Comparative morphology of uredinia and urediniospores of six Puccinia species parasitic on Poaceae in Saudi Arabia

Abstract

Uredinia and urediniospores of six Puccinia species growing on Poaceae in southwestern Saudi Arabia were morphologically compared by light and scanning electron microscopy (SEM). Puccinia cenchri, P. fragosoana and P. isiacae were recorded for the first time in Saudi Arabia. Many differences between uredinia and urediniospores of studied Puccinia species were recorded. These differences are not related to host plant but may be due to the species of Puccinia itself. Observations by SEM led to more information in distinguishing between these Puccinia species particularly the presence of paraphyses and density and length of spines.

Full text

COMPARATIVE MORPHOLOGY OF UREDINIA AND
UREDINIOSPORES OF SIX PUCCINIA SPECIES
PARASITIC ON POACEAE IN SAUDI ARABIA
ZAKARIA A.M. BAKA*, HUSSIEN M. ALWADIE and YASSER S. MOSTAFA
Department of Biology, College of Science, King Khalid University, Abha PO Box 9004, Saudi Arabia.
(Received 20 November 2003)
Uredinia and urediniospores of six Puccinia species growing on Poaceae in southwestern Saudi Arabia were
morphologically compared by light and scanning electron microscopy (SEM). Puccinia cenchri,P. fragosoana
and P. isiacae were recorded for the first time in Saudi Arabia. Many differences between uredinia and
urediniospores of studied Puccinia species were recorded. These differences are not related to host plant but
may be due to the species of Puccinia itself. Observations by SEM led to more information in distinguishing
between these Puccinia species particularly the presence of paraphyses and density and length of spines.
Keywords:Puccinia; Rust fungi; Saudi Arabia; SEM; Urediniospores
INTRODUCTION
Fungi belonging to the order Uredinales are commonly referred to as rust fungi. Rust
fungi, which are obligate pathogens of vascular plants, are unique in possessing up to
six morphological and functional spore state, which can exist in one species (Hiratsuka,
1988). Peterson (1974) pointed out that the life cycle of a rust fungus exhibits an
extremely plastic and usually complex series of events.
Puccinia is the major genus of the family Pucciniaceae and represents a significant
proportion of all known rust fungi. It includes autoecious, heteroecious, macrocyclic
and microcyclic species that occur on an extremely wide range of angiospermous hosts
(Brown and Brotzman, 1979).
Although various techniques of molecular biology now contribute to our under-
standing of fungal systematics, fungi are mostly classified on the basis of their
morphology and a good knowledge of morphological features, life cycles, and
biotrophic interactions with host plants remains necessary for the identification of
rust fungi (Hiratsuka and Sato, 1982), and for their investigation as important plant
*Corresponding author: Dr Zakaria A.M. Baka, Department of Biology, College of Science, King Khalid
University, Abha PO Box 9004, Saudi Arabia. Tel: 00966 7 2280942. Fax: 00966 7 2290165. E-mail:
zakariabaka@hotmail.com
Permanent address for Dr Zakaria A.M. Baka: Department of Botany, Faculty of Science, University of
Mansoura, Mansoura, Egypt
Archives of Phytopathology and Plant Protection
May, 2004, Vol. 37, pp. 89 –101
ISSN 0323-5408 print; ISSN 1477-2906 online #2004 Taylor & Francis Ltd
DOI: 10.1080/0323540042000202685

