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Plant Disease / January 2005 17
Infection Structures of Host-Specialized Isolates of Uromyces viciae-fabae
and of Other Species of Uromyces Infecting Leguminous Crops
A. A. Emeran, Instituto de Agricultura Sostenible (CSIC), Apdo 4084, 14080 Córdoba, Spain; J. C. Sillero, CIFA
Alameda del Obispo, Apdo 4240, 14080 Córdoba, Spain; R. E. Niks, Department of Plant Breeding, P.O. Box 386,
6700 AJ Wageningen, The Netherlands; and D. Rubiales, Instituto de Agricultura Sostenible (CSIC), Córdoba, Spain
Many species of Uromyces can cause
important diseases of grain legume and
forage legume crops: Uromyces appen-
diculatus (Pers.:Pers.) Unger on common
bean (Phaseolus vulgaris L.), U. ciceris-
arietini Jacz. in Boyer & Jacz. on chickpea
(Cicer arietinum L.), U. lupinicolus Bub.
on lupine (Lupinus albus L.), U. pisi
((Pers.) D.C.) Wint. on pea (Pisum sativum
L.) and grasspea (Lathyrus sp.), U. striatus
J. Schröt. on alfalfa (Medicago sativa L.),
U. viciae-fabae (Pers.) J. Schröt. on faba
bean (Vicia faba L.), and U. vignae Bar-
clay on cowpea (Vigna unguiculata (L.)
Walp.) (13).
Identification of species of Uromyces on
legumes currently is based on the mor-
phology of telia, teliospores, uredinia, and
urediniospores. In many cases, however,
telia are not available because their forma-
tion depends on rust species, host proper-
ties, and environmental conditions. Addi-
tionally, rust species often are difficult to
identify on the basis of urediniospore mor-
phology alone; two common features,
germ pore number and arrangement, may
not be easy to determine and often are not
diagnostic in any case. The host species
also is used in identification, but several
rust species may infect the same host plant
species. It also is possible that a rust fun-
gus may infect a plant species that previ-
ously was thought to be resistant.
The morphology of infection structures
of rust fungi may be helpful in the diagno-
sis of rust species and subspecific taxa
(11,12,21). The infection structures of rust
fungi form in sequence: germ tube, appres-
sorium, substomatal vesicle (SSV), pri-
mary infection hyphae (PIH), haustorial
mother cells (HMCs), secondary hyphae
(SIH), and haustoria. In previous studies,
the morphology, dimensions, and orienta-
tion of SSV, PIH, HMC, and SIH differed
among rust species and subspecific taxa
(11,12,21).
U. viciae-fabae sensu lato has been re-
ported all over the world on dozens of
species of Lathyrus, Lens, Phaseolus,
Pisum, and Vic ia (6), although it is most
commonly reported as the rust of faba
bean (Vicia faba) (4–7,15,17,22). Its broad,
compiled host range is in conflict with a
few preliminary demonstrations of host
specialization (7,15). Species complexes
are a common phenomenon among rust
fungi (3,10). Such complexes are charac-
terized by cryptic species that are repro-
ductively isolated from one another due to
the absence of a common host. Closer
examination can reveal subtly distinctive
morphology among host-specialized spe-
cies that previously were thought to be
impossible to distinguish. Thus, further
consideration of both morphological varia-
tion and host specialization within U. vi-
ciae-fabae sensu lato would appear justi-
fied.
The first objective of this work was to
observe the morphology of infection struc-
tures of a number of species of Uromyces
that infect legume crops. Second, we
sought to determine whether isolates of U.
viciae-fabae sensu lato are host specialized
and, if so, whether infection structures of
such isolates would prove distinctive.
MATERIALS AND METHODS
Rust isolates. Twelve isolates of six rust
species on eight legumes were collected in
Spain, Morocco, Egypt, Italy, and Canada
(Table 1). Single pustule isolates were
obtained from each rust sample and in-
creased in isolation on seedlings of the
respective host species (Table 1) in sepa-
rate growth chambers with filtered ventila-
tion.
