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Department of Plant Sciences and the Institute for Cereal Crops Improvement, Faculty of Life Sciences, Tel Aviv University, Ramat Aviv 69978, Israel
K. J. Leonard 1
Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, USA 55108 (formerly, U.S. Department of Agriculture, Agricultural Research Service, Cereal Disease Laboratory, University of Minnesota)
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ABSTRACT |
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A new morphotype of Puccinia coronata, pathogenic to Bromus inermis, a common roadside and pasture grass in the northern United States, was discovered in the 1990s and described as P. coronata f. sp. bromi by Delgado et al in 2001. Puccinia coronata f. sp. bromi does not require fertilization of pycnia to produce aecia on its alternate host, whereas fertilization is required in all other varieties or formae speciales of P. coronata with aecial hosts in the family Rhamnaceae and for which life cycles have been described. Promycelia of P. coronata f. sp. bromi produce only two basidiospores, and each receives a pair of nuclei from the promycelium. The nuclei divide again so that mature basidiospores each contain four nuclei. Puccinia coronata f. sp. bromi has smaller teliospores than P. coronata var. avenae, and its substomatal vesicles are non-septate and distinctly shaped compared to those of P. coronata var. avenae. In addition, nuclei of P. coronata f. sp. bromi contain less DNA than those of P. coronata var. avenae. Puccinia coronata f. sp. bromi is further distinguished from P. coronata var. avenae and P. coronata var. hordei in being avirulent on both oat and barley, whereas neither P. coronata var. avenae nor P. coronata var. hordei are virulent on Bromus inermis.
Key words: Bromus inermis, crown rust, nuclear DNA content, Rhamnus cathartica, R. palaestina, substomatal vesicle, teliospore germination
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INTRODUCTION |
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). The fungus was provisionally designated P. coronata f. sp. bromi sensu Mühlethaler by Delgado et al (2001) to distinguish it from another morphotype that was designated P. coronata var. bromi by Fraser and Ledingham (1933), but which they reported to be avirulent on B. inermis. Puccinia coronata f. sp. bromi sensu Mühlethaler was discovered independently on B. inermis in South Dakota in 1997 (Y. Jin pers comm) and on B. inermis and R. cathartica in St. Paul, Minnesota, in 1998 by K. J. Leonard. Subsequently, the fungus has been found in many sites in Wisconsin, North Dakota, South Dakota, and Minnesota.
Previous reports of crown rust on Bromus spp. in North America either provide no morphological information (Anonymous 1960, Cash 1953) or refer to a type of crown rust quite distinct from the morphotype found on B. inermis in the upper Midwest of the U.S. in the 1990s (Delgado et al 2001). Puccinia coronata var. bromi, described by Fraser and Ledingham (1933) in Canada, produced its aecial stage on Lepargyraea canadensis (Elaeagnaceae) but not Rhamnus cathartica. Furthermore, the Puccinia coronata var. bromi described by Fraser and Ledingham was avirulent to B. inermis and had short apical projections on the teliospores rather than long projections typical of the new morphotype described by Delgado et al (2001).
Teliospores of P. coronata f. sp. bromi sensu Mühlethaler, which henceforth we refer to as simply P. coronata f. sp. bromi, are morphologically similar to those of P. coronata var. hordei Jin & Steffenson (Jin and Steffenson 1999), which is avirulent to B. inermis. Puccinia coronata var. hordei appears to be the same as P. coronata f. sp. secalis described on rye in Canada by Peturson (1954) and a morphotype of P. coronata found on Elytrigia repens (= Agropyron repens) in North Dakota by Schwinghamer (1955). Like P. coronata var. hordei, both of these morphotypes of P. coronata were avirulent on B. inermis.
