Revision of the nomenclature of differential host-pathogen interactions of Venturia inaequalis and Malus

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/264158785
A proposal for the nomenclature of Venturia inaequalis races
Article  in  Acta horticulturae · September 2007
CITATIONS
28
READS
578
19 authors, including:
Some of the authors of this publication are also working on these related projects:
Controlling recombination in plants View project
Genetic mapping of resistance to Pseudomonas syringae pv Actinidiae (Psa) in kiwifruit View project
H.s. Aldwinckle
Cornell University
233 PUBLICATIONS   4,217 CITATIONS
SEE PROFILE
Valerie Caffier
French National Institute for Agriculture, Food, and Environment (INRAE)
50 PUBLICATIONS   844 CITATIONS
SEE PROFILE
Susan Elizabeth Gardiner
Plant and Food Research
202 PUBLICATIONS   5,992 CITATIONS
SEE PROFILE
All content following this page was uploaded by Kim M Plummer on 29 July 2014.
The user has requested enhancement of the downloaded file.

PY49CH19-Bus ARI 15 July 2011 17:26
Revision of the Nomenclature
of the Differential Host-
Pathogen Interactions of
Venturia inaequalis and Malus
Vincent G.M. Bus,1
Erik H.A. Rikkerink,2
Valérie Caffier,3
Charles-Eric Durel,4
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 Végétale – PaVé, INRA/ACO/UA, IFR QUASAV, BP 60057,
F-49071 Beaucouzé, France; email: Valerie.Caffier@angers.inra.fr
4
INRA, UMR 1259 Genetics and Horticulture – GenHort, INRA/ACO/UA, IFR
QUASAV, BP 60057, F-49071 Beaucouzé, France; email: Charles-Eric.Durel@angers.inra.fr
5
La Trobe University, Department of Botany, Bundoora, Vic. 3086, Australia;
email: K.Plummer@latrobe.edu.au
Annu. Rev. Phytopathol. 2011. 49:391–413
The Annual Review of Phytopathology is online at
phyto.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 the
first systems for which Flor’s concept of gene-for-gene (GfG) relation-
ships 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 pre-
requisite for effectively manipulating these host resistance factors. An
accurate means of identification of specific resistance and consistent
use of gene nomenclature is critical for this process. A set of univer-
sally available, differentially resistant hosts is described, which will be
followed by a set of defined 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
Annu.Rev.Phytopathol.2011.49:391-413.Downloadedfromwww.annualreviews.org
byLaTrobeUniversity-Bendigoon10/09/11.Forpersonaluseonly.
Click here for quick links to
Annual Reviews content online,
including:
• Other articles in this volume
• Top cited articles
• Top downloaded articles
• Our comprehensive search
FurtherANNUAL
REVIEWS

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 world’s 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 specific epithet reflect the di-
verse ancestry of this species, with various hy-
bridizations between Malus species giving rise
to the domesticated apple (76). Nevertheless, it
was recognized as one of the 33 primary Malus
species in five sections based on the classifi-
cation 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 ex-
pected of commercial apples today. M. sieversii
has also been confirmed as the main progeni-
tor 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 first extensive ge-
netic 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 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 fungus
Venturia inaequalis (Cke) Wint. (anamorph: Spi-
locaea pomi Fries), is one of the most damaging
in 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 apple
scab, and as many as 18–25 fungicide applica-
tions per growing season may be required (139).
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 culti-
vars is the consumer antagonism to non-natural
compounds 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 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 re-
sistance through traditional breeding is a slow
process but can be accelerated by adding re-
sistance into existing high quality cultivars by
marker-assisted fast breeding (138) or cisgene-
sis (116). Ultimately, an in-depth understand-
ing of host-pathogen interactions, including the
specific 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 strate-
gies (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 sufficiently
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 Pyra-
cantha, Eriobotrya, and accessions of Kageneckia
and 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. pyracanthae
on Pyracantha spp. and f.sp. pomi on Malus spp.
Recent research indicated that V. inaequalis
392 Bus et al.

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-specific ef-
fectors. 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-for-
gene (GfG) relationships and present an up-
dated nomenclature system.
THE VENTURIA
INAEQUALIS–MALUS
PATHOSYSTEM
An intricate host-pathogen interaction struc-
ture has evolved in the V. inaequalis–Malus
pathosystem (89). Recent research supports the
idea that the disease emerged in the center of
origin 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 of
the world as people migrated to new territories,
and scab probably became more prevalent be-
cause 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 intro-
ductions have been relatively recent, much later
than the introduction of apple (89).
An important aspect of the life cycle of V. in-
aequalis is its annual sexual phase on leaf litter in
winter. Pseudothecia are formed only from het-
erothallic mating, requiring two different mat-
ing types (73). Each pseudothecium contains
many asci, each containing four pairs (tetrad) of
ascospores resulting from a meiotic division fol-
lowed 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
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 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 corresponding
gene 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 of
the first examples for which GfG relationships
were suggested based on the segregation of Avr
genes in the fungus (13, 145). Today, the resis-
tance relationship is commonly hypothesized
to be a specific recognition event, either di-
rect or indirect, between a host R gene prod-
uct and a corresponding pathogen Avr gene
product (69), the complexity of which is still
not completely clear. Additionally, many ma-
jor R gene loci in apple condition distinct phe-
notypic reactions, which have been assigned
to resistance classes (Table 1; Supplemen-
tal Table 1, follow the Supplemental Mate-
rial link from the Annual Reviews home page
at http://www.annualreviews.org): hypersen-
sitive 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 multipli-
cation during the growing season provides
V. inaequalis opportunities for adaptive selec-
tion 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 well-
characterized 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
Supplemental Material

Table 1 Nomenclature of the gene-for-gene relationships between Venturia inaequalis and Malus. The races are defined by
the avirulence genes they are lacking, hence resulting in susceptibility on the complementary host
Malus Venturia inaequalis
Differential host Resistance locus
Avirulence
locus
Number Accession Phenotype Historical LGa New New Old Race
h(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
821b
hypersensitive 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
#2b
chlorosis Vb 12 Rvi12 AvrRvi12d (12)
h(13) Durello di Forl`ı stellate necrosis Vd 10 Rvi13 AvrRvi13d (13)
h(14) Dülmener
Rosenapfelb
chlorosis Vdr1 06 Rvi14 AvrRvi14d (14)
h(15) GMAL2473 hypersensitive response Vr2 02 Rvi15 AvrRvi15d (15)
h(16) MIS op 93.051
G07–098b
hypersensitive response Vmis 03 Rvi16 AvrRvi16d (16)
h(17) Antonovka
APF22b
chlorosis Va1 01 Rvi17 AvrRvi17d (17)
a
LG = linkage group of apple.
b
Temporary differential host until the host has been confirmed 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 confirmed to date.
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 iden-
tification of new ones. In the past, a number
of isolates poorly defined on a low number of
differential hosts have been used for genetic
studies (Supplemental Table 2), which has
led to uncertainty about specific interactions.
Definition of a Race
We define a single-spore isolate of the pathogen
as a race when it is able to overcome completely
the resistance in a host. Determination of the
race status is based on the premise that a mu-
tation at the Avr locus in the pathogen leads
to nonrecognition by the host, hence leading
to complete susceptibility. The race spectrum
is defined by the combination of R genes it can
overcome.
The effect of resistance genes covers a con-
tinuum from immunity for major effect genes
to near-susceptibility for quantitative resistance
loci (QRLs), depending on its genetic back-
ground, the pathogen, and the environment
394 Bus et al.

