4382

Advances in
Life Sciences
Advances in Life Sciences 5(11), Print : ISSN 2278-3849,
4382-4387,
20165(11), 2016

REVIEW PAPER

Insight in Mapping Quantitative Trait Loci Associated with Disease Resistance

in Crops: Sensed and Reached
PARTHASARATHY SEETHAPATHY*1 , THIRUMAL RAJ SANNASI 2, RAJALAKSHMI
JAYARAMAN3 AND PRABAKAR KUPPUSAMY4
1,3&4

Department of Plant Pathology, Centre for Plant Protection Studies, Tamil Nadu Agricultural
University, Coimbatore-641 003, Tamil Nadu, India.
2
Department of Fruit Crops, Horticultural College and Research Institute, Tamil Nadu Agricultural
University, Coimbatore-641 003, Tamil Nadu, India.
*email: spsarathyagri@gmail.com

ABSTRACT
The transition to a new era of disease resistance research
is underway, and both the public and private sectors are
moving to exploit the new tools and opportunities presented
by genetics and molecular biology. Most disease resistance
traits are polygenic in nature and controlled by many genes
residing at so called quantitative trait loci (QTLs). In
addition, sources of resistance are usually found in wild
relatives or cultivars with lower agronomical value, so
introgression of resistance characters into commercial
peach cultivars usually requires several generations of
backcrossing to reinstate the favorable genotype.
Molecular-assisted breeding (MAB), however, allow the
pre-selection of traits long before they are expressed. Plant
scientists have used disease resistance genes (R genes)
to control plant disease since the turn of the century.
Molecular cloning of R genes that enable plants to resist
a diverse range of pathogens has revealed that the proteins
encoded by these genes have several features in common.
These findings suggest that plants may have evolved
common signal transduction mechanisms for the
expression of resistance to a wide range of unrelated
pathogens. Characterization of the molecular signals
involved in pathogen recognition and of the molecular
events that specify the expression of resistance may lead
to novel strategies for plant disease control.
Key words

Defence response gene, Disease resistance,

Map based cloning, Mapping gene loci, R
genes.

The genetics of plant disease resistance has been

extensively characterized over many years (Crute, 1985;
Pryor and Ellis, 1993). Classical genetic analyses have
shown that resistance to many diseases is determined
by individual members of clusters of dominant genes,
each member conferring resistance to specific strains
of a pathogen. Genes conferring resistance to different
pathogens may be co-located in the genome. This led
to the hypothesis that some resistance genes are related
in function and evolution, individual members of these

multigene families having diverged to confer different

specificities. The mapping and isolation of the above
genes were made possible because of the advances in
molecular biology during the last two decades, which
provided new classes of genetic markers at the level of
DNA. They include Restriction Fragment Length
Polymorphism (RFLP), Randomly Amplified
Polymorphic DNA (RAPD), Sequence Tagged Sites
(STS), Expressed Sequence Tags (EST), Sequence
Characterized Amplified Regions (SCAR), Simple
Sequence Repeats (SSR), Short Tandem Repeats (STR),
Inter-Simple Sequence Repeat (ISSR) and Amplified
Fragment Length Polymorphism (AFLP), Arbitrarily
Primed PCR (AP-PCR), Cleaved Amplified Polymorphic
Sequence (CAPS), Single Nucleotide Polymorphism
(SNP), Simple Sequence Conformational Polymorphism
(SSCP) and Variable Number Tandem Repeat (VNTR).
The unlimited availability of all these markers enabled
plant geneticists, breeders and pathologists to locate
many of the genes associated with disease resistance.
These developments have stimulated new interest in
exploring the functionality of genes associated with
disease resistance in crop plants.

