Vol.1, No.2, 56-61 (2010)
doi:10.4236/as.2010.12008
Copyright © 2010 SciRes. Openly accessi ble at http://www.scirp.org/journal/AS/
Agricultural Sciences
The HLP mutation confers enhanced resistance to
leaf-rust in different wheat genetic backgrounds
——Lesion-mimic mutation confers resistance in wheat
Cristina Andrea Kamlofski1, Alberto Acevedo2*
1Estación Experimental Agropecuaria Concepción del Uruguay, CRER, INTA, Concepción del Uruguay, Entre Ríos, Argentina
2Centro de Investigación de Recursos Naturales, INTA Castelar, Castelar, Buenos Aires, Argentina;
*Corresponding author: aacevedo@cnia.inta.gov.ar
Received 8 July 2010; revised 19 July 2010; accepted 20 July 2010.
ABSTRACT
In several plant species, lesion-mimic mutants
simulate the disease-resistance response in the
absence of pathogens. Interestingly, some of
these mutants confer broad-spectrum resistance
to diverse pathogens. We previously demon-
strated that the HLP (hypersensitive-like phe-
notype) mutant of bread wheat (Triticum aesti-
vum L.) exhibited spontaneous hypersensitive
response (HR) in the absence of any pathogen
input. However, when HLP plants showing HR
phenotype were challenged with leaf-rust (Puc-
cinia triticina) they were more resistant than
plants of the mother-line of comparable devel-
opmental stage that did not show spontaneous
HR, suggesting that the HLP mutation may
confer enhanced resistance to the fungus. In
this paper we validate the aforementioned find-
ing in several wheat genetic backgrounds. Two-
way crosses were performed among the HLP
mutant and eight wheat commercial stocks, and
third backcross progenies with and without
spontaneous HR were challenged with leaf-rust
to investigate the response to the fungus.
Backcrosses to cv. Sinvalocho M.A., the mother-
line, and cv. Purplestraw, highly susceptible to
leaf-rust attack, were used as controls. Third
backcross progenies of cvs. Sinvalocho M.A.,
Purplestraw, Buck Guaraní and Pro INTA Impe-
rial bearing spontaneous HR phenotype were
more resistant to the fungal pathogen than third
backcross progenies that did not carry the HLP
mutation. Other four wheat stocks were as
healthy as the HLP mutant. As expected, back-
cross to the mother-line demonstrated that the
HLP mutation conferred an additional resistance
to the alread y healthy performan ce d isplay ed by
the mother-line at adult plant stage. The intro-
gression of the HLP mutation conferred heigh-
tened leaf-rust resistance and caused no kernel
weight red uction on th e backcr ossed pr ogenies.
Taken together, these data validate the direct
use of this type of mutations in disease-resis-
tance breeding.
Keywords: Hypersensitive Response;
Lesion-Mimic Mutant; Puccinia Triticina,
Wheat Commercial Stocks
1. INTRODUCTION
Plants have evolved several defense mechanisms to
overcome pathogen attack. One of the most common and
effective defense responses in plants is the hypersensi-
tive response (HR), which results in localized cell death
at the site of pathogen infection [1]. Mutants have been
identified in several plant species that spontaneously
form localized areas of dead tissue resembling those
seen in the HR. In these class of mutants, hereafter re-
ferred to as lesion-mimic mutants, disease symptoms or
HR cell death occur in the absence of pathogens.
Several lesion-mimic mutants have been identified
and characterized in Arabidopsis: acd [2-4]; dll [5]; hlm
[6]; len [7]; lsd [8]; ssi [9,10]. The LSD1 gene coding for
a novel zinc finger protein functions as a negative reg ula -
tor of plant cell death. Interestingly, the lsd1 mutants
were resistant to the bacterial pathogen Pseudomonas
syringae and the oomycete Peronospora parasitica [11].
The HLM1 gene encodes a cyclic nucleotide-gated chan-
nel that is permeable to K+ and Na+ ions and is activated
by cGMP and cAMP. The hlm1 mutants also exhibited
increased resistance to a virulent strain of Pseudomonas
syringae pv tomato [6].