In preliminary studies of the brome grass crown rust fungus, we suspended leaves of B. inermis bearing overwintered telia over R. cathartica plants in a dew chamber to inoculate them with basidiospores of P. coronata f. sp. bromi. Although pycnial infection was very sparse on the inoculated R. cathartica leaves, an abundance of aecia formed on the lower sides of the leaves within 5 to 7 d. This observation led us to suspect that P. coronata f. sp. bromi might exhibit self-fertility as described in P. mesnieriana (Anikster 1984, Anikster and Wahl 1985) and, thus, differ from other varieties and formae speciales of P. coronata in the development of its sexual stage on hosts in the family Rhamnaceae. Fraser and Ledingham described two varieties of P. coronata with aecial hosts in the family Elaeagnaceae that produced either no pycnia or rare pycnia in association with abundant aecia on their alternate hosts. Both varieties may be self-fertile, although Fraser and Ledingham did not describe the nature of teliospore germination in those varieties.
The objectives of this study were: 1) to determine the nuclear condition of basidiospores and whether pycnial fertilization plays any role in the development of aecia by P. coronata f. sp. bromi; and 2) to compare host range, DNA content of nuclei, and morphology of spores and infection structures to determine whether there are distinct differences between P. coronata f. sp. bromi and other varieties and formae speciales of P. coronata that produce aecia on R. cathartica.
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MATERIALS AND METHODS |
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), were collected from oversummered naturally infected buds of Rhamnus palaestina in natural habitats at two sites in Israel.
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Spore morphology – For microscopic examination, teliospores were scraped from dry leaves of B. inermis, A. sativa, or R. palaestina for P. coronata f. sp. bromi, P. coronata var. avenae, or P. mesnieriana, respectively. The teliospores were mounted in 50% glycerol on glass slides, and video images were taken with a Zeiss Axioscop microscope using 20x objective and 10x ocular lenses. Video images were obtained with a CCD B/W video camera (LIS—700 Applitec, Israel). The images were digitized and analyzed using image analysis software (NIH Image, 1.62). The length of spores excluding their pedicel, their width at the widest part of the spore, and the cross sectional area of the spore excluding the pedicel were determined as the number of pixels along the maximal length and width of the spore or the sum of pixels within the spore boundaries, calibrated to the dimension units. At least 50 teliospores were measured for each collection.
Basidiospores were collected by exposing glass slides overnight under telia-bearing leaf pieces of overwintered collections of infected B. inermis and A. sativa that had been pre-treated to induce teliospore germination. The basidiospores were mounted in lactophenol cotton blue, slightly heated for 5 min, and their cross-sectional areas were measured as described for teliospores. Urediniospores of P. coronata f. sp. bromi and P. coronata var. avenae were collected from uredinia on plants of B. inermis and A. sativa in the greenhouse. Aeciospores were collected from aecia on R. palaestina plants inoculated with P. coronata f. sp. bromi and P. coronata var. avenae in the greenhouse. Urediniospores and aeciospores were mounted in 50% glycerol, and their cross sectional areas measured as described above. Means, standard deviations, and coefficients of variation for all spore measurements were calculated.
Germ pores of urediniospores of P. coronata f. sp. bromi and P. coronata var. avenae were counted using a modification of the squash technique of Jennings et al (1989). Cotton blue was used to stain the urediniospores. The spores were heated on slides until "smoke" came out of the slide. A cover slip was placed over the spores and pressed hard against them. Zeiss fluorescence optics filter set 05 (395–440, FT 460, LP470) was used to accentuate the germ pores. Germ pores were counted for at least 100 spores of each type per collection.
Substomatal vesicles –
Leaves of barley cultivar L-94 were inoculated with urediniospores for production of substomatal vesicles of both P. coronata f. sp. bromi and P. coronata var. avenae in accordance with Niks's (1986) evidence that substomatal vesicles in non-host grasses or cereals have identical morphology to those in susceptible hosts of cereal and grass rusts. Barley seedlings were inoculated with urediniospores of P. coronata f. sp. bromi and P. coronata var. avenae by applying a thick spore suspension to the first seedling leaf with a cotton swab. Inoculated seedlings were incubated in a dew chamber for 24 h.
Substomatal vesicles were examined in leaf mounts following the procedure of Niks (1986) with two modifications. Leaf segments were boiled in 0.03% (rather than 0.005%) Trypan blue in lactophenol-ethanol (1:2, v/v) for 30 s in a microwave oven (rather than boiling for 15 min). Leaf segments were then cleared with chloral hydrate (5:2, w/v) and mounted in lactophenol for viewing with a Zeiss microscope 630x using DIC optics. Images were taken with a Nikon Coolpix 990 digital camera.
