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135
Review Czech J. Genet. Plant Breed., 50, 2014 (2): 135–143
Resistance to Rusts (Uromyces pisi and U. viciae-fabae) in Pea
E BARILLI 1, J C SILLERO 2, E PR ATS 1 and D RUBIALES1
1Institute for Sustainable Agriculture, Spanish National Research Council (CSIC), Córdoba,
Spain; 2Andalusian Institute of Agricultural Research and Training (IFAPA), Córdoba, Spain
Abstract
B E., S J.C., P E., R D. (2014): Resistance to rusts (Uromyces pisi and U. viciae-fabae)
in pea. Czech J. Genet. Plant Breed., 50: 135–143.
Pea is the second most important food legume crop in the world. Rust is a pea disease widely distributed, par-
ticularly in regions with warm, humid weather. Pea rust can be incited by Uromyces viciae-fabae and by U. pisi.
U. viciae-fabae prevails in tropical and subtropical regions such as India and China, while U. pisi prevails in
temperate regions. Chemical control of rust is possible, but the use of host plant resistance is the most desired
means of rust control. In this paper we revise and discuss the occurrence and incidence of both pathogens on
peas, the availability of resistance sources and the present state of the art in pea breeding against this disease.
Keywords: breeding; histology; Pisum sativum; resistance; rust
Grain legumes are important crops which can de-
crease the marked deficit of high-protein feedstuff
and contribute to a large extent to the sustainability
of crop-livestock systems (C et al. 2003;
A & I 2008). Among them,
dry pea (Pisum sativum L.) is the second most im-
portant food legume crop in the world because of its
high yield potential (A & I
2008; R et al. 2011a; S et al. 2012).
Pea rust has become an important pathogen of
dry pea since the mid-1980s and is mostly distrib-
uted in Europe, North and South America, India,
China, Australia and New Zealand, particularly in
regions with warm, humid weather (EPPO 2012).
The pathogen usually appears during mid-spring
when the crop is at flowering or podding stage. In
years of epidemics, affected leaves dry up and fall off,
and pods remain undeveloped, which consequently
results in yield losses of higher than 30% (EPPO
2012). Chemical control of rust is possible (S
et al. 2004; E et al. 2011), but the use of host
plant resistance is the most desired means of rust
control (R et al. 2011a).
Pea rust has been reported to be caused either by
the fungus Uromyces viciae-fabae (Pers.) J. Schröt
[syn. U. fabae (Pers.) de Bary] (P et al. 1980; X
& W 2001; S et al. 2004; V-
et al. 2005; K et al. 2006) or by U.pisi
[(Pers.) Wint.] (E et al. 2005; B et al.
2009a, b). The species complex U. viciae-fabae, com-
monly referred to as faba bean rust, is an autoecious
fungus reported to infect pea besides faba bean (Vi-
cia faba L.), lentil (Lens culinaris L.) and common
vetch (Vicia sativa L.) (C 1978). Isolates of
U. viciae-fabae are specialized with respect to their
hosts, with each isolate exclusively infecting cultivars
of the species from which it was collected (E
et al. 2005; R et al. 2013). U. viciae-fabae is
the principal causal agent of pea rust in tropical and
subtropical regions like India and China, where warm
humid weather is suitable for the appearance of both
the uredial and the aecidial stage (K et al.
2006). However, in temperate regions, it has been
observed that although pea seedlings can be infected
by U. viciae-fabae, it barely gets established and pro-
gresses under field conditions slowly (B et al.
2009c). These observations were confirmed by gath-
ering several rust isolates from highly damaged pea
crops from different geographical regions (Canada,
Czech Republic, Egypt, Morocco and Spain). Mo-
lecular analyses confirmed that all isolates belonged
to U. pisi rather than to U. viciae-fabae (B et
al. 2011). U. pisi is a heteroecious macrocyclic fun-
gus that completes its life cycle on the spontaneous
136
Czech J. Genet. Plant Breed., 50, 2014 (2): 135–143 Review
Euphorbia cyparissias (cypress spurge) (P 1952),
over the vegetation residues of which the fungus
overwinters as teliospores (P & R 2000).
Spermatogonia and aecia develop on this alternate
host, while the pathogen produces several generations
of urediniospores on pea leaves and stems. In India
it has been reported that U. viciae-fabae aeciospores
act as repeating spores and play an important role in
the outbreak of the disease (K et al. 2006),
whereas in temperate regions urediospores are the
only infecting spores in the case of U. pisi (X &
W 2001).
The U. pisi host range is wide, being able to affect
plant species from many other genera (Astragalus,
Cicer, Euphorbia, Lathyrus, Lens, Medicago, Oro-
bus, Pisum and Vicia, among others) (B et al.
2012a; F et al. 2008; V P et al. 2009a).
U.viciae-fabae is circumglobal on Lathyrus, Pisum
and Vicia, with V. f aba the host of the neotype (C-
1978). However, host-specialized isolates that
cannot infect V. fab a have been reported (E
et al. 2005, 2008; R et al. 2013). In addition,
the pathogen has been described infecting plants
from the genera Ervum, Lens, Melilotus and Orobus
(F et al. 2008).