An underlying agronomic feature of some gramina-
C. A. Kamlofski et al. / Agricultural Sciences 1 (2010) 56-61
Copyright © 2010 SciRes. Openly accessi ble at http://www.scirp.org/journal/AS/
57
ceous lesion-mimic mutants is that they confer broad-
spectrum resistance to different pathogens. Mutations of
the barley Mlo gene conferred expression of a lesion-
mimic phenotype which provided resistance to all kn own
races of the fungus responsible for powdery mildew
(Blumeria graminis f.sp. hordei). However, barley seed-
lings carrying the mlo mutation showed enhanced sus-
ceptibility to the rice blast fungus Magnaporthe grisea
[12], and resistance genes ml-o5, ml-o6, and ml-10 were
responsible for grain yield reduction in chromosome-
doubled haploid lines of barley tested in a disease-free
field trial [13]. In rice, some lesion-mimic mutants dis-
played enhanced resistance to pathogens: cdr1, cdr2 and
cdr3 exhibited heightened resistance to M. grisea [14],
spl4, spl5-1, spl5-2, spl7, spl10, spl11, spl12, spl13,
spl14 and Spl15 conferred non-race-specific resistance to
rice blast and bacterial blight [15,16] and ebr3 showed
increased resistance to M. grisea and the bacterial
pathogen Xanthomonas oryzae pv. oryzae [17]. Co-seg-
regation analyses of blast and bacterial blight resistance
and lesion-mimic phenotypes in segregating populations
of spl17 and Spl26 demonstrated that enhanced resis-
tance to the two diseases was conferred by mutations in
the lesion-mimic genes [18]. The wheat mutant M66
showed enhanced resistance to powdery mildew and
yellow and brown rusts although its yield was 50% that
of the control, (cv. Guardian) [19-21]. Conversely, the
HLP mutant of wheat that exhibited spontaneous HR
lesions showed also heightened resistance to leaf-rust
(Puccinia triticina) and similar yield to that of its mother
line (cv. Sinvalocho M.A.) [22]. Because enhanced re-
sistance coincided w ith the presence of spontaneous HR,
the HLP mutant was backcrossed to different wheat ge-
netic stocks and challenged with leaf-rust to genetically
validate the phenomenon.
We report in this paper that the introgression of the
HLP mutation into different wheat genetic stock s confers
heightened levels of resistance to leaf-rust and does not
affect kernel weight.
2. MATERIALS AND METHODS
2.1. Plant Material and Backcross Program
A backcross program was performed among the HLP
mutant of bread wheat (Triticum aestivum L.) and eight
wheat cultivars to incorporate the mutation induced in
HLP into the eight different genetic backgrounds. Culti-
var Sinvalocho M.A., mother-line of HLP, and cv. Pur-
plestraw, highly susceptible to Puccinia triticina, were
selected because they have been used for many years in
Argentina as differential hosts in genetic studies involv-
ing leaf rust [23-25]. The remaining six wheat cultivars
(Pro INTA Don Alberto, Pro INTA Isla Verde, Granero
INTA, Pro INTA Imperial, Buck Guaraní, and Klein Ca-
cique) were selected from the large public (INTA) and
private (Buck and Klein) breeding programs because the
average genetic diversity within each of these programs
was very similar to the total genetic diversity present in
the complete Argentine germplasm [26].
Since the mutation induced in HLP controls the ex-
pression of visible and spontaneous HR lesions, its in-
trogression into the wheat genetic stocks was traced, by
the naked eye, simply by selfing the plant receptor and
selecting the HR phenotypes in the plant receptor prog-
eny.
2.2. Pathogen Infection Study and Kernel
Weight Evaluation
A spontaneous leaf-rust infection study was carried out
in the experimental field at the Agricultural Experimen-
tal Station of Concepción del Uruguay, Entre Ríos, Ar-
gentina. Ther e were two sowing dates, 30 May 2006 and
23 May 2007, each with two repetitions. Seeds of third
backcross progenies corresponding to the aforemen-
tioned crosses were sown in the field in 1.2-m rows
separated by 0.2-m. For each cross, natural leaf-rust in-
fection was evaluated by scoring the number of pustules
on the flag leaf of 10 plants that carried the HLP muta-
tion and 10 plants that did not. Evaluated plants were
chosen at random. Results were the means of two inde-
pendent experiments.
The type of infection was also recorded according to
the classification described by Mains and Jackson [27].
The evaluation of the kernel weight trait was per-
formed by using the same experimental design described
for the spontaneous leaf-rust study. Results were the
means of two independent experiments.
2.3. Statistical Analyses
The Mann-Whitney test was used to statistically analyze
the leaf-rust infection response and the kernel weight
trait in third backcross progenies with and without spon-
taneous HR.