Spore morphology. Freshly collected
urediniospores and teliospores from inocu-
lated susceptible host plants were mounted
in lactophenol-ethanol and observed with
bright-field microscopy. Thirty spores
from each isolate were measured and the
color and spore surface morphology were
determined. The number and location of
the germ pores also were recorded after
mounting the urediniospores in lactophe-
nol/ethanol 0.05% trypan blue and gentle
heating.
Plant inoculation. Four plants of each
host (Table 1) with their third to fourth
leaves fully expanded were inoculated by
dusting freshly collected urediniospores
(0.5 mg/plant) mixed with pure talcum
powder (1:10, vol/vol). Isolates VICLCI1
and VICVSI1 were inoculated on P. sati-
vum cv. Messire because we found that the
infection structures could be more clearly
observed on that host than on their respec-
tive hosts. Morphology of infection struc-
tures has been reported to be independent
of the plant species on which they are
grown (11,21). This was verified by also
observing infection structures developed
on their respective hosts, confirming that
the host did not influence infection struc-
ture morphology. Inoculated plants were
incubated at 100% relative humidity at
20°C in darkness for 24 h. Lupinus albus
developed necrotic lesions after 24 h of
incubation; therefore, it was incubated for
only 8 h.
Sample preparation and observation.
At least four leaf segments (2 to 3 cm2
each) per inoculated plant were harvested
47 h after inoculation (hai). They were
fixed in acetic acid-ethanol (1:3, vol/vol)
for 30 min, boiled in 0.05% trypan blue in
lactophenol-ethanol (1:2, vol/vol) for 10
ABSTRACT
Emeran, A. A., Sillero, J. C., Niks, R. E., and Rubiales, D. 2005. Infection structures of host-
specialized isolates of Uromyces viciae-fabae and of other species of Uromyces infecting legu-
minous crops. Plant Dis. 89:17-22.
A study was made of the morphology of urediniospores and primary infection structures of 12
isolates of six legume-infecting species of Uromyces. Infection structures were sufficient to
distinguish among species. Isolates of Uromyces viciae-fabae proved to be specialized with
respect to host, because each isolate infected only cultivars of the species from which it was
collected. Host-specialized isolates of U. viciae-fabae also were morphologically distinct, differ-
ing in both spore dimensions and infection structure morphology. In particular, the shape and
dimensions of the substomatal vesicle were distinctive. These results support the view that U.
viciae-fabae sensu lato is a species complex.
Additional keywords: rust, teliospore
Corresponding author: D. Rubiales
E-mail: ge2ruozd@uco.es
Accepted for publication 19 July 2004.
DOI: 10.1094/PD-89-0017
© 2005 The American Phytopathological Society
18 Plant Disease / Vol. 89 No. 1
min, and cleared in a nearly saturated
aqueous solution of chloral hydrate (5:2,
wt/vol) for at least 24 h (16). Segments
then were mounted in glycerol on object
slides for microscopy.
At least 30 germlings per leaf segment
were studied using white light, phase con-
trast microscopy at ×1,000 magnification.
Occasionally, germlings were found that
had developed malformed infection struc-
tures. These germlings were ignored. For
each germling, the morphology of infec-
tion structures, especially SSV and PIH,
was determined. This included dimension
and shape of the SSV, presence or absence
of septa, and number, diameter, and orien-
tation of PIH. Typical germlings per spe-
cies were photographed.
Host range of U. viciae-fabae. Seed-
lings of two cultivars each of V. faba, V.