pathogens or potential biological control agents. It is very important to have a good
understanding of morphological features, life cycles, and host –rust relationships in the
study of rust fungi as important plant pathogens or interesting biological agents.
Uredinia, in which urediniospores, the abundant ‘repeating spore’ state of rust fungi,
are produced on a dikaryotic mycelium, arise from infection of compatible host plants
by dikaryotic urediniospores from the same host species or by aeciospores produced by
dikaryotization of the haploid mycelium in the same, or the case of heteroecious rusts,
the alternate host species. Kenny (1970) recognized 14 different types of uredinia among
rust fungi, based on such characteristics as the presence or absence of bounding
structures, position of the hymenium in the host tissue, and growth pattern of the
hymenium.
The uredinial sorus may vary greatly in morphology, having a well-developed
peridium (e.g., Milesina, Pucciniastrum), or may contain paraphyses but with no or
obscure peridium (e.g., Melampsora), or be devoid of both features (e.g., most species of
Puccinia) (Cummins and Hiratsuka, 1983).
The special taxonomical problems presented by host specialization within morpho-
logically recognizable rust species have pointed out in relation to rusts on Allium
(Jennings et al. 1990). Since such physiological characteristics and the occurrence of
more than one rust species on a single host may not be reliable taxonomic criteria, the
identification of rusts is based on morphological characters (Shoemaker, 1981).
Scanning electron microscopy (SEM), which permits more detailed examination of
additional morphological features on surfaces of spores, has been used extensively in for
many taxa (Littlefield and Heath, 1979). Spore length and width have been shown to
differ between pustules, leaves or individual host plants, and also with environmental
conditions (Littlefield, 1981). Germ pore numbers is also a good taxonomic character
(Cummins and Hiratsuka, 1983) and surface ornamentation, such as spines, warts, and
reticulum on the urediniospores are sometimes of value in the identification of rust
fungi (Corlett, 1970). Savile (1965) used differences in size, the height of spines and
warts, and the average distances between their bases, to distinguish species, host limited
varieties, and geographic populations. However, the height and diameter of such
features are often less than one micron, close to the limits of resolution of the light
microscope, and are difficult to measure accurately (Corlett, 1970).
Although the diploid teliospores which usually form in the later development of the
dikaryotic mycelium, are important in the classification of rust fungi (Littlefield and
Heath, 1979), further information may be contributed by urediniospores produced
earlier in the dikaryotic phase of the life cycle. So far, no detailed studies on Saudi
rusts, particularly using high resolution microscopy, have been reported. The purpose
of the present work is to elucidate the taxonomy of six graminincolous species of
Puccinia, by comparing their uredinia and urediniospores, by both light microscopy
(LM) and SEM.
MATERIALS AND METHODS
Rust material
The leaves of hosts bearing uredinia and urediniospores of various Puccinia species were
collected from different localities in southwestern Saudi Arabia (Table I) and brought
into the laboratory.
90 ZAKARIA A.M. BAKA et al.

Light microscopy
For LM examinations, hand sections were cut from fresh material, mounted in
lactophenol containing cotton blue, examined (at 500 6) and photographed.
Dimensions of uredinia (length and width), urediniospores (length, width, wall
thickness in optical section, at the centre of the spore), were measured, using a Leitz
optical micrometer, and germ pore numbers recorded. Twenty-five leaf specimens has
been taken from five different infected plants. For each specimen, 50 uredinia and
urediniospores were measured.
Scanning electron microscopy
Small pieces of leaf were removed with a sharp razor blade and fixed for 24 h at 48Cin
2.5% glutaraldehyde in 0.1 M cacodylate buffer at pH 7.2. These small pieces were then
postfixed in 1% OsO
4
in the same buffer and at the same pH, dehydrated through a
graded series to 100% ethanol. At this point, the tissue was removed from the ethanol
and cut into many smaller pieces (Mercer and Birbeck, 1972). The pieces were quickly
returned to ethanol and then critical point dried with liquid CO
2
, mounted on
aluminum stubs with silver paint, coated with gold-palladium and examined with a
JOEL SEM. Spine density was measured as the number of spines on and within a
100 mm
2
circle about the spore surface.
RESULTS AND DISCUSSION
The morphological characteristics, observed under LM, of uredinia and urediniospores
of the six Puccinia species studied here are recorded in Tables II – VI. Light and SEM
micrographs are presented in Figures 1 – 27.
All Puccinia species studied here were characterized by uredinia arranged in elongated
files on the leaf surface parallel to the main axis of the main blade. In each case uredinial
postules were amphigenous. All Puccinia species recorded here are macrocyclic and
heterocious.
Puccinia cenchri Diet. & Holw
Holway Bot. Gaz. 24: 28 (1897).
Syn. Uredo cenchricola P. Henn., Mus. Congo Anal. 2: 223 (1908).
On Cenchrus biflorus Roxb.
TABLE I Puccinia species and their hosts under study
Puccinia species Host Locality
Puccinia cenchri Diet. & Holw Cenchrus biflorus Roxb. AsSuda
P. fragosoana Beltron Imperata cylindrica (L.) Raeuschel Khamis Musheet
P. graminis Pers. Cynodon dactylon (L.) Pers. AsSuda
P. isiacae Wint. Phragmites australis (Cav.) Trin. Abha
P. recondita Roberge ex Desm. Lolium perenne L. Khamis Musheet
P. striiformis Westend. Lolium perenne L. Khamis Musheet
91COMPARATIVE MORPHOLOGY OF PUCCINIA SPECIES FROM SAUDI ARABIA