1 cm 1 mm 1 cm
a b c
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).
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
(109). The effect is independent of the spec-
trum 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 field (see References 8, 112) does not
necessarily mean the presence of a breaking
race but instead can represent opportunistic in-
fections by avirulent strains under conditions
highly conducive to the disease. Follow-up re-
search is therefore always required to confirm
the virulence status of putative race isolates (see
References 22, 23, 105).
Differential Interactions in the
Venturia inaequalis–Malus
Pathosystem
Interestingly, the initial focus of genetic stud-
ies on the V. inaequalis–Malus pathosystem was
on avirulence in the pathogen rather than re-
sistance in the host. Genetic analysis of over
23,000 asci resulted in the identification of 19
Avr genes, named pathogenicity ( p) genes (12,
13) (Supplemental Table 3). The first 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. in-
aequalis reported to date are inherited indepen-
dently (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 identified in a mapping study of
V. inaequalis Avr genes (17).
Many of the first described interactions
involved genes conferring resistance effective
against a low proportion of the pathogen pop-
ulation, i.e., they were narrow spectrum (versus
broad 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. inaequalis
geneticists also realized that it was impractical
to name all the races, as the isolates carrying
the first 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 over-
come broad spectrum R genes with potential
for resistance breeding were defined in the race
nomenclature (89), comprising eight races that
have been described to date (Supplemental
Table 4). This old nomenclature system, how-
ever, was cumbersome as a single race number
could involve several GfG relationships, e.g.,
race (2) isolate 356-2 could overcome the dif-
ferent resistances in Dolgo, Geneva, and certain
segregates of Russian apple R12740-7A (121).
A system where all compatible interactions can

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.
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 complemen-
tary scab resistance genes. The nomenclature
for the latter was based on identifying them by
their source of resistance, therefore the GfG re-
lationships between the resistance genes in the
host and the avirulence genes in the pathogen
were not obvious. This anomaly will be cor-
rected in the nomenclature system proposed
here, which is based on the system first pro-
posed for Phytophthora infestans and potato (9)
and is commonly used for other host-pathogen
interactions.
The Nomenclature Model
In describing GfG relationships, where k rep-
resents the number of the specific 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, identi-
fied as avrk, at the Avrk locus. Once the in-
dividual Rk-Avrk interaction has been defined,
isolates lacking multiple avirulences can then
be identified by their formula based on the
combination of the individual virulences. It ac-
commodates complex loci as well as QRLs for
which differential host-pathogen interactions
are demonstrated. Simultaneously with the re-
vision of these GfG relationships, we align the
nomenclature of apple scab R genes with the in-
ternational standard of gene nomenclature for
Arabidopsis (97). The names of major R genes
start with R and contain an abbreviation of the
pathogen V. inaequalis to give the general locus
prefix Rvi.
The proposed system is based on the fol-
lowing 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 (sufficiently)
been shown to be novel either with the aid
of a breaking race that has been screened
against all other reference hosts to estab-
lish that the new Avr allele is different
from existing alleles or preferably also by
screening 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 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 dif-
ferent loci will be identified 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 identified
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.
Venturia inaequalis–Malus
Gene-for-Gene Relationships
Below we describe the 17 GfG relationships
defined to date and add relationship (0) in-
volving host (0) that does not carry any resis-
tance genes to correct the erroneous use of
396 Bus et al.

race (1) to date. We identify the knowledge
gaps and confirm the genetics of resistance and
(a)virulence in different accessions and races. In
the development of the new numerical nomen-
clature 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 differ-
ential hosts for races (2) to (7) remain largely
the 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-characterized
genes with temporary working names that are
used in breeding will be assigned Rvi-AvrRvi re-
lationship numbers for inclusion in the nomen-
clature system. We also recognize that some
of 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 these
cases, 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 a
later stage.
Relationship (0). Host (0) can be defined as
the host that does not carry any R genes and
hence is susceptible to all isolates of V. inae-
qualis. 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. 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 been
selected to represent h(0) (Table 1). On the
pathogen side, the common race (121, 145) of
V. inaequalis was originally defined as race (1),
which is inconsistent with the race names in
other pathosystems. We therefore rename it
race (0) and define it as the race that is avir-
ulent 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 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 premise
that narrow spectrum R genes should be ex-
cluded from the nomenclature is made for the
Rvi1 (Vg) gene from Golden Delicious. Al-
though this gene is overcome by an estimated
87% of the pathogen population in Europe
(103), both host (1) and race (1) have been ex-
tensively characterized, which makes this an
important model system to advance our un-
derstanding of the basis of ephemeral, versus
durable, R genes. The inclusion of relationship
(1) also reduces the degree of confusion be-
tween races (0) and (1), as isolates described as
race (1) in the old nomenclature before the dis-
covery 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 first demonstrated with
avirulent isolate 101 (84) and confirmed with
isolate 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 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 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 was
used in the attempt to clone AvrRvi1 (18).
Relationship (2). Early genetic studies on
Russian apple R12740-7A, whose resistance re-
actions ranged from Class 0 (no macroscopic
symptoms) to Class 2 (necrosis), depending on
the 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

LG1
Rvi10
Rvi6
Rvi17
AG11
CH05g08
CH-Vf1
Rvi15
Rvi4
CH02c02a
Rvi16
CH03e03
CH03g07
Hi03d06
AU223657
Rvi3
Hi08e04
Rvi14
CH03d12
CH03c01
CH03d07
HB09
CH0202b
CH05d02
CH1d03y
CH04e02
CH03g12y
CH03g12a
Rvi11
Rvi9
Rvi2
Rvi8
Aco-1
CH03d01
CH05e03
LG2 LG3 LG4 LG6
LG8
Rvi7
Rvi13
CH02b07
CH05h12
CH04f03
CH03d11
GD100
Rvi1
Rvi12
CH01d03z
Hi07f01
CH01f02
CH01g12
CH05d04
Rvi5
Hi07h02
NZ17e06
CH04c06
CH02g04
CH04f08
CH01e12
CH01c06
CH05a02y
CH01h10
Hi15h11
LG10 LG12 LG17
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 N’Diaye et al. (99).
known races of V. inaequalis at that time (32),
and the Russian apple derivatives Si and S’i were
the differential hosts for races (2) and (4), re-
spectively (82, 100). Host (2), first shown to be
overcome 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 with
the SN phenotype (1), but this error was cor-
rected 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 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 as
being accession TSR34T132 (104, 105), an
error perpetuated in other papers (e.g., 50,
89, 112). However, the correct identifica-
tion numbers are TSR34T15 (correspondence
E.B. Williams to Y. Lespinasse, 20 February
1984) and PRI 384-1 (26). In the same cor-
respondence TSR34T15 is also identified 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,
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 the
Rvi2 gene (26), but AvrRvi2 in this isolate seg-
regated 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 iso-
lates predominantly induce SN reactions but
were able to sporulate under extended mois-
ture conditions in lesions described as 2 → 4
(121). In fact, Geneva was shown to carry two
resistance genes, and the authors’ interpreta-
tion was that the p-10 locus induced Class 2
resistance reactions with one R gene and the in-
dependently segregating p-11 locus the 2 → 4
398 Bus et al.