3. RESULTS
3.1. Expression of Resistance of HLP
Mutation to Leaf Rust in Different
Wheat Stocks
Preferentially, lesion mimic mutations have been char-
acterized only in the genetic background where they
were isolated. Even though it is h ighly d esirable to know
as well if the candidate mutation is functional in other
genetic stocks different from the original one, knowl-
C. A. Kamlofski et al. / Agricultural Sciences 1 (2010) 56-61
Copyright © 2010 SciRes. Openly accessi ble at http://www.scirp.org/journal/AS/
58
edge about this matter appears to be scarce. Moreover,
this information is mandatory to decid e whether the mu-
tation is a useful genetic factor to be considered in plant
breeding pro gr ams.
In a previous investigation we demonstrated that adult
HLP plants that exhibited spontaneous HR lesions were
more resistant to leaf-rust attack than Sinvalocho M.A.
plants of a comparable developmental stage, indicating
that the HLP mutation, traced by the naked-eye by the
presence of spontaneous HR, was phenotypically associ-
ated with fungal resistance.
In an effort to validate at the genetic level, whether the
HLP mutation also conferred pathogen resistance in
other genetic backgrounds, the HLP mutant was back-
crossed to two wheat controls and six commercial culti-
vars, and field-grown plants of progenitors and third
backcrossed progenies were challenged with natural leaf-
rust infections. Two-way backcrosses to cv. Sinvalocho
M.A., the mother-line, and cv. Purplestraw, highly sus-
ceptible to leaf-rust attack, demonstrated that adult
plants of progenitor HLP exhibiting spontaneous HR
accumulated lower numbers of leaf-rust pustules per cm2
of flag leaf (3.00 ± 0.89) that in general terms were also
smaller (infection type 1) than those observed on control
plants of progenitors Sinvalocho M.A. (12.00 ± 2.58; U
= 1; P < 0.001; infection type 2–2 ++) (Figure 1(a)) and
Purplestraw (38.50 ± 4.58; U = 0; P < 0.001; infection
type 2–3) (Figure 1(b)), of a comparable developmental
stage (Ta ble 1, Fig ure 1). Third backcrossed progenies
derived from HLP × Sinvalocho M.A. cross demon-
strated that adult plants carrying the HLP mutation were
more resistant (4.00 ± 2.16 pustules/flag leaf cm2) to the
fungal pathogen than adult plants that did not carry the
mutation (12.75 ± 3.09 pustules/flag leaf cm2; U = 1; P <
0.001) and therefore they did not exhibit spontaneous
HR lesions (Figure 1). Accordingly, third backcrossed
progenies derived from HLP × Purplestraw cross
showed that adult plants bearing spontaneous HR phe-
notype were more resistant (4.10 ± 2.30 pustules/flag
leaf cm2) to leaf-rust than adult plants that did not ex-
hibit spontaneous HR lesion (43.40 ± 5.15 pustules/flag
leaf cm2; U = 0; P < 0.001) (Figure 1). On average, the
accumulation of rust pustules/flag leaf area allowed the
classification of naturally infected plants in two groups.
In one group the number of pustules ranged from 33.92
to 48.55 and it was composed of plants of cv. Purples-
traw and plants of third backcrossed progenies that ex-
hibited no spontaneous HR. The other group was com-
posed of plants of the HLP mutant and plants of third
backcrossed progenies that showed spontaneous HR, and
the accumulation of pustules ranged from 1.80 to 6.40.
Interestingly, to 6.40. Interestingly, not only the latter
group accumulated a small number of rust pustules com-
(a)
(b)
Figure 1. Differential response of HLP, Sinvalocho M.A. (a),
Purplestraw (b), and their corresponding backcrossed proge-
nies to leaf rust attack. Note that field-grown plants from HLP
and backcrossed progenies that carry the HLP mutation accu-
mulated less rust pustules than plants of Sinvalocho M.A.,
Purplestraw, and backcrossed progenies that did not carry the
mutation.
pared to the first one, but it also showed a common fea-
ture, i.e., all their members carried the HLP mutation.
Since an elevated number of leaf-rust pustules were de-
tected in the susceptible wheat control, this meant that
the experiments were performed under conditions of
good spontaneous leaf-rust infection (Table 1, Figure
1(b)).
Adult plants of four commercial cultivars (Klein Ca-
cique, Pro INTA Don Alberto, Pro INTA Isla Verde, and
Granero INTA) out of the six cultivars analyzed did not
differ from the response displayed by the HLP mutant to
leaf-rust attack (Table 1); however, flag leaves of cvs.
Pro INTA Imperial (U = 1; P < 0.001; infection type
2–2++) (Figure 2(a)) and Buck Guaraní (U = 1; P <
0.001; infection type 2–2++) (Figure 2(b)) accumulated
higher numbers of leaf-rust pustules compared to HLP
(Table 1, Figure 2). Third backcrossed progenies de-
rived from both HLP × P. Imperial and HLP × B.