sativa L., and Lens culinaris Medik. were
inoculated in the growth chamber as indi-
cated above with isolates VICI1, VICVS,
and VICLC, collected on V. faba, V. sativa,
and L. culinaris, respectively. Twelve days
after inoculation, infection type (IT) and
disease severity (DS) were assessed. IT
was recorded following the scale of Stak-
man et al. (19), where 0 = no symptoms, ;
= necrotic flecks, 1 = minute pustules
Tab le 2 . Features of urediniospores and teliospores of different Uromyces spp. infecting legume cropsx
Urediniospore Teliospore dimensions (µm)
Avg. dimensions (µm) Germ pores Pedicel
Rust sample Length Width Avg. no. Positiony Length Width Length Widthz Apex length
Uromyces ciceris-arietini (CICE1) 20.7 d 19.8 ab 6.8 a Scattered 20.3 e 18.3 c 5.8 d 7.3 b nd
U. lupinicolus (LUPI1) 20.5 d 19.7 b 3.0 c Scattered 20 e 17.6 cd nd nd nd
U. pisi (PISI1) 20.8 d 19.8 ab 3.9 b Near. eq. 22 d 17 d 25.3 c 5.2 c nd
U. striatus (STRI1) 19.7 e 18.2 c 6.0 c Eq. 20.3 e 16.1 e 5.5 d 3.6 d nd
U. viciae-fabae ex Vicia faba (VICI1) 24.2 a 20.5 a 3.5 b Eq. to near. eq. 31 a 22.7 a 66.9 a 7.3 b 7 a
U. viciae-fabae ex V. sativa (VICVSI1) 21.7 c 18.3 c 3.6 b Eq. to near. eq. 27.2 c 20.7 b 51.6 b 7.4 b 6.3 b
U. viciae-fabae ex Lens culinaris (VICLCI1) 21.4 cd 19.9 ab 3.4 bc Eq. to near. eq. 29.3 b 21.0 b 52.0 b 9.0 a 5.1 c
U. vignae (VIGN1) 23.4 b 20.1 ab 1.9 d Supraeq. 31 a 20.8 b 23.2 c 7.3 b 3.5 d
x Means within a column followed by the same letter are not significantly different according to Duncan’s multiple-range test (P < 0.05).
y Near. = nearly, eq. = equatorial, avg. = average, nd = not determined.
z Pedicel width at union with spore.
Tab le 1 . Host and origin of rust isolates
Isolate Species Collected on Geographic origin Multiplied on
CICE1 Uromyces ciceris-arietini Chickpea (Cicer arietinum) Córdoba, Spain Chickpea cv. Fardón
LUPI1 U. lupinicolus Lupine (Lupinus albus) Huelva, Spain Lupin cv. Arthur
PISI1 U. pisi Pea (Pisum sativum) Córdoba, Spain Pea cv. Messire
PISI2 U. pisi Pea (Pisum sativum) Winnipeg, Canada Pea cv. Messire
PISI3 U. pisi Pea (Pisum sativum) Kafr El-Sheikh, Egypt Pea cv. Messire
STRI1 U. striatus Alfalfa (Medicago sativa) Jerez, Spain Alfalfa cv. Baraka
VICI1 U. viciae-fabae ex V. faba Faba bean (Vicia faba) Córdoba, Spain Faba bean cv. Baraca
VICI2 U. viciae-fabae ex V. faba Faba bean (Vicia faba) Kafr El-Sheikh, Egypt Faba bean cv. Baraca
VICI3 U. viciae-fabae ex V. faba Faba bean (Vicia faba) Sicily, Italy Faba bean cv. Baraca
VICVSI1 U. viciae-fabae ex V. sativa Common vetch (Vicia sativa) Córdoba, Spain Common vetch line A-01
VICLCI1 U. viciae-fabae ex L. culinaris Lentil (Lens culinaris) Morocco Lentil cv. Eston
VIGN1 U. vignae Cowpea (Vigna unguiculata) Kafr El-Sheikh, Egypt Cowpea local cultivar
Fig. 1. Teliospores of A, Uromyces ciceris-arietini, B, U. lupinicolus, C, U. pisi, D, U. striatus, E, U. viciae-fabae ex Vicia fabae, and F, U. vignae. The bar
represents 10 µm.
Plant Disease / January 2005 19
barely sporulating, 2 = necrotic halo sur-
rounding small pustules, 3 = chlorotic
halo, and 4 = well-formed pustules with no
associated chlorosis or necrosis. DS was
recorded as a visual estimation of the per-
centage of leaf area covered by rust pus-
tules.
RESULTS
Urediniospore and teliospore morphol-
ogy of rust species differed in quantitative
traits, such as number and position of
germ pores of the urediniospores and
length and width of the teliospores, and in
qualitative traits, such as presence or ab-
sence of a thick apex on the teliospores
(Table 2; Fig. 1).