phenotype with another gene (Supplemental
Table 5). However, a Chl-conditioning gene
was also observed in Geneva (145), which sug-
gests 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 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 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 elu-
cidation, 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 definitely associ-
ated 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
identification 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 mapped
definitively 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 per-
formed 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
TSR34T15 (PRI 384-1; OR42T173)
Host (2)
McIntosh
Russian apple R12740-7A
R7T81 (PRI 45-39)
Delicious
Host (4) Wealthy
Dg. R13T43 (PRI 27-330)
TSR33T239 (PRI 478-33; W7AR44T20) Russian apple R12740-7A
Delicious
Host (5)
McIntosh
9-AR2T196 (PRI 643) Wolf River
R14T102 (PRI 76-29)
M. micromalus 245-38
McIntosh
OR45T132 (PRI 333-9) Wolf River
R16T52 (PRI 69-118)
M. x atrosanguinea 804
Host (6)
Starking Delicious
Priscilla (PRI 1659-1) McIntosh
PRI 610-2 Golden Delicious
PRI 14-266
26829-2-2
Host (8)
Sciearly
B45
M. sieversii GMAL4302-X8
Sciros
N23
M. sieversii GMAL4026-X435
Host (9)
Elstar M. baccata
K2 M. x robusta
Dolgo M. prunifolia
Open-pollinated
Host (10)
Worcester Pearmain
A723-6
PI 172623 (B VIII 33,25)
McIntosh
PRI 1841-11 (CCR3T11) PI 172633 (B VIII 34,6)
PRI 703-1 (9-AR6T136)
Jonared
Host (11)
Starking
A722-7
M. baccata jackii
Figure 3
The pedigrees of Malus differential hosts for apple scab derived from mostly
polygenic 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 was
completely compatible with hosts carrying the
Rvi4 gene (Figure 4) (20).
Relationship (5). Malus micromalus 245-38
and Malus x atrosanguinea 804 were identified
early in the PRI breeding program (63) as
highly resistant sources conditioning HR, vis-
ible within three days after inoculation (119,

a
EU-NL19 EU-NL19 EU-B05
1638 1638 1638
b c
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 first 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 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 in
progeny of F1 accession PRI 76-27 (118) and
was 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 gene
in both original sources (33). By that stage, a
race of V. inaequalis had been identified 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. microma-
lus derivative 9-AR2T196 (Figure 3) has been
selected as the reference h(5). Genetic markers
for Rvi5 were identified 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 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 the
AvrRvi5 effector.
Relationship (6). The genetics of the resis-
tance from Malus x floribunda 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 al-
lelic sources of Rvi6 have been identified (33,
142,143),someof which havebeen suggested to
also carry the gene based on the specific linkage
of 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 may
also be renamed if its functionality (92) is con-
firmed as having sufficiently broad utility.
Rvi6-associated resistance is variable in both
segregation ratios and resistance levels (30), and
a range of explanations for this has been pro-
posed, e.g., influence 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 sim-
pler explanation, however, is that some plants
presented 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 confirm
Rvi6 being present in most seedlings in this
class (49). In early backcross generations, the
M. x floribunda 821 resistance clearly segregated
as a single major gene (64) (Supplemental
Table 7), but differential interactions among
F2 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), but
to date many of the commonly used h(6) acces-
sions (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
400 Bus et al.

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 identification of the HR-conditioning
Rvi7 (Vfh) gene in M. x floribunda 821. It seg-
regates 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 floribunda 821 progeny is in
progress.
A GfG relationship for Rvi7 was most clearly
demonstrated through the differential interac-
tions of the incompatible isolates 104, 301, 302,
and 1093, and the compatible isolate 1066 on
certain progeny of a Golden Delicious x M. x
floribunda 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 Kaza-
khstan, 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 be-
causeisolateNZ188B.2cannotinfecth(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.2
was clearly demonstrated in a range of M. siev-
ersii hosts (22), suggesting that Rvi8 is preva-
lent in the Kazakh accessions sampled. Two
more differential hosts have been selected from
this germplasm: B45 derived from accession
GMAL4302-X8 and N23 from GMAL4026-
X435 (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 stud-
ies (Supplemental Table 9) (3, 118; V.G.M.
Bus, unpublished data). From the fact that Rvi2-
and Rvi9-conditioning SN resistance reactions
are indistinguishable from each other and that
the 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 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 (Supplemen-
tal 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 Avr-
Rvi9 (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 in-
teractions of the EU-B04 and 1639 parents
confirmed the presence of the previously
surmised second scab gene in Dolgo (145),
which is identified 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 identified 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 con-
firmed 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 con-
firm its resistance being monogenic given that
differential interactions, compared with puta-
tive 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 re-
gion on LG1 (58) (Figure 2). This confirmed
earlier findings that the phosphoglucomutase
(PGM-1) marker (90, 93) is linked to both genes
but contradicts the reported independent seg-
regation of Rvi6 and Rvi10 (32). We note, how-
ever, 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 devel-
oped before a reference race (10) can be identi-
fied [see relationship (17) below].
Relationship (11). Malus baccata jackiiwasrec-
ognized 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
confirmed as being monogenic since M. baccata
jackii 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’s
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 definitively mapped to
LG12 (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 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`ı 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 EU-
D42, to sporulating Chl reactions when inocu-
lated with a mixture of isolates (131). Although
Durello di Forl`ı appears to carry broad spec-
trum resistance to apple scab that may involve
more than one R gene or QRL (50), certain iso-
lates, such as 1066 and EU-NL05, are able to
overcome Rvi13 (79, 103).
Relationship (14). The potential of
Dülmener Rosenapfel, a scab-resistant cultivar
raised from open-pollinated Gravenstein,
in resistance breeding was confirmed as it
demonstrated broad spectrum resistance (79).
The resistance complex includes the Chl-
conditioning gene Rvi14, previously known
under the working name Vdr1 (38), which is the
first scab resistance gene to have been reported
under the new nomenclature system presented
here and also is the first 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
402 Bus et al.

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 closely
linked 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 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 identified to date.
Relationship (16). The Rvi16 gene, with the
working 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 was
mapped to the lower end of LG3, near SSR
marker 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 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 as-
signed Rvi17 (37). The gene was identified in a
progeny screened in the field and confirmed 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 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 determination
of differential interactions with V. inaequalis.
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-
ify the identity of new genes. Some genes, such
as 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 at
this time. With 992 NBS-LRR and 575 LRR-
kinase candidate resistance genes identified 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.
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 find. For example, reference
race candidate for relationship (1) EU-B04 can
overcome Rvi14 besides Rvi1, hence it is identi-
fied 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 fa-
cilitate the selection of reference isolates. For
example, 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 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. Complemen-
tary to the race nomenclature, hosts carrying
multiple 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 the
table on the host-pathogen interactions of the
current reference isolates or their replacement
isolates, including reevaluation of several inter-
actions, as some tests have been contradictory
and/or inconclusive. Additional reference iso-
lates need to be identified and characterized on