Nuclear condition of promycelia and basidiospores – Teliospores of P. coronata f. sp. bromi, P. coronata var. avenae, and P. mesnieriana that had been pre-treated to induce germination were scraped from host leaf tissue and washed onto the surface of water agar in petri dishes for observations of germination. Germinating teliospores were stained with a solution of TRIS-HCl buffer (0.18 M, pH 7.2) containing propidium iodide (PI) at 4 µg/mL, RNase at 50 µg/mL, and TritonX-100 at 4 µg/mL (all chemicals from Sigma Chemical Company, St.Louis, Missouri). A drop of the stain solution was placed on the agar surface with germinating teliospores and covered with a cover slip at room temperature for 30 min. Stained nuclei in the promycelia and basidiospores were examined with a Zeiss fluorescence microscope with filter set 14 (510–560, FT580, LT590) which passes green excitation to the specimen and red emission to the viewer.
Basidiospores were collected on glass slides in a petri dish by placing telia-bearing pieces of host leaves on wet filter paper fixed to the petri dish lid. Basidiospores that had stuck to the slides were stained with PI, and microscope observation was as described above for promycelia.
DNA content of pycniospore nuclei –
Relative DNA content of pycniospores was determined by flow cytometry of propidium iodide stained spores as described by Eilam et al (1994). Pycniospores were harvested from R. palaestina plants inoculated with basidiospores of P. coronata f. sp. bromi or P. coronata var. avenae at 10–20 d after inoculation. Even though fewer than 5% of the P. coronata f. sp. bromi infections produced pycniospores, sufficient numbers of pycniospores were obtained for DNA measurements. The buffer-dye solution previously described for PI staining was drawn into a glass haematocrit capillary tube (1 mm inside diameter) and the tip of the tube was touched to a pycnial cluster to allow pycnial nectar and pycniospores to enter the tube. When sufficient spores were collected, from multiple pycnial clusters if necessary, the spore suspension was blown from the tube into 200 µL of buffer-dye solution in a test tube. Pycniospores were allowed to stain for 2–3 h before being introduced into the flow cytometer. If stained spores could not be used immediately, they were stored at -20 C until use.
A Becton Dickinson (Mountain View, California) FACS IV flow cytometer equipped with an argon laser was used to measure fluorescence intensity of stained pycniospores. The flow cytometer was calibrated daily with chicken red blood cells as a standard, bringing the output with 650 mW to channel 100. Excitation was at 488 nm; a 570 nm emission filter was used. Pycniospores of P. hordei harvested and processed in parallel with each P. coronata collection were used as a standard for comparison of relative DNA content, with the output of the flow cytometer set at channel 100 for P. hordei pycniospores. Fluorescent intensity of samples is expressed as channel number.
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RESULTS |
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), the nuclei were paired in two cells of the promycelium, and a pair of nuclei migrated to each of the two basidiospores that formed (Fig. 2). Apparently, the paired nuclei were of opposite mating type, because >95% of the infections produced by basidiospores of P. coronata f. sp. bromi on R. palaestina developed aecia without being fertilized manually (Table III). Pycnial formation by P. coronata f. sp. bromi was sparse, and no pycnia were seen in P. mesnieriana (Fig. 3). Teliospore germination and basidiospore formation by P. coronata var. hordei was similar to that of P. coronata f. sp. bromi; >94% of the infections from basidiospores developed aecia without fertilization. Conversely, pycnial infections of P. coronata var. avenae rarely produced aecia unless they were manually fertilized by transferring pycnial nectar and pycniospores from other pycnia to them.
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) in frequently having dichotomous branching.