Infection structures of the rust species
studied were distinct. SSVs of U. ciceris-
arietini were globoid, normally with one
protrusion but occasionally two. Two PIH
or, rarely, one of semivertical orientation
Fig. 2. Micrographs of germlings of leguminous rust fungi in whole mount preparations of seedling leaves. The bars represents 10 µm. A, Uromyces ciceris-
arietini. Note the protrusion (arrow) and two primary infection hyphae (PIH) that formed from the substomatal vesicle (SSV). B, Germling of U. lupinicolus.
The SSV is narrowly oblong with three PIH (arrows). C, SSV of U. pis i. D, Germling of U. striatus. The SSV has three protrusions (arrows) and three PIH.
E, Germling of U. viciae-fabae ex Vicia fabae. Note the septa (arrows). F, Germling of U. viciae-fabae ex Lens culinaris. The SSV is globoid and has two
PIH. G, Germling of U. viciae-fabae ex V. sativa. The SSV has a croissant-like shape with four PIH (arrows). H, Clear globoid SSV of U. vignae.
20 Plant Disease / Vol. 89 No. 1
grew from the SSV (Figs. 2A and 3A).
SSVs of U. lupinicolus were irregular and
more or less narrowly oblong to globoid,
from which two to many PIH grew with
semivertical orientation (Figs. 2B and 3B).
SSVs of U. pisi were oblong to oval, with
both ends curved deeply into the meso-
phyll to form one PIH each. Because of
this vertical orientation of PIH, germlings
were difficult to photograph (Figs. 2C and
3C). The two additional samples of U. pisi
sampled from Canada and Egypt also
showed this morphology. SSVs of U. stria-
tus were more or less globoid, with one to
four protrusions and one to three PIH. The
protrusions may be initials of PIH, and
could have delimited an HMC. PIH started
horizontally but then grew semivertically
(Figs. 2D and 3D). SSVs of U. vignae
were globoid with one PIH, which grew
vertically but then horizontally, and
branched to form a network of hyphae
(Figs. 2H and 3H).
The host-specialized isolates of U. vi-
ciae-fabae were similar in general shape
and color of spores, but differed in spore
dimensions (Table 2) and in infection
structure morphology (Table 3). Uredinio-
spores of the three samples were globoid
or ovoid, yellowish brown, and echinulate,
with three to four equatorial to nearly
equatorial germ pores. Teliospores were
ovoid to subgloboid, dark amber brown, and
smooth, with long, golden-yellow pedicels.
The isolate of U. viciae-fabae ex V. faba
differed significantly from the other two in
urediniospore and teliospore dimensions,
length of the teliospore pedicels, and apex
length. There were significant differences
between the isolates from V. s a tiva and L.
culinaris in teliospore length, pedicel width,
and apex length (Table 2).
SSVs of U. viciae-fabae ex V. faba were
fusiform to cylindrical tubes, growing as a
continuum from the appressorium directly
into the mesophyll; therefore, at one pole
there was the appressorium and at the
other pole two PIH were formed that grew
horizontally. Occasionally a septum was
present in the PIH (Figs. 2E and 3E). The
two additional samples of U. viciae-fabae
ex V. faba collected in Egypt and Italy also
showed this morphology.
SSVs of U. viciae-fabae ex L. culinaris
had no consistent shape. They varied from
oval to globoid, normally with two PIH.
Most of the PIH had a vertical orientation
(Figs. 2F and 3F). The SSV of U. viciae-
fabae ex V. s a t iva also were variable, rang-
ing from oval to croissant-like, sausage-
like, or triangular. The SSVs had three to
four PIH, arising from various positions.
They often showed a swelling where side
branches arose. The orientation of the PIH
was semivertical (Figs. 2G and 3G).
The three isolates of U. viciae-fabae,
each collected from a different host spe-
cies, only caused substantial infection on
cultivars of the species from which they
were collected (Table 4). This suggests that
U. viciae-fabae sensu lato consists of host-
specialized populations.