Nature of host resistance to pathogens

The problems of breeding for plant resistance to
pathogens arise mainly from the fact of genetic
variability for plant resistance that exists in the host and
for the capacity of infection from pathogens. An area
of great importance therefore to the breeder is to
understand the complexity involved in the host pest
environment interaction (Arnold et al., 1976). The gene
for gene concept proposed by Flor (1956) resulted in
establishing not all variations associated with plant
resistance follow the same pattern as proposed. van
der Plank (1963, 1982) differentiated two types of
relationships between host and pathogen which he called
vertical and horizontal resistance. The former is based
on complex interactions of genes of host and genes of
pathogen in turn with varying environments.

PARTHASARATHY, et al., Insight in Mapping Quantitative Trait Loci Associated with Disease Resistance in Crops

Understanding the evolution of complex plant resistance

to pathogens requires an understanding on dynamics
of genetic variation for resistance traits within natural
population.
These dynamics depend largely on three major
factors:
1)
2)
3)

The extent to which a trait is genetically controlled

and heritable,
The probability with which chance effects can
change the distribution of a trait and
The nature of natural selection that may act on a
trait. Mapping Quantitative Trait Loci (QTL) and
candidate gene loci will resolve the dynamics of
above said factors for the better planning of
resistance breeding.

Mapping genetic loci and genes associated

with disease resistance
Numerous direct applications of molecular marker
technology to facilitate plant breeding programmes have
been recommended. Because of the large numbers of
DNA markers available in populations of interest, one
of the most important applications of DNA markers is
to establish gene marker linkage for the traits of having
qualitative inheritance. The gene marker linkage helps
the breeder to go for indirect selection based on marker
inheritance for the traits, which are difficult or expensive
to evaluate. In the same manner, one can locate the
genetic loci (otherwise called as quantitative trait loci
or QTL) associated with traits having complex mode
of inheritance if a genetic map of molecular markers is
made available. To these maps, the already established
genetic loci (otherwise called as candidate gene loci or
CGL) can also be integrated. Mapping of QTL and CGL
will help to go for indirect selection and to understand
the dynamic behind the inheritance of complex traits.
Several morphological and biochemical factors
contribute towards the plant resistance to pathogens.
The genetic loci controlling these factors can be easily
located on a genetic map if the trait is measurable.
Locating the genetic loci will help to establish relationship
with already identified major genes/candidate genes, to
associate the QTL with genes controlling the metabolic
pathway of resistance factors, to identify genetic loci
associated with resistance to common group of
pathogens and to identify the differential association of
genetic loci with a particular resistance factor during a
developmental stage of host and parasite.

Plant resistance to pathogens and QTL

mapping
Knowledge of the biological significance
underlying QTL for disease resistance is generally
limited. In the past, quantitative disease resistance was

4383

done based on the genetic analysis of various cross

combinations involving resistant and susceptible
parents. Traditional estimates of the number of effective
factors for quantitative resistance (QR) can only be
(QR) regarded as the lower limit of the actual gene
number. In recent years, advances in plant microbe
interaction and genome mapping have lead to an increase
in understanding of plant defense and quantitative disease
resistance. Mapping of QR-related genes (complex and
polygenic forms of disease resistance) have been
described (Yu et al., 1991; Heun, 1992; Bubeck et al.,
1993; Young et al., 1993; Leonards-Schippers et al.,
1994; Wang et al., 1994; Pecchioni et al., 1996;
Steffenson et al., 1996; Young, 1996; Faris et al., 1997;
Grube et al., 2000; Emma et al., 2003; Gururani et al.,
2012).
The late blight of potato disease system caused
by the fungus (Phytophthora infestans) is one of the
classic examples in the field of qualitative resistance. It
was used by van der Plank to develop his ideas on vertical
and horizontal resistance (van der Plank, 1982). In a
recent QTL mapping study of P. infestans resistance
(Leonardes-Schippers et al., 1994), race-specificity of
QTL, the relationship between qualitative and quantitative
resistance loci, and the possibility that QTL and host
response genes might be one and the same were
examined in detail. In the study, the disease responses
of 197 F1 progeny from a cross between two highly
heterozygous, diploid potato parents with differing levels
of late blight resistance were determined by leaf disk
assays and compared with genotype of 102 RFLP
marker loci.
Eleven genomic segments on nine chromosomes
were found to be associated with resistance at p < 0.05
(a relatively lenient cut-off). Three types of QTL were
discriminated based on race-specificity; seven QTL
specific to race 1 of P. infestans, seven QTL specific
to race 0, and four QTLs that were nonspecific for
these two races (some loci showed different types of
race-specificity depending upon parental allele). These
results indicate that quantitative resistance to P.
infestans, which has been described as race
nonspecific (van der Plank, 1968), is a cumulative
phenotype resulting from a small number of racenonspecific and other race-specific resistance loci. One
QTL on chromosome 4, which was especially significant
in this study, coincided in location with a known
qualitative resistance gene (R1) (Leonardes-Schippers
et al., 1992), another suggestion that qualitative mutants
phenotypes may be extreme allelic variants of QTLs
(Robertson, 1989). QTL for late blight also mapped in
the same genomic regions as two resistance genes for
potato virus X (Ritter et al., 1991). QTL mapping of
fruit rot resistance to the plant pathogen Phytophthora
capsici successfully done in a recombinant inbred line