Screening and sources of resistance
Many efforts have been made to identify sources
of resistance in pea against U. viciae-fabae (P
et al. 1980; X & W 2001; S et al.
2004; V et al. 2005; K et
al. 2006). These studies revealed that the major-
ity of the studied pea genotypes were susceptible,
though genotypic differences in the rust intensity
described as of slow rusting type have been reported
(K et al. 1994; C et al. 2006) (Table 1).
Slow rusting resistance against U. viciae-fabae has
been characterised by measuring the area under the
disease progress curve (AUDPC), the disease sever-
ity (DS), the number of pustules/leaf or infection
frequency(IF) and the pustule size (C et al.
2006). The authors considered that AUDPC values
were more precise for genotype selection than DS.
An exception was reported for the accessions
PJ22211, PJ207508, EC109188, which were found
to be immune to U. viciae-fabae infection (P et
al. 1979), while in F2 and backcross generation there
were symptoms of hypersensitive reaction to the
pathogen that were typified by the presence of large
numbers of minute brown islands on the leaves.
Little work has been performed with U. pisi resist-
ance in Pisum and only recently a pea germplasm
collection has been screened to identify sources of
resistance to this pathogen both under field and growth
chamber conditions (B et al. 2009b) (Table 1).
Different epidemiological parameters, such as DS and
AUDPC (as mentioned above), as well as infection
type(IT), epidemic growth rate (r) and time of the
first pustule appearance (t0) were investigated, as well
as the relationship between them, in order to identify
the parameters that better characterize the resistance
to U. pisi in both conditions. No complete resistance
has been identified so far. However, incomplete resist-
ance was common in the collection, with more than
60% of the accessions showing markedly lower severity
values than the susceptible check. All the accessions
displayed a compatible interaction (high infection
type) both in adult plants under field conditions and
in seedlings under growth chamber conditions, but
with varying levels of disease reduction (B et al.
2009b) (Figure 1), suggesting the existence of partial
resistance sensu P (1983). The correlation
observed between DS values measured under field
conditions during three growing seasons, and between
DS and AUDPC was high (B et al. 2009b) sug-
gesting that the final DS estimation on pea provides a
feasible estimation of partial resistance. DS estimation
Table 1. Reported sources of pea resistance to Uromyces viciae-fabae and U. pisi
Disease Source of resistance Gene related References
U. viciae-fabae Bridzor,EC4294, EC9218, EC955 EC9908,
NP29, Perf 3268, IC4604
S et al. (1974)
PJ207508, PJ22211, EC109188 monogenic inheritance P et al. (1979, 1980)
RPB-22, RA-10-5, RC-35-2 A and P (1990)
Pant P11, FC1, HUDP 16, JPBB 3, HUP 14 monogenic (putative Ruf )
inheritance
C et al. (2006);
K et al. (2006)
U. pisi IFPI3260, PI347321, PI347336, PI347347,
PI343935, PI343965, PI347310
inheritance under study B et al. (2009a, b)
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Review Czech J. Genet. Plant Breed., 50, 2014 (2): 135–143
needs less computation and is less time-consuming
than assessing AUDPC, epidemic growth rate (r) or
the first pustule appearance (t0). The epidemic growth
rate and the first pustule appearance were poor esti-
mators of U. pisi partial resistance as they were less
discriminating than the other parameters and showed
a low correlation within experimental designs.
Growth chamber studies have shown that DS values
are higher on the abaxial than on the adaxial leaf
surface. The vertical shape of a U. pisi substomatal
vesicle that penetrates deeper into the leaf mesophyll
should be the cause of this finding (E et al.
2005). There was a good correlation between DS
measured in the growth chamber and adult plants in
the field, proving that selection for partial resistance
to pea rust can be effectively performed in seedlings.
Lack of durability of resistance is a problem of
airborne fungal pathogens like rusts. Several mecha-
nisms may prevent the rust infection prior to stomatal
penetration (R & N 1996; S & R-
2002; S et al. 2006; P et al. 2007a;
R et al. 2011b). These can include limited
germination or germling adhesion to the leaf surface
(M 1978) and/or altered stomatal guard
cell morphology (W 1976). The limited varietal
differences in spore germination observed in the
U.pisi-pea pathosystem agreed with previous reports
in which reduction of urediospore germination and
fungal development on the leaf surface are of marginal
importance in reducing infection levels within the
host species (N & R 2002). In general,
most resistance mechanisms to rust infection occur
after the formation of substomatal vesicles, before
or after mesophyll cell penetration. A relatively high
proportion of germlings failing to form any haustoria
in mesophyll cells causing “early aborted colonies”
has been observed in some pea accessions (Table 2).