DISCUSSION
The morphology of infection structures
was found to provide additional character-
istics to identify rust taxa independently
from the host, as reported for rusts of
grasses (11,21) and onions and leeks (12).
In the present work, the morphology of
infection structures was similar for three
U. pisi isolates and also for three isolates
of U. viciae-fabae ex V. faba from three
provenances. These results provide pre-
liminary support for the conclusion that the
morphology of infection structures hardly
varies within taxa, as has been dem-
onstrated in grass rusts (11,21). The germ-
ling morphology of the VICLCI1 isolate of
U. viciae-fabae ex L. culinaris was very
similar irrespective of whether they devel-
oped on pea or on lentil. Although the
structures were more easily observed on
pea, their morphology was not affected by
the host. The same applies for isolate
VICVSI1 of U. viciae-fabae ex V. sativa,
for which infection structures were the
same on pea and common vetch. The inde-
pendence of infection structure morphol-
ogy from plant species in which the infec-
tion takes place also has been reported for
grass rusts (11,21).
Fig. 3. Drawing of typical germlings of leguminous rust isolates. A, Uromyces ciceris-arietini. Note
the protrusion and two primary infection hyphae (PIH) that formed from the substomatal vesicle
(SSV). B, Germling of U. lupinicolus. The SSV is narrowly oblong with three PIH. C, SSV of U. pisi.
D, Germling of U. striatus. The SSV has three protrusions and three PIH. E, Germling of U. viciae-
f
abae ex Vic ia fa ba. Note the septa. F, Germling of U. viciae-fabae ex Lens culinaris. The SSV is
globoid and has two PIH. G, Germling of U. viciae-fabae ex V. sativae. The SSV has a croissant-like
shape with four PIH. H, Clear globoid SSV of U. vignae.
Plant Disease / January 2005 21
The procedure followed here is simple
and does not require microtomy. However,
a drawback of infection-structure morphol-
ogy as a character for identification is the
requirement of viable inoculum. Thus,
herbarium specimens cannot be included
in such studies. The method also is not as
sensitive as identification on the basis of
molecular markers (23). On the other hand,
even when teliospores are available, U.
lupinicolus and U. ciceris-arietini are dif-
ficult to distinguish (Fig 1; Table 2), but
their infection structures are distinctive
(Fig 2; Table 3). U. vignae could be sepa-
rated from all other rusts used in this study
on the basis of teliospore morphology
(Table 2; Fig 1), but teliospores of U.
vignae are similar to those of U. appen-
diculatus (4); therefore, it would be useful
to see if the morphology of germlings can
separate these two species.
The differences in infection structures
among species may be exploited in certain
phytopathological studies, where a host is
inoculated with two rust species to investi-
gate induced resistance and induced sus-
ceptibility. Infection structures also could
be useful in epidemiological studies in-
volving several rust taxa where it is neces-
sary to identify individual sporelings for
which the host is unknown (e.g., trapped
airborne spores). These differences also
could be useful to quantify contamination
of inoculum by a second species or to
carry out competition studies involving
several species; for example, in studies of
C. arietinum infected with both U. ciceris-
arietini and U. striatus (8,18) or pea in-
fected with both U. pisi and U. viciae-fa-
bae (13). The differences between germ-
lings of each taxon were substantial and
should enable differentiation of the two
species at the level of individual spore-
lings.
The present study confirmed that U. vi-
ciae-fabae sensu lato is a species complex.
Cummins (4) stated that U. viciae-fabae is
circumglobal on Lathyrus, Pisum, and
Vic ia spp., with V. faba the host of the
neotype. However, we demonstrated here
the existence of host-specialized isolates
that cannot infect V. faba. A degree of host
specialization within U. viciae-fabae was
already acknowledged by Gäumann (7),
but all the formae speciales suggested by
Gäumann were able to infect V. faba. Sey-
mour (15) also reported that the rust of V.
sativa did not infect V. faba, but did not
study the morphology of that rust and sim-
ply considered it to be a race of U. viciae-
fabae. Our data indicate that U. viciae-
fabae may be subdivided into populations
with differential pathogenicity to V. faba,
V. sativa, or L. culinaris (Tables 2 and 4).
More research is needed to further clarify
the ultimate classification of the U. viciae-
fabae complex.