4384

Advances in Life Sciences 5(11), 2016

chilli population (Naegele et al., 2014).

Mapping QTL with candidate resistance

genes
The candidate-gene approach has emerged as a
promising method of merging QTL analysis with the
extensive data available on the cloning and
characterization of genes involved in plant defense
(Bowles, 1990; Yun et al., 1997). Here, genes potentially
involved in the biochemical pathways leading to trait
expression are employed as molecular markers of
resistance QTL analysis. This approach has been applied
successfully in several experiments (Goldman et al.,
1993; Causse et al., 1995). However, Byrne et al.
(1996) presented the most compelling case for linking
candidate genes involved in the flavone synthesis
pathway of maize with the host defense response
phenotype associated with QTL resistance to corn
earworm. Mapping QTL associated with Verticillium
dahliae resistance in biparental cross of octoploid
strawberry (Fragaria ananassa) (Antanaviciute et al.,
2015) here, a clear and statistically significant
relationship was observed between resistant, tolerant
and susceptible material and the total number of markers
present in the different resistance classes. By using
candidate genes as probes, it is possible to map known
genes onto the phenotypically determined QTL
conferring resistance. Once the phenotypic contribution
of a candidate gene is confirmed by co-segregation
analysis, the gene can be used to identify alleles of higher
phenotypic values in the germplasm pool.

Candidate genes associated with disease

resistance
The past few years witnessed a breakthrough in
the molecular cloning of disease-resistance genes. The
growing list of cloned resistance genes includes HM1
in maize (Johal and Briggs, 1992), Pto (Martin et al.,
1993) and Cf9 (Jones et al., 1994) in tomato, N in
tobacco (Whitham et al., 1994), L6 in flax (Lawrence
et al., 1995), RPS2 (Bent et al., 1994, Mindrinos et al.,
1994) and RPM1 (Grant et al., 1995) in Arabidopsis,
and Xa 21 in rice (Song et al., 1995). The successful
cloning of each of these resistance genes was facilitated
by the rapid advances in the technology of transposon
tagging and map-based cloning. Nonetheless, the cloning
of new resistance genes using the same approaches
will still be laborious and time consuming.
Biochemical and molecular studies have
demonstrated that two classes of genes contribute to
the resistance reaction: resistance (R) genes involved
in the recognition process and genes involved in the
defense response (DR genes). Recently, the cloning of
above mentioned multiple R genes from various plant
species has revealed conserved domains at the amino

acid level (Michelmore, 1995a; Meyers et al., 1999;

