Copyright 2000 by the Genetics Society of America

Comparative Genetics of Disease Resistance Within the Solanaceae

Rebecca C. Grube, Elaine R. Radwanski and Molly Jahn
Department of Plant Breeding, Cornell University, Ithaca, New York 14853
Manuscript received December 7, 1999
Accepted for publication February 21, 2000
ABSTRACT
Genomic positions of phenotypically defined disease resistance genes (R genes) and R gene homologues
were analyzed in three solanaceous crop genera, Lycopersicon (tomato), Solanum (potato), and Capsicum
(pepper). R genes occurred at corresponding positions in two or more genomes more frequently than
expected by chance; however, in only two cases, both involving Phytophthora spp., did genes at corresponding
positions have specificity for closely related pathogen taxa. In contrast, resistances to Globodera spp., potato
virus Y, tobacco mosaic virus, and tomato spotted wilt virus were mapped in two or more genera and did
not occur in corresponding positions. Without exception, pepper homologues of the cloned R genes
Sw-5, N, Pto, Prf, and I2 were found in syntenous positions in other solanaceous genomes and in some
cases also mapped to additional positions near phenotypically defined solanaceous R genes. This detailed
analysis and synthesis of all available data for solanaceous R genes suggests a working hypothesis regarding
the evolution of R genes. Specifically, while the taxonomic specificity of host R genes may be evolving rapidly,
general functions of R alleles (e.g., initiation of resistance response) may be conserved at homologous loci
in related plant genera.

LANT disease resistance genes (R genes) are an

agriculturally important class of genes that are increasingly well characterized at the molecular level; however, fundamental questions regarding their mechanisms of action and their evolution remain. While
remarkable conservation of gene order and function
has been observed for genes that govern morphological
and physiological traits in many plant families (reviewed
in Gale and Devos 1998), the structural and functional
correspondence of R genes has yet to be examined
systematically across plant genera. If R genes follow the
patterns of conservation observed for other types of
plant genes, loci conferring resistance to identical or
related pathogens should be found at corresponding
positions in genomes of related host taxa. However, if
the molecular changes occurring at R loci throughout
divergence of genera drastically alter taxonomic specificity but not overall function, the orthologous R genes
should occur at corresponding positions in related taxa,
although alleles at these loci may be involved in recognizing very different pathogens. Another alternative is
that R genes may evolve so rapidly that no conservation
of sequence or function will be apparent across genera.
Within an individual plant species, clustering of genes
that confer resistance to unrelated pathogens is well
documented (Polzin et al. 1994; Witsenboer et al.
1995; De Jong et al. 1997; Ashfield et al. 1998; Speulman et al. 1998), and detailed molecular analyses at
several R loci have revealed complex loci consisting of

Corresponding author: Molly Jahn, 312 Bradfield Hall, Cornell University, Ithaca, NY 14853. E-mail: mmk9@cornell.edu
Genetics 155: 873887 ( June 2000)

tightly linked R gene homologues (Martin et al. 1994;

Dixon et al. 1996; Parniske et al. 1997; Simons et al.
1998; Thomas et al. 1998; Williamson 1998). Between
sexually compatible species, the pathogen strain specificity and the number of R gene homologues at a given
locus have been shown to vary (Thomas et al. 1998).
Little is known about the variation in structure and
function of orthologous R loci in different genera. One
approach to examine this question depends upon domains shared among cloned R genes. These similarities
have allowed structurally related sequences, termed R
gene analogues (RGAs), to be isolated from many host
species (Kanazin et al. 1996; Leister et al. 1996, 1998;
Y. G. Yu et al. 1996; Aarts et al. 1998; Seah et al. 1998;
Shen et al. 1998; Rivkin et al. 1999). RGAs are found
in abundance in plant genomes, comprising an estimated 2% of the Arabidopsis genome (Michelmore
and Meyers 1998). In a comparative study in the Gramineae, Leister et al. (1998) observed significant variation
in RGA copy number and position and found that specific RGA classes usually do not map to similar positions
in different genera or even in closely related species.
Although this experiment is not informative about conservation of R gene function, it suggests that there is
limited conservation of genomic position for R-genelike sequences, which contrasts with results obtained
for other types of plant genes. Whether phenotypically
defined R genes exhibit a similar lack of conservation,
as proposed by Leister et al. (1998), remains to be seen.
Since genome mapping in the Solanaceae was last
reviewed (Pillen et al. 1996), a more complete pepper
map has been constructed, allowing comparisons of the
three major solanaceous crop genera, Lycopersicon (to-