The rust of pea has been ascribed to ei-
ther U. viciae-fabae (1,4,7) or U. pisi
(7,14,20,22). Our three pea isolates, col-
lected in Spain, Canada, and Egypt, belong
to U. pisi based on infection structures and
host range. We cannot exclude the possi-
bility of U. viciae-fabae isolates infecting
pea. In fact, we have observed high levels
of infection on pea in the growth chamber
after inoculation with U. viciae-fabae iso-
lates from faba bean, but we were unable
to get U. viciae-fabae established in the
field in any of 200 pea accessions, even
after repeated artificial inoculations (un-
published results). It would be interesting
to attempt to confirm reports of infections
of pea by U. viciae-fabae under field con-
ditions (2,9,17).
This is the first report of U. lupinicolus
on Lupinus albus, U. striatus on Medicago
sativa, U. viciae-fabae on Vicia sativa, and
U. pisi on P. sativum occurring in Spain.
All were collected in the south of the coun-
try. U. lupinicolus and U. striatus were
observed late in the crop season and
caused little damage. U. viciae-fabae on
vetch and U. pisi, observed early in the
crop season in small experimental plots,
appeared to be quite aggressive pathogens
in those plots, and could become serious
agricultural problems.
ACKNOWLEDGMENTS
We thank A. Moral for technical assistance, S.
Fondevilla for the drawings of Figure 3, and project
AGL2002-03248 of Spanish CICYT (Comisión
Interministerial de Ciencia y Tecnología) for finan-
cial support.
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Tab le 3 . Features of primary infection structures of different Uromyces spp. infecting legume cropsx
Substomatal vesicle
Primary infection hyphae Avg. dimension (µm) Avg. number
Rust sample Number Growthy Avg. width (µm) Shapez Length Width Protrusions Septa
Uromyces ciceris-arietini (CICE1) 2 SV 4.7 ef Glob 13.1 f 11.9 bc 1.1 0
U. lupinicolus (LUPI1) >2 SV 5.2 bc Ob to glo 13 f 10.9 cd 0 0
U. pisi (PISI1) 2 V 4.2 g Ob to oval 16.5 cd 9.7 e 0 0
U. striatus (STRI1) 1–3 SV 4.8 e Glo 15.2 de 12 bc 2.3 0
U. viciae-fabae ex V. faba (VICI1) 2 H 4.9 de Fus to cyn 29.9 a 9.8 de 0 0.4
U. viciae-fabae ex V. sativa (VICVSI1) 3–4 SV 5.6 a Oval to cro 17.7 c 13.7 a 0 0
U. viciae-fabae ex L. culinaris (VICLCI1) 2 V 5.3 ab Oval to glo 20.1 b 11.8 c 0 0
U. vignae (VIGN1) 1 V then H 4.4 fg Glo 14 ef 12.5 b 0 0
x Means within a column followed by the same letter are not significantly different according to Duncan’s multiple-range test (P < 0.05).
y Direction of growth: SV = semivertical, V = vertical, H = horizontal.
z Glo = globoid, Ob = oblong, Fus = fusiform, cyn = cylindrical, cro = croissant-like.
Tab le 4 . Host range of Uromyces viciae-fabae isolatesz
U. viciae-fabae ex
V. faba (VICI1)
U. viciae-fabae ex
V. sativa (VICVSI1)
U. viciae-fabae ex
L. culinaris
(VICLCI1)
Host (entrada) IT DS (%) IT DS (%) IT DS (%)
V. faba cv. Amcor 4 25 0 0 0 0
V. faba cv. Baraca 4 30 0 0 0 0
L. culinaris cv. Indian Head 0 0 0 0 4 30
L. culinaris cv. Eston ; 0 1 1 4 30
V. sativa line V01 0 0 4 15 0 0
V. sativa line V08 0 0 4 20 0 0
z IT = infection type, on a 0-to-4 scale according to Stakman et al. (19) and DS = disease severity
expressed as percentage of leaf area covered by rust symptoms.
22 Plant Disease / Vol. 89 No. 1
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