The uredinia of P. cenchri are mainly on adaxial leaf surface, oblong, surrounded by a
ruptured epidermis, cinnamon-brown. Single pustule is up to 750 6187 mm.
Urediniospores of P. cenchri were ellipsoid, brown, 32.8 625.3 mm; wall cinnamon-
brown, 2.4 mm thick with 4– 5 equatorial germ pores, echinulate, spine density was
11.52, spine length was 0.80 mm. The distance between spines was 1.53 mm.
Puccinia cenchri was previously recorded on Cenchrus ciliaris and C. biflorus in Africa
(Cummins, 1971; Baka and Gjaerum, 1996, respectively), on C. echinatus and C. brownii
in Asia (Gardner and Hodges, 1989; Hiratsuka et al., 1992, respectively).
Puccinia fragosoana Beltron
Roy. Soc. Espan. Hist. Nat. 50: 249 (1921).
TABLE II Qualitative features of uredinia of Puccinia species studied
Species Location Type Colour Margin Paraphyses
P. cenchri Leaves, mainly adaxial Oblong CB RE –
P. fragosoana Leaves, mainly adaxial Oblong DB N +
P. graminis Stem and leaf-sheath Elongated CB RE –
P. isiacae Leaves, in large groups Oblong CB RE –
P. recondita Leaves and stems Obovoid CB RE –
P. striiformis Leaves as linear series Elongated O RE +
CB = cinnamon-brown; DB = Dark-brown; O = Orange; RE = Ruptured epidermis; N = Naked; + = Presence;
7=Absence.
TABLE III Mean of dimensions (mm) of uredinia and paraphysis heads of Puccinia species studied
Uredinia Paraphysis heads
Species Length Breadth Length Breadth Wall thickness
P. cenchri 750+36 187 +6.0 –
P. fragosoana 507 +16 93 +3.0 11.5 +0.5 8.2 +0.20 2.5 +0.2
P. graminis 977 +60 738 +21 –
P. isiacae 1752 +34 246 +6.0 –
P. recondita 288 +3.0 177 +11 –
P. striiformis 89 +2.0 25 +1.0 16.0 +1.0 7. 5 +0.5 0.8 +0.05
+= Standard error of mean; 7=Absent.
TABLE IV Qualitative features of urediniospores of Puccinia species studied
Species Type Colour Wall colour
P. cenchri Ellipsoid Brown Cinnamon-brown
P. fragosoana Obovoid Golden-brown Yellow
P. graminis Ellipsoid Orange Cinnamon-brown
P. isiacae Ellipsoid Golden Cinnamon-brown
P. recondita Obovoid Yellow Yellowish-brown
P. striiformis Broadly ellipsoid Yellow Pale yellowish
92 ZAKARIA A.M. BAKA et al.

