Accepted Manuscript

Title: Mechanisms of quantitative disease resistance in plants

Author: Elizabeth French Bong-Suk Kim Anjali S.

Iyer-Pascuzzi

PII: S1084-9521(16)30141-0
DOI: http://dx.doi.org/doi:10.1016/j.semcdb.2016.05.015
Reference: YSCDB 2040

To appear in: Seminars in Cell & Developmental Biology

Received date: 23-2-2016

Revised date: 14-5-2016
Accepted date: 18-5-2016

Please cite this article as: French Elizabeth, Kim Bong-Suk, Iyer-Pascuzzi Anjali
S.Mechanisms of quantitative disease resistance in plants.Seminars in Cell and
Developmental Biology http://dx.doi.org/10.1016/j.semcdb.2016.05.015

This is a PDF file of an unedited manuscript that has been accepted for publication.
As a service to our customers we are providing this early version of the manuscript.
The manuscript will undergo copyediting, typesetting, and review of the resulting proof
before it is published in its final form. Please note that during the production process
errors may be discovered which could affect the content, and all legal disclaimers that
apply to the journal pertain.
 Mechanisms of quantitative disease resistance in plants
Elizabeth French, Bong-Suk Kim, and Anjali S. Iyer-Pascuzzi
Department of Botany and Plant Pathology, Purdue University, West Lafayette IN 47907

1
Abstract: Quantitative disease resistance (QDR) causes the reduction, but not absence, of
disease, and is a major type of disease resistance for many crop species. QDR results in a
continuous distribution of disease scores across a segregating population, and is typically due to
many genes with small effects. It may also be a source of durable resistance. The past decade has
seen significant progress in cloning genes underlying QDR. In this review, we focus on these
recently cloned genes and identify new themes of QDR emerging from these studies.

Keywords: Plant immunity, quantitative disease resistance, durable resistance, partial resistance,
spatio-temporal disease resistance, crop plants

2
1. Introduction
1.1 What is Quantitative Disease Resistance?
Plant disease resistance responses are complex and multilayered (reviewed in [1 -5]).
Historically, plant immunity has been divided broadly into two categories: incomplete resistance
provided by quantitative disease resistance (QDR) genes and complete resistance mediated by
resistance (R) proteins [1-3]. More recently, recognition of the role of microbial elicitors and
their host receptors led to the idea of microbial triggered immunity (MTI). The zig-zag model
of plant immunity accounts for the latter two categories, incorporating general pathogen elicitors,
their host receptors, and R-protein mediated resistance into a single model [4]. In this model, one
of the first lines of plant defense is recognition of microbial elicitors such as flagellin and chitin.
These Microbe Associated Molecular Patterns (MAMPs) are recognized by pattern recognition
receptors (PRR) at the cell surface that initiate a signaling cascade leading to generally weak
defense responses and MTI. Some pathogens can overcome this level of resistance by secreting
effector proteins that interfere with host metabolism and act to promote pathogen virulence.
Plants have evolved to recognize and defend themselves against such effectors; this immunity is
known as Effector-Triggered Immunity, or ETI, and typically leads to full resistance with no
disease symptoms. Plant proteins that recognize effectors are termed R proteins, and are
frequently in a class of proteins known as Nucleotide Binding Site Leucine Rich Receptors
(NBS-LRRs).
Although the zig-zag model has been extremely useful for thinking about two seemingly
separate parts of plant immunity - MTI and ETI - the model is limited largely to describing
interactions between hosts and biotrophic pathogens. It is less suitable for understanding host-
necrotrophic interactions, and does not (by design) account for the complexities of host-pathogen
interactions that lead to a wide range of host immune responses [5, 6]. The Invasion Model,
which describes plant immunity as a surveillance system that continually evolves to detect
microbial invasion, may be more useful for describing the nuanced layers of plant defense [6]. In
this model, plants recognize invasion patterns (IP) that are derived from microbes (such as
MAMPS or effectors) or endogenous elicitors that result from infection, such as Damage
Associated Molecular Patterns or DAMPs. IPs are recognized by IP triggered receptors
(IPTRs). MTI and ETI are viewed less as strictly contrasting responses and instead as continuous
immune outputs resulting from variation between different IPs and IPTRs.
Such a model accounts for Quantitative Disease Resistance (QDR). QDR has been
traditionally recognized but is less well understood than MTI or ETI [6-8]. QDR refers to host
plant resistance that leads to a reduction in disease, but not the absence of disease [1, 2, 7]. As a
quantitative trait, QDR is controlled by multiple genes that can interact with the environment and
with each other. Recent work has shown however, that the cumulative effects of pyramiding
many QDR loci can result in high levels of resistance [8-11]. Phenotypically, QDR exhibits a
continuous distribution of resistance values that do not fit Mendelian segregation ratios [1, 7].
This is in contrast to a qualitative trait, in which the variation is typically due to differences at
one locus, and the effects of different alleles at the locus are large relative to the environment.
An important point is that a resistance phenotype can vary within a population for reasons not
due to genes controlling QDR [7]. For example, varying levels of resistance within a population
could result from the effects of one gene with low heritability or low penetrance [7].
Alternatively, a host population may contain a series of R genes that each provides complete
resistance against one strain of a pathogen. However, when infected with a highly complex

3
pathogen population, such a host population may exhibit a continuous distribution of resistance
[7]. Genetic analyses must be used to determine if observed variable levels of resistance are due
to QDR. Additionally, care must be taken with the phenotyping approach used for such analyses,
as this may affect the outcome. For example, the use of a 5-point scale for disease severity could
potentially make a continuous distribution of disease severity appear to be discrete and may
result in errant conclusions.
Recent work suggests that QDR can result from quantitative variation in the components
of either MTI or ETI [1, 2], as well as through completely different mechanisms ([1, 2] and
references in this review). This fits within the framework of the Invasion Model, and supports
the idea of plant immunity as a continuum with quantitative variation in both pathogenic elicitors
and host responses leading to a spectrum from disease to resistance [6]. Consistent with this,
tolerance the hosts ability to withstand high pathogen load with limited disease symptoms or
fitness cost appears to be a component of QDR in several pathosystems, including Arabidopsis
R. solanacearum [12], and Arabidopsis Pseudomonas syringae [13].
The potential mechanisms underlying QDR have frequently been deliberated [1-3, 7, 14].
Recent years have seen a significant increase in the genes cloned that contribute to QDR. In this
review we focus on these genes and discuss new insights into the mechanisms of QDR gained
from their functions. Although QDR may result from the pathogens ability to suppress
immunity (effector triggered susceptibility, [15]), our focus here is not on susceptibility alleles,
but on plant genes that lead to QDR. For reviews and papers that highlight more historical
concepts of QDR, the reader is directed to [1, 7, 14, 16].