874

R. C. Grube, E. R. Radwanski and M. Jahn

mato), Solanum (potato), and Capsicum (pepper) (Livingstone et al. 1999). Many single genes and quantitative trait loci (QTL) that confer resistance to all major
classes of plant pathogens (virus, bacteria, nematode,
fungus, and insect) have been mapped and/or cloned
from solanaceous species (Pillen et al. 1996). Further,
a number of pathogens infect broadly within the Solanaceae, allowing direct comparison of genes conferring
resistance to the same pathogen in different hosts.
In this study, we present a comparative analysis of
genomic organization of solanaceous R genes and R
gene homologues to examine the degree to which structure and/or function is conserved in related genomes.
The term R gene refers to phenotypically defined
single genes or quantitative resistance loci (QRL) that
function to confer disease resistance to a particular
pathogen, for which sequence information may or may
not be available. R gene homologues are sequences
with a close evolutionary relationship to R genes, as
determined by a high percentage of sequence similarity,
with no implication of related function. The first part
of our analysis was restricted to phenotypically defined
R genes for which positions on the pepper, tomato, or
potato comparative maps have been obtained. For the
second part of the analysis, a Southern hybridizationbased approach was used to identify and map pepper
homologues of cloned solanaceous R genes.
MATERIALS AND METHODS
Consensus map construction: The comparative maps used
in this analysis were based on the following populations: tomato, (Lycopersicon esculentum L. pennellii) F2, 1276 cM,
1000 loci (Pillen et al. 1996); potato, (Solanum tuberosum
S. berthaultii) S. berthaultii, 684 cM, 183 loci (Tanksley
et al. 1992); pepper, (Capsicum annuum C. chinense) F2, 1246
cM, 1000 loci (Livingstone et al. 1999). Additional potato
maps were examined (Bonierbale et al. 1988; Gebhardt et
al. 1991), and positions of R loci were inferred from references
in Table 1. The tomato-potato and tomato-pepper alignments,
based upon common restriction fragment length polymorphism (RFLP) order, have been previously published (Tanksley et al. 1992; Livingstone et al. 1999). Similar to results
from the Gramineae, 20% of loci in both pepper and tomato
did not occur in strict colinear order within homeologous
segments (Bennetzen et al. 1998; Livingstone et al. 1999);
nevertheless, colinearity within homeologous regions was assumed as a reasonable approximation.
Cross-generic resistance gene clusters: All published chromosomal locations for R genes and major QRL (LOD 2 or
P 0.01) for tomato, potato, and pepper were placed on the
comparative map (Table 1; Figure 1). In Figure 1, phenotypically defined R genes were placed on a circular diagram showing their positions in host genomes and the chromosomal
rearrangements between the three genera. Ninety-three R loci
are listed in Table 1 with original references. For clarity, some
loci were named or renamed for ease of display. Most positions
were inferred from linkage to reference markers and should
be considered a best approximation. Comparisons of maps
across genera and the use of different mapping population
structures and sizes yields an unknown degree of error in
estimation of genetic distance; however, as a reasonable ap-

proximation, genetic distances were treated as constant across

all molecular maps. Cross-generic gene clusters were defined
by the presence of two or more genes in distinct genera within
15 cM. This interval was selected to be conservative in light
of the observation of Michelmore and Meyers (1998) that
intrageneric R gene clusters vary in size from 0 to 30 cM
and to remain informative given the inherent imprecision of
comparative mapping. The clusters identified are shown in
Table 2, and the RFLP markers associated with each cluster
were described by Tanksley et al. 1992 (TG, tomato random
genomic DNA; CD, tomato whole-leaf cDNA; CT, tomato leaf
epidermal cDNA) and Gebhardt et al. 1989 (GP, size-selected
potato genomic DNA). Nine genes were placed on the map
but excluded from analyses because of imprecise localization
or an unclear relationship between comparative maps in a
given region (potato loci Gro1, GroVI, and Pi1; tomato loci
Ph-1 and Ph-3; pepper QRL phyt2 and pepper loci Pvr4, Pvr7,
and Me3). Other mapped loci, such as QRL conferring resistance to cucumber mosaic virus (CMV) in pepper (Caranta
et al. 1997a) and the recessive pepper veinal mottle virus resistance gene pvr6 (Caranta et al. 1997b), could not be assigned
a definitive position in comparative maps due to a lack of
common markers or a lack of shared marker order between
mapping studies. Solanaceous homologues of cloned solanaceous R genes (discussed below) were also included in Figure
1 and Table 1, but were not included when defining R gene
clusters.
Mapping disease resistance loci in pepper: Tsw confers resistance to tomato spotted wilt virus (TSWV) in pepper and a
single map position was obtained in our interspecific mapping
population ( Jahn et al. 2000). Four CMV QRL that were detected in multiple environments were identified in an intraspecific C. annuum Maor Perennial population and placed
upon our comparative map by proximity to common RFLP
markers (I. Paran, unpublished results). For these loci, tentatively named cmv11.1, cmv2.1, cmv3.1, and cmv3.2, CMV resistance was evaluated quantitatively over several environments,
and linked loci were determined by regression of marker genotypes on CMV resistance. cmv11.1 had a significant effect on
resistance on its own (P 0.0001), while cmv2.1 had a significant effect on resistance only when present in conjunction
with cmv11.1 (P 0.01). cmv3.1 and 3.2 also interacted in
multiple environments to produce a significant effect on resistance (P 0.001). Map positions for Pvr4 and Pvr7, tightly
linked potyvirus resistance genes, were obtained by analyzing
DNA samples from our interspecific mapping population for
a Pvr4-linked sequence characterized amplified region marker
tightly linked to Pvr4 (Caranta et al. 1999; Grube et al. 2000).
Mapping disease resistance gene homologues in pepper:
The clone SL8 (nucleotides 28374014 of the tomato disease
resistance gene I2C-1) was provided by R. Fluhr (Weizmann
Institute of Science, Rehovot, Israel). The full-length cDNA
clones of Cf-9 and N were provided by J. D. G. Jones ( John
Innes Centre, Norwich, United Kingdom) and B. Baker (University of California, Berkeley, CA), respectively. The fulllength cDNA clones of Pto and Fen genes were provided by
G. Martin and the Sw-5 cDNA was used for RFLP analysis
with our pepper mapping filters by S. D. Tanksley (Cornell
University, Ithaca, NY). Hybridization of orthologous probes
and mapping were performed as previously described (Livingstone et al. 1999); a significance level of LOD 2.0 was used
to assign map positions of R gene homologues.