Guaraní crosses showed that adult plants that carried the
HLP mutation were more resistant (4.00 ± 2.58 pus-
tules/flag leaf cm2, and 4.25 ± 1.50 pustules/flag leaf
cm2, respectively) to leaf-rust than adult plants that did
not carry the mutation (10.50 ± 2.64 pustules/flag leaf
cm2; U = 1; P < 0.001, and 14.00 ± 2.94 pustules/flag
leaf cm2 ; U = 1; P < 0.001, respectively), and thus they
did not exhibit spont aneous HR phenotypes ( Figure 2).
C. A. Kamlofski et al. / Agricultural Sciences 1 (2010) 56-61
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59
Table 1. Natural leaf-rust infection levels in field-grown plants
of several wheat genetic stocks.
Progenitors Pustules/Flag leaf
(Number cm-2)
Mutant
HLP 3.00 ± 0.89
Controls
Sinvalocho M.A. 12.00 ± 2.58
Purplestraw 38.50 ± 4.58
Commercial cultivars
Pro INTA Imperial 13.25 ± 4.57
Buck Guaraní 13.50 ± 2.38
Klein Cacique 3.10 ± 1.43
Pro INTA Don Alberto 2.80 ± 1.14
Pro INTA Isla Verde 2.15 ± 0.93
Granero INTA 2.35 ± 0.90
Notes: Four commercial cultivars were as healthy as the HLP mutant.
Data represent the average of two independent experiments with repe-
titions.
(a)
(b)
Figure 2. Differential response of HLP, Pro INTA Imperial (a),
Buck Guaraní (b), and their corresponding backcrossed proge-
nies to natural leaf-rust infection. Note that field-grown plants
from the HLP mutant and from backcrossed progenies that carr y
the HLP mutation showed less rust pustules than developmen-
tally comparable plants of P. Imperial, B. Guaraní, and back-
crossed progenies that did not carry the mutation.
3.2. Kernel Weight Evaluation
Because wheat is both nutritionally and economically an
important crop worldwide, it is desirable that the muta-
tion induced in the HLP mutant causes no detrimental
pleiotropic effects in agronomic traits that are compo-
nents of the cereal yield. Field-grown plants that were
naturally infected with leaf-rust demonstrated, for each
cross, that no kernel weight differences (P > 0.05) were
detected between plants of third backcrossed progenies
that showed spontaneous HR and plants that did not
(Table 2), indicating that the HLP mutation, traced by
the naked-eye by the presence of spontaneous HR le-
sions, did not have a substantial effect on the kernel
weight of the different genetic backgrounds examined.
4. DISCUSSION
The fact that most lesion-mimic mutations have been
solely studied in the gen etic background of the wild-typ e
indicates that any putative association between the le-
sion-mimic mutation and a genetic trait of agronomic
Table 2. Kernel weight values in progenitors and backcross
progenies carrying and not carrying the HLP mutation.
Plant material 100 Kernel weight (g)
Progenitors
HLP 3.74 ± 0.16
Sinvalocho M.A. 3.72 ± 0.19
Purplestraw 3.72 ± 0.21
Buck Guaraní 3.82 ± 0.26
Pro INTA Imperial 3.49 ± 0.59
Backcrosses
HLP × Sinvalocho M.A.
(spontaneous HR) 3.75 ± 0.15
HLP × Sinvalocho M.A.
(without HR) 3.71 ± 0.18
Purplestraw × HLP
(spontaneous HR) 3.70 ± 0.24
Purplestraw × HLP
(without HR) 3.70 ± 0.23
Buck Guaraní × HLP
(spontaneous HR) 3.84 ± 0.32
Buck Guaraní × HLP
(without HR) 3.48 ± 0.29
HLP × Pro INTA Imperial
(spontaneous HR) 4.15 ± 0.22
HLP × Pro INTA Imperial
(without HR) 3.42 ± 0.35
Notes: The introgression of the HLP mutation, traced by the observa-
tion of spontaneous HR lesions, caused no kernel weight reduction.
Data represent the average of two independent experiments with repe-
titions.
C. A. Kamlofski et al. / Agricultural Sciences 1 (2010) 56-61
Copyright © 2010 SciRes. Openly accessi ble at http://www.scirp.org/journal/AS/
60
interest represents a phenotypic correlation that should
be validated at the genetic level by crossing the genotype
that carries the lesion mimic mutation to other genetic
backgrounds and verifying if the genetic correlation be-
tween the mutation and the agronomic trait exists. This
validation is deemed important to co nsider the direct use
of this type of mutations in breeding programs.