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for collections of P. coronata from Avena sativa, Holcus lanatus, Lolium perenne, Agrostis capillaris, and Alopecurus pratensis from the Netherlands; the vesicles were elongated with a single transverse septum to one side of the penetration peg (Fig. 8A). Substomatal vesicles of P. coronata f. sp. bromi differed distinctly from those of P. coronata var. avenae. They were shorter, non-septate, and slightly arched to give an appearance resembling that of the inverted cross section of a mushroom cap (Fig. 8B)
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DISCUSSION |
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). It seems highly improbable that a widespread rust fungus on such a prominent grass could go unnoticed through the period of active research on rust fungi in the first half of the 20th century. On the other hand, there is no obvious explanation of where it came from or how it arose. Puccinia coronata var. hordei, for which no European counterpart has been found, apparently has occurred widely in North America since at least the 1950s (Peturson 1954, Schwinghamer 1955).
The new morphotype of crown rust described for the first time on B. inermis as P. coronata f. sp. bromi by Delgado et al (2001) is clearly distinct from all other known varieties and formae speciales of P. coronata. Not only is its pathogenicity to B. inermis unique, at least in North America, but also its characteristic two-spored promycelium, four nucleate basidiospores, and self fertile infections leading to aecial production on Rhamnus have not been described in any other varieties or formae speciales of P. coronata that have aecial hosts in the Rhamnaceae. Fraser and Ledingham (1933) described P. coronata var. bromi and P. coronata var. elaeagni as producing either no pycnia or rare pycnia associated with abundant aecia on Lepargyraea canadensis and Elaeagnus commutata, respectively. Neither of these varieties has any known counterpart in Europe, and both differ from other varieties and formae speciales of P. coronata in being unable to infect species of Rhamnus. Fraser and Ledingham did not describe teliospore germination of the P. coronata varieties that they described, but it seems likely that their P. coronata var. bromi and P. coronata var. elaeagni are self fertile. Preliminary evidence (Table III) indicates that teliospore germination in P. coronata var. hordei is similar to that of P. coronata f. sp. bromi. The only other closely related rust that shares the characters of two-spored promycelia and four-nucleate basidiospores is the microcyclic P. mesnieriana, which is self fertile in producing telia on Rhamnus (Anikster and Wahl 1985). The self-fertility of P. coronata f. sp. bromi might limit gene exchange between P. coronata f. sp. bromi and other varieties and formae speciales of P. coronata, because nearly all infections on Rhamnus by basidiospores of P. coronata f. sp. bromi result in the initiation of aecia without any delay during which fertilization might occur.
Puccinia coronata f. sp. bromi differs from P. coronata var. avenae in several other morphological traits in addition to its two-spored promycelia and four-nucleate basidiospores. The most prominent of these differences is in the substomatal vesicles. According to Niks (1986), the morphology of substomatal vesicles and associated infection structures is a useful characteristic in distinguishing between species of rusts of cereals and grasses. Swertz (1994) studied substomatal vesicles of nine collections of P. coronata var. avenae from oat in northern and central Europe, Ecuador, Israel, and Ethiopia, and 83 collections of P. coronata var. coronata Urban & Markova from eight genera of wild grasses in five countries of northern and central Europe and from Ecuador. She found that all collections of P. coronata var avenae and P. coronata var. coronata produced substomatal vesicles of the same general shape except that isolates from oat produced substomatal vesicles considerably longer and somewhat narrower than those of isolates from wild grasses. In either case, the substomatal vesicles were rectangular with a transverse septum that often was eccentrically located. The one exception that Swertz noted was for an unclassified isolate of P. coronata (presumably P. coronata var. hordei) collected from Elytrigia repens in Ontario, Canada. That isolate produced ellipsoid to narrowly ellipsoid substomatal vesicles with acute ends. Substomatal vesicles formed by germinating urediniospores of P. coronata f. sp. bromi (Fig. 8B) lack the transverse septum found in P. coronata var. avenae and P. coronata, var. coronata, are shorter than those of P. coronata var. avenae, and are characteristically curved rather than rectangular as in P. coronata var. avenae and P. coronata, var. coronata.