RESULTS

R genes and R gene clusters occur at corresponding

genomic locations across plant genera: In total, 12 R

L. peruvianum
C. annuum
C. annuum
L. pimpinellifolium
Lycopersicon
S. spegazzinii
S. tuberosum subsp. andigena
S. spegazzinii
S. spegazzinii
S. spegazzinii
S. vernei
S. vernei, S. oplocense, S. tuberosum subsp.
andigena
S. tuberosum subsp. andigena
L. pimpinellifolium
L. pimpinellifolium
L. pimpinellifolium
L. pennellii
C. annuum
Lycopersicon
C. annuum
L. peruvianum
L. peruvianum
N. tabacum
S. tuberosum
S. phureja

G. rostochiensis
G. rostochiensis
G. pallida, G. rostochiensis

G. rostochiensis
G. rostochiensis
F. oxysporum
F. oxysporum
F. oxysporum

TMV
Leveuillula taurica
Meloidogyne spp.
Meloidogyne spp., Macrosiphum
euphorbiae
M. incognita, M. javanica
TMV

PVX
PVX

H1
Hero
I1
I2
I3

L
Lv
Me3
Mi

Mi-3
N

Nb
Nxphu

L. pimpinellifolium
L. pimpinellifolium
Lycopersicon
L. pimpinellifolium
L. hirsutum
L. esculentum var. cerasiforme
L pimpinellifolium

L. pennellii

Originc

Clavibacter michiganensis
CMV
CMV
HR to Fenthion
Fusarium oxysporum
Globodera pallida
G. pallida
G. rostochiensis
G. rostochiensis

Alternaria alternata f. sp.

lycopersici
Ralstonia solanacearum
R. solanacearum
Cladosporium fulvum
C. fulvum
C. fulvum
C. fulvum
C. fulvum

Pathogenb

Cm 1.110.1 (Q)
cmv11.1 (Q)
cmv2.1, 3.1, 3.2 (Q)
Fen
Fr1
Gpa (Q)
Gpa2
Gro1
Gro1.2 (Q),
Gro1.3 (Q)
Gro1.4 (Q)
GroVI
Grp1

Bw-1,3 (Q)
Bw-4,5 (Q)
Cf-1
Cf-2
Cf-4
Cf-5
Cf-9

Asc

Genea

Yaghoobi et al. (1995)

Whitham et al. (1994); Dinesh-Kumar et al.
(1995)
De Jong et al. (1997)
Tommiska et al. (1998)

V
4
7
11
7

12
12
V
IX

(Continued)

Pineda et al. (1992); Gebhardt et al. (1993)

Ganal et al. (1995)
Sarfatti et al. (1989, 1991)
Bournival et al. (1989)
Tanksley and Costello (1991); Laterrot and
Moretti (1995)
Lefebvre et al. (1995)
Chunwongse et al. (1994); Blaker et al. (1995)
Dijan-Caporalino et al. (1998)
Williamson et al. (1994); Rossi et al. (1998)

III
V
V

11
12
9
6

Kreike et al. (1996)

Jacobs et al. (1996)
Van der Voort et al. (1998)

1, 6, 7, 8, 9, 10
11
2, 3, 9
5
9
V
XII
VII
X, XI

Van der Biezen et al. (1995)

Referencee

Danesh et al. (1994)

Thoquet et al. (1996)
Dickinson et al. (1993)
Dickinson et al. (1993)
Jones et al. (1992)
Balint-Kurti et al. (1994)
Balint-Kurti et al. (1994); Jones et al. (1994);
Leister et al. (1996)
Sandbrink et al. (1995)
(p)
(p)
Martin et al. (1994)
Vakalounakis et al. (1997)
Kreike et al. (1994)
Van der Voort et al. (1997)
Barone et al. (1990); Ballvora et al. (1995)
Kreike et al. (1993)

6, 10
4, 6
1
6
1
6
1

Chromosomal
locationd

Summary of resistance genes and resistance gene homologues mapped in Capsicum (pepper), Lycopersicon (tomato), and Solanum (potato)

TABLE 1

Comparative Mapping of R Genes

875

TYLCV
Verticillium dahliae

Ty-2
Ve

pvr1
pvr2
Pvr4
Pvr7
pvy 1-4 (Q)
py-1
R1
R2
R3
R6
R7
Raadg
Rmci
Rx
Rx1
rx-1, rx-2,
rx-3
Rx2
Ryadg
Rysto
Sen1
Sm
Sw-5
Tm-1
Tm-2a
Tsw
Ty-1 (Q)

Oidium lycopersicon
Phytophthora infestans
P. infestans
P. infestans
P. capsici
P. infestans
P. infestans
P. infestans
Required for Pto/Fen
Pseudomonas syringae pv.
tomato
PepMoV, PVY, TEV
PVY
PVY, PepMoV
PepMoV, PVY
PVY
Pyrenochaeta lycopersici
P. infestans
P. infestans
P. infestans
P. infestans
P. infestans
PVA
M. chitwoodii
PVX
PVX
Xanthomonas campestris
pv. vesicatoria
PVX
PVY
PVY
Synchytrium endobioticum
Stemphylium
TSWV
TMV
TMV
TSWV
TYLCV

Pathogenb

Ol-1
Ph-1
Ph-2
Ph-3
phyt 1-3 (Q)
phyt1-7 (Q)
phyt8 (Q)
Pi1, Pi01 (Q)
Prf
Pto

Genea

Referencee

(Continued)

Hanson et al. (2000)

Juvick et al. (1991); Zamir et al. (1995); Diwan et al. (1999)

Ritter et al. (1991)

Hamalainen et al. (1997)
Brigneti et al. (1997)
Hehl et al. (1999)
Behare et al. (1991)
Stevens et al. (1995); Brommenschenkel and Tanksley (1997)
Levesque et al. (1990)
Young et al. (1988)
Jahn et al. (2000)
Zamir et al. (1994); Chague et al. (1997)

V
XI
XI
XI
11
9
2
9
10
6

S. acaule
S. tuberosum subsp. andigena
S. stoloniferum
S. tuberosum
L. pimpinellifolium
L. peruvianum
L. hirsutum
L. peruvianum
C. chinense
L. chilense, L. hirstutum, L. pimpinellifolium,
L. cheesmanii
L. hirsutum
L. esculentum

11
9

Murphy et al. (1998)

Caranta et al. (1997b)
Caranta et al. (1999); Grube et al. (2000)
Grube et al. (2000)
Caranta et al. (1997b)
Doganlar et al. (1998)
Leonards-Schippers et al. (1992); Meksem et al. (1995)
Li et al. (1998)
El-Kharbotly et al. (1994)
El-Kharbotly et al. (1996)
El-Kharbotly et al. (1996)
Hamalainen et al. (1998)
Brown et al. (1996)
Bendahmane et al. (1997)
Ritter et al. (1991)
Yu et al. (1995)