Richter and Ronald, 2000). In contrast, many DR genes
have been isolated from various plant species, and these
encode a diverse array of enzymes. Their structure,
expression, and function have been thoroughly
documented (Bent, 1996; Bowles, 1990; HammondKosack and Jones, 1996; Staskawicz et al., 1995; Yun
et al., 1997). A notable finding from the cloned diseaseresistance genes is their similarity in amino acid
sequences or conserved structure (Michelmore,
1995b). In particular, a majority of resistance genes
have a nucleotide-binding site (NBS) and leucine-rich
repeats (LRR) (Gururani et al., 2012). If these highly
conserved structures are common among many
resistance genes, an enormous potential exists for
isolating new resistance genes based on sequence
homology.
The first report of the cloning of an R gene from
Brassica napus, LepR3, is operating against
Leptosphaeria maculans. Larkan et al. 2013, produced
backcross generations of B. napus segregating for this
R gene to map the resistance locus. After confirming
co linearity of the genomic region with A. thaliana, and
the recently sequenced Brassica rapa, the authors
created targeted markers with which the position of
the LepR3 locus was revised. The cloning of LepR3,
orthologous to AtRLP32 (Wang et al., 2010), revealed
that the predicted LepR3 protein is a receptor-like protein
(RLP), similar to that found for the Cf R genes in the
model system Cladosporium fulvumtomato.

Disease resistance (R) genes

As mentioned, a number of R genes have been
shown to share common sequence motifs, reflecting
related functions in signal-transduction pathways.
However, the R genes can be categorised into five
different groups based on the predicted products from
the R genes (Table 1).

Defense response (DR) genes

DR genes produce products that are directly
implicated in plant compounds such as phytoalexin.
Many DR genes have been cloned and characterized,
but their chromosomal locations and their contributions
to phenotypic expression are not well known. Some
DR genes are to act downstream from R genes and are
probably regulated by one or more signal-transduction
pathways, while others are constitutively expressed or
pathogen-inducible. It is therefore possible that DR
genes may be responsible for the effects of some
resistance QTL.

Identification R genes using candidate genes

The candidate gene mapping should greatly facilitate
the molecular cloning of disease-resistance genes. To

PARTHASARATHY, et al., Insight in Mapping Quantitative Trait Loci Associated with Disease Resistance in Crops

4385

Table 1. Classification of R genes based on their gene products

Groups
Detoxifying
enzymes
Kinases

R Genes
HM 1 of maize

NBS/LRR proteins

RPS 2 and Rpm1 in

Arabidopsis
N in tobacco
Prf in tomato
L6 in flax
Cf9 in tomato

Extra
cellular
receptors
Receptor kinases

Pto of tomato

Xa 21 in rice

Gene products
NADPH dependent HC toxin reductase
which inactivates the HC toxin
Proteins with similarity to serine-threonine
protein kinases (STK)
Proteins with Leucin Rich Repeats (LRR),
putative cytoplasmic signalling domains and
Nuclear Binding Sites (NBS)

References
Johal and Briggs, 1992

Putative
membrane
anchored
cytoplasmic glycoproteins
Putative receptor kinase

Jones et al., 1994

exploit the potentials of candidate genes, the isolation

of representative genes remains as the primary step.
This can be made easy by employing the polymerase
chain reaction (PCR) using degenerate oligonucleotide
primers to isolate various domains of disease-resistance
genes. The use of PCR, nonetheless, could result in the
identification of numerous genes that have a common
conserved domain but nothing to do with disease
resistance, especially if genes containing these domains
of are overabundant. This approach will help to
determine the abundance of domains of diseaseresistance genes and to screen for candidate genes or
multigene families for a number of previously mapped
disease resistance genes using near isogenic lines and
segregating populations.
Yu et al. (1996) made an attempt to amplify and
clone disease resistance genes in soybean using
degenerate oligonucleotide primers for the NBS region
of N and RPS2. Each of these PCR-derived NBS clones
detected low-or moderate-copy soybean DNA
sequences and belongs to 1 of 11 different classes.
Sequence analysis showed that all PCR clones encode
three motifs (P-loop, kinase-2, and kinase-3a) of NBS
nearly identical to those in N and RPS2. The intervening
region between P-loop and kinase-3a of the 11 classes
has high (26% average) amino acid sequence similarity
to the N gene although not as high (19% average) to
RPS2. These 11 classes represent a superfamily of NBScontaining soybean genes that are homologous to N and
RPS2. Each class or subfamily was assessed for its
positional association with known soybean diseaseresistance genes through near-isogenic line assays,
followed by linkage analysis in F2 populations using
restriction fragment length polymorphisms. Five of the
11 subfamilies have thus far been mapped to the vicinity
of known soybean genes for resistance to potyviruses
(Rsv1 and Rpv), Phytophthora root rot (Rps1, Rps2,
and Rps3), and powdery mildew (rmd). The conserved
N or RPS2 homologous NBS sequences and their
positional associations with mapped soybean resistance
genes suggest that a number of the soybean disease