Probably, epidermal cells developed papillae and/or
cell wall strengthening under the site of the attempted
attack avoiding the fungus penetration, as described
previously in other plant-rust interactions (P
et al. 2007b; R-M et al. 2007). Further
studies are currently carried out to study host cell
Figure 1. Symptoms observed two weeks after Uromyces
pisi inoculation on pea susceptible (Messire, right) and
partially resistant (PI347321, left) genotypes
Table 2. Reaction of selected accessions of Pisum spp. to inoculation with Uromyces pisi under growth chamber condi-
tions (according to B et al. 2009a)
Accession Species
Macroscopical components
of resistance
Microscopical components of resistance
2 DAI 6 DAI
IT LP (%) IF early abortion
(%)
No. of haust/
colony
colony size
(mm2)
Messire (check)
P. sativum
4100 100.0 0.0 10.8 0.6
PI347321 4108* 25.9* 10.5* 3.5* 0.38*
PI347336 4106* 30.9* 3.5* 6.4* 0.38*
PI347347 4104* 30.2* 6.0* 5.2* 0.41*
PI343965 4104* 30.9* 0.0 6.3* 0.36*
PI347310 4104* 29.5* 0.0 4.2* 0.41*
IFPI3260 P. fulvum 4107* 13.7* 20.0* 2.2* 0.26*
*Significantly different from Messire (LSD test, P <0.01); IT – infection type according to S et al. (1962) scale;
LP – latent period measured as period of time (h) between inoculation and sporulation of 50% of the pustules; values
are presented as % with respect to the susceptible Messire (= 200 h); IF – infection frequency measured as number of
pustules per cm2; values are presented as % with respect to the susceptible Messire (= 139 pustules/cm2); DAI– days
after inoculation
138
Czech J. Genet. Plant Breed., 50, 2014 (2): 135–143 Review
wall modifications in response to U. pisi. In several
resistant genotypes the first haustorial mother cells
succeeded in penetrating the mesophyll cell and form-
ing a haustorium, subsequent penetration attempts
by secondary hyphae failed, reducing the number
of haustoria per colony and therefore hindering the
number of hyphal tips and the growth of the colony
(B et al. 2009a). A similar resistance mecha-
nism was found in Lathyrus sativum and L. cicera,
Medicago truncatula, wheat, garlic, chickpea and
faba bean against U. pisi (V P et al. 2009a,b),
U.striatus (R & M 2004; R
et al. 2011b), Puccinia triticina (R & N
1995), P. allii (F-A et al. 2011),
U.ciceris-arietini (S et al. 2012) and U.viciae-
fabae (S et al. 2000; S & R
2002), respectively. All the selected accessions to
U. pisi showed a critical decrease in the number of
hyphal tips per colony compared to the susceptible
check suggesting that haustorial mother cells have
been formed but are not functional or that they have
a reduced ability to successfully develop a hausto-
rium in the plant cell, as found in faba bean against
U. viciae-fabae (R & S 2003). Thus,
penetration resistance is an important mechanism
to prevent the full development of U.pisi infection
structures. This resistance is initially expressed with
the arrest of the infection by early abortion, and con-
tinued by hampering subsequent haustoria formation.
Macroscopically, penetration resistance resulted in
smaller colonies that developed more slowly than
the susceptible control as reflected by the negative
correlation observed between latent period (LP) and
colony size (CS) at any day after inoculation.
When the haustoria invade host cells, hypersensi-
tive response (HR) can be triggered. The HR is often
mediated by the genetic interaction of a host-encoded
resistance (R) gene product with that of a pathogen
avirulence (avr) gene leading to programmed cell
death, thus limiting fungal development (S &
R 2002). The HR is common in biotrophic
pathogen-plant interactions and was described in
cereal and legume responses to rust, among others
(T & R 1990; S & R
2002; S et al. 2006). HR may be triggered early
or late depending on the specific host genotype. How-
ever, we did not observe any HR in pea against U. pisi.
Resistance was not associated with host cell death
2days after inoculation (DAI) in any of the accessions
studied (B et al. 2009a), discarding the fast HR
hypothesis. Neither was host cell death observed later
(6 DAI) (B et al. 2009b) discarding also the pos-
sibility of late-acting HR that was reported in other
interactions such as L. cicera-U. viciae-fabae (V
P et al. 2009b), V. f ab a-U. viciae-fabae (H
et al. 2001; S & R 2002) and barley-
Puccinia hordei (N 1986). Incomplete resistance
identified in pea against U. pisi is not therefore based
on HR, fitting the definition of Partial Resistance (PR)
(P & V O 1975). Similarly, PR
against rusts has also been reported in other legumes
such as faba bean (S et al. 2000; H et
al. 2001), common bean (S & MV 1987),
grass pea (V P et al. 2009a), chickling pea
(V P et al. 2009b) and chickpea (M et
al. 2008; S et al. 2012).
The fact that the studied resistant accessions
showed pre-penetration resistance offers breeding
opportunities for this trait. This is important since
penetration resistance is usually non-race dependent
and based on multiple genes. Thus, such resistance
is expected to be more durable than single gene
controlled race-specific resistance that, although
easily manipulated in plant breeding, is also easily
overcome by new races of pathogens. Accessions
IFPI3260 and PI347321 have been included in our
breeding programmes and their molecular bases of
resistance to U. pisi are under study.