Syn. Uredo schizachyrii Doidge, Bothalia 2: 508 (1928).
On Imperata cylindrica (L.) Raeuschel
The uredinia of P.fragosoana are oblong, naked, dark brown measuring 507 – 593 mm.
The uredinia includes capitate colourless paraphyses measuring 11.5 68.2 mm, with
thin wall measuring 2.5 mm at apex. Urediniospores of P. fragosoana were obovoid,
golden to brown, 37.4 622.9 mm, wall yellow, 2.0 mm thick, with 4 –5 equatorial germ
pores, echinulate, spine density was 11.92, spine length was 0.80 mm. The distance
between spines was 1.07 mm.
Puccinia fragosoana was previously recorded on Imperata cylindrica in Africa
(Cummins, 1971; Baka and Gjaerum, 1996; Evans, 1987), Asia (Cummins, 1971; Abbasi
et al., 2002) and Europe (Cummins, 1971).
Puccinia graminis Pers.
Syn. Meth. Fung. P. 228 (1801).
Syn. P. albigensis Mayor, Rev. Mycol. 22: 279 (1957).
On Cynodon dactylon.
Uredinia are most commonly on sheaths and stems, cinnamon-brown, elongated,
surrounded by a ruptured epidermis measuring 977 6738 mm. Urediniospores of P.
graminis were ellipsoid, orange, 29.2 619.2 mm, wall cinnamon-brown, 1.8 mm thick,
with 3 – 5 equatorial germ pores, echinulate, spine density was 15.60, spine length was
0.65 mm. The distance between spines was 1.75 mm.
Puccinia graminis, the black rust, is circumglobal, occurring on many genera of
Poaceae. Cynodon dactylon is a new host for this rust in Saudi Arabia.
TABLE V Mean of dimensions (mm) of urediniospores and number of germ pores of Puccinia species studied
Species Length Breadth Wall thickness Germ pores
P. cenchri 32.8 +0.7 25.3 +0.6 2.4 +0.08 4 – 5 equatorial
P. fragosoana 37.4 +0.9 22.9 +0.5 2.0 +0.08 4 – 5 equatorial
P. graminis 29.2 +1.0 19.2 +0. 6 1.8 +0.05 3 – 5 equatorial
P. isiacae 26.2 +0.8 20.4 +0.2 3.5 +0. 08 3 equatorial
P. recondita 29.2 +0. 7 22.4 +0.5 1.5 +0.08 6 – 9 scattered
P. striiformis 26.2 +0.6 20.6 +0. 5 1.8 +0.05 9 – 1 3 scattered
+= Standard error of mean.
TABLE VI Mean of the dimensions (mm) of urediniospore spines of Puccinia species studied
Species Spine density/100 mm
2
Length Distance between spines
P. cenchri 11.52 +1.8 0.80 +0.01 1.53 +0.05
P. fragosoana 11.92+1.9 0.80 +0.02 1.07 +0.02
P. graminis 15.60 +2.1 0.65 +0.01 1.75 +0.05
P. isiacae 12.80 +1.6 0.55 +0.01 2.72 +0.04
P. recondita 16.20 +2.8 0.94 +0.03 1.39 +0.05
P. striiformis 11.50 +1.5 0.55 +0.01 1.10 +0.02
+= Standard error of mean.
93COMPARATIVE MORPHOLOGY OF PUCCINIA SPECIES FROM SAUDI ARABIA

Puccinia isiacae Wint.
O. Kuntze Plantae orient-ross. P. 127 (1887).
On Phragmites australis (Cav.) Trin.
The uredinia scattered on leaves in large groups, oblong, surrounded by a ruptured
epidermis measuring 1752 6246 mm. Urediniospores of P. isiacae were ellipsoid,
golden, 26.2 620.4 mm, wall cinnamon-brown, 3.5 mm thick, with three equatorial
germ pores, echinulate, spine density was 12.80, spine length was 0.55 mm. The distance
between spines was 2.72 mm.
FIGURES 1 – 4 Puccinia cenchri. (1 – 3) are SEM micrographs. (1) An uredinium with ruptured epidermis (E).
Bar = 100.0 mm. (2) A magnified part of an uredinium showing a group of urediniospores. Bar= 10.0 mm. (3) A
magnified urediniospore showing the echinulation on its surface. Note the scar (arrowhead). Bar= 5.0 mm. (4) LM
micrograph of a single urediniospore. Bar = 20.0 mm.
94 ZAKARIA A.M. BAKA et al.

Puccinia isiacae was previously recorded on P. communis and P.maximus in Europe
and Africa (Cummins, 1971), on P. australis in Africa (Baka and Gjaerum 1996).
Puccinia recondita Roberge ex Desm.
Bull. Soc. Bot. France, 4: 798 (1857).
Syn. Puccinia dasypyri Guyot & Malen. Trav. Inst. Sci. Chefir Ser. Bot. 28: 62 (1963).
On Lolium perenne L.
FIGURES 5 – 8 Puccinia fragosoana. (5 – 7) are SEM micrographs. (5) A naked uredinium. Bar = 100.0 mm. (6)
A magnified part of an uredinum showing a group of uredinispores. Note the paraphysis (P). Bar = 10.0 mm. (7) A
magnified urediniospore. Note the reticulation (arrowheads) and echinulation on its surface. Bar= 5.0 mm. (8) LM
micrograph of a an urediniospore. Note the equatorial germ pores (arrows). Bar =20.0 mm.
95COMPARATIVE MORPHOLOGY OF PUCCINIA SPECIES FROM SAUDI ARABIA