B
B, 4
10
10
3, 10, 7, B
3
V
IV
XI
XI
XI
XI
XI
XII
XII
1

6
Van der Beek et al. (1994)
7
Pierce (1971)
10
Moreau et al. (1998)
9
Chunwongse et al. (1998)
4, 11, 11
Lefebvre and Palloix (1996)
III, V, VI, IX, XI Oberhagemann et al. (1999)
VIII
Meyer et al. (1998)
IV
Leonards-Schippers et al. (1994)
5
Salmeron et al. (1996)
5
Martin et al. (1993)

Chromosomal
locationd

C. chinense
C. annuum
C. annuum
C. chinense
C. annuum
L. peruvianum
S. demissum
S. demissum
S. demissum
S. demissum
S. demissum
S. tuberosum subsp. andigena
S. bulbocastum
S. tuberosum subsp. andigena
S. tuberosum subsp. andigena
L. esculentum

L. hirsutum
L. pimpinellifolium
L. pimpinellifolium
L. pimpinellifolium
C. annuum
Solanum
S. tuberosum
S. tuberosum
L. pimpinellifolium
L. pimpinellifolium

Originc

(Continued)

TABLE 1

876
R. C. Grube, E. R. Radwanski and M. Jahn

Tomato

Tomato
Tomato

Tobacco

Tomato

I2

Prf
Pto/Fen

Sw-5

Tomato
Potato
Pepper
Tomato
Pepper
Pepper
Potato
Pepper
Potato
Pepper
Tomato

Homologues mapped in
1
1
11
8, 9, 11
5
5, 6, 9, 12
5
11
11
9, 7, 5
9, 12

Leister et al. (1996)

Jahn et al. (2000)
Jahn et al. (2000); (t)

Leister et al. (1996)

Ori et al. (1997); Simons et al. (1998)

Parniske et al. (1997)

Leister et al. (1996)

References

Underlined gene names given by the authors for simplicity; Q in parentheses following gene name designates QTL; all others qualitative loci.
Viral pathogen abbreviations are as follows: CMV, cucumber mosaic virus; PepMoV, pepper mottle virus; PVA, potato virus A; PVMV, pepper veinal mottle virus; PVX,
potato virus X; PVY, potato virus Y; TMV, tobacco mosaic virus; TSWV, tomato spotted wilt virus; TYLCV, tomato yellow leaf curl virus.
c
Only genus name given when species data not available.
d
Chromosomal locations in genomes of origin.
e
Abbreviations for selected references are: (t) S. D. Tanksley, A. Frary and S. H. Brommenshenkel (unpublished results); (p) I. Paran and M. K. Jahn (unpublished
results). If blank, results reported for the first time in this publication.
f
Position of R gene homologues, referring to the tomato genetic map.

Tomato

Origin

Cf-9

Gene

Tomato
chromosome
no.f

(Continued)

TABLE 1

Comparative Mapping of R Genes

877

878

R. C. Grube, E. R. Radwanski and M. Jahn

Figure 1.Resistance gene organization in the Solanaceae. The tomato genome is represented by the outer circle, proceeding
clockwise from top to bottom of each chromosome. The potato and pepper genomes are represented by the middle and inner
circles, respectively. Inversions that distinguish the three genomes are indicated by arrows within the rearranged portions of the
potato and pepper maps. Solid lines indicate breaks between chromosomes, and dashed lines indicate the borders of rearranged
regions. The five translocations between the pepper and tomato genomes are shown by splitting each of pepper chromosomes
3, 5, 9, 11, and 12 into two halves, each half syntenous to different tomato chromosomes. Resistance genes are designated by
solid type; resistance gene homologues are designated by the letter H in outlined type followed by the gene name in subscript.
Dark bars along the length of the chromosome are used to denote regions of a chromosome associated with a gene if imprecisely
located; names of genes excluded from analyses due to imprecise location are underlined. Ovals are drawn around cross-generic
and intrageneric R gene clusters (15 cM) identified by this analysis. Note that genomes are not drawn to scale.

gene clusters spanned two or more genera (Figure 1;

Table 2). Representative RFLP markers are given for
each cluster in Table 2. Tomato-potato clusters are
found on T6, T9, T10, and T12; tomato-pepper clusters
were found on T1 and T7; and a single pepper-potato
cluster exists on T8. Finally, there are 5 gene clusters
that involve all three solanaceous genera, located on
T3, T4, T9, and T11. These 12 clusters plus 6 additional

clusters that occur in only one genus were distributed

throughout the genomes. Over half (48/84) of the
genes included in this analysis were located within 15
cM of positions of R genes in other genera. Only 14 R
genes did not occur in any R gene cluster.
To test the hypothesis that this degree of clustering
across genera would be observed by chance, we assumed
that within each crop genus, each R gene or intrageneric

pvy1 (v)
pvr1 (v), pvr2 (v),
pvy2 (v)
cmv3.2 (v)
phyt1 (f)

pvy3 (v)

pvy4 (v)

cmv3.1 (v)

L (v), cmv4 (v), phyt3 (f)

T1
T3

T5
T6

T7
T7
T8
T9
T9
T9
T10
T11

T11

T12

phyt8 (f)
phyt6 (f)

Nxphu (v)
Gro1.2 (n)
Rysto (v), Ryadg (v), Rmci (n),
Raadg (v), Sen1 (f)
R3 (f), R6 (f), R7 (f),
phyt7 (f), Gro1.3 (n)
Rx (v), Rx1 (v), Gpa2 (n)

phyt2 (f)
R2 (f)
Gpa, Pi01 (f), R1 (f)
Rx2 (v), Nb (v), Grp1 (n),
phyt3 (f)

phyt4 (f)

Gro1.4 (n)

Potato

Lv (f)