extra

Martin et al., 1993

Mindrinos et al., 1994; Grant et
al., 1995; Whitham et al., 1994;
Salmeron et al., 1996; Dodds et
al., 2001.

Song et al., 1995

resistance genes may belong to this superfamily.

Map based cloning of disease resistance

genes
Map-based cloning involves the identification of
closely linked DNA markers and use of these markers
to isolate a genomic clone that spans the target locus.
The genomic clone is used to identify candidate genes
by sequencing, complementation of a mutant plant with
sub clones, or by use of the clone as a hybridization
probe to isolate corresponding cDNA clones. Key
developments in this strategy have been the realization
that saturation of the target region with markers and
the development of very high-resolution maps (with less
than 1cM between the target locus and linked marker)
can greatly expedite gene cloning. It is relatively easy in
plants to analyze large segregating populations, and the
development of high- throughput DNA markers has
expedited high resolution mapping of many loci. The
classical example in this area is the cloning of Pto gene
in tomato (Martin et al., 1993). One marker that cosegregated with Pto was used to isolate a single YAC
clone. This YAC was used to screen a leaf cDNA library.
Studies on two related cDNAs are also reported.
Southern hybridizations revealed small multigene families
in tomato and other species. Complementation was
attempted with two cDNAs expressed from the 35s
promoter, and two plants transformed with one of the
cDNAs were found to be resistant. Thorough analysis
of these transformants is described. Sequence similarity
and differences in complexity were demonstrated
between the homologous L and M loci. Map-based
cloning is rapidly increasing in efficiency in part due to
the developments in the human genome program and in
part due to the efforts of plant geneticists seeking to
minimize the various brute-force steps involved.
Jones et al. (1994) described the isolation of the
tomato Cf-9 gene for resistance to Cladosporium fulvum
by transposon tagging. In this, effective positive
selection of U-9 mutants using transgenic plants
expressing the bacterial avirulence factor Avlf was

4386

Advances in Life Sciences 5(11), 2016

achieved. A Ds element linked to the 0-9 target was

activated by a stabilized AC element. 63 independent
mutants were generated, 37 of which seemed to result
from Ds insertion into 0-9. Hybridization revealed no
introns in U-9. Genomic Southern and northern blots
indicated the presence of a small multigene family of
related LRR sequences.

Causse, M., Rocher, J.P., Henry, A.M., Charcosset, A., Prioul,

J.L. and de Vienne, D. 1995. Genetic relationship between
carbon metabolism and early growth in maize, with emphasis
on the key enzyme lock. Mol. Breed., 1: 259: 272.

The single gene approach to deal with the plant

resistance to diseases is already reaching the end of its
short life, and a holistic approach is seen as the natural
next step which is nothing but horizontal resistance
(quantitative resistance) with greater amount of
complexity (Flor, 1971). Quantitative resistance, with
its continuous distribution, intermediate heritability and
environmental sensitivity has frequently been considered
as a polygenic character (Geiger and Heun, 1989). The
pace of understanding quantitative resistance to various
diseases is more when compared to the same with
regard to insects. The major hurdle in understanding
the quantitative resistance is the non-availability of
reliable screening methods and tediousness and
complexity in the available methods. Moreover, most
of the quantitative resistance to diseases differ in nature
according to the host age, developmental biology,
assessing methods and pathogen biology. No doubt that
mapping of QTLs and candidate genes has enormous
potential to expand our understanding about the
complexity in resistance to diseases.