Inheritance of resistance
To date, studies on the genetic basis of resistance
to U. viciae-fabae have indicated either monogenic
(P et al. 1979; K & R 1987) or polygenic
control (K et al. 1994; V et al.
2005). The dominant nature of partial resistance
against faba bean rust U. viciae-fabae in pea, recorded
as reduced infection frequency, has been justified
as the expression of a single major gene, for which
the symbol Ruf was proposed (V et al.
2005), but the authors also presented some evidence
suggesting involvement of some polygenes as well.
Further, none of the pea genotypes has been reported
to be free from U. viciae-fabae infection (S &
S 1985; C et al. 2006) suggesting a
polygenic type of resistance or based on incomplete
gene expression.
More recently, R et al. (2011) suggested that the
Ruf gene proposed by V et al. (2005)
be now redesigned as Qruf to signify the quantita-
tive nature of its action and detected another minor
quantitative trait loci (QTL) (named Qruf1). Both
QTLs were located on LGVII. Qruf was flanked by
SSR markers, AA505 and AA446 (10.8 cM), explaining
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Review Czech J. Genet. Plant Breed., 50, 2014 (2): 135–143
22.2–42.4% and 23.5–58.8% of the total phenotypic
variation for IF and AUDPC, respectively. Qruf was
consistently identified across four environments.
Therefore, the SSR markers flanking Qruf would be
useful for marker-assisted selection for U. viciae-fabae
resistance. The minor QTL was environment-specific,
and it was detected only in the polyhouse (logarithm
(base 10) of odds values 4.2 and 4.8). It was flanked
by SSR markers, AD146 and AA416 (7.3 cM), and ex-
plained 11.2–12.4% of the total phenotypic variation.
In pea, two segregating populations derived from
the crosses between a resistant and a susceptible ac-
cession of P. fulvum L. (IFPI3260 × IFPI3251) and of
P. sativum (PI347321 × Messire) have recently been
developed to study the resistance against U.pisi. In
an early study using the IFPI3260 × IFPI3251 cross,
F2 plants were evaluated in the field and F3fami-
lies under growth chamber conditions assessing DS
and IT values as mentioned above. A wide range
of disease reactions was found in the population,
although high IT values, indicating the absence of
hypersensitive response, were observed on all the
lines. Preliminary results on this population revealed
polygenic inheritance. A single QTL was detected,
UP1, located between markers OPY11_1316 and
OPV17_1078 to govern the resistance of P. fulvum
accession IFPI3260 to U. pisi under controlled con-
ditions, although there was a hint of a second QTL
between markers OPAB12_125 and OPY11_1361. This
QTL, UP1, explained up to 60% of the phenotypic
variance (B et al. 2010a).
A RIL (Recombined Inbred Line) population de-
rived from this cross is being developed at present
in order to perform the required replications of field
tests, characterizing their effects and validating the
stability of QTLs across environments. Besides, a
RIL population derived from the cross PI347321×
Messire (P. sativum intraspecific cross) has also been
developed and F6 plants have been evaluated against
U. pisi under both natural and controlled conditions
(unpublished data) and QTL analysis is under study
in this moment.
Molecular markers linked to resistance genes could
facilitate the selection of rust resistant segregants
and thereby improve breeding efficiency. So far, re-
ports on molecular mapping of resistance to U. pisi
are limited and more robust markers are needed.
But rust resistance breeding is not only slow due to
these still insufficient genomic resources, but also,
and mainly because of the little knowledge of the
biology of various rust pathogens, it still lacks the
knowledge of the basic aspects such as the existence
of races and their distribution. Only after significant
input to improve the existing knowledge of biology
of the causal agents as well as of the plant, resistance
breeding will be efficiently accelerated.
Induced resistance
In order to validate alternative pea rust control
methods, a preliminary study on systemic acquired
resistance (SAR) induction on this plant-pathogen
interaction was developed using both biotic (U. pisi
and U. appendiculatus) and abiotic (salicylic acid
(SA), benzo-(1,2,3)-thiadiazole-7-carbothionic acid
(BTH) and DL-β-aminobutyric acid (BABA)) inducers
(B et al. 2010b). Results obtained showed a
significant reduction of infection levels locally and
systemically with BTH and BABA foliar treatments,
whereas neither biotic inducers nor SA had any
significant effect hampering the rust development.
BTH is a chemical SAR inducer against a wide range
of pathogens even though its effect varied with the
concentrations used and the pathosystems considered
(V L 2001). The expression of BTH-induced
SAR has been associated with transcriptional acti-
vation of gene encoding pathogenesis-related (PR)
proteins promoted by endogenous accumulation of
SA (J et al. 2008). In the rust-sunflower and rust-
wheat interaction, BTH-induced SAR has also been
associated with the excretion of phytoalexins to the
leaf surface, which inhibited urediospore germination
and appressorium formation (P et al. 2002).