Differences in spore morphology between P. coronata f. sp. bromi and P. coronata var. avenae are not so distinct, although teliospores of P. coronata f. sp. bromi were significantly smaller in their cross sectional area than those of P. coronata var. avenae. Cross sectional area was found to be a more useful measure than either length or width in comparing teliospores of P. recondita, rye leaf rust, and P. triticina, wheat leaf rust (Anikster et al 1997). Comparisons of urediniospore morphology were less conclusive. We found no significant difference in cross sectional area of urediniospores of P. coronata f. sp. bromi and P. coronata var. avenae. Swertz (1994) concluded that size of urediniospores is variable among different varieties and formae speciales of P. coronata and of little use for identification. Jin and Steffenson (1999) reported a range of 5 to 8 germ pores in urediniospores of P. coronata var. hordei, which is fewer than our observations of 7 to 11 germ pores for P. coronata f. sp. bromi and 8 to 12 for P. coronata var. avenae. Urban and Markova (1994) reported ranges of 8–10 for P. coronata var. coronata and (8–) 9–11 (–14) for P. coronata var. avenae from oat. Cummins (1971) also reported that numbers of germ pores in P. coronata var. avenae were mostly in the range of 9 to 11.
The life cycle of P. coronata f. sp. bromi suggests an intermediate step that might have occurred in the evolution of the microcyclic P. mesnieriana. Dietel (1918) concluded that P. mesnieriana originated from P. coronata, and Tranzschel (1939) agreed that P. mesnieriana descended from P. coronata by losing the aecial and uredinial stages. The first step in this evolutionary process might have been the development of self-fertility and loss of the role of pycnia as an essential stage in the life cycle. Self-fertility creates a barrier to gene flow that otherwise might impede divergence into a new species. Buller (1950) regarded self-fertility as an advantage under adverse environmental conditions, because it reduces the time required for sporulation on the alternate host as well as the risk of non-fertilization when population densities are low.
Uromyces viennot-bourginii Wahl & Anikst., a rust that inhabits small areas in the central Negev Desert in Israel, exhibits self-fertility (Anikster et al 1977). This fungus forms uredinia and telia on Hordeum spontaneum, an annual wild barley, and aecia on the liliaceous Bellevalia eigii. Pycnia are rare, occurring with only 1–2% of aecial clusters. Teliospores of U. viennot-bourginii germinate to produce two-celled promycelia that produce two dikaryont (tetra-nuclear) basidiospores. In the habitat of this fungus, there is a very short growing season with an annual rainfall of 80 mm. The saving of 2 wk in producing aeciospores can be critical under those conditions. Several other species of Uromyces found at high elevations or in arid areas of Israel are self fertile (Anikster 1984, Anikster et al 1980).
Unlike U. viennot-bourginii, P. coronata f. sp. bromi does not appear to require self-fertility for survival in its current habitat in the north central United States. Both B. inermis and R. cathartica are common from eastern North Dakota and South Dakota through Minnesota and Wisconsin. On the other hand, self-fertility might have served as an isolating mechanism that allowed P. coronata f. sp. bromi to develop uredinial host specificity on B. inermis without requiring physical separation from the much more common P. coronata var. avenae.
In the buckthorn nursery at St. Paul, Minnesota, P. coronata var. avenae coexists with P. coronata f. sp. bromi and P. coronata var. hordei in the aecial stage on leaves of the same R. cathartica plants. Teliospores of P. coronata var. avenae are produced on Avena sativa plants sown between hedges of R. cathartica within the nursery. Teliospores of P. coronata f. sp. bromi and P. coronata var. hordei are produced on Bromus inermis and Elytrigia repens, respectively, growing at the margins along three sides of the nursery. In addition, some crown rust-infected plants of E. repens can be found annually growing as a weed within the nursery. In spite of their proximity in the St. Paul buckthorn nursery, P. coronata f. sp. bromi and P. coronata var. avenae remain morphologically distinct and separated by telial hosts. Delgado et al (2001) described the similar coexistence of P. coronata f. sp. bromi and P. coronata var. avenae as distinct types infecting the same R. cathartica plants in Wisconsin.
DNA content of nuclei of haploid pycniospores provides further evidence that hybridization does not occur between P. coronata f. sp. bromi and P. coronata var. avenae in nature. Nuclei of P. coronata f. sp. bromi have significantly less DNA than those of P. coronata var. avenae. Therefore, it appears that the self-fertility of P. coronata f. sp. bromi prevents hybridization between it and P. coronata var. avenae. We have not completed our studies of P. coronata var. hordei, but preliminary evidence suggests that it is genetically isolated from both P. coronata f. sp. bromi and P. coronata var. avenae.