1.2 How important is QDR?

If ETI offers complete resistance, why is there interest in the genes underlying QDR,
which provides only a decrease in disease? First, although ETI produces complete resistance,
since this resistance is due primarily to one R protein, pathogen effector proteins can evolve to
overcome the R protein and ETI-mediated resistance [17]. In contrast, because multiple genes
underlie QDR, the evolutionary pressure on pathogens is significantly decreased. QDR may
therefore be a good source of durable resistance (resistance that remains effective over a long
period of time even with wide crop cultivation). Indeed, several genes underlying QDR have
been used in breeding programs for more than half a century with no signs of increased pathogen
virulence [18, 19].
The second reason for interest in QDR is that ETI is most effective against biotrophic
pathogens. ETI frequently results in a cell death known as the hypersensitive response (HR). The
HR limits biotrophic pathogen growth and colonization and typically leads to full resistance
against these pathogens. However, necrotrophic pathogens, which feed on dead tissues, exploit
this cell death to increase their own virulence. In contrast to ETI, QDR provides an effective
means of control for both biotrophic and necrotrophic pathogens.
Another reason for interest in QDR is that many QDR loci are effective against multiple
races of a given pathogen, providing broad-spectrum resistance, or are effective against multiple
pathogens [18]. However, QDR loci involved in race or isolate-specific resistance are becoming
increasingly common [1, 2]. Such loci have been identified for resistance to tomato bacterial wilt
(Ralstonia solanacearum) [20]; vascular wilt in melon (Fusarium oxysporum) [21], stripe rust in
wheat (Puccinia striiformis f.sp. tritici) [22], powdery mildew in grape (Erysiphe necator) [23],
and barley leaf rust (Puccinia hordei) [24], among others. Isolate-specific QTL may represent
evidence for the minor-gene-for-minor-gene model of QDR, originally conceptualized by[16].

4
 Finally, QDR is effective against a wide range of microbe classes bacteria, fungal, viral
and nematodes and against pathogens that infect different parts or different developmental
stages of the plant [1].
Cloning loci involved in QDR has proven challenging, in part because of the small effect
of many QDR loci and the difficulty in consistently phenotyping disease traits across a variety of
environments [1, 25]. However, there has been tremendous progress in the last few years in
cloning genes underlying quantitative disease resistance (Table 1). In this review, we discuss
potential mechanisms underlying QDR revealed from these recently cloned genes. Several new
themes are becoming apparent, including spatio-temporal resistance and the importance of
resistance gene expression. Additionally, new work has highlighted the importance of weak or
variant NBS-LRRs in QDR.

2. Recent insight into QDR mechanisms from cloned QDR loci

2.1. Spatio-temporal and environment-specific resistance: QDR results from being at the right
place at the right time in the right environment.
The importance of plant development in plant defense is well recognized [26]. However,
recent work, described below, has demonstrated the importance of development in QDR. This
work suggests that spatio-temporal resistance resistance expressed at the right time and at the
right place - is a theme of QDR. Several recently cloned QDR loci show expression at a specific
developmental (or ontogenic) stage (Lr34 [18] and ZmWAK [27]) or in a specific environment
(Yr36) [28]. As spatio-temporal resistance would lower pathogen selection pressure, it may also
be a mechanism for durable resistance.

2.1.1 Developmental stage-specific expression: ZmWAK

Although a large number of QDR loci have been mapped in maize to a wide range of
pathogens [29], very few have been cloned. Zuo et al. (2015) [27] used map-based cloning to
identify the causal gene underlying the quantitative resistance locus qHSR. qHSR1 provides
resistance to Sporisorium reilianum, a soil-borne fungus and the causal agent of head smut in
maize. ZmWAK encodes a receptor-like protein with a domain characteristic of wall-associated
kinases (WAKs), and localizes to the plasma membrane in onion epidermal cells and maize
protoplasts. Experiments with chimeric receptors demonstrated that the kinase activity of
ZmWAK is necessary for its signaling function.
Expression of ZmWAK is induced 24 hours after infection with S. reilianum. The soil-
borne pathogen infects maize seedlings through the root [30], and moves shootward to eventually
invade the shoot meristem [31]. In a susceptible maize plant the fungus travels from the
mesocotyl upwards towards the coleoptile, resulting in an uneven fungal distribution with higher
levels in the mesocotyl. However, in maize lines expressing the ZmWAK gene, the fungus is
largely prevented from moving farther than the mesocotyl, resulting in significantly reduced
levels of fungal growth in the coleoptile. Not only is expression of ZmWAK induced after
infection, but it is induced primarily in the mesocotyl. S. reilianum colonizes the phloem of the
mesocotyl, and ZmWAK expression appears to be primarily in the phloem and xylem
parenchyma cells surrounding the phloem. Investigation of the ZmWAK genomic sequence in
additional susceptible lines identified eight different amino acid substitutions, none of which
were predicted to lead to altered function of ZmWAK. However, mesocotyl expression of
ZmWAK, but not that of roots or leaves, was reduced in these susceptible lines, suggesting that
resistance is due to increased expression of ZmWAK in the mesocotyl. Together, these data

5
suggest that in resistant lines, induction of ZmWAK specifically in the mesocotyl results in
resistance signaling that reduces fungal infection [27]. It is intriguing to speculate how many
other genes underlying QDR result from such tightly controlled spatiotemporal gene expression.

