04e02 Rvi14 HB09 CH1d03y CH03d07

CH05d02 CH03d12 Rvi3 Hi08e04

CH02g04 CH01g12 CH01f02 Rvi12 CH04f08

Hi07f01 GD100 CH01d03z Rvi1 NZ17e06

Dg. R13T43 (PRI 27-330) Delicious

Wealthy Russian apple R12740-7A

OR45T132 (PRI 333-9)

Starking Delicious PRI 610-2

McIntosh PRI 14-266

Golden Delicious 26829-2-2

PRI 1841-11 (CCR3T11)

Starking M. baccata jackii

Complex Races and Hosts

Potential Additional Differential Hosts

Genetic and Genomic Tractability of Host and Pathogen

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Annual Review of Phytopathology

Volume 49, 2011

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