The cellular and molecular mechanisms through
which BABA exerts its action are not so well re-
ported as those of BTH. Also, its capacity to confer
protection against basidiomycetes in general, and
rusts in particular, is contradictory (A &
C 2007). In sunflower, unlikely BTH, BABA
does not seem to induce any inhibitory effect on
Puccinia helianthi on the events prior to stomatal
penetration (A & C 2007), suggesting
that the resistance induced by these two chemicals
operates via different pathways.
To clarify the underlying mechanisms acting in the
BTH and BABA-induced resistance in pea against
U. pisi, the specific enzymatic activity enhanced in
a susceptible and in a partially resistant pea geno-
type was studied (B et al. 2010c). The disease
reduction observed after treatment with the induc-
ers was not complete. Treatment with 10mM BTH
and 50mM BABA effectively reduced the infection
frequency, with this reduction being higher in the
partially resistant than in the susceptible genotype.
140
Czech J. Genet. Plant Breed., 50, 2014 (2): 135–143 Review
The reduction in IF cannot be attributed to the toxic
effect of the chemicals on the fungus, as neither of
them showed a fungistatic activity against U. pisi
urediospores. Furthermore, the observed protective
effect was related to triggering of defence responses,
as reported for other plant-pathogen interactions
(P et al. 2002; I & F 2003; A
& C 2007).
Resistance was characterized by reduced infection
frequency mainly due to decreases in appressorium
formation, stomatal penetration, growth of infec-
tion hyphae and haustorium formation. Changes in
β-1,3-glucanase, chitinase, phenylalanine ammonia-
lyase and peroxidase activities and in total phenolic
content demonstrate that U. pisi resistance is in-
duced by BTH and BABA treatments at early and
late stages of the fungal infection process, but that
the chemicals operate via different mechanisms. In
fact, we should observe that BTH treatment primed
the activity of pathogenesis-related proteins such as
β-1,3-glucanase, chitinase and peroxidase in both
susceptible and resistant genotypes. On the other
hand, BABA treatment did not increase the enzymatic
activities in the studied genotypes, but significantly
increased their total phenolic contents. This increase
was also observed in BTH treated plants. In addi-
tion, preliminary results showed differences in the
amount and nature of particular phenolic compounds,
excreted to the leaf surface following the treatment
with both inducers (unpublished). This suggests a role
for phenolic compounds in the induced resistance
exerted by both BTH and BABA. It has been well
documented in different pathosystems that phenolic
compounds can play an important role in disease
resistance, limiting fungal germ tube development
or appressorium formation and contributing to the
cell wall strengthening (lignins), thus preventing the
plant tissue colonisation (P et al. 2002). The
induction of the phenolic biosynthesis pathway by
both inducers might therefore actively contribute to
the resistance to U. pisi. In order to confirm this hy-
pothesis, a proteomic approach was applied (B
et al. 2012b). Two-dimensional electrophoresis (2-DE)
was used in order to compare the leaf proteome of the
susceptible and the partially resistant pea genotypes
in response to parasite infection under the effect
of BTH and BABA. Multivariate statistical analysis
identified 126 differential protein spots under the
experimental conditions (genotypes/treatments). All
of these 126 protein spots were subjected to MALDI-
TOF/TOF mass spectrometry to deduce their pos-
sible functions. A total of 50 proteins were identified
using a combination of peptide mass fingerprinting
(PMF) and MSMS fragmentation. Most of the identi-
fied proteins corresponded to enzymes belonging to
photosynthesis, metabolism, biosynthesis, binding
and defence response, whose behaviour pattern was
different in relation to susceptibility/resistance of the
studied genotypes and to the BTH/BABA induction
to pathogen response. Results obtained in this work
suggested that plants could reduce their photosyn-
thesis and other energy metabolism and enhance
the production of defence-related proteins to cope
with the stress. On the other side, we postulated that
resistance induced by the chemicals operates via
different mechanisms: BABA inducer could act via
phenolic biosynthesis pathway, whereas resistance
provided by BTH inducer seems to be mediated by
defence and stress-related proteins. These results
provide a step to understand the molecular basis of
the induced resistance to rust in pea. Nevertheless,
a higher collection of candidates will be essential
to elucidate target key elements involved in SAR
response using integrated studies.
CONCLUSIONS
Pea rust is a serious disease of pea of the world-
wide distribution. Although no completely effective
source of resistance has been found, considerable
progress has been made in identifying germplasm
with moderate levels of resistance. The effectiveness
of these incomplete levels of resistance in reducing
U. pisi infection remains to be quantified, but might
represent a major progress when compared to the
lack of any means for the control of this rust one
or two decades ago. Peas can be protected now by
combining this resistance with cultural management
options, selective fungicides and by biocontrol agents
representing opportunities that did not exist before.