2.1.2 Developmental-stage specific expression 2: Lr34

The wheat Lr34 QTL encodes a putative ABC transporter that confers resistance to
multiple diseases, including fungal stripe rust (Puccinia striiformis), leaf rust (Puccinia triticina),
stem rust (Puccinia graminis), and powdery mildew (Blumeria graminis) [18]. Lr34 has
remained a durable source of resistance to these fungal pathogens for over 50 years. Lr34 results
in partial adult plant resistance at 20C and seedling resistance at low temperature. The gene is
expressed during the grain-filling stage of wheat in the uppermost (or flag) leaf of wheat [14],
and when pyramided with other adult wheat resistance genes provides near-complete adult
resistance levels.
Map-based cloning and mutant analysis of Lr34 demonstrated that Lr34 is identical to the
QTL Yr18 (controlling adult resistance to stripe rust), and Pm38 (controlling resistance to
powdery mildew) [18]. Sequencing of the Lr34 genomic region in resistant and susceptible
wheat cultivars identified three differences, two of which were in an exon that encoded the
transmembrane region of the protein. These sequence differences may lead to changes in the
conformation of the protein and alter substrate specificity of the transporter. No sequence
differences were observed in the promoter region, consistent with the fact that no differences in
expression were identified between the resistant and susceptible lines [18].
How Lr34 provides resistance is not well understood, but leaf senescence processes may
play a role [18]. Alternatively, as Lr34 belongs to the pleiotropic drug resistance subfamily of
ABC transporters, a possible mechanism for Lr34-mediated resistance may be the transport of
toxic substances out of the plant cell [18]. In Arabidopsis, the PEN3/PDR8 gene, encoding a
pleiotropic drug resistance transporter, contributes to non-host resistance to barley powdery
mildew [32]. It will be intriguing to discover whether similar mechanisms operate in non-host
resistance and durable resistance.
Attempts to introduce Lr34 into other crop species have shown that it can provide broad-
spectrum QDR to a number of host-specific diseases including rice blast (Magnaporthe oryzae)
[33], barley leaf rust (Puccinia hordei), stem rust (Puccinia graminis f. sp. tritici) and barley
powdery mildew (Blumeria graminis f. sp. hordei) [34,35].

2.1.3 Environment-specific expression of QDR: Yr36

In wheat, the Yr36 locus for partial resistance to wheat stripe rust (Puccinia striiformis)
encodes WHEAT KINASE-START 1 (WKS1), a novel protein consisting of a kinase and a START
domain [28]. Yr36 is effective in adult wheat plants at high temperatures (25 to 35C) but
susceptible at lower temperature (~15C). START domains in humans play a role in lipid-
binding and metabolism [36], but their function in plant cells is not well characterized. The
kinase domain in WKS1 has similarity to several WAK-like kinases in Arabidopsis, but WKS1 is
likely to function somewhat differently as it does not have the extracellular receptor domain or
transmembrane domain typical of WAKs. Additional research is needed to understand how
WKS1 functions in partial resistance to leaf rust. The identification of two completely different
genes underlying QTL for resistance to wheat stripe rust highlights the diversity of mechanisms
underlying QDR, even for the same pathogen in the same species [28].

6
2.2 QDR results from high expression levels of genes with roles in resistance: Rhg1 and RKS1

2.2.1 Rhg1 and copy number variation

The soybean Rhg1 locus provides QDR to the soybean cyst nematode (SCN) pathogen
Heterodera glycines [37]. High-resolution mapping narrowed the region contained Rhg1 to a 67
kb interval containing 11 predicted genes. Silencing any of three dissimilar genes in the interval
a predicted amino acid transporter, an -SNAP protein that may be involved in membrane
trafficking, and a poorly characterized protein with a wound-inducible 12 region led to
decreases in resistance. Overexpression of any one of these genes did not lead to enhanced
resistance, but overexpression of all three genes was necessary to achieve resistance.
Investigation of the genomic region in a resistant line revealed that a 31.2 kb genomic segment
encoding these three genes was present in multiple copies. This genomic repeat region was
present in multiple resistance lines but not in any of four susceptible lines. qPCR revealed that
each of these three genes was more highly expressed in roots of SCN-resistant lines than in
susceptible lines. Together, these results suggest that copy number variation leading to increased
transcript level for three different genes underlies the Rhg1 locus for SCN resistance [37].

2.2.2 Gene expression differences: RKS1

Xanthomonas campestris pv. campestris (Xcc) is the causal agent of black rot disease,
one of the most economically destructive diseases of crucifers. The major QTL QRX3
(Quantitative Resistance to Xcc568) is responsible for over 50% of the variation in resistance to
multiple strains of Xcc and was recently shown to encode the gene RKS1 (Resistance-related
KinaSe1) [38]. Although BLAST analysis showed high similarity between RKS1 and protein
kinases, inspection of the RKS1 sequence revealed the predicted protein is missing residues
critical for kinase catalytic function. Consistent with this, no kinase activity was detected for
RKS1. RKS1 is thus referred to as an atypical or pseudokinase. Only one amino acid difference
resulting from one SNP in the coding region was found for the R and S alleles from Col-5 and
Kas-1, respectively. Xcc first infects leaves, and the authors demonstrated that RKS1 inhibits
pathogen colonization in leaf vasculature. In line with this, transcript analysis identified a long
RKS1 transcript (RKS1-L) expressed more than 235 times greater in leaves of resistant plants
compared to leaves of susceptible plants, in which a short (RKS1-S) transcript was more highly
expressed. A general correlation was observed between higher levels of resistance and higher
levels of leaf expression of RKS1-L, indicating that transcript abundance in leaves may be one
element of resistance. Analysis of RKS1 expression in multiple Arabidopsis accessions showed
that resistance was associated with a higher level of RKS1 expression, further demonstrating the
importance of gene expression as the basis for QXR3 resistance [38].
In addition to Rhg1 and RKS1, expression levels of genes in the Germin-Like Protein
(GLP) family may underlie QDR to both rice blast (Magnaporthe oryzae) and sheath blight
(Rhizoctonia solani) in rice [39].