We previously demonstrated that adult plants of HLP
showing spontaneous HR were more resistant to leaf-
rust attack compared with plants of the mother-line of
comparable developmental stage that did not show
spontaneous HR. This finding indicated that the muta-
tion induced in HLP was phenotypically associated with
fungal resistance [22].
In this study we have genetically validated the afore-
mentioned finding by challenging with leaf-rust infec-
tions the backcross-mediated introgression of the HLP
mutation into sev eral wheat genetic background s besides
the mother-line. We have demonstrated that adult plants
of third backcrossed progenies bearing spontaneous HR
phenotype were more resistant to leaf-rust attack than
adult plants of third backcrossed progenies that did not
carry the HLP mutation (Figures 1 and 2). The intro-
gression of the mutation induced in HLP conferred simi-
lar levels of resistance to the fungal pathogen in different
wheat genetic backgrounds. Interestingly, similarity co-
efficient among cultivars used as progenitors ranged
from 0.7784 (P. Imperial and P. Don Alberto) to 0.6296
(Granero INTA and P. Isla Verde), and it was 0.6625 in
the specific case of P. Imperial and B. Guaraní (Mani-
festo, pers. comm.), indicating that the HLP mutation
proved to be functionally efficient against the fungal
pathogen in genetically diverse wheat germplasm.
Even though the mother-line of the HLP mutant car-
ries at least two leaf-rust (Lr) genes [25] that may ex-
plain the durable resistance that Sinvalocho M.A. has
shown for decades, the possibility that those genes con-
fer the enhanced resistance observed in plants of third
backcross progenies that show ed HR phenotype is fairly
low.
Diseases are a leading cause of crop losses, primarily
leaf-rust that may reduce yield greatly [28]. Currently,
the introgression of disease resistance genes into wheat
breeding programs requires DNA-molecular-marker-
assisted selection to trace those genes in the p lant breed-
ing materials. However, because the mutation induced in
HLP controls the expression of visible and spontaneous
HR lesions, its introgression into wheat genetic back-
grounds has the advantage that it can be traced, by the
naked eye, simply by selfing the plant receptor and se-
lecting the HR phenotypes in the plant receptor progeny.
Indeed, this visual method represents a simpler and more
economic way of tracing the mutation, compared to DNA-
molecular-marker-assisted selection method.
On the other hand, several investigations have dem-
onstrated that resistance mediated by lesion-mimic mu-
tations is accompanied, in most plants, by lower yield,
stunted growth or other abnormal characteristics that
prevent the direct use of these mutations in disease-resis-
tance breeding. Yield of the wheat mutant M66 was 50%
lower than that of the control [19]. Mutagen induced
resistance genes ml-o5, ml-o6, and ml-10 conferred a
four per cent reduction in grain yield caused mainly by
lower thousand grain weight in a population of 198
chromosome-doubled haploid lines of spring barley
tested in a disease-free field trial [13]. In contrast to the
suppressor of SA insensitivity1 (ssi1), accelerated cell
death6 (acd6) and lsd6 mutations of Arabidopsis, and to
most spl and cdr mutations of rice, which reduced final
plant height [3,9,15,29] and shorter life cycle [14] and
resulted in a lower yield [16], the mutation induced in
HLP caused no detrimental pleiotropic effects that af-
fected the agronomic performance of the plant [22] and
did not affect kernel weight when it was backcrossed-
incorporated in several genetic stocks (Table 2). The
latter finding, coupled with the fact that backcrossed-
mediated introgression of the HLP mutation in several
wheat genetic stocks heightened leaf-rust resistance vali-
dates the direct use of this mutation in disease-resistance
breeding.
5. CONCLUSIONS
The introgression of the HLP mutation into different
wheat genetic stocks confers heightened levels of resis-
tance to leaf-rust, similar to the reported for the intro-
gression of the mutation into the genetic background of
the mother-line. To our knowledge this is the first report
of a lesion-mimic mutation that enhances pathogen re-
sistance without affecting kernel weight in genetically
diverse wheat germplasm. Taken together, both findings
validate the direct use of this mutation in disease-resis-
tance breeding.
6. ACKNOWLEDGEMENTS
We thank Dr Marcela M. Manifesto (Instituto de Recursos Biológicos,
INTA, Argentina) for providing wheat similarity coefficient data. This
research was supported by a grant from the Secretariat of Science and
Technology (BID 1201 OC-AR PICT N° 0 8-9555) to AA.
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