The current focus in applied breeding is taking
advantage of biotechnological tools to develop more
and better markers to allow marker-assisted selection
with the hope that this will accelerate the delivery of
improved cultivars to the farmer. Our understand-
ing of the genetics of resistance to pea rust in the
available germplasm has improved considerably,
but progress in marker development and delivery
of useful markers is still limited. We are currently
facing an accelerated progress in genomic and bio-
technological research, which should soon provide
important understandings on pathogen-host interac-
tions and will provide candidate genes for resistance
to pea rust. The effectiveness of MAS might soon
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Review Czech J. Genet. Plant Breed., 50, 2014 (2): 135–143
increase with the adoption of new improvements in
marker technology together with the integration of
comparative mapping and functional genomics. For
this reason, the new genome-wide approach is emerg-
ing as a powerful tool for identifying quantitative
characters, and its application to U. pisi resistance
offers a significant potential.
Comprehensive studies on the host status and
virulence of causal agents are often missing being
a major limitation for any breeding programme.
Only after a significant input to improve the exist-
ing knowledge of the biology of causal agents as
well as of the host plant, resistance breeding will be
accelerated efficiently.
Acknowledgements. e authors would like to thank pro-
jects AGL2011-22524, co-financed by FEDER for financial
support and to Ana Moral for technical assistance along the
years. Eleonora Barilli is postdoc funded by I3P program.
References
A B., P A.B. (1990): Association of rust resist-
ance with some biochemicals in peas. Indian Journal of
Horticulture, 47: 66–69.
A E., C Y. (2007): Comparative efficacy of sys-
temic acquired resistance-inducing compounds against
rust infection in sunflower plants. Phytopathology, 97:
179–186.
A P., I A. (2008): Adaptation strat-
egy, germplasm type and adaptive traits for field pea
improvement in Italy based on variety responses across
climatically contrasting environments. Field Crop Re-
search, 108: 133–142.
B E., S J.C., R D. (2009a): Characteri-
zation of resistance mechanisms to Uromyces pisi in pea.
Plant Breeding, 128: 665–670.
B E., S J.C., F-A M., R-
D. (2009b): Identification of resistance to Uromyces
pisi (Pers.) Wint. in Pisum spp. germplasm. Field Crop
Research, 114: 198–203.
B E., S J.C., S A., R D. (2009c):
Differential response of pea (Pisum sativum) to rusts
incited by Uromyces viciae-fabae and U. pisi. Crop Pro-
tection, 28: 980–986.
B E., R D., T A.M. (2010a): Mapping
of quantitative trait loci controlling partial resistance
against rust incited by Uromyces pisi (Pers.) Wint. in
a Pisum fulvum L. intraspecific cross. Euphytica, 175:
151–159.
B E., S J.C., R D. (2010b): Induc-
tion of systemic acquired resistance in pea against rust
(Uromyces pisi) by exogenous application of biotic and
abiotic inducers. Journal of Phytopathology, 158: 30–34.
B E., P E., R D. (2010c): Benzothia-
diazole and BABA improve resistance to Uromyces pisi
(Pers.) Wint. in Pisum sativum L. with an enhancement of
enzymatic activities and total phenolic content. European
Journal of Plant Pathology, 128: 483–493.
B E., S Z., S J.C., R D., T
A.M. (2011): Phylogenetic analysis of Uromyces species
infecting grain and forage legumes by sequence analysis
of nuclear ribosomal Internal Transcribed Spacer region.
Journal of Phytopathology, 159: 137–145.
B E., M A., S J.C., R D. (2012a):
Clarification on rust species potentially infecting pea
(Pisum sativum L.) crop and host range of Uromyces pisi
(Pers.) Wint. Crop Protection, 37: 65–70.
B E., R D., C M.A. (2012b): Com-
parative proteomic analysis of BTH and BABA-induced re-
sistance in pea (Pisum sativum) toward infection with pea
rust (Uromyces pisi). Journal of Proteomics, 75: 5189–5205.
C B., C K., P C. (2003): Les pro-
téagineux: intérêt dans les systémes de production four-
ragers français et européens. Fourrages, 174: 163–182.
C R., S C.P., S B.D., S S.B.
(2006): Identification and characterization of slow rusting
components in pea (Pisum sativum L.). Genetic Resources
and Crop Evolution, 53: 219–224.
C G.B. (1978): Rust Fungi on Legumes and Com-
posites in North America. University of Arizona Press,
Tucson, 351–353.
E A.A., S J.C., N R.E., R D. (2005):
Infection structures of host-specialized isolates of Uro-
myces viciae-fabae and of others Uromyces infecting
leguminous crops. Plant Disease, 89: 17–22.
E A.A., R B., S J.C., S Z., R-
D. (2008): Genetic variation among and within
Uromyces species infecting legumes. Journal of Phyto-
pathology, 156: 419–424.
E A.A., S J.C., F-A M.,
R D. (2011): Chemical control of faba bean rust
(Uromyces viciae-fabae). Crop Protection, 30: 907–912.
EPPO (2012): Standards Pea. Available at http://archives.
eppo.org/EPPOStandards/PP2_GPP/pp2-14-e.doc (ac-
cessed December 13, 2012).
F D.F., R A.Y., P M.E. (2008): Fungal data-
bases. Available at http://nt.ars-grin.gov/fungaldatabases.
Systematic Mycology and Microbiology Laboratory, ARS,
USDA.