2.3. QDR results from Wall Associated Kinases (WAKs)

2.3.1 The ZmWAK gene for resistance to maize head smut, is discussed above and is one
example of WAKs that underlie QDR. An additional QTL encoding a wall-associated receptor
like kinase was recently cloned from maize [40]. Htn1 encodes ZmWAK-RLK1 and provides
quantitative resistance to the hemibiotrophic fungus Exserohilum turcicum, causal agent of

7
Northern Corn Leaf Blight (NCLB). Wall-associated receptor like kinases have an extracellular
elicitor binding receptor domain, a transmembrane domain, and an intracellular kinase signaling
domain. Sequencing of the resistant allele from maize cultivar RP1Htn1 and the susceptible
allele from cultivar RP1 revealed few amino acid changes in the kinase domain of the predicted
protein, which was over 98% identical between the resistant and susceptible parents. In contrast,
the extracellular domain was extremely divergent, with 46 amino acid changes, 19 amino acid
deletions, and 2 amino acid insertions in the predicted sequence of the susceptible protein
compared to the resistant. This resulted in less than 80% sequence identity in the extracellular
domain of the resistant and susceptible predicted proteins. In maize reference line B73, the
closest homolog to Htn1 was well conserved in the kinase domain but again shared only weak
conservation with Htn1 in the extracellular domain, while the rice homolog had 83% identity in
the kinase domain but only 49% in the extracellular domain. Pathogen infection did not induce
expression of Htn1 in either the resistant or susceptible parent. These data indicate that Htn1
mediated resistance is likely due to differences in the extracellular domain of the protein [40].

2.3.2 RFO/WAKL22
In a study to find QTL for disease resistance to Fusarium oxysporum in Arabidopsis,
Ausubel and Diener (2005) [41] found six loci. The major QTL RFO1 was found to encode a
protein identical to WAKL22, a wall-associated kinase-like protein containing an RLK domain
structurally similar to other identified R proteins Xa21 and Xa26 in rice. RFO1/WAKL22
provided stronger resistance when RFO2, RFO4 or RFO6 loci were present, suggesting an
interactive effect that may result from increases in gene expression of RFO1/WAKL22.
The diversity and prevalence of wall associated receptor-like kinases in monocots,
combined with the recent findings that they underlie three resistance QTL to different fungal
pathogens (ZmWAK, Htn1, RFO) suggests the possibility that they may be a common mechanism
underlying QDR.
This idea is intriguing considering that another wall associated kinase, Arabidopsis
WAK1, was recently shown to be a receptor for oligogalacturonides, which are DAMPs resulting
from the breakdown of the pectin polysaccharide homogalacturonan [42]. DAMPs are
endogenous danger signals caused by damaged cells or tissues. Recognition of these
endogenous invasion patterns by host receptors leads to plant perception of self-damage, and
provokes an immune response. However, whether WAK1 or other DAMP receptors such as
DORN1, a kinase that recognizes extracellular ATP [43], are components of QDR, remains to be
established.

2.4 QDR results from altered forms of NBS-LRR R genes

Several studies have shown that NBS-LRR genes act as the causal loci underlying
quantitative disease resistance. In some cases, these are altered or weak forms of the genes [44,
45], while in other studies the same gene(s) appear to be involved in multiple types of resistance
[46].

2.4.1. The R gene pair RRS1/RPS4.

To identify non-RKS1 dependent genes underlying QDR to Xcc, Debieu et al. [46] used nested
association mapping. They identified two regions: one containing the gene At5g22540, the other
containing the R gene pair RRS1/RPS4. The RRS1/RPS4 gene pair has been previously
characterized for its role in effector-triggered immunity (ETI) to strains of Pseudomonas

8
syringae secreting the effector AvrRps4 [47-49] the soil-borne pathogen Ralstonia solanacearum
secreting the effector PopP2 [47-49], and is involved in resistance to the fungal pathogen
Colletotrichum higginsianum [47]. Since RPS4 acts in tandem with RRS1, the authors tested
whether single rps4 or rrs1 mutants, or the double rps4 rrs1 mutant, showed increased
susceptibility to Xcc. All three mutants showed increased bacterial colonization and disease
lesion index after inoculation with strains of race 6 Xcc, but not other races, suggesting that the
RRS1/RPS4 gene pair may function in QDR to Xcc [46].
Interestingly, RRS1 PopP2 interaction is required for tolerance to strain BCCF402 of R.
solanacearum in ecotype Kil-0 of Arabidopsis [12]. The Kil-0 ecotype allows high levels of
pathogen colonization without bacterial wilt symptoms, consistent with the idea that pathogen
tolerance represents another facet of QDR. It is currently unclear whether RPS4 functions in
tolerance in the R. solanacearum-Kil-0 pathosystem.
Increasingly, it appears that QDR spans a wide range of mechanisms. For example, the
same gene(s) may contribute to both QDR and ETI, possibly dependent on genetic background
of both host and pathogen strain. For example, in the R. solanacearum- Arabidopsis interaction,
ETI to R. solanacearum strain GMI1000 is found in the Arabidopsis accession Nd-1, but
tolerance is observed in the Kil-0 ecotype to a different R. solanacearum strain. Although not
part of a R gene pair, the R gene RPM1 also has a role in both tolerance and ETI (Roux et al.
2010), with host genetic background and initial inoculum density influencing the defense
outcome.

2.4.2. Poly-allelic variation at R gene loci underlying QDR: Pi35 and durable resistance
The rice Magnaporthe oryzae pathosystem has provided multiple insights into
quantitative disease resistance. M. orzyae is the causal agent of rice blast, and more than 90
genes from a wide range of rice cultivars have been implicated in either qualitative, gene-for-
gene resistance or QDR. Nearly all of the race-specific, gene-for-gene blast R genes encode
NBS-LRRs, but typical for QDR, blast resistance genes underlying this phenomenon appear to
be different. The Pi35 QTL for blast resistance has been used in Japan since the early 1960s, and
has been a durable source of blast resistance [45]. Recent work by Fukuoka et al. (2014) [45]
showed that Pi35 encodes a different allele of Pish, a NBS-LRR gene that had already been
implicated in race-specific qualitative resistance to blast. Unlike Pish, which causes an HR-
induced resistance to the M. oryzae isolate Kyu77-07A, the Pi35 allele provides moderate levels
of resistance against multiple races of M. oryzae, and results in smaller lesion size, but does not
cause a HR [45]. The genomic sequences of Pish and Pi35 differ both in the NBS and LRR
domain. Chimeric proteins with the NBS and LRR domains from either Pish or Pi35 (NBS/Pish
LRR/Pi35 or NBS/Pi35-LRR/Pish), showed that much of the functional difference between Pish
and Pi35 is due to changes in the LRR region of the encoded protein. The chimeric protein
NBS/Pi35-LRR/Pish lost the QTL-mediated resistance of the wild-type Pi35 protein, and had
similar susceptibility to a virulent isolate as the wild-type Pish protein. Thus the difference
between race-specific, qualitative resistance and QTL-mediated resistance was due to differences
in two alleles at the same locus [45]. This work demonstrates that allelic differences at the same
locus can be responsible for two different types of resistance phenomena and shows the close
linkage of gene-for-gene and quantitative disease resistance.