Pto (b), Fen (b), Prf (b)

Cm6.1 (b), Mi (n, i),
Ty-1 (v), Ol-1 (f), Cf-2 (f),
Cf-5 (f), Bw-5 (b)
Cm7.1 (b)
I-3 (f), I-1 (f)

Ve (f), Cm9.1 (b)

Tm-2a (v), Fr1 (f)
Sw-5 (v)
Ph-2 (f)

I2 (f), Sm (f), Ty-2 (v)

Asc (f)
Hero (n)

Cf-1 (f), Cf-4 (f),

Cf-9 (f), rx-1 (b)
Cm1.1 (b)
py-1 (f)

Tomato

TG61, TG166A, TG133

CT44, TG170
TG346, CT252
TG254, TG9, CT143
TG101, CD3, CD32
TG424, CT220
TG63, TG233
CT182, TG508, CD17, GP259,
GP125, CP58
GP185, GP250, TG105, TG36,
TG26, TG104
CT99, CT100, CT129, CP60

TG379, TG619, CT155

TG178, TG231, TG232, CT83, TG153

TG184, TG301, CT268, TG236

TG334
TG59, TG71
TG56, TG135, TG132, TG130
TG324, TG479
TG457, TG42, TG134
CT229, TG123, GP261, TG62, TG483
GP21, GP179, TG432, GP213

Associated RFLP markers

Clusters were defined by the presence of two or more resistance genes from one or more solanaceous genera within 15 cM, as described in text. Gene names are followed
by letters designating the major pathogen group controlled: (b) bacteria, (f) fungus or oomycete, (n) nematode, (v) virus, (i) insect.

T3
T4
T5

Pepper

T1

Location

Solanaceous resistance gene clusters and RFLP markers associated with each cluster

TABLE 2

Comparative Mapping of R Genes

879

880

R. C. Grube, E. R. Radwanski and M. Jahn

R gene cluster was independent and occupied a single

genomic position. Each of the 12 chromosomes was
then divided into five equal 15- to 20-cM portions. Out
of 60 possible positions in each genome, R genes/gene
clusters occupied 25, 15, and 12 positions in tomato,
potato, and pepper, respectively. Assuming random
placement, the probability that genes/gene clusters
from all three genera would co-occur within corresponding genome segments was calculated as a twostage problem. First, Y represented the number of times
that genes/gene clusters from any two genera (e.g., tomato, potato) are found in corresponding positions. Y is
distributed according to the hypergeometric probability
distribution (Larsen and Marx 1986) and the probabilities of obtaining all possible values of Y were calculated
for the above parameters. The probability that clusters
from the third genus correspond with clusters from the
other two genera is dependent upon the value of Y and
is calculated in the same way. The combined probability
that R genes/gene clusters are found in corresponding
positions five or more times in the three host genera,
as observed, is 0.0028. This is a rough approximation
that does not reflect the nonrandom distribution of
functional genes in plant genomes; however, the positions of R gene/gene clusters in tomato, potato, and
pepper are unlikely to be independent.
R gene inheritance and taxonomic specificity at corresponding positions across plant genera: Recessive genes,
dominant genes, and QRL were all found to occur in
cross-generic R gene clusters. Our data set contained
only six mapped recessive genes, three of which were
found in one cross-generic cluster that contained no
dominant genes. The other three recessive genes were
not part of any R gene clusters. Of the remaining crossgeneric clusters, three contained QRL only, two contained dominant genes only, and six contained a mixture of dominant genes and QRL.
Most cross-generic clusters (10/12) included R genes
that control pathogens from two or more major pathogen groupings (e.g., fungi, nematodes, etc.; Figure 1).
R genes from different host genera that confer resistance to the same major pathogen group occurred at
corresponding positions less frequently (in 6/12 clusters). For example, three virus resistance genes, one for
resistance to tomato yellow leaf curl virus in tomato,
one for tobacco mosaic virus (TMV) in pepper, and a
CMV QRL in pepper, are linked to TG36 (Lefevbre et
al. 1995; Hanson et al. 2000; I. Paran, unpublished
results). Similarly, the potato potexvirus R gene Nxphu is
linked to TG424, which is 12 cM from the tospovirus R
gene Sw-5 on T9 and a cucumovirus QRL on pepper
chromosome 3 (Stevens et al. 1995; Brommenschenkel and Tanksley 1997; Tommiska et al. 1998; I. Paran,
unpublished results). Finally, potato and pepper alleles
conferring resistance to the pathogenic oomycete Phytophthora were found in positions corresponding to
tomato genes conferring resistance to the true fungal