the differential hosts for the scab R genes, for
which no reference race isolates have been iden-
tified to date (assuming they exist).
Genetic and Genomic Tractability
of Host and Pathogen
Genetics and genomics of both the host and
pathogen in the Malus–V. inaequalis interac-
tion 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 his-
tory of the Rosaceae subfamily to which it be-
longs. 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 sequenc-
ing skim reads from selected hosts carrying al-
leles of interest. Other genomic aids, such as
transformation (67, 91, 151) and gene knock-
down using RNAi (51) are also practical in the
host 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. Le
Cam, personal communication) and in planta
transcriptomics (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 multiplication
in vitro for use in phytopathological and ge-
nomic studies. In addition, transformation sys-
tems are available that enable complementation
and RNAi-based knockdown of genes (42, 43)
to validate fungal effector function as candidates
are identified (16, 77). Heterologous expression
in apple or yeast, combined with purification of
individual V. inaequalis avirulence proteins, may
also allow elucidation of specific GfG interac-
tions. Thus, both host and pathogen systems
are now eminently tractable and the pace of ad-
vances in Malus–V. inaequalis research can be
expected to accelerate in the next decade.
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 identification of dif-
ferential hosts with monogenic resistances will
assist in the monitoring of pathogen popula-
tions to determine the potential of specific 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. De-
veloping durable strategies will require signifi-
cant knowledge advances in several areas: iden-
tification 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 re-
late to quantitative resistances; and how non-
host 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 resis-
tance in apple involve gene pyramiding with
both 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 R
genes and QRLs available to them for creat-
ing polygenic resistances. Currently in tradi-
tional breeding, marker-assisted selection, most
effectively 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 and
diseases. Unless breeders have detailed knowl-
edge of the most effective R gene and/or QRL
combinations, genes will continue to be pyra-
mided at random, until research shows that cer-
tain R genes/QRLs may be superior in terms
of their individual durability. This is conceiv-
able as some of the resistance proteins are likely
to recognize effector proteins significant to the
pathogen infection process and/or have a dif-
ferent mode of action.
404 Bus et al.

Although many natural scab resistance pyra-
mids of major R genes have been identified in
germplasm, this does not necessarily translate
into durable resistance. Combinations present
in, for example, Russian apple R12740–7A and
M. micromalus have not been deployed exten-
sively in temporal or spatial terms to confirm
their durability, and the development of race
(6,7) on M. x floribunda (7), at first 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 releas-
ing 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 pyra-
miding 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
fitness 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 fit-
ness leading to their disappearance from the
pathogen population (61). Similarly, isolates
of race (6) were shown to exhibit a lower fit-
ness 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 increas-
ingly reduce the fitness of the pathogen until
the combined losses become insurmountable,
which would lead to stabilizing selection (132).
The efficacy of gene combinations will be
partly determined by the geographical distribu-
tion of cognate races. V. inaequalis populations
are highly diverse genetically, both within or-
chards 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. inae-
qualis in apple production regions and to de-
velop 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 differ-
ential hosts (107). Breeders and researchers can
register to participate in this project at the web-
site http://www.vinquest.ch and will receive
budwood of the differential host set. Newly
confirmed GfG relationships can be reported
through the same website for inclusion in the
revised nomenclature system.
Race monitoring will be aided by the iden-
tification of Avr/effector proteins, which will in
turn facilitate R gene identification and deploy-
ment. To date, no Avr genes have been cloned;
however, the identification of SSR markers in
V. inaequalis (55, 134) and mapping of aviru-
lence loci (17) have been the first step toward
the mapping and cloning of the first 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 interac-
tions (e.g., 94) has thrown new light on GfG
relationships. In the arms race, the host evolves
new resistance specificities through intragenic
recombination (65) and sometimes only small
changes are required to change specificity (see
References 36, 70). As some R genes carry sig-
nificant fitness 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). Follow-
ing research on host-pathogen interactions in
major agricultural crops, molecular research on
the host-pathogen interaction of scab in ap-
ple is progressing in both the host, e.g., R
gene 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 and
proteins (16, 43, 146). R gene transformation

may range from transferring genes within the
genus through cisgenesis (116), to artificially
constructed genes effective against a range of
pathogens (66). A major advantage of transfor-
mation systems in the host is that gene cassettes
can 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 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 re-
lationships in the V. inaequalis–Malus pathosys-
tem. Host-specific resistance has an important
role to play in this pathosystem provided some
measure 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 promise
for generating lasting resistance. Understand-
ing of the molecular basis of fungal effector
function and their influence 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 significant problems
and was in need of updating.
2. A comprehensive new nomenclature system and a set of rules for defining new GfG
relationships in the V. inaequalis–Malus pathosystem is presented.
3. Information on the first 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
identified 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 confirmation.
3. The pathotyping information will be used to identify virulence patterns that may improve
our understanding on fitness 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-nonspecific genes, nonhost
resistance, and manipulation of the specificity of resistance genes.
406 Bus et al.

5. The ultimate goal is to integrate various resistance and disease management strategies
to achieve resistance that is durable in the field.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial 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 con-
tributions to a preliminary proposal and support to update the scab race nomenclature (25): Herb
Aldwinckle, Susan Gardiner, Cesare Gessler, Remmelt Groenwold, François 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
1. Aldwinckle HS, Gustafson HL, Lamb RC. 1976. Early determination of genotypes for apple scab resis-
tance by forced flowering of test cross progenies. Euphytica 25:185–91
2. Bagga HS, Boone DM. 1968. Genes in Venturia inaequalis controlling pathogenicity to crabapples.
Phytopathology 58:1176–82
3. Bagga HS, Boone DM. 1968. Inheritance of resistance to Venturia inaequalis in crabapples. Phytopathology
58:1183–87
4. Barbara DJ, Roberts AL, Xu XM. 2008. Virulence characteristics of apple scab (Venturia inaequalis)
isolates from monoculture and mixed orchards. Plant Pathol. 57:552–61
5. Belfanti E, Silfverberg-Dilworth E, Tartarini S, Patocchi A, Barbieri M, et al. 2004. The HcrVf2 gene
from a wild apple confers scab resistance to a transgenic cultivated variety. Proc. Natl. Acad. Sci. USA
101:886–90
6. Belkhadir Y, Subramaniam R, Dangl JL. 2004. Plant disease resistance protein signalling: NBS-LRR
proteins and their partners. Curr. Opin. Plant Biol. 7:391–99
7. Bénaouf G, Parisi L. 2000. Genetics of host-pathogen relationships between Venturia inaequalis races 6
and 7 and Malus species. Phytopathology 90:236–42
8. Bengtsson M, Lindhard H, Grauslund J. 2000. Occurrence of races of Venturia inaequalis in apple scab
race screening orchard in Denmark. IOBC/WPRS Bull. 23(12):225–29
9. Black W, Mastenbroek C, Mills WR, Peterson LC. 1953. A proposal for an international nomenclature of
races of Phytophthora infestans and genes controlling immunity in Solanum demissum derivatives. Euphytica
2:173–79
10. Blaise P, Gessler C. 1994. Cultivar mixtures in apple orchards as a mean to control apple scab? Norweg.
J. Agric. Sci. 17:105–12
11. Bolar JP, Norelli JL, Wong KW, Hayes CK, Harman GE, Aldwinckle HS. 2000. Expression of endo-
chitinase from Trichoderma harzianum in transgenic apple increases resistance to apple scab and reduces
vigor. Phytopathology 90:72–77
12. Boone DM. 1971. Genetics of Venturia inaequalis. Annu. Rev. Phytopathol. 9:297–318
13. Boone DM, Keitt GW. 1957. Venturia inaequalis (Cke.) Wint. XII. Genes controlling pathogenicity of
wild-type lines. Phytopathology 47:403–9
14. Boudichevskaia A, Flachowsky H, Peil A, Fischer C, Dunemann F. 2006. Development of a multial-
lelic SCAR marker for the scab resistance gene Vr1/Vh4/Vx from R12740–7A apple and its utility for
molecular breeding. Tree Genet. Genomes 2:186–95