Dodds, P.N., Lawrence, G.J. and Ellis, J.G. 2001. Contrasting

modes of evolution acting on the complex N locus for rust
resistance in flax. Plant J., 27: 439-453.

LITERATURE CITED
Antanaviciute, L., Urbanovski, N.S., Harrison, N., McLeary, K.J.,
Simpson, D.W., Wilson, F., Sargent, D.J. and Harrison, R.J.
2015. Mapping QTL associated with Verticillium dahliae
resistance in the cultivated strawberry (Fragaria ananassa).
Horticulture Research, 2: 1-8.
Arnold, M.H., Innes, N.L. and Brown, S.J. 1976. Resistance
breeding. In: Agricultural research for development. (eds M.H.
Arnold). The Namulonge contribution. Cambridge University
Press, Cambridge. pp. 175-195.
Bent, A.F., Kunkel, B.N., Dahlbeck, D., Brown, K.L., Schmidt,
R., Giraudat, J., Leung, J. and Staskawicz, B.J. 1994. RPS2 of
Arabidopsis thaliana: leucine rich repeat class of plant
resistance genes. Science. 265: 1856-1860.
Bent, A.F. 1996. Plant disease resistance genes: function meets
structure. Plant cell, 8: 1757-1771.
Bowles, D.J. 1990. Defense related proteins in higher plants.
Annual Review of Biochemistry, 59: 873-907.
Bubeck, D.M., Goddman, M.M., Beavis, W.D. and Grant, D.
1993. Quantitative trait loci controlling grey leaf spot in maize.
Crop Science, 33: 838-847.
Byrne, P.F., McMullen, M.D., Snook, M.E., Musket, T.A.,
Theuri, J.M., Widstrom, N.W., Wiseman, B.R. and Coe, E.H.
1996. Quantitative trait loci and metabolic pathways: Genetic
control of the concentration of maysin, a corn ear worm
resistance factor in maize silks. Proc. Natl. Acad. Sci., USA.
93: 8820-8825.

Crute, I.R. 1985. The genetic basis of relationships between

microbial parasites and their hosts. In: Mechanisms of
resistance in plant diseases. (eds R.S.S. Fraser). Kluwer
Academic Press, The Netherlands. pp. 80-142.

Emma, E.G., Olusola, O.S. and Simeon, O.K. 2003. The molecular
initiation and subsequent acquisition of disease resistance in
plants. African Journal of Biotechnology. 2(2): 26-32.
Faris, J.D., Anderson, J.A., Francl, L.J. and Jordahl, J.G. 1997.
RFLP mapping of resistance to chlorosis induction by
Pyrenophora graminea in wheat. Theor Appl Genet., 94: 98103.
Flor, H.H. 1956. The complementary genetic systems in flax and
flax rust. Adv. Genetics., 8: 29-54.
Flor, H.H. 1971. Current status of gene for gene concept. Annu.
Rev. Phytopathol., 9: 275-296.
Geiger, H.H. and Heun, M. 1989. Genetics of quantitative
resistance to fungal diseases. Annu. Rev. Phytopathol., 27:
317-341.
Goldman, I.L., Rocheford, T.R. and Dudley, J.W. 1993.
Quantitative trait loci influencing protein and starch
concentration in the Illinois long term selection maize strains.
Theor. Appl. Genet., 87: 217-224.
Grant, M.R., Godiard, L., Straube, E., Ashfield, T., Lewald, J.,
Satller, A., Innes, R.W. and Dangl, J.L. 1995. Structure of
Arabidopsis RPM1 gene enabling dual specificity disease
resistance. Science. 269: 843-846.
Grube, R.C., Radwanski, E.R. and Jahn, M. 2000. Comparative
genetics of disease resistance within the Solanaceae. Genetics.
155: 873-887.
Gururani, M.A., Venkatesh, J., Upadhyaya, C.P., Nookaraju, A.,
Pandey, S.K. and Park, S.W. 2012. Plant disease resistance
genes: current status and future directions. Physiological and
Molecular Plant Pathology. 78: 5165.
Hammond-Kosack, K.E. and Jones, J.D.G. 1996. Resistance gene
dependent plant defense response. Plant Cell. 8: 1773-1791.
Heun, M. 1992. Mapping quantitative powdery mildew resistance
of barley using a restriction fragment length polymorphism
map. Genome. 35:1019-1025.
Johal, G.S., Briggs, S.P. 1992. Reductase activity encoded by the
HM1 disease resistance gene in maize. Science. 258 (5084):
985-997.
Jones, D.A., Thomas, C.M., Hammond-Kosack, K.F., BalintKurti, P.J. and Jones, J.D.G. 1994. Isolation of tomato Cf9
gene for resistance to Cladosporium fulvum by transposon
tagging. Science. 266: 985-7.
Lawrence, G.J., Finnegan, E.J., Ayliffe, M.A. and Ellis, J.G. 1995.
Cloning a rust resistance gene in flax. Plant Cell. 7: 11951206.
Larkan, N.J., Lydiate, D.J., Parkin, I.A.P., Nelson, M.N., Epp,
D.J., Cowling, W.A., Rimmer, S.R. and Borhan, M.H. 2013.
The Brassica napus blackleg resistance gene LepR3 encodes a