pathogens Oidium, Stemphylium, Cladosporium, Fusarium, Verticillium, and Alternaria on T3, T4, T6, and
T9 (Behare et al. 1991; Dickinson et al. 1993; BalintKurti et al. 1994; Van der Beek et al. 1994; Van der
Biezen et al. 1995; Lefebvre and Palloix 1996; Vakalounakis et al. 1997; Li et al. 1998; Oberhagemann et
al. 1999).
In only two cases, both involving Phytophthora species, genes for resistance to the same pathogen genus
were found in corresponding genomic locations in different host genera. In pepper, a QRL (phyt3) for resistance to Phytophthora capsici is associated with TG104
(P 0.005; Lefebvre and Palloix 1996), which is
located 6 cM from TG105 on T11 (Pillen et al. 1996).
In potato, R3, R6, and R7 for resistance to P. infestans
are tightly linked to GP250 and GP185 (El-Kharbotly
et al. 1994, 1996), which in turn are tightly linked to
TG105 (Hamalainen et al. 1997). A potato Phytophthora QRL (phyt7) is also located in this region (Oberhagemann et al. 1999). A second P. capsici QRL (phyt1)
in pepper is associated with TG483, which was reported
to be unlinked to any pepper linkage group (Lefebvre
and Palloix 1996). On our pepper map, TG483 is
located on Capsicum chromosome 5, syntenous to its
location on T4. In potato, R2 was localized to a region
of T4 spanning TG483 (Li et al. 1998), and, although
imprecisely mapped, the potato QRL Pi1 was also located in this region (Leonards-Schippers et al. 1994).
The three mapped P. infestans R genes from tomato,
Ph-1, Ph-2, and Ph-3, were unlinked and did not correspond to any of the positions identified in potato or
pepper for Phytophthora resistance (Pierce 1971;
Moreau et al. 1998).
Comparative mapping of R genes with similar taxonomic specificity across plant genera: If R gene specificity is conserved across genera, genes conferring resistance to closely related or identical pathogens should
be found in corresponding positions in related genera.
For several pathogen genera or species, R genes have
been mapped in more than one solanaceous genus,
thereby allowing a test of this assertion. Pathogens that
infect more than one host genus include TMV, TSWV,
potato virus Y (PVY), Globodera, Meloidogyne, and Phytophthora species. A total of 38 genes conferring resistance to these pathogens have been mapped in two or
more host genera, and only 7 of these were found in
regions corresponding to R genes with similar taxonomic specificity in another genus. Of these 7 genes
(all Phytophthora genes mentioned above), 4 potato
major genes and QRL and one pepper QRL were found
in one location, and the remaining pepper and potato
QRL were found in a second position.
Six mapped PVY R loci in pepper that occur at four
unlinked positions failed to correspond to the position
of two linked PVY R loci in potato. Similarly, none of
seven Globodera R genes in six unlinked positions in
potato corresponded to the single Globodera R gene

Comparative Mapping of R Genes

mapped in tomato. A similar lack of correspondence

was observed for TMV R loci (one in tobacco, two in
tomato, one in pepper), TSWV R loci (one in pepper,
one in tomato; Jahn et al. 2000), and loci conferring
resistance to Meloidogyne species (one in pepper, one
in potato, two in tomato). A fourth Meloidogyne R gene,
the pepper gene Me3, was excluded from our analysis
because a precise comparative map position could not
be ascertained; however, the interval to which Me3 can
be definitively assigned corresponds to the position for
Mi-3 in tomato, which confers resistance to the same
strain of M. incognita (Dijan-Caporalino et al. 1998).
To examine more closely the organization and relationship between R loci with similar taxonomic specificity in related hosts, we selected a pathogen, TMV, that
infects across host species and for which a cloned solanaceous R gene was available (Whitham et al. 1994). Resistance to TMV is controlled by the genes N in tobacco
(Holmes 1938), Tm-1 (Levesque et al. 1990) and Tm-2
(Young et al. 1988) in tomato, and L in pepper (Lefebvre et al. 1995). We used the tobacco N full-length cDNA
to identify homologues in pepper by hybridization. Although several (6) fragments were detected, all five
polymorphic fragments mapped to only two chromosomal locations. Both locations were on the short arm
of the pepper chromosome corresponding to T11, one
5 cM distal to CP58 and the other 30 cM distal from
the first. In tobacco, a family of related sequences cluster
at the N locus, which is linked to CP58, with additional
related sequences linked at an unspecified distance
(Whitham et al. 1994); thus the two positions mapped
in pepper may be orthologous to the tobacco loci. These
two positions obtained for N homologues in pepper
did not correspond to any of the known positions of
phenotypically similar TMV R genes in tomato or pepper (see Figure 1). Similarly, in tomato, no N-related
sequences have been mapped to regions containing
Tm-1 or Tm-2 (Ohmori et al. 1998).
While the N homologues in pepper did not cosegregate with any phenotypic resistances mapped to date in
pepper or tomato, including resistance to TMV, the
position of one homologue coincided precisely with the
position of potato loci for potyvirus resistance (Ryadg/
Rysto and Raadg), Meloidogyne nematode resistance (Rmci),
and Synchytrium resistance (Sen1), as well as potato
homologues of N (Leister et al. 1996; Hehl et al. 1999).
Although these results suggest that Tm-1, Tm-2, and L
may not be homologous to the functional N allele from
tobacco, N homologues in these genera may be related
to other phenotypically defined R genes or may represent as yet undescribed TMV resistance loci. We have
also obtained similar results with genes for dominant
necrotic localizing resistance to TSWV in tomato and
pepper (Jahn et al. 2000). Pepper homologues of the
tomato gene Sw-5 did not map near the pepper gene
Tsw, although they mapped to positions very close to

881

other potato and tomato R genes (see Figure 1 and

below).
Comparative mapping of resistance gene homologues: To examine the correspondence between genomic positions of R gene homologues and known R genes
in other species more comprehensively, homologues of
five cloned R genes were mapped in pepper. Our results,
information from collaborators, and published information are compiled in Figure 1. Pepper homologues of
N were found in positions corresponding to the potato
Rysto/Ryadg , Rmci, and Sen1, as presented above. Pepper
homologues of Sw-5 were found in two positions, one
of which corresponded to tomato Sw-5, potato Nxphu,
and the pepper QRL cmv3.1 on T9 (Jahn et al. 2000). An
additional Sw-5 homologue was found near the tomato
QRL Cm7.1 on T7. The high percentage of sequence
similarity between Pto and Fen (Loh and Martin 1995)
resulted in identical patterns of hybridization using either sequence as radiolabeled probe under our conditions. Five genomic regions, each containing one or
more pepper Pto/Fen homologues, were also clearly
identified in pepper. One Pto/Fen homologue and two
polymorphic fragments hybridizing to Prf corresponded
exactly to the position of Pto, Fen, and Prf in tomato, as
well as a Pto homologue in potato (Leister et al. 1996).
The other locations of Pto/Fen homologues are shown
in Figure 1: the top of T5 near TG432, corresponding
to a large R gene cluster in potato (Grp1, phyt3, Gpa,
Pi01, R1, Rx-2, Nb); the top of T6 near TG178, corresponding to a large R gene cluster in tomato (Cm6.1,
Mi, Ty-1, Ol-1, Cf-2, Cf-5); and on T9 and T12, where
no known Pto/Fen homologues exist in tomato and no
mapped R genes occur in any species. One to four
additional fragments hybridizing to Prf were identified
but were monomorphic in pepper and therefore could
not be mapped. The precise number of Prf homologues
in the pepper genome and whether they are associated
with the additional Pto/Fen homologues found throughout the genome (suggesting duplication of the entire
regions surrounding Pto in tomato) remain unknown.
Pepper homologues of I2C were also detected in regions
corresponding to their positions in the genus of their
origin (Ori et al. 1997; Simons et al. 1998). As with Sw-5,
Prf, and N, several additional monomorphic fragments
hybridizing to I2C were also detected but could not
be mapped. Cf-9 homologues were also abundant in
pepper, although none could be mapped due to a complete lack of polymorphism for all identified fragments
in our pepper mapping populations.
In summary, pepper homologues of all R genes examined (N, Sw-5, Pto, Prf, and I2C) were detected in regions
syntenous to their positions on the genus of origin, as
expected given the degree of conservation of order of
random cDNA and genomic clones between genera. In
some cases, additional unique positions of homologues
were identified either in the genus of origin or in related
genera. While in several cases a homologue of one gene