In contrast to our results, Eshed and Dinoor (1980) concluded that in Israel there are no distinct separations between formae speciales of P. coronata. Aecial isolates obtained from R. palaestina showed overlapping host ranges among grass species present in Israel. Thus, it appears that hybridization occurs readily among P. coronata genotypes that occur naturally on a wide range of grasses in Israel. Significantly, there is no evidence for occurrence of P. coronata f. sp. bromi in Israel, and both P. coronata f. sp. bromi and P. coronata var. hordei are morphologically distinct from all types of P. coronata known to occur in Israel.
Our results indicate that P. coronata f. sp. bromi can be distinguished from other varieties and formae speciales of P. coronata in several ways. Non-viable specimens of P. coronata f. sp. bromi can be distinguished from P. coronata var. avenae by their smaller teliospores. If viable urediniospores are available, P. coronata f. sp. bromi can be recognized by the distinctive morphology of its substomatal vesicles and by its narrow host range, which apparently is unique with Bromus inermis as the primary host, at least in North America. Perhaps most important, if teliospores are induced to germinate, the characteristic two-celled promycelium bearing just two sterigmata and basidiospores distinguishes P. coronata f. sp. bromi from all other varieties and formae speciales of P. coronata except P. coronata var. hordei which, according to our preliminary evidence, shares with P. coronata f. sp. bromi the characteristic two-spored promycelium and tetra-nucleate basidiospores. Puccinia coronata var. bromi Fraser & Ledingham and P. coronata var. elaeagni Fraser & Ledingham may produce two-spored promycelia, although this is not known for certain. Both P. coronata var. bromi Fraser & Ledingham and P. coronata var. elaeagni Fraser & Ledingham produce aecia on species in the family Elaeagnaceae but not in Rhamnaceae, and neither infected B. inermis in Fraser and Ledingham's (1933) tests.
The low DNA content of its nuclei is evidence that P. coronata f. sp. bromi could be recognized as a separate species. Eilam et al (1994) showed that the genetically compatible P. graminis f. sp. secalis and P. graminis f. sp. tritici do not differ in their nuclear DNA content. The nuclear DNA content of P. coronata f. sp. bromi not only differs significantly from that of P. coronata var. avenae, but also is lower than that reported for any of the other 12 rust species tested by Eilam et al (1994). Morphological comparisons of P. coronata f. sp. bromi with varieties and formae speciales of P. coronata found in Europe might help determine whether P. coronata f. sp. bromi as described by Delgado et al (2001) is distinct from P. coronata f. sp. bromi described on Bromus inermis in Europe by Mühlethaler (1911). In the most comprehensive review of varieties and formae speciales of P. coronata in Europe, Urban and Markova (1994) did not report evidence of significant morphological distinctions between collections of P. coronata from Bromus and those of P. coronata var. coronata collections from other grasses in Europe. Therefore, we believe that the P. coronata f. sp. bromi of Delgado et al (2001) is not the same as Mühlethaler's (1911) P. coronata f. sp. bromi.
It has occurred to us, of course, that the morphological differences, the difference in nuclear DNA content, and the distinct life cycle of P. coronata f. sp. bromi justify naming it a new species separate from P. coronata var. avenae. We have delayed that step, partly because it would leave P. coronata var. hordei with uncertain status. Our studies of the morphology of teliospore germination and substomatal vesicle formation in P. coronata var. hordei and the DNA content of its nuclei are not complete, but preliminary evidence suggests that P. coronata var. hordei is more closely related to P. coronata f. sp. bromi than to P. coronata var. avenae or other varieties of P. coronata that resemble P. coronata var. avenae. It is not clear yet whether P. coronata f. sp. bromi and P. coronata var. hordei should be considered formae speciales or varieties of a single species or whether they are separate species. Studies of rDNA sequences (Zambino and Szabo, 1993) will