F-A M., B E., M F., R-
D. (2011): Identification and characterisation of
resistance against rust (Puccini a allii) in garlic (Alliumsp.)
germplasm. Annals of Applied Biology, 159: 93–98.
142
Czech J. Genet. Plant Breed., 50, 2014 (2): 135–143 Review
H I.H.M.H.B., S F.L., M D.R.
(2001): Evaluating faba beans for rust resistance using
detached leaves. Euphytica, 117: 47–57.
I M., F F. (2003): Benzothiadiazole (BTH) induces
cell-death independent resistance in Phaseolus vulgaris
against Uromyces appendiculatus. Journal of Phytopa-
thology, 151: 171–180.
J S., P P., I H. (2008): Ultrastructural study on
Acibenzolar-S-methyl-induced scab resistance in epider-
mal pectin layers of Japanese pear leaves. Phytopathology,
98: 585–591.
K R.P., R R.S. (1987): Genetics of rust resistance
in pea. Indian Journal of Genetics and Plant Breeding,
47: 46–48.
K T.B.A., R K.T., R K. (1994): Assess-
ment of tall field pea genotypes for slow rusting resist-
ance. Legume Research, 17: 79–82.
K C., C R., S C. (2006): Role
of aeciospores in outbreaks of pea (Pisum sativum) rust
(Uromyces fabae). European Journal of Plant Pathology,
115: 323–330.
M E., R D., M A., M M.T., M-
T., G J., R J. (2008): Mechanism and molecular
markers associated with rust resistance in a chickpea
interspecific cross (Cicer arietinum × Cicer reticulatum).
European Journal of Plant Pathology, 121: 43–53.
M K. (1978): Attachment of bean rust cell wall
material to host and non-host plant tissue. Archives of
Microbiology, 119: 113–117.
N R.E. (1986): Failure of haustorial development as a
factor in slow growth and development of Puccinia hordei
in partially resistant barley seedlings. Physiological and
Molecular Plant Pathology, 28: 309–322.
N R.E., R D. (2002): Potentially durable resist-
ance mechanisms in plant to specialized fungal patho-
gens. Euphytica, 124: 201–216.
P A.B., B H.S., S H.S., R R.D. (1979):
Studies on inheritance to rust (Uromyces fabae (Pers) de
Barry) on peas. SABRAO Journal, 11: 101–103.
P A.B., B H.S., R R.D.,U B.A.
(1980): Field resistance of pea germplasm to powdery
mildew (Erysiphe polygoni) and rust (Uromyces fabae).
Plant Disease, 64: 1085–1086.
P J.E. (1983): Models explaining the specificity
and durability of host resistance derived from the obser-
vations on the barley-Puccinia hordei system. In: L-
F., W J.M., V G N.A. (eds.): Durable
Resistance in Crops. Plenum Press, New York, 57–80.
P J.E., V O A. (1975): Partial resist-
ance of barley rust, Puccinia hordei. II. Relationship
between field trials, microplot tests and latent period.
Euphytica, 24: 293–303.
P M., R B. (2000): Pollinator-mediated interac-
tions between a pathogenic fungus, Uromyces pisi (Puc-
ciniaceae), and its host plant, Euphorbia cyparrissias
(Euphorbiaceae). American Journal of Botany, 87: 48–55.
P P.E. (1952): Etude physiologique du parasitisme de
l’Uromyces pisi (Pers.) de By., sur l’Euphorbia cyparissias
L. Experientia, 9: 300–302.
P E., R D., J J. (2002): Acibenzolar-S-
methyl-induced resistance to sunflower rust (Puccinia
helianthi) is associated with an enhancement of cou-
marins on foliar surface. Physiological and Molecular
Plant Pathology, 60: 155–162.
P E., L M.J., J J., R D. (2007a):
Constitutive coumarin accumulation on sunflower leaf
surface prevents rust germ tube growth and appressorium
differentiation. Crop Science, 47: 1119–1124.
P E., M F., R-M M.M., R
D. (2007b): Differential effects of phenylalanine ammonia
lyase, cinnamyl alcohol dehydrogenase, and energetic
metabolism inhibition on resistance of appropriate host
and nonhost cereal–rust interactions. Phytopathology,
97: 1578–1583.
R R., S A.K., S B.D., J A.K., C R.,
S C.P. (2011): Molecular mapping for resistan-
ce to pea rust caused by Uromyces fabae (Pers.) de-Bary.
Theoretical and Applied Genetics, 123: 803–813.
R-M M.M., R D., P E., S J.C.
(2007): Effects of phenylpropanoid and energetic metabo-
lism inhibition on Faba bean resistance mechanisms to
rust. Phytopathology, 97: 60–65.
R D., N R.E. (1995): Characterization of Lr34,
a major gene conferring nonhypersensitive resistance to
wheat leaf rust. Plant Disease, 79: 1208–1212.
R D., N R.E. (1996): e pre-appressorial avoid-
ance mechanism to rust fungi in Hordeum chilense geno-
types. Physiological and Molecular Plant Pathology, 49:
89–101.