15. Bowen JK, Mesarich CH, Bus VGM, Beresford RM, Plummer KM, Templeton MD. 2011. Venturia
inaequalis: the causal agent of apple scab. Mol. Plant Pathol. 12:105–22
16. Bowen JK, Mesarich CH, Rees-George J, Cui W, Fitzgerald A, et al. 2009. Candidate effector gene
identification in the ascomycete fungal phytopathogen Venturia inaequalis by expressed sequence tag
analysis. Mol. Plant Pathol. 10:431–48
17. Broggini GAL, Bus VGM, Parrivicini G, Kumar S, Groenwold R, Gessler C. 2011. Genetic mapping of
14 avirulence genes in an EU-B04 × 1639 progeny of Venturia inaequalis. Fungal Genet. Biol. 48:166–76
18. Broggini GAL, Le Cam B, Parisi L, Wu C, Zhang HB, et al. 2007. Construction of a contig of BAC
clones spanning the region of the apple scab avirulence gene AvrVg. Fungal Genet. Biol. 44:44–51
19. Brun H, Chevre AM, Fitt BDL, Powers S, Besnard AL, et al. 2010. Quantitative resistance increases the
durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol. 185:285–99
20. Bus VGM. 2006. Differential host-pathogen interactions of Venturia inaequalis and Malus. PhD thesis. Univ.
Auckland, New Zealand. 158 pp.
21. Bus VGM, Bassett HCM, Bowatte D, Chagné D, Ranatunga CA, et al. 2010. Genome mapping of an
apple scab, a powdery mildew and a woolly apple aphid resistance gene from open-pollinated mildew
immune selection. Tree Genet. Genomes 6:477–87
22. Bus VGM, Laurens FND, van de Weg WE, Rusholme RL, Rikkerink EHA, et al. 2005. The Vh8 locus
of a new gene-for-gene interaction between Venturia inaequalis and the wild apple Malus sieversii is closely
linked to the Vh2 locus in Malus pumila R12740–7A. New Phytol. 166:1035–49
23. Bus V, Plummer K, Rikkerink E, Luby J. 2000. Evaluation of the pathogenicity of two scab isolates
derived from the Vf-resistant apple cultivar ‘Baujade’. IOBC wprs Bull. 23(12):231–37
24. Bus V, Ranatunga C, Gardiner S, Bassett H, Rikkerink E. 2000. Marker assisted selection for pest and
disease resistance in the New Zealand apple breeding programme. Acta Hortic. 538:541–47
25. Bus V, Rikkerink E, Aldwinckle HS, Caffier V, Durel CE, et al. 2009. A proposal for the nomenclature
of Venturia inaequalis races. Acta Hortic. 814:739–46
26. Bus VGM, Rikkerink EHA, van de Weg WE, Rusholme RL, Gardiner SE, et al. 2005. The Vh2 and
Vh4 scab resistance genes in two differential hosts derived from Russian apple R12740–7A map to the
same linkage group of apple. Mol. Breed. 15:103–16
27. Caffier V, Didelot F, Pumo B, Causeur D, Durel CE, Parisi L. 2010. Aggressiveness of eight Venturia
inaequalis isolates virulent and avirulent to the major resistance gene Rvi6 on a non-Rvi6 apple cultivar.
Plant Pathol. 59:1072–80
28. Calenge F, Faure A, Goerre M, Gebhardt C, van de Weg WE, et al. 2004. Quantitative trait loci (QTL)
analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in an apple progeny
challenged with eight isolates of Venturia inaequalis. Phytopathology 94:370–79
28a. Celton J-M, Christoffels A, Sargent DJ, Xu X, Rees DJG. 2010. Genome-wide SNP identification
by high-throughput sequencing and selective mapping allows sequence assembly positioning using a
framework genetic linkage map. BMC Biol. 8:155
29. Cheng FS, Weeden NF, Brown SK, Aldwinckle HS, Gardiner SE, Bus VG. 1998. Development of a
DNA marker for Vm, a gene conferring resistance to apple scab. Genome 41:208–14
30. Chevalier M, Lespinasse Y, Renaudin S. 1991. A microscopic study of the different classes of symptoms
coded by the Vf gene in apple for resistance to scab (Venturia inaequalis). Plant Pathol. 40:249–56
31. Chevalier M, Parisi L. 2000. Expression of Golden Delicious resistance to race 7 of Venturia inaequalis.
IOBC wprs Bull. 23(12):239–44
32. Dayton DF, Williams EB. 1968. Independent genes in Malus for resistance to Venturia inaequalis. Proc.
Am. Soc. Hortic. Sci. 92:89–94
33. Dayton DF, Williams EB. 1970. Additional allelic genes in Malus for scab resistance of two reaction
types. Proc. Am. Soc. Hortic. Sci. 95:735–36
34. Dayton DF, Shay JR, Hough LF. 1953. Apple scab resistance from R12740–7A, a Russian apple. Proc.
35. Didelot F, Brun L, Parisi L. 2007. Effects of cultivar mixtures on scab control in apple orchards. Plant
Pathol. 56:1014–22
408 Bus et al.

36. Dodds PN, Lawrence GJ, Ellis JG. 2001. Six amino acid changes confined to the leucine-rich repeat
B-strand/B-turn motif determine the difference between the P and P2 rust resistance specificities in flax.
Plant Cell 13:163–78
37. Dunemann F, Egerer J. 2010. A major resistance gene from Russian apple ‘Antonovka’ conferring field
immunity against apple scab is closely linked to the Vf locus. Tree Genet. Genomes 6:627–33
38. Durel CE, Freslon V, Denancé C, Laurens F, Lespinasse Y, et al. 2006. Genetic localisation of new
major and minor pest and disease resistance factors in the apple genome. 3rd Int. Rosaceae Genomics Conf.,
19–22 March 2006, Napier, New Zealand, p. 5 (Abstr.)
39. Durel CE, Parisi L, Laurens F, van de Weg WE, Liebhard R, Jourjon MF. 2003. Genetic dissection of
partial resistance to race 6 of Venturia inaequalis in apple. Genome 46:224–34
40. Durel CE, van de Weg E, Venisse JS, Parisi L. 2000. Localisation of a major gene for scab resistance on
the European genetic map of the Prima x Fiesta cross. IOBC wprs Bull. 23(12):245–48
41. Erdin N, Tartarini S, Broggini GAL, Gennari F, Sansavini S, et al. 2006. Mapping of the apple scab-
resistance gene Vb. Genome 49:1238–45
42. Fitzgerald A, Mudge AM, Gleave AP, Plummer KM. 2003. Agrobacterium and PEG-mediated transfor-
mation of the phytopathogen Venturia inaequalis. Mycol. Res. 7:803–10
43. Fitzgerald A, van Kan JAL, Plummer KM. 2004. Simultaneous silencing of multiple genes in the apple
scab fungus, Venturia inaequalis, by expression of RNA with chimeric inverted repeats. Fungal Genet. Biol.
41:963–71
44. Flor HH. 1971. Current status of the gene-for-gene concept. Ann. Rev. Phytopathol. 9:275–96
45. Galli P, Broggini GAL, Gessler C, Patocchi A. 2010. Phenotypic characterization of the Rvi15 (Vr2)
apple scab resistance. J. Plant Pathol. 92:219–26
46. Galli P, Broggini GAL, Kellerhals M, Gessler C, Patocchi A. 2010. High-resolution genetic map of the
Rvi15 (Vr2) apple scab resistance locus. Mol. Breed. 26:561–72
47. Galli P, Patocchi A, Broggini GAL, Gessler C. 2010. The Rvi15 (Vr2) apple scab resistance locus contains
three TIR-NBS-LRR genes. Mol. Plant-Microbe Interact. 23:608–17
48. Gao Z, van de Weg W. 2006. The Vf gene for scab resistance in apple is linked to sub-lethal genes.
Euphytica 151:123–33
49. Gardiner SE, Bassett HCM, Noiton DAM, Bus VG, Hofstee ME, et al. 1996. A detailed linkage map
around an apple scab resistance gene demonstrates that two disease resistance classes both carry the Vf
gene. Theor. Appl. Genet. 93:485–93
50. Gessler C, Patocchi A, Sansavini S, Tartarini S, Gianfranceschi L. 2006. Venturia inaequalis resistance
in apple. Crit. Rev. Plant Sci. 25:473–503
51. Gilissen LJWJ, Bolhaar STHP, Matos CI, Rouwendal GJA, Boone MJ, et al. 2005. Silencing the major
apple allergen Mal d 1 by using the RNA interference approach. J. Allergy Clin. Immunol. 115:364–69
52. Gladieux P, Caffier V, Le Cam B. 2010. Host-specific differentiation among populations of Venturia
inaequalis causing scab on apple, pyrcantha and loquat. Fungal Genet. Biol. 47:511–22
53. Gladieux P, Zhang XG, Afoufa-Bastien D, Valdebenito Sanhueza RM, Sbaghi M, Le Cam B. 2008. On
the origin and spread of the scab disease of apple: out of Central Asia. PLoS ONE 3(1):e1455
54. Gladieux P, Zhang XG, Roldan-Ruiz I, Caffier V, Leroy T, et al. 2010. Evolution of the population
structure of Venturia inaequalis, the apple scab fungus, associated with the domestication of its host. Mol.
Ecol. 19:658–74
55. Guérin F, Franck P, Loiseau A, Devaux M, Le Cam B. 2004. Isolation of 21 new polymorphic microsatel-
lite loci in the phytopathogenic fungus Venturia inaequalis. Mol. Ecol. Notes 4:268–70
56. Guérin F, Gladieux P, Le Cam B. 2007. Origin and colonization history of newly virulent strains of the
phytopathogenic fungus Venturia inaequalis. Fungal Genet. Biol. 44:284–92
57. Gygax M, Gianfranceschi L, Liebhard R, Kellerhals M, Gessler C, Patocchi A. 2004. Molecular markers
linked to the apple scab resistance gene Vbj derived from Malus baccata jackii. Theor. Appl. Genet. 109:1702–
9
58. Hemmat M, Brown SK, Aldwinckle HS, Mehlenbacher SA, Weeden NF. 2003. Identification and map-
ping of markers for resistance to apple scab from ‘Antonovka’ and ‘Hansen’s baccata #2’. Acta Hortic.
622:153–61