882

R. C. Grube, E. R. Radwanski and M. Jahn

corresponded precisely to the position of phenotypic

resistance to a different pathogen in another host, in
no case have we identified an R gene whose homologue
cosegregates with resistance of similar pathogen specificity in another genus.
DISCUSSION

This is the first comprehensive examination of the

genomic organization of a wide array of R genes in more
than two host genera. This analysis has revealed several
cross-generic R gene clusters, suggesting that the chromosomal locations of R genes may be quite broadly
conserved through speciation. This trend may be similar
to the conservation of genomic position and function
that has been observed for several other major categories of plant genes (Van Deynze et al. 1995; Lee 1996;
Osborn et al. 1997; Gale and Devos 1998) and contrasts
with previous hypotheses about the behavior of R loci
through evolution (Leister et al. 1998). The apparent
contrast between our findings and those of Leister et
al. (1998) may be a result of our focus on phenotypically
defined R genes conferring resistance to a wide array
of pathogens, as opposed to sequence-defined classes
of RGAs with unknown function. More limited studies
and unpublished results from the Gramineae and Leguminoseae are consistent with the results of the present
study. In maize and oat, two rust resistance loci (giving
resistance to the pathogens Puccinia sorghi and P. coronata) and resistances to powdery mildew and wheat
streak mosaic virus occur on homeologous linkage
blocks, although they may be separated by 30 cM or
more (G. X. Yu et al. 1996). Similarly, a cyst nematode
R gene in soybean is located in a position corresponding
to an anthracnose R gene in common bean (P. Gepts,
personal communication).
One potential use of comparative mapping is the
rapid identification of genes similar to those already
mapped in related genera. The success of this approach
for identification of R genes will require not only that
the positions of R loci are conserved across genera, but
also that alleles at these loci maintain similar function
and specificity for the same or related pathogen taxa.
Although 12 cross-generic R gene clusters were identified, R genes with specificity for the same pathogen
genus (Phytophthora) occurred only twice at corresponding positions in different host genera, Solanum
and Capsicum. Although not definitive, Melodogyne R
genes from Capsicum and Lycopersicon may also be
located in corresponding map positions (Dijan-Caporalino et al. 1998). In contrast, genes conferring resistance to Globodera, TMV, TSWV, and PVY have also
been mapped in two or more solanaceous genera and
thus far have not been identified in corresponding regions. While absolute conclusions cannot be made because an exhaustive analysis of all R genes that exist in
these three genera is not possible, our results suggest

two testable hypotheses. The first possibility is that alleles at orthologous loci in different plant genera are
nonfunctional or do not typically confer resistance to
the same or closely related pathogens. An alternative is
that orthologous genes usually do confer resistance to
related pathogens. This could be reconciled with our
observations if each host genus has an array of R genes
targeting a given pathogen or pathogen family, and the
subset of genes mapped thus far in different genera by
chance are not orthologous. Resolution of these questions will require detailed sequence and functional comparison at loci clearly established to be orthologous. In
either case, results from the present study highlight
the potential difficulties of using a direct comparative
approach to identify similar R genes in related plant
genera.
In several (6/12) of the cross-generic clusters identified, genes conferring resistance to the same major
pathogen group (e.g., virus, nematode, fungus, bacteria)
were found in corresponding positions. Whether the
occurrence of these genes in similar locations reflects
shared biology or components involved in plant-pathogen interactions remains to be seen. Due to the imprecision of comparative mapping, positional correspondence does not necessarily imply homology. Further
examination of these loci, however, may reveal that
small changes in nucleotide sequence have given rise
to homologues or orthologues with radically different
pathogen specificity. Emerging evidence suggests that
minimal changes in R gene sequence can slightly alter
taxonomic specificity, resulting in the recognition of
different pathogen strains or pathotypes (Thomas et al.
1998; Wang et al. 1998; Ellis et al. 1999). Relatively
small changes in sequence may also result in radical
shifts in specificity, especially if avirulence molecules
from very different pathogens are structurally similar
(Bendahmane et al. 1999; Rouppe van der Voort et
al. 1999; Van der Vossen et al. 1999). An extreme example is the single gene Mi, which gives resistance to a
nematode and an aphid (Rossi et al. 1998; Williamson
1999). This could also account for positional correspondence of R genes for pathogens with no apparent taxonomic relationship, e.g., the possible correspondence
between the two unlinked Phytophthora resistance loci
in tomato and two Globodera resistance alleles in potato, and the correspondence of two unlinked PVY QRL
in pepper with two tomato QRL conferring resistance
to Clavibacter michiganensis.
For two pathogens, an R gene had been cloned from
a solanaceous genus, providing an additional molecular
tool to examine the relationship between resistance alleles from different genera (Whitham et al. 1994;
S. D. Tanksley, A. Frary and S. H. Brommenshenkel,
unpublished results). Pepper homologues of N and
Sw-5, similar to pepper homologues of other solanaceous R genes, were found in positions corresponding
to N and Sw-5 in tobacco and tomato, respectively, as well