2.4.3. The defeated or Weak R gene: Xa4 and bacterial blight of rice

9
 The concept of the defeated R gene, in which the resistance provided by an R gene has
been overcome by a new strain of its respective pathogen, but the gene continues to provide a
reduced level of resistance against the pathogen, has frequently been considered as a basis for
QDR [1]. One example of a defeated R gene is the rice bacterial blight disease resistance gene
Xa4. In a study to examine the genetic components of resistance to multiple strains of
Xanthomonas oryzae pv. oryzae (Xoo), Li et al., (1999) [44] screened a RIL population in which
one of the parents contained the dominant Xa4 allele, a well-characterized R gene that had been
overcome by the CR6 Xoo strain with a mutant avrXa4 locus. The group found a number of
QDR loci against the strains studied; most interestingly that against the CR6 strain, Xa4 acts as a
recessive QDR locus. As a QTL, Xa4 provides about 50% of the level of resistance that it
provided as a major R gene. Many of the QTL discovered in this study map to similar locations
as known dominant R genes. Additional defeated R genes that may contribute to QDR include
those in the wheat powdery mildew [50] and wheat - stem rust pathosystems [51]. Together,
these results suggest that some QTL for QDR may be the same genes as major dominant R
genes, but encode a weaker allele that leads to residual resistance [44].

2.5. Pattern recognition receptors (PRRs) as a basis for QDR

PRRs, the receptors that form the first line of defense in basal resistance or MTI, may
also play a role in quantitative resistance. Levels of FLS2 (Flagellin Sensing 2), the PRR that
recognizes flg22 (bacterial flagellin) vary quantitatively in different ecotypes of Arabidopsis and
close relatives. Levels of flg22 binding in each genotype also varied and correlated positively
with the amount of FLS2 present. Increasing levels of flg22 ligand binding negatively correlated
with P. syringae proliferation in Arabidopsis, suggesting a QDR response [52]. Moreover,
Forsyth et al., (2010) [53] identified FLS2 as a QTL governing QDR in non-host resistance
against P. syringae pv. phaseolica in an Arabidopsis RIL population.
Further evidence for the activity of PRRs in QDR comes from an increase in resistance
resulting from the cross-family transfer of PRRs. Lacombe et al., (2010) [54] introduced EFR
(Elongation Factor Tu Receptor), the PRR exclusive to Brassicaceae that recognizes bacterial
EF-Tu, into Nicotiana benthamiana and tomato (Solanum lycopersicum). They found that EFR
conferred broad-spectrum quantitative resistance to both Ralstonia solanacearum (bacterial wilt)
and Xanthomonas perforans (bacterial spot). Similarly, the expression of EFR in rice conferred
resistance to weakly virulent strains of Xanthomonas oryzae pv. oryzae (bacterial blight), though
the resistance was overcome by highly virulent strains, suggesting that EFR expression induced
MTI in the transgenic plants [55]. Whether other PRRs, such as the chitin-binding receptors
LYK5 [56] and CERK1 [57-59], have roles in QDR remains to be established.

2.6 QDR resulting from loss-of-function susceptibility allele: Pi21

Rice lines carrying pi21, which provides QDR against rice blast (M. oryzae), have been
used as a form of durable blast resistance to multiple blast races for over a century in Japan [19].
In lines with pi21 resistance, the pathogen can enter the cell, but cannot move to the adjacent
cell, and the first signs of a HR - cytoplasmic granules - are observed at 96 hours. Resistance in
these lines therefore seems to take a little longer than in lines with true gene-for-gene resistance
[15]. High-resolution map-based cloning delimited the pi21 allele to a single gene encoding a
proline-rich protein that may have a role in metal transport [19]. Transformation of the resistant
allele into a S cultivar did not restore resistance to the cultivar, yet transformation of the S allele
into a R background increased susceptibility. This suggests that the Pi21 allele is a susceptibility

10
allele and the recessive pi21 allele is a loss-of-function mutation. Of the 12 different haplotypes
observed at the Pi21 locus in a variety of rice cultivars, only that with a large deletion in the
proline consensus motif (PxxPxxP) was resistant. Since this motif is part of the protein-protein
interaction domain, it is tempting to speculate that perhaps the loss of this domain renders the
resistant protein unable to interact with a pathogen virulence factor, leading to resistance [19].

2.7 Variation in host metabolism as the basis for QDR

One mechanism underlying QDR may be genes with roles in host metabolism. We
highlight one example below.

2.7.1 Rhg4: Supporting a role for primary metabolism in QDR, the soybean Rhg4 gene
underlying QDR to the soybean nematode (Heterodera glycines) pathogen encodes a serine
hydroxymethyltransferase (SHMT) [60]. SHMT enzymes play major roles in folate-dependent
one-carbon (C1) metabolism [61] and are well conserved across biological kingdoms [62]. C1
metabolism is crucial to organisms, as it involves the generation, interconversion and transfer of
C1 groups [62, 63]. SHMT catalyzes the reversible reaction of serine and tetrahydrofolate (THF)
to glycine and 5,10-methylene THF, and is a major entry point for folate-dependent metabolism
[62, 63]. One-carbon metabolism is important for the development of nematode feeding cells
(syncytia) in plant roots [64, 65], and thus disturbing folate metabolism may lead to detrimental
effects on nematode life cycle. Five nucleotide differences were identified in the genomic
sequences from the resistant and susceptible lines used for map-based cloning of Rhg4. Two of
these resulted in an amino acid change. The SHMT enzyme from each of the resistant and
susceptible parents was able to complement an E. coli glycine auxotroph, suggesting that both
are functional as SHMT enzymes. Although it is not clear exactly how the amino acid change
leads to resistance, kinetic studies showed that the resistant and susceptible SHMT proteins have
different kinetic properties. This may result in an altered or new function in planta that leads to
resistance [60].
In addition to Rhg4, several studies have shown that camalexin, a secondary metabolite
derived from tryptophan, has a major role in QDR against multiple pathogens in Arabidopsis [66
- 69].