59. Hemmat M, Brown SK, Weeden NF. 2002. Tagging and mapping scab resistance genes from R12740–
7A apple. J. Am. Soc. Hortic. Sci. 127:365–70
60. Hemmat M, Weeden NF, Brown SK. 2003. Mapping and evaluation of Malus x domestica microsatellites
in apple and pear. J. Am. Soc. Hortic. Sci. 128:515–20
61. Hernández CD. 1990. La tavelure du pommier Venturia inaequalis (Cke.) Wint.: étude du pouvoir
pathogène des races 1 et 5 et essai de lutte raisonnée. PhD thesis. Univ. Nantes, France. 163 pp.
62. Hernández CFD, Parisi L, Lespinasse Y. 1994. Heredabilidad de la resistencia del hibrido de manzano
X 2045 a Venturia inaequalis (Cke.) Wint. Rev. Mexic. Fitopatol. 12:27–29
63. Hough LF. 1944. A survey of the scab resistance of the foliage on seedlings in selected apple progenies.
Proc. Am. Soc. Hortic. Sci. 44:260–72
64. Hough LF, Shay JR, Dayton DF. 1953. Apple scab resistance from Malus floribunda Sieb. Proc. Am. Soc.
Hortic. Sci. 62:341–47
65. Huang L, Brooks S, Li W, Fellers J, Nelson JC, Gill B. 2009. Evolution of new disease specificity at
a simple resistance locus in a crop-weed complex: reconstitution of the Lr21 gene in wheat. Genetics
182:595–602
66. Hulbert SH, Webb CA, Smith SM, Sun Q. 2001. Resistance gene complexes: evolution and utilization.
Ann. Rev. Phytopathol. 39:285–312
67. James DJ, Passey AJ, Barbara DJ, Bevan MJ. 1989. Genetic transformation of apple (Malus pumila Mill.)
using disarmed Ti-binary vector. Plant Cell Rep. 7:658–61
68. Jefferson RM. 1970. History, Progeny, and Location of Crabapples of Documented Authentic Origin.
Washington, DC: U.S. Dep. Agric. 107 pp.
69. Jones JDG, Dangl JF. 2006. The plant immune system. Nature 444:323–29
70. Joosten MHAJ, Cozijnsen TJ, de Wit PJGM. 1994. Host resistance to a fungal tomato pathogen lost by
a single base-pair change in an avirulence gene. Nature 367:384–86
71. Julien JB, Spangelo LPS. 1957. Physiological races of Venturia inaequalis. Can. J. Plant Sci. 37:102–7
72. Juniper BE, Watkins R, Harris SA. 1999. The origin of the apple. Acta Hortic. 484:27–33
73. Keitt GW, Palmiter DH. 1938. Heterothallism and variability in Venturia inaequalis. Am. J. Bot. 25:338–
45
74. Kellerhals M, Fouillet A, Lespinasse Y. 1993. Effect of the scab inoculum and the susceptible parent
on the resistance to apple scab (Venturia inaequalis) in the progenies of crosses to the scab resistant cv
‘Florina’. Agronomie 13:631–36
75. Korban SS, Chen H. 1992. Apple. In Biotechnology of Perennial Fruit Crops, ed. FA Hammerschlag, RE
Litz, pp. 203–27. Wallingford, UK: CABI
76. Korban SS, Skirvin RM. 1984. Nomenclature of the cultivated apple. HortScience 19:177–80
77. Kucheryava N, Bowen JK, Sutherland PW, Conolly JJ, Mesarich CH, et al. 2008. Two novel Venturia
inaequalis genes induced upon morphogenetic differentiation during infection and in vitro growth on
cellophane. Fungal Genet. Biol. 45:1329–39
78. Lamb RC, Hamilton JM. 1969. Environmental and genetic factors influencing the expression of resis-
tance to scab (Venturia inaequalis Cke. Wint.) in apple progenies. J. Am. Soc. Hortic. Sci. 94:554–57
79. Laurens F, Chevalier M, Dolega E, Gennari F, Goerre M, et al. 2004. Local European cultivars as
sources of durable scab resistance in apple. Acta Hortic. 663:115–21
80. Le Cam B, Parisi L, Arene L. 2002. Evidence of two formae speciales in Venturia inaequalis, responsible
for apple and pyracantha scab. Phytopathology 92:314–20
81. Leach JE, Vera Cruz CM, Bai J, Leung H. 2001. Pathogen fitness penalty as a predictor of durability of
disease resistance genes. Ann. Rev. Phytopathol. 39:187–224
82. Lespinasse Y. 1989. Breeding pome fruits with stable resistance to diseases. 3. Genes, resistance mecha-
nisms, present work and prospects. IOBC wprs Bull. 12(6):100–15
83. Lespinasse Y. 1994. Apple scab resistance and durability. New races and strategies for the future.
In Progress in Temperate Fruit Breeding, ed. H Schmidt, M Kellerhals, pp. 105–106. Dordrecht, The
Netherlands: Kluwer Acad. Publ.
84. Lespinasse Y, Olivier JM, Godicheau M. 1979. Études enterprises dans le cadre de la résistance à la
tavelure du pommier. Proc. Tree Fruit Breed. Symp. Eucarpia Fruit Sect. Angers, pp. 97–110. Angers:
INRA
410 Bus et al.

85. Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, et al. 2002. Development and charac-
terisation of 140 new microsatellites in apple (Malus x domestica Borkh.). Mol. Breed. 10:217–41
86. Liebhard R, Koller B, Patocchi A, Kellerhals M, Pfammatter W, et al. 2003. Mapping quantitative field
resistance against apple scab in a ‘Fiesta’ x ‘Discovery’ progeny. Phytopathology 93:493–501
87. Luby J, Forsline P, Aldwinckle H, Bus V, Geibel M. 2001. Silk road apples: collection, evaluation, and
utilization of Malus sieversii from Central Asia. HortScience 36:225–31
88. Mabberley DJ, Jarvis CE, Juniper BE. 2001. The name of the apple. Telopea 9:421–30
89. MacHardy WE. 1996. Apple Scab: Biology, Epidemiology, and Management. St. Paul, MN: APS Press. 545
pp.
90. Maliepaard C, Alston FH, van Arkel G, Brown LM, Chevreau E, et al. 1998. Aligning male and female
linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor. Appl. Genet. 97:60–73
91. Malnoy M, Boresjza-Wysocka EE, Norelli JL, Flaishman MA, Gidoni D, Aldwinckle HS. 2010. Genetic
transformation of apple (Malus x domestica) without use of a selectable marker gene. Tree Genet. Genomes
6:423–33
92. Malnoy M, Xu M, Borejsza-Wysocka E, Korban SS, Aldwinckle HS. 2008. Two receptor-like genes,
Vfa1 and Vfa2, confer resistance to the fungal pathogen Venturia inaequalis inciting apple scab disease.
Mol. Plant-Microbe Interact. 21:448–58
93. Manganaris AG, Alston FH, Weeden NF, Aldwinckle HS, Gustafson HL, Brown SK. 1994. Isozyme
locus Pgm-1 is tightly linked to a gene (Vf) for scab resistance in apple. J. Am. Soc. Hortic. Sci. 119:1286–88
94. Maor R, Shirasu K. 2005. The arms race continues: battle strategies between plants and fungal pathogens.
Curr. Opin. Microbiol. 8:399–404
95. Mattison H, Nybom H. 2005. Application of DNA markers for detection of scab resistant apple cultivars
and selections. Int. J. Hortic. Sci. 11(3):59–63
96. McCrory SA, Shay JR. 1951. Apple scab resistance survey of South Dakota apple varieties and breeding
stocks. Plant Dis. Rep. 35:433–34
97. Meinke D, Koornneef M. 1997. Community standards for Arabidopsis genetics. Plant J. 12:247–53
98. Mundt CC. 1990. Probability of mutation to multiple virulence and durability of resistance gene pyra-
mids. Phytopathology 80:221–23
99. N’Diaye A, van de Weg WE, Kodde LP, Koller B, Dunemann F, et al. 2008. Construction of an
integrated consensus map of the apple genome based on four mapping populations. Tree Genet. Genom.
4:727–43
100. Olivier JM, Lespinasse Y. 1982. Résistance du pommier à la tavelure Venturia inaequalis (Cke.) Wint.:
sources de résistance, comportement du parasite, programme de sélection. Cryptogamie, Mycologie 3:361–
75
101. Palloix A, Ayme V, Moury B. 2009. Durability of plant major resistance genes to pathogens depends on
the genetic background, experimental evidence and consequences for breeding strategies. New Phytol.
183:190–99
102. Paris R, Cova V, Pagliarani G, Tartarini S, Komjanc M, Sansavini S. 2009. Expression profiling in
HcrVf2-transformed apple plants in response to Venturia inaequalis. Tree Genet. Genom. 5:81–91
103. Parisi L, Fouillet V, Schouten HJ, Groenwold R, Laurens F, et al. 2004. Variability of the pathogenicity
of Venturia inaequalis in Europe. Acta Hortic. 663:107–13
104. Parisi L, Lespinasse Y. 1996. Pathogenicity of Venturia inaequalis strains of race 6 on apple clones (Malus
sp.). Plant Dis. 80:1179–83
105. Parisi L, Lespinasse Y, Guillaumes J, Krüger J. 1993. A new race of Venturia inaequalis virulent to apples
with resistance due to Vf gene. Phytopathology 83:533–37
106. Patocchi A, Bigler, B, Koller B, Kellerhals M, Gessler C. 2004. Vr2: a new apple scab resistance gene.
Theor. Appl. Genet. 109:1087–92
107. Patocchi A, Frei A, Frey JE, Kellerhals M. 2009. Towards improvement of marker assisted selection
of apple scab resistant cultivars: Venturia inaequalis virulence surveys and standardization of molecular
marker alleles associated with resistance genes. Mol. Breed. 24:337–47
108. Patocchi A, Walser M, Tartarini S, Broggini GAL, Gennari F, et al. 2005. Identification by genome
scanning approach (GSA) of a microsatellite tightly associated with the apple scab resistance gene Vm.
Genome 48:630–36

109. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ. 2009. Shades of gray: the world of quanti-
tative disease resistance. Trends Plant Sci. 14:21–29
110. Raabe RD, Gardner MW. 1972. Scab of pyracantha, loquat, toyon, and kageneckia. Phytopathology
62:914–16
111. Rousselle GL, Williams EB, Hough LF. 1974. Modification of the level of resistance to apple scab from
the Vf gene. Proc. 19th Int. Hortic. Congress, Vol. 3, pp. 19–26. Warsaw: ISHS
112. Sandskär B, Liljeroth E. 2005. Incidence of races of the apple scab pathogen (Venturia inaequalis) in apple
growing districts in Sweden. Acta Agric. Scand. Section B Soil Plant Sci. 55:143–50
113. Sapoukhina N, Durel CE, Le Cam B. 2009. Spatial deployment of gene-for-gene resistance governs
evolution and spread of pathogen populations. Theor. Ecol. 2:229–38
114. Schmidt M. 1938. Venturia inaequalis (Cooke) aderhold. VIII. Weitere Untersuchungen zur Züchtung
schorfwiderstandsfähiger Apfelsorten. Züchter 10:280–91
115. Schnabel G, Schnabel EL, Jones AL. 1999. Characterization of ribosomal DNA from Venturia inaequalis
and its phylogenetic relationship to rDNA from other tree-fruit Venturia species. Phytopathology 89:100–8
116. Schouten H, Krens FA, Jacobsen E. 2006. Cisgenic plants are similar to traditionally bred plants. EMBO
Rep. 7:750–53
117. Servin B, Martin OC, Mezard M, Hospital F. 2004. Toward a theory of marker-assisted gene pyramiding.
Genetics 168:513–53
118. Shay JR, Dayton DF, Hough LF. 1953. Apple scab resistance from a number of Malus species. Proc. Am.
Soc. Hortic. Sci. 62:348–56
119. Shay JR, Hough LF. 1952. Evaluation of apple scab resistance in selections of Malus. Am. J. Bot. 39:288–
97
120. Shay JR, Williams EB. 1953. Physiologic specialization in Venturia inaequalis. Phytopathology 43:483–84
(Abstr.)
121. Shay JR, Williams EB. 1956. Identification of three physiologic races of Venturia inaequalis. Phytopathology
46:190–93
122. Shay JR, Williams EB, Janick J. 1962. Disease resistance in apple and pear. Proc. Am. Soc. Hortic. Sci.
80:97–104
123. Sierotzki H, Gessler C. 1998. Inheritance of virulence of Venturia inaequalis toward Malus x domestica
cultivars. J. Phytopathol. 146:509–14
124. Sierotzki H, Gessler C. 1998. Genetic analysis of a cross of two Venturia inaequalis strains that differ in
virulence. J. Phytopathol. 146:515–19
125. Sierotzki H, Eggenschwiler M, Boillat O, McDermott JM, Gessler C. 1994. Detection of variation in
virulence toward susceptible apple cultivars in natural populations of Venturia inaequalis. Phytopathology
84:1005–9
126. Silfverberg-Dilworth E, Besse S, Paris R, Belfanti E, Tartarini S, et al. 2005. Identification of functional
apple scab resistance gene promoters. Theor. Appl. Genet. 110:1119–26
127. Soriano JM, Joshi SG, van Kaauwen M, Noordijk Y, Groenwold R, et al. 2009. Identification and mapping
of the novel apple scab resistance gene Vd3. Tree Genet. Genom. 5:475–82
128. Soufflet-Freslon V, Gianfranceschi L, Patocchi A, Durel CE. 2008. Inheritance studies of apple scab
resistance and identification of Rvi14, a new major gene that acts together with other broad-spectrum
QTL. Genome 51:657–67
129. Spangelo LPS, Julien JB, Racicot HN, Blair DS. 1956. Breeding apples for resistance to scab. Can. J.
Agric. Sci. 36:329–38
130. Stukenbrock EH, McDonald BA. 2008. The origins of plant pathogens in agro-ecosystems. Annu. Rev.
Phytopathol. 46:75–100
131. Tartarini S, Gennari F, Pratesi D, Palazetti C, Sansavini S, et al. 2004. Characterisation and genetic
mapping of a major scab resistance gene from the old Italian apple cultivar ‘Durello di Forl`ı’. Acta Hortic.
663:129–33
132. Tellier A, Brown JKM. 2007. Polymorphism in multilocus host-parasite coevolutionary interactions.
Genetics 177:1777–90
133. Tenzer I, Gessler C. 1997. Subdivision and genetic structure of four populations of Venturia inaequalis
in Switzerland. Eur. J. Plant Pathol. 103:565–71
412 Bus et al.