PARTHASARATHY, et al., Insight in Mapping Quantitative Trait Loci Associated with Disease Resistance in Crops
receptor-like protein triggered by the Leptosphaeria maculans
effector AVRLM1. New Phytologist. 197: 595605.
Leonards-Shippers, C., Gieffers, W., Schafer, P.R.E., Knapp, S.J.,
Salamini, F. and Gebhardt. 1994. Quantitative resistance to
Phytophthora infestans in potato: a case study for QTL
mapping in an allogamous plant species. Genetics. 137: 6777.
Martin, G.B., Brommonschenkel, S.H., Chunwongse, J., Frary,
A., Ganal, M.W., Spiwey, R., Wu, T., Earle, E.D. and
Tanksley, S.D. 1993. Map based cloning of a protein kinase
gene conferring disease resistance in tomato. Science. 262:
1432-1436.
Meyers, B.C., Dickerman, A.W., Michelmore, R.W.,
Sivaramakrishnan, S., Sobral, B.W. and Young, N.D. 1999.
Plant disease resistance genes encode members of an ancient
and diverse protein family within the nucleotide binding
superfamily. Plant J. 20: 317-332.
Michelmore, R. 1995a. Molecular approaches to manipulation of
disease resistance genes. Annu. Rev. Phytopathol., 15: 393427.

4387

press, Cold Spring Harbour, New York. pp 81-88.

Salmeron, J.M., Oldroyd, G.E., Rommens, C.M., Scoceld, S.R.,
Kim, H.S., Lavelle, D.T., Dahlbeck, D. and Staskawicz. 1996.
Tomato Prf is a member of the leucine-rich repeat class of
plant disease resistance genes and lies embedded within the
Pto kinase gene cluster. Cell. 86:123-133.
Song, W.Y., Wang, G.L., Chen, L.L., Kim, H.S., Pi, L.Y., Holsten,
T., Gardner, J., Wang, B., Zhai, W.X., Zhu, L.H., Fauquet, C.
and Ronald, P.C. 1995. A receptor kinase like protein encoded
by the rice disease resistance gene, Xa 21. Science. 270: 18041806.
Staskawicz, B.J., Ausubel, F.M., Backer, B.J., Ellis, J.B. and
Jones, J.D. 1995. Molecular genetics of plant disease
resistance. Science. 268: 661-667.
Steffenson, B.J., Hayes, P.M. and Kleinhofs, A. 1996. Genetics
of seedling and adult plant resistance to net blotch
(Pyrenophora teres f. teres) and spot blotch (Cochliobolus
sativus) in barley. Theor. Appl. Genet., 92: 552-558.
van der Plank, J.E. 1963. Plant diseases: epidemics and control.
Academic press. London. 349 p.