3. Pyramiding genes leads to increased QDR

One of the major goals in plant pathology is sustainable, durable disease resistance. This
is both difficult to achieve and to assess, as durability is not easy to measure in a short period of
time. Further, examining the resistance mediated by different QTL over several years is
hampered if these QTL are in different genetic backgrounds, as the effect of a QDR locus
depends on its genetic background. For example, a resistance QTL may have a more significant
effect when introgressed or transformed into a highly susceptible background.
Many reports have shown the value of pyramiding multiple loci for QDR to a range of
pathogens [8-11, 70-74]. We highlight two examples here. Pyramiding one or two-gene
combinations of three rice blast QDR genes, pi21, Pi34, and Pi35, revealed two major resistance
phenotypes [10]: Either the combination of two resistance QDR genes was stronger than either
gene alone, or, more commonly, the combination of two resistance QDR genes gave a level of
resistance similar to that of the most effective resistance gene in the pair. The authors suggest
that one reason for the latter may be cell-type or tissue-type specific expression of a given

11
resistance gene. Given that spatio-temporal resistance gene expression is one mechanism of
QDR, this is an interesting hypothesis for further investigation.
Recently, Fukuoka et al. 2015 [8], methodically tested the blast resistance provided by
four independent QTL in rice by introgressing different combinations of these QTL into the same
genetic background. They show that multiple, different QTL combinations within the same
genetic background provide increased levels of resistance compared to any individual QTL
alone, and that there is a positive correlation between the amount of resistance QTL in a given
genetic background and resistance levels. Rice lines containing four Blast resistance QTL allow
M. oryzae penetration into rice cells, but do not allow further fungal development. The authors
speculate that this may reduce selection pressure on the pathogen, and may ultimately lead to
longer-lasting durable resistance.

4. Conclusions
The recent cloning of several genes underlying QDR has made it clear that many different types
of genes and mechanisms lead to QDR. Indeed, QDR fits well within the idea of plant immunity
as a monitoring system to detect many different invasion patterns that can lead to a range of
defense phenotypes [6]. The cloned genes underlying QDR now offer the prospect to investigate
the relationship between QDR and other types of resistance. For example, several recently
cloned QDR loci have been effective in the field for decades, providing the opportunity to dissect
durable resistance and its relationship to QDR. Given the wide range of genes controlling QDR
among them kinases, metabolic enzymes, transporters, and altered NBS-LRRs, it is likely that as
additional genes underlying QDR are cloned, new mechanisms will become apparent. The
valuable insights gained from these studies will enhance our ability to effectively use
quantitative disease resistance in crop improvement.

Acknowledgements
Our work is supported by Purdue Universitys Center for Global Food Security, and Purdue
University start-up funds. EF is supported by a NSF Graduate Research Fellowship, grant
number DGE-1333468.

12
References

[1] Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ. Shades of gray: the world of
quantitative disease resistance. Trends in Plant Sci 2009; 14:21-29.
[2] Roux F, Voisin D, Badet T, Balague C, Barlet X, Huard-Chauveau et al. Resistance to
phytopathogens e tutti quanti: placing plant quantitative disease resistance on the map. Mol Plant
Pathol 2014; 15:427-432.
[3] Kou Y, Wang S. Broad-spectrum and durability: understanding of quantitative disease
resistance. Curr Opin Plant Biol 2010; 13:181-185.
[4] Jones JD, Dangl JL. The plant immune system. Nature 2006; 444:323-329.
[5] Pritchard L, Birch PR. The zigzag model of plant-microbe interactions: is it time to move on?
Mol Plant Pathol 2014; 15:865-870.
[6] Cook DE, Mesarich CH, Thomma BP. Understanding plant immunity as a surveillance
system to detect invasion. Ann Rev Phytopathol 2015; 53:541-563.
[7] St Clair DA. Quantitative disease resistance and quantitative resistance Loci in breeding. Ann
Rev Phytopathol 2010; 48:247-268.
[8] Fukuoka S, Saka N, Mizukami Y, Koga H, Yamanouchi U, Yoshioka Y et al. Gene
pyramiding enhances durable blast disease resistance in rice. Sci Rep 2015; 5:7773.
[9] Das G, Rao GJ. Molecular marker assisted gene stacking for biotic and abiotic stress
resistance genes in an elite rice cultivar. Front Plant Sci 2015; 6:698.
[10] Yasuda N, Mitsunaga T, Hayashi K, Koizumi S, Fujita Y. Effects of Pyramiding
Quantitative Resistance Genes pi21, Pi34, and Pi35 on Rice Leaf Blast Disease. Plant Disease
2015:904-909.
[11] Ellur RK, Khanna A, Yadav A, Pathania S, Rajashekara H, Singh VK et al. Improvement of
Basmati rice varieties for resistance to blast and bacterial blight diseases using marker assisted
backcross breeding. Plant Sci 2016; 242:330-341.
[12] Van der Linden L, Bredenkamp J, Naidoo S, Fouch-Weich J, Denby KJ, Genin S et al.
Gene-for-gene tolerance to bacterial wilt in Arabidopsis. Mol Plant Microbe Interact 2013;
26:398-406.
[13] Roux F, Gao L, Bergelson J. Impact of initial pathogen density on resistance and tolerance
in a polymorphic disease resistance gene system in Arabidopsis thaliana. Genetics 2010;
185:283-291.
[14] Young ND. QTL mapping and quantitative disease resistance in plants. Ann Rev
Phytopathol 1996; 34:479-501.
[15] Faris JD, Zhang Z, Lu H, Lu S, Reddy L, Cloutier S et al.A unique wheat disease resistance-
like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci
USA 2010; 107:13544-13549.
[16] Parlevliet JE, Zadoks JC. Integrated Concept of Disease Resistance - New View Including
Horizontal and Vertical Resistance in Plants. Euphytica 1977; 26:5-21.
[17] Anderson JP, Gleason CA, Foley RC, Thrall PH, Burdon JB, Singh KB. Plants versus
pathogens: an evolutionary arms race. Funct Plant Biol 2010; 37:499-512.
[18] Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H et al.
A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat.
Science 2009; 323:1360-1363.