134. Tenzer I, Gessler C. 1999. Genetic diversity of Venturia inaequalis across Europe. Eur. J. Plant Pathol.
105:545–52
135. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, et al. 2010. The genome of the domesticated
apple (Malus x domestica Borkh.). Nat. Genet. 42:833–39
136. Vinatzer BA, Patocchi A, Gianfranceschi L, Tartarini S, Zhang HB, et al. 2001. Apple contains receptor-
like genes homologous to the Cladosporium fulvum resistance gene family of tomato with a cluster of genes
cosegregating with Vf apple scab resistance. Mol. Plant-Microbe Interact. 14:508–15
137. Vinatzer BA, Patocchi A, Tartarini S, Gianfranceschi L, Sansavini S, Gessler C. 2004. Isolation of two
microsatellite markers from BAC clones of the Vf scab resistance region and molecular characterization
of scab-resistant accessions in Malus germplasm. Mol. Breed. 123:1–6
138. Volz R, Rikkerink E, Austin P, Lawrence T, De Silva N, Bus V. 2009. “Fast-breeding” in apple: a strategy
to accelerate introgression of new traits into elite germplasm. Acta Hortic. 814:163–68
139. Way RD, Aldwinckle HS, Lamb RC, Rejman A, Sansavini S, et al. 1989. Apples (Malus). Acta Hortic.
290:1–62
140. Westerink N, Joosten MHAJ, de Wit PJGM. 2004. Fungal (a)virulence factors at the crossroads of
disease susceptibility and resistance. In Fungal Disease Resistance in Plants, ed. ZK Punja, pp. 93–137.
New York, NY: Haworth Press
141. Williams EB, Brown AG. 1968. A new physiologic race of Venturia inaequalis, incitant of apple scab.
Plant Dis. Rep. 52:799–801
142. Williams EB, Dayton DF. 1968. Four additional sources of the Vf locus for Malus scab resistance. Proc.
143. Williams EB, Dayton DF, Shay JR. 1966. Allelic genes in Malus for resistance to Venturia inaequalis.
Proc. Am. Soc. Hortic. Sci. 88:52–56
144. Williams EB, Ku´c J. 1969. Resistance in Malus to Venturia inaequalis. Ann. Rev. Phytopathol. 7:223–46
145. Williams EB, Shay JR. 1957. The relationship of genes for pathogenicity and certain other characters in
Venturia inaequalis (Cke.) Wint. Genetics 42:704–11
146. Win J, Greenwood DR, Plummer KM. 2003. Characterisation of a protein from Venturia inaequalis that
induces necrosis in Malus carrying the Vm resistance gene. Physiol. Mol. Plant Pathol. 62:193–202
147. Win J, Morgan W, Bos J, Krasileva KV, Cano LM, et al. 2007. Adaptive evolution has targeted the
C-terminal domain of RXLR effectors of plant pathogenic oomycetes. Plant Cell 19:2349–69
148. Xu M, Korban SS. 2002. A cluster of four receptor-like genes resides in the Vf locus that confers resistance
to apple scab disease. Genetics 162:1995–2006
149. Xu XM, Roberts T, Barbara DJ, Harvey NG, Gao L, Sargent DJ. 2009. A genetic linkage map of Venturia
inaequalis, the causal agent of apple scab. BMC Res. Notes 2:163
150. Xu XM, Yang JR, Thakur V, Roberts A, Barbara DJ. 2008. Population variation of apple scab (Venturia
inaequalis) isolates from Asia and Europe. Plant Disease 92:247–52
151. Yao JL, Cohen D, Atkinson R, Richardson K, Morris B. 1995. Regeneration of transgenic plants from
the commercial apple cultivar Royal Gala. Plant Cell Rep. 14:407–12
152. Zini E. 2005. Construzione di una mappa di associazione della popolazione di melo ‘Golden Delicious’ x
‘Freedom’ e caratterizzazione del gene di resistenza Va a ticchiolatura. PhD thesis, Univ. Bologna, Italy.
126 pp.

PY49-FrontMatter ARI 8 July 2011 9:55
Annual Review of
Phytopathology
Volume 49, 2011
Contents
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 d’ ´Etat: 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 ﬂavus
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. Hovmøller, Chris K. Sørensen, 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
v

Emerging Virus Diseases Transmitted by Whiteflies
Jesús Navas-Castillo, Elvira Fiallo-Olivé, and Sonia Sánchez-Campos p p p p p p p p p p p p p p p p p 219
Evolution and Population Genetics of Exotic and Re-Emerging
Pathogens: Novel Tools and Approaches
Niklaus J. Grünwald 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. O’Brien, 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 Aurélien 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
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, Valérie Caffier, Charles-Eric Durel,
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-Solińska, 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
vi Contents

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/
Contents vii
View publication statsView publication stats

Revision of the nomenclature of differential host-pathogen interactions of Venturia inaequalis and Malus

Recommended

Recommended

More Related Content

What's hot

What's hot (20)

Similar to Revision of the nomenclature of differential host-pathogen interactions of Venturia inaequalis and Malus

Similar to Revision of the nomenclature of differential host-pathogen interactions of Venturia inaequalis and Malus (20)

Recently uploaded

Recently uploaded (20)

Revision of the nomenclature of differential host-pathogen interactions of Venturia inaequalis and Malus