The uredinia of P. recondita are obovoid, surrounded by a ruptured epidermis,
cinnamon-brown. Single uredinium is measuring 288 6177 mm. Urediniospores of P.
recondita were broadly obovoid, yellowish, 29.2 622.4 mm, wall yellowish-brown,
1.5 mm thick, with 6 – 9 scattered germ pores, echinulate, spine density was 16.20, spine
length was 0.94 mm. The distance between spines was 1.39 mm.
Puccinia recondita, the brown leaf rust, is a circumglobal rust species, most common
in temperate areas occurring on a large number of host genera of Poaceae (Cummins,
1971) and in Africa on L. perenne (Baka and Gjaerum, 1996), and L. temulentum
(Reichert, 1921).
Puccinia striiformis Westend
Bull. Roy. Acad. Belg., Cl. Sci. 21: 235 (1854).
FIGUREs9–12 Puccinia graminis. (9 – 11) are SEM micrographs. (9) A number of uredinia (short arrows) in
linear manner. Bar = 500 mm. (10) A magnified part of an uredinium with ruptured epidermis (E). Bar =10 mm.
(11) A magnified urediniospore showing the echinulation on its surface. Note germ pore (arrowhead).
Bar = 5.0 mm. (12) LM micrograph of urediniospores. Bar= 20.0 mm.
96 ZAKARIA A.M. BAKA et al.

Syn. Uredo glumarum J. K. Schmidt, Allgem. Oekon-tech., Fl. 1: 27 (1827).
On Lolium perenne
The uredinia of P. striiformis appear in linear series in chlorotic streaks, surrounded by
a ruptured epidermis, orange. Single uredinum was up to 89 625 mm. The uredinium
contains saccate paraphyses with colourless wall. Paraphysis heads were measuring
16.0 67.5 mm, the wall thickness at apex was 0.8 mm. Urediniospores of P. striiformis
were broadly ellipsoid, yellowish, 26.2 620.6 mm, wall pale yellowish, 1.8 mm thick,
with 9 – 13 scattered germ pores, echinulate, spine density was 11.5, spine length was
0.55 mm. The distance between spines was 1.39 mm.
Puccinia striiformis, the stripe rust, is circumglobal, specially in the northern
hemisphere, where it lives on many species of Poaceae. It was reported before in Africa
on L. perenne (Baka and Gjaerum, 1996).
There were qualitative morphological differences between uredinia and uredinios-
pores of the different Puccinia species when observed under both light and electron
microscopes. As indicated in Table II, the uredinia of the species examined differ in
FIGURES 13 – 17 Puccinia isiacae. (13 – 15) are SEM micrographs. (13) An uredinium contains huge number of
urediniospores. Note ruptured epidermis (E). Bar = 250.0 mm. (14) A magnified part of an uredinium showing a
group of elongated urediniospores. Bar = 25.0 mm. (15) Magnified urediniospores showing the echinulation on
their surfaces. Bar = 25.0 mm. (16 – 17) are LM micrographs. (16) A part of an uredinium showing a group of
urediniospores. Bar = 20. 0 mm. (17) Magnified urediniospores with equatorial germ pores (arrowheads).
Bar = 20.0 mm.
97COMPARATIVE MORPHOLOGY OF PUCCINIA SPECIES FROM SAUDI ARABIA