13
[19] Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, Ebana K. et al. Loss of function of a
proline-containing protein confers durable disease resistance in rice. Science 2009; 325:998-
1001.
[20] Wang JF, Olivier J, Thoquet P, Mangin B, Sauviac L, Grimsley NH. Resistance of tomato
line Hawaii7996 to Ralstonia solanacearum Pss4 in Taiwan is controlled mainly by a major
strain-specific locus. Mol Plant Microbe Interact 2000; 13:6-13.
[21] Perchepied L, Dogimont C, Pitrat M. Strain-specific and recessive QTLs involved in the
control of partial resistance to Fusarium oxysporum f. sp. melonis race 1.2 in a recombinant
inbred line population of melon. Theor Appl Genet 2005; 111:65-74.
[22] Naruoka Y, Garland-Campbell KA, Carter AH. Genome-wide association mapping for
stripe rust (Puccinia striiformis f. sp. tritici) in US Pacific Northwest winter wheat (Triticum
aestivum L.). Theor Appl Genet 2015; 128:1083-1101.
[23] Barba P, Cadle-Davidson L, Galarneau E, Reisch B. Vitis rupestris B38 Confers Isolate-
Specific Quantitative Resistance to Penetration by Erysiphe necator. Phytopathology 2015;
105:1097-1103.
[24] Marcel TC, Gorguet B, Ta MT, Kohutova Z, Vels A, Niks RE. Isolate specificity of
quantitative trait loci for partial resistance of barley to Puccinia hordei confirmed in mapping
populations and near-isogenic lines. New Phytol 2008; 177:743-755.
[25] Salvi S, Tuberosa R. To clone or not to clone plant QTLs: present and future challenges.
Trends Plant Sci 2005; 10:297-304.
[26] Whalen MC. Host defence in a developmental context. Mol Plant Pathol 2005; 6:347-360.
[27] Zuo W, Chao Q, Zhang N, Ye J, Tan G, Li B et al. A maize wall-associated kinase confers
quantitative resistance to head smut. Nature Genet 2015; 47:151-157.
[28] Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X et al. A kinase-START gene
confers temperature-dependent resistance to wheat stripe rust. Science 2009; 323:1357-1360.
[29] Wisser RJ, Balint-Kurti PJ, Nelson RJ. The genetic architecture of disease resistance in
maize: a synthesis of published studies. Phytopathology 2006; 96:120-129.
[30] Martinez C, Jauneau A, Roux C, Savy C, Dargent R. Early infection of maize root by
Sporisorium reilianum f. sp. zeae. Protoplasma 2000; 89:247-253.
[31] Martinez C, Roux C, Dargent R. Biotrophic development of Sporisorium reilianum zeae in
maize shoot apex. Phytopathology 1999; 89:247-253.
[32] Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A, Schulze-Lefert P et al.
Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance
to inappropriate pathogens that enter by direct penetration. Plant Cell 2006; 18:731-746.
[33] Krattinger SG, Sucher J, Selter LL, Chauhan H, Zhou B, Tang M et al. The wheat durable,
multipathogen resistance gene Lr34 confers partial blast resistance in rice. Plant Biotech J 2015.
[34] Risk JM, Selter LL, Chauhan H, Krattinger SG, Kumlehn J, Hensel G et al. The wheat Lr34
gene provides resistance against multiple fungal pathogens in barley. Plant Biotech J 2013;
11:847-854.
[35] Chauhan H, Boni R, Bucher R, Kuhn B, Buchmann G, Sucher J et al. The wheat resistance
gene Lr34 results in the constitutive induction of multiple defense pathways in transgenic barley.
Plant J 2015; 84:202-215.
[36] Clark BJ. The mammalian START domain protein family in lipid transport in health and
disease. J Endocrinol. 2012; 212:257-275.
[37] Cook DE, Lee TG, Guo X et al. Copy number variation of multiple genes at Rhg1 mediates
nematode resistance in soybean. Science 2012; 338:1206-1209.

14
[38] Huard-Chauveau C, Perchepied L, Debieu M, Rivas S, Kroj T, Kars I et al. An atypical
kinase under balancing selection confers broad-spectrum disease resistance in Arabidopsis. PLoS
Genet 2013; 9:e1003766.
[39] Manosalva PM, Davidson RM, Liu B, Zhu X, Hulbert SH, Leung H et al. A germin-like
protein gene family functions as a complex quantitative trait locus conferring broad-spectrum
disease resistance in rice. Plant Physiol 2009; 149:286-296.
[40] Hurni S, Scheuermann D, Krattinger SG, Kessel B, Wicker T, Herren G et al. The maize
disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-
like kinase. Proc Natl Acad Sci USA 2015; 112:8780-8785.
[41] Diener AC, Ausubel FM. RESISTANCE TO FUSARIUM OXYSPORUM 1, a dominant
Arabidopsis disease-resistance gene, is not race specific. Genetics 2005; 171:305-321.
[42] Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G. A domain swap approach reveals
a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc
Natl Acad Sci USA 2010; 107:9452-9457.
[43] Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y et al. Identification of a plant receptor for
extracellular ATP. Science 2014; 343:290-294.
[44] Li ZK, Luo LJ, Mei HW, Paterson AH, Zhao XH, Zhong DB et al. A "defeated" rice
resistance gene acts as a QTL against a virulent strain of Xanthomonas oryzae pv. oryzae. Molec
Genet Genomics 1999; 261:58-63.
[45] Fukuoka S, Yamanouchi U, Mizobuchi R, Yamanouchi U, Ono K, Kitazawa N et al.
Multiple functional polymorphisms in a single disease resistance gene in rice enhance durable
resistance to blast. Sci Rep 2014; 4:4550.
[46] Debieu M, Huard-Chauveau C, Genissel A, Roux F, Roby D. Quantitative disease resistance
to the bacterial pathogen Xanthomonas campestris involves an Arabidopsis immune receptor pair
and a gene of unknown function. Mol Plant Pathol 2015.
[47] Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, Iwabuchi M et al. RRS1 and
RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J
2009; 60:218-226.
[48] Le Roux C, Huet G, Jauneau A, Camborde L, Tremousaygue D, Kraut A et al. A receptor
pair with an integrated decoy converts pathogen disabling of transcription factors to immunity.
Cell 2015; 161:1074-1088.
[49] Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C, Sklenar J et al. A Plant Immune
Receptor Detects Pathogen Effectors that Target WRKY Transcription Factors. Cell 2015;
161:1089-1100.
[50] Nass HA, Pedersen WL, Mackenzie DR, Nelson RR. The Residual Effects of Some
Defeated Powdery Mildew Resistance Genes in Isolines of Winter-Wheat. Phytopathology 1981;
71:1315-1318.
[51] Brodny U, Nelson RR, Gregory LV. The Residual and Interactive Expressions of Defeated
Wheat-Stem Rust Resistance Genes. Phytopathology 1986; 76:546-549.
[52] Vetter MM, Kronholm I, He F, Haweker H, Reymond M, Bergelson J, et al. Flagellin
perception varies quantitatively in Arabidopsis thaliana and its relatives. Mol Biol Evol 2012;
29:1655-1667.
[53] Forsyth A, Mansfield JW, Grabov N, de Torres M, Sinapidou E et al. Genetic dissection of
basal resistance to Pseudomonas syringae pv. phaseolicola in accessions of Arabidopsis. Mol
Plant Microbe Interact 2010; 23:1545-1552.