R D., S J.C. (2003): Uromyces viciae-fabae
haustorium formation in susceptible and resistant faba
bean lines. European Journal of Plant Pathology, 109:
71–73.
R D., M A. (2004): Prehaustorial resistance
against alfalfa rust (Uromyces striatus) in Medicago
truncatula. European Journal of Plant Pathology, 110:
239–243.
R D., A M.J., D C., B J.
(2011a): Pea (Pisum sativum L.). In: P V
M., T A.M., C J.I., K C. (eds): Genetics,
Genomics and Breeding of Cool Season Grain Legumes.
Science Publishers, Enfiled, New Hampshire, 1–49.
R D., C M.A., M E., B E.,
R N. (2011b): Legume breeding for rust resistance:
143
Review Czech J. Genet. Plant Breed., 50, 2014 (2): 135–143
lessons to learn from the modelMedicago truncatula.
Euphytica, 180: 89–98.
R D., S J.C., E A.A. (2013): Response of
vetches (Vicia spp.) to specialized forms of Uromyces vicia-
fabae and to Uromyces pisi. Crop Protection, 46: 38–43.
S M.J.Y., S J.C., R D. (2006): Identifi-
cation of resistance against a new pathotype of Puccinia
hordei with virulence for the resistance gene Rph7. Eu-
ropean Journal Plant Pathology, 115: 309–321.
S J.C., R D. (2002): Histological characteriza-
tion of resistance to Uromyces viciae-fabae in faba bean.
Phytopathology, 92: 294–299.
S J.C., M M.T., R D. (2000): Char-
acterization of new sources of resistance to Uromyces
viciae-fabae in a germplasm collection of Vicia faba.
Plant Pathology, 49: 389–395.
S J.C., F S., D J., V P
M.C., W T.D., T J., R D. (2006):
Screening techniques and sources of resistance to rusts
and mildews in grain legumes. Euphytica, 147: 255–272.
S J.C., M-A I., R D. (2012): Identi-
fication and characterization of resistance to rust (Uromy-
ces ciceris-arietini (Grognot) Jacz. & Boyd) in a germplasm
collection of Cicer spp. Euphytica, 188: 229–238.
S R.M., S C.P. (1985): Evaluation, classifi-
cation and usefulness of pea germplasm for quantitative
characters. Legume Research, 8: 68–73.
S R.A., D R.K., C R.G. (2004): Influence of
spray time of mancozeb on pea rust caused by Uromyces
viciae-fabae. Indian Journal of Agricultural Sciences,
74: 502–504.
S P., A G., B J., C C.J., E
N.T.H., F A.J., F R., H M., M J.,
N P., MP K.E., R R.J., R
D., W J.L., W T.D. (2012): Pea (Pisum
sativum L.) in the genomic era. Agronomy, 2: 74–115.
S H.S., S S.S., R R.D. (1974): Varietal reac-
tion of peas to powdery mildew (Erysiphe polygoni) and
rust (Uromyces fabae). Mysore Journal of Agriculture and
Science, 8: 529–532.
S E.C., S D.M., L W.Q. (1962):
Identification of Physiologic Races of Puccinia graminis
var. tritici. USDA, Agricultural Research Service. E617.
Washington.
S G.D., MV M.A. (1987): Partial resistance to
Uromyces appendiculatus in dry edible beans. Phytopa-
thology, 77: 1101–1103.
T R., R H.J. (1990): Resistance of wheat to
Puccinia g raminis f. sp. tritici association of the hypersen-
sitive reaction with the cellular accumulation of lignin-
like material and callose. Physiological and Molecular
Plant Pathology, 36: 109–120.
V L L.C. (2001): Systemic induced resistance. In:
S A.J., F R.S.S., V L L.C. (eds):
Mechanisms of Resistance to Plant Diseases. Kluwer
Academic Publishers, Dordrecht, 521–574.
V P M.C., R D. (2009a): Identification and
characterization of partial resistance to rust in a germ-
plasm collection of Lathyrus sativus L. Plant Breeding,
128: 495–500.
V P M.C., F-A M., M A.,
R D. (2009b): Pre and posthaustorial resistance
to rusts in Lathyrus cicera L. Euphytica, 165: 27–34.
V S., Y K., K C., S S.B.,
S C.P., C R., S B.D. (2005): Identi-
fication of RAPD markers linked to the rust (Uromyces
fabae) resistance gene in pea (Pisum sativum). Euphytica,
144: 265–274.
W W.K. (1976): Appressorial formation over stomata
by bean rust: Response to a surface contact stimulus.
Phytopathology, 66: 136–146.
X A.G., W T.D. (2001): Reaction of field pea
varieties to three isolates of Uromyces fabae. Plant Sci-
ence, 82: 253–255.
Receieved for publication June 16, 2013
Accepted after corrections November 27, 2013
Corresponding author:
Dr. E B, Institute for Sustainable Agriculture, Spanish National Research Council (CSIC),
Apdo. 4084, E-14080 Córdoba, Spain; e-mail: ebarilli@ias.csic.es