location, form, colour, and in the presence of sterile paraphyses. Apart from P.
graminis, in which they occur mainly on stem and leaf sheaths, the uredinia of these
species are generally found between the veins on leaves, often forming linear series
which, in P. recondita, occur in chlorotic streaks of leaf tissue, whereas those of P.
isiaceae are scattered in large groups. Uredinia emerge on the adaxial surface of P.
cenchri leaves but are abaxial in P. fragosoana. Uredinia of P. cenchri and P. graminis
are elongated but those of the other species are mainly oblong, sometimes becoming
confluent. Uredinia of P. cenchri, P. graminis, P. isiaceae and P. recondita are
cinnamon-brown in colour, those of P.fragosoana dark brown, and those of P.
striiformis orange.
Paraphyses, long-stalked, colourless, sterile capitate structures, of differing size and
wall thickness, were present in uredinia of two species: P.fragosoana where they were
FIGURES 18 – 22 Puccinia recondita. (18 – 20) are SEM micrographs. (18) Uredinia with ruptured epidermis (E).
Bar = 100.0 mm. (19) A part of an uredinium showing urediniospores. Bar = 10.0 mm. (20) A magnified
urediniospore showing the echinulation on its surface. Bar = 5.0 mm. (21 – 22) LM micrographs. (21) An
urediniospore showing germ pore (arrow). Bar = 20.0 mm. (22) Other view showing the wall (arrowhead) of
urediniospores. Bar = 20.0 mm.
98 ZAKARIA A.M. BAKA et al.

found at the periphery of the uredinium, and in P. striiformis where the paraphyses
appeared saccate (Table III). Those of P. fragosoana were smallest in length and
breadth while the wall of P. striiformis paraphyses was much thinner than in the other
species.
This study is the first report to compare graminicolous Saudi rusts using both
qualitative and quantitative morphology. These methods indicated that, urediniospore
stages of the six Puccinia species can be distinguished. This investigation showed that
the differences between urediniospores of these Puccinia species are not related to the
type of host plant, since both P. recondita and P. striiformis are clearly recognized
although they are growing on one host plant, Lolium prenne. Puccinia striiformis had
FIGURES 23 – 27 Puccinia striiformis. (23 – 26) are SEM micrographs. (23) An uredinium with ruptured
epidermis (E). (24) A part of an uredinium showing urediniospores intermixed with paraphyses (P). Bar = 10.0 mm.
(25) A magnified urediniospore showing its echinulation. Bar = 5.0 mm. (26) A magnified part of an urediniospore
showing spines (arrows) located in depressions (D) and enclosed by annuli (A). Bar = 0.5 mm. (27) LM micrograph
showing urediniospores. Bar = 20.0 mm.
99COMPARATIVE MORPHOLOGY OF PUCCINIA SPECIES FROM SAUDI ARABIA

paraphyses and P. recondita had not. Moreover, the highest number of germ pores was
recorded in case of P. striiformis. These germ pores were scattered in both P. striiformis
and P. recondita and in other Puccinia species were equatorial. These variations in germ
pore number and distribution may play a role in the classification of graminicolous rust
fungi. Cummins and Hiratsuka (1983) reported that germ numbers is a good taxonomic
character.
Observation by SEM led to more information in distinguishing between the rust
species studied here particularly urediniospore surface, spines density and spine length.
Surface ornamentation, such as spines, warts, and reticulum on urediniospores are
sometimes of value in the identification of rust fungi (Corlett, 1970). The spine
morphology on the studied Puccinia species is in agreement with the descriptions for
most other rust fungi (Littlefield and Heath, 1979) as being conical and sometimes
curved at the tip, with the angle between the spines and the spore surface (Amerson and
Van Dyke, 1978). Surface morphology and ornamentation features of rust uredinios-
pores have been studied extensively with SEM (Stanbridge and Gay, 1969; Corlett,
1970; Amerson and Van Dyke, 1978; Brown and Brotzman, 1979; Littlefield and Heath,
1979; Harder, 1984; Gardner and Hodges, 1985; Woods and Beckett, 1987; Baka and
Lo
¨sel, 1992; Baka, 1992, 1996a, 1996b, 2003). The depressions and raised annuli around
spines observed here are common in Puccinia and Uromyces species (Littlefield and
Heath, 1979).
Germling morphology of urediniospores may clarify some of the difficulties of the
identification and classification of grass rust fungi. In addition, nuclear DNA content or
isozyme analysis may also add more information about rust fungi classification.
Acknowledgement
The authors would like to thank Dr Dorothy M. Lo
¨sel, Department of Animal and
Plant Sciences, University of Sheffield, England for valuable comments.
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101COMPARATIVE MORPHOLOGY OF PUCCINIA SPECIES FROM SAUDI ARABIA