Michelmore, R. 1995b. Flood warning resistance gene unleashed.

Nature Genetics. 14: 376-378.

van der Plank, J.E. 1968 Disease resistance in plants. Academic

press. New York. 199 p.

Mindrinos, M., Katagiri, F., Yu, G. and Ausubel, F.M. 1994. The
Arabidopsis thaliana disease resistance gene RPS2 encodes a
protein containing a nucleotide-binding site and leucine rich
repeats. Cell. 78: 1089-1099.

van der Plank, J.E. 1982. Host pathogen interactions in plant

disease. Academic press. London. 210 p.

Naegele, R.P., Ashrafi, H., Hill, T.A., Reyes, S., Chin-Wo, A., Van
Deynze, E. and Hausbeck, M.K. 2014. QTL mapping of
fruit rot resistance to the plant pathogen Phytophthora capsici
in a recombinant inbred line Capsicum annuum population.
Phytopathology. 104 (5): 479-483.
Peechioni, N., Faccioli, P., Toubia-Rahme, H., Vale, G. and Terzi,
V. 1996. Quantitative resistance to barley leaf stripe
(Pyrenophora graminea) is dominated by one major locus.
Theor. Appl. Genet., 93: 97-101.

Wang, G., Mackill, D., Bonmann, J.M., McCouch, S.R. and

Nelson. R.J. 1994. RFLP mapping of genes conferring
complete and partial resistance to blast disease in a durably
resistant rice cultivar. Genetics. 136: 1421-1434.
Wang, G., Fiers, M., Ellendorff, U., Wang, Z., de Wit, P.G.J.M.,
Angenent, G.C., Thomma, B.P.H.J. 2010. The diverse roles
of extracellular Leucine-Rich Repeat-containing ReceptorLike Proteins in plants. Critical Reviews in Plant Science. 29:
285299.

Pryor, T. and Ellis, J. 1993. The genetic complexity of fungal

resistance genes in plants. Adv. Plant Pathol., 10: 281-305.

Whitham. S., Dinesh Kumar, S.P., Choi, D., Hehl, R., Corr, C.
and Baker, B. 1994. The product of tobacco mosiac virus
resistance gene N: similarity to Toll and the interleuhkin 1
receptor. Cell. 78: 1101-1115.

Richter, T.E. and Ronald, P.C. 2000. The evolution of disease

resistance genes. Plant Mol. Biol., 42: 195-204.

Young, N.D. 1996. QTL mapping and quantitative disease

resistance in plants. Annu. Rev. Phytopathol., 34: 479-501.

Ritter, E.T.D., Barone, A., Salamini, F. and Gebhardt, C. 1991.

RFLP mapping on potato chromosomes of two genes
controlling extreme resistance to Potato virus X (PVX). Mol.
Gene. Genet., 227: 81-85.

Young, N.D., Danesh, D., Menancio-Hautea, D. and Kumar, L.

1993. Mapping oligogenic resistance to powdery mildew in
mung bean with RFLPs. Theor. Appl. Genet., 87: 243-249.

Robertson, D.S. 1989. Understanding the relationship between

qualitative and quantitative genetics. In: Development and
Application of Molecular Markers to problems in plant
genetics (eds. T. Helentjaris and B. Burr). Cold Spring Harbour

Yu, Y.G., Buss, G.R. and Saghai Maroof, M.A. 1996. Isolation of
a super family of candidate disease resistance genes in soybean
based on the conserved nucleotide binding site. Proc. Natl.
Acad. Sci., USA 93: 11751-11756.
Yun, D.J., Bressan, R.A. and Hasegawa, P.M. 1997. Plant
antifungal proteins. Plant Breed. Rev., 14: 39-88.
Received on 11-05-2016

Accepted on 16-05-2016