15
[54] Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, van Esse HP et al.
Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial
resistance. Nature Biotechnol 2010; 28:365-369.
[55] Schwessinger B, Bahar O, Thomas N, Holton N, Nekrasov V, Ruan D et al. Transgenic
expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-
dependent activation of defense responses. PLoS Pathog 2015; 11:e1004809.
[56] Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP et al. The kinase LYK5 is a major
chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1.
eLife 2014; 3.
[57] Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K et al. CERK1, a LysM
receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA
2007; 104:19613-19618.
[58] Petutschnig EK, Jones AM, Serazetdinova L, Lipka U, Lipka V. The lysin motif receptor-
like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and
subject to chitin-induced phosphorylation. J Biol Chem 2010; 285:28902-28911.
[59] Petutschnig EK, Stolze M, Lipka U, Kopishke M, Horlacher J, Valerius O et al. A novel
Arabidopsis CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) mutant with enhanced
pathogen-induced cell death and altered receptor processing. New Phytol 2014; 204:955-967.
[60] Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R, Alden J et al. A soybean cyst
nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature
2012; 492:256-260.
[61] Li R, Moore M, King J. Investigating the regulation of one-carbon metabolism in
Arabidopsis thaliana. Plant Cell Physiol 2003; 44:233-241.
[62] Locasale JW. Serine, glycine and one-carbon units: cancer metabolism in full circle. Nature
reviews. Cancer 2013; 13:572-583.
[63] Fox JT, Stover PJ. Folate-mediated one-carbon metabolism. Vitamins and hormones 2008;
79:1-44.
[64] Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, Mitchum MG. Developmental transcript
profiling of cyst nematode feeding cells in soybean roots. Mol Plant Microbe Int 2007; 20:510-
525.
[65] Hofmann J, El Ashry Ael N, Anwar S, Erban A, Kopka J, Grundler F. Metabolic profiling
reveals local and systemic responses of host plants to nematode parasitism. Plant J 2010;
62:1058-1071.
[66] Glawischnig E. Camalexin. Phytochemistry 2007; 68:401-406.
[67] Staal J, Kaliff M, Bohman S, Dixelius C. Transgressive segregation reveals two Arabidopsis
TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of
blackleg disease. Plant J 2006; 46:218-230.
[68] Lemarie S, Robert-Seilaniantz A, Lariagon C, Lemoine J, Marnet N, Levrel A et al.
Camalexin contributes to the partial resistance of Arabidopsis thaliana to the biotrophic soilborne
protist Plasmodiophora brassicae. Front Plant Sci 2015; 6:539.
[69] Denby KJ, Kumar P, Kliebenstein DJ. Identification of Botrytis cinerea susceptibility loci in
Arabidopsis thaliana. Plant J 2004; 38:473-486.
[70] Hittalmani S, Parco A, Mew TV, Zeigler RS, Huang N. Fine mapping and DNA marker-
assisted pyramiding of the three major genes for blast resistance in rice. Theor Appl Genet 2000;
100:1121-1128.

16
[71] Liu J, Liu D, Tao W, Li W, Wang S, Chen P et al. Molecular marker-facilitated pyramiding
of different genes for powdery mildew resistance in wheat. Plant Breed 2000; 19:21-24.
[72] Singh S, Sidhu JS, Huang N, Vikal Y, Li Z, Brar DS et al. Pyramiding three bacterial blight
resistance genes (xa5, xa13 and Xa21) using marker-assisted selection into indica rice cultivar
PR106. Theor Appl Genet 2001; 102:1011-1015.
[73] Jiang G, Xu CG, Tu JM, Li XH, He YQ, Zhang QF. Pyramiding of insect- and disease-
resistance genes into an elite indica, cytoplasm male sterile restorer line of rice, 'Minghui 63'.
Plant Breed 2004; 123:112-116.
[74] Zhang J, Li X, Jiang G, Xu Y, He Y. Pyramiding of Xa7 and Xa21 for the improvement of
disease resistance to bacterial blight in hybrid rice. Plant Breed 2006; 125:600-605.

Table 1: Genes contributing to QDR

Gene Type Pathogen(s) Disease Host Reference
ZmWAK wall-associated Sporisorium head smut maize [21]
kinase, non RD reilianum
Htn1 wall-associated Exserohilum Northern maize [37]
kinase, non RD turcicum Corn Leaf
Blight
Yr36 kinase with Puccinia stripe rust wheat [22]
START domain striiformis
RFO1/WAKL22 Wall associated- Fusarium wilt Arabidopsis [38]
like kinase oxysporum f.
sp. matthioli
RKS1 atypical kinase Xanthomonas black rot Arabidopsis [35]
campestris pv. disease
campestris
Lr34 putative ABC Puccinia stripe rust, wheat [14]
transporter striiformis, leaf rust,
Puccinia powdery
triticina, mildew
Blumeria
graminis
pi21 proline Magnaporthe rice blast rice [15]
containing oryzae
protein
Rhg4 serine hydroxy- Heterodera cyst soybean [50]
methyl glycines nematode
transferase

17
Rhg1 copy number Heterodera cyst soybean [34]
variation for an glycines nematode
amino acid
transporter, an -
SNAP protein,
and a wound-
inducible protein
Pi35 NBS-LRR Magnaporthe rice blast rice [40]
oryzae
RPS4/RRS1 R gene pair: Xanthomonas black rot Arabidopsis [41]
NBS-LRR and campestris pv. disease
NBS-LRR- campestris
WRKY

18