Comparative Mapping of R Genes

as in additional positions (Jahn et al. 2000). N and Sw-5

homologues were not, however, found in positions corresponding to TMV or TSWV resistance loci in other
genera. Comparative mapping results therefore suggest
that resistance to the same viral pathogen is controlled
by nonhomologous genes in different genera, although
this approach is limited by our inability to definitively
map all homologues due to lack of polymorphism. Additional information about mutations in the viral genomes
that overcome different R genes (Watanabe et al. 1987;
Meshi et al. 1988, 1989; Padgett and Beachy 1993)
also suggest that TMV and TSWV resistances appear
to be controlled by nonhomologous loci in different
solanaceous genera. Nonhomologous R genes may trigger the same conserved response cascade, which would
reconcile the phenotypic similarity of the resistance response observed in distinct genera with the apparent
lack of a genetic relationship between these loci (Innes
1998). To our knowledge, only one case has been reported in which homologous genes at corresponding
positions (putative orthologues) confer resistance to
identical pathogens in closely related host genera. Multani et al. (1998) have shown that orthologues of the
maize loci Hm-1 and Hm-2, which confer resistance to
Cochliobolus carbonum, exist in corresponding positions
and appear to function, giving nonhost resistance to C.
carbonum in sorghum and rice. It may be important to
note that these genes produce a detoxifying enzyme,
which is a fundamentally different host response than
is thought to be involved in typical gene-for-gene interactions. Putative orthologues with similar pathogen
specificity, if identified in the Solanaceae, might represent critical genes that have been under constant selection pressure throughout host divergence. A potentially
significant observation from this study is the co-occurrence of an R gene homologue in one species with
phenotypic resistance of different pathogen specificity
in another. The next step will be to determine the relationship between the sequences of R gene homologues
(e.g., N, Sw-5) and the functional R genes in close proximity (e.g., Rysto/Ryadg , Raadg , Rmci, Sen1, cmv3.1, Nxphu). If
genes conferring resistance to different pathogens in
related hosts are homologous, this suggests that the
general function of R genes may be conserved, although
taxonomic specificity has changed during host speciation.
Dominant, recessive, and quantitatively inherited
genes were all found in cross-generic clusters, in proportions similar to their frequency in the overall data set.
It is striking that all three recessive loci that occurred
in cross-generic clusters were in the same cluster, which
did not contain any dominant genes. This is consistent
with the hypothesis that recessive and dominant R genes
will be unrelated mechanistically or evolutionarily. Also
consistent with this hypothesis is the observation that
the recessive barley powdery mildew R gene mlo bears
no structural similarity to other cloned R genes (Buschges

883

et al. 1997). Further analysis as more recessive R genes

are mapped and cloned will shed light on these possibilities.
A majority of cross-generic R gene clusters, including
four of the five clusters that comprise genes from all
three host genera, were located in close proximity to the
end of a chromosome or to a division between conserved
linkage blocks. This may be meaningful in light of observations correlating the presence of transposable elements with both large-scale genomic rearrangements
(Robbins et al. 1989; Kim et al. 1998) and disease resistance gene clusters (Meyers et al. 1998; Song et al.
1998). Transposable elements may play a role in the
creation and maintenance of these clusters and perhaps
even in shifts of specificity that may become apparent
as we examine the content of these positions through
speciation (Meyers et al. 1998; Michelmore and Meyers 1998).
In conclusion, this study has revealed limited positional correspondence of phenotypically defined genes
conferring resistance to related or identical pathogens
across three solanaceous genera. There were two notable exceptions: a pair of unlinked genomic regions contained both resistance to P. infestans in potato and P.
capsici in pepper, in addition to the possible correspondence of Me3 and Mi-3. This analysis also revealed unexpected positional correspondence of genes conferring
resistance to apparently unrelated pathogens. For example, tomato P. infestans R loci and potato Globodera
resistance loci were twice found in roughly corresponding positions, as were tomato Clavibacter QRL and potato PVY QRL. Further, pepper homologues of cloned
R genes (e.g., N, Sw-5) were found in positions corresponding with phenotypically defined solanaceous
genes that confer resistance to unrelated pathogens, as
also seen by Hehl et al. (1999). While we cannot exclude
the possibility that the observed correspondence across
genera is coincidental, these pairings suggest intriguing
hypotheses about the evolutionary relationships between R genes with apparently unrelated specificities
that may be tested easily as sequence information from
cloned R genes continues to accrue. Trends emerging
from studies in this and other plant families should
allow both the definition and resolution of the processes
and patterns that govern the function and evolution of
this important class of plant genes.
The authors thank K. D. Livingstone, V. K. Lackney, J. P. Jantz, C.
Lewis, A. Frary, and R. Silady for their technical assistance and S. D.
Tanksley, B. Baker, R. Fluhr, C. Gebhardt, and B. Staskawicz for
generously providing experimental materials and/or unpublished results. We also thank N. Young, G. Martin, W. Frye, L. Landry, A.
Matern, and M. Cadle for review of this manuscript. This work was
supported in part by U.S. Department of Agriculture National Research Initiative Competitive Grants Program Award Nos. 91-373006564 and 94-37300-0333, U.S.-Israel Binational Agricultural Research
and Development Award IS-2389-94, and the California Pepper Improvement Foundation/California Pepper Commission. R.C.G. was
supported by a Department of Energy/National Science Foundation/

884

R. C. Grube, E. R. Radwanski and M. Jahn

United States Department of Agriculture grant to the Research Training Group in Molecular Mechanisms of Plant Processes and gifts from
Seminis Vegetable Seeds, Novartis, M. Lavallard, and C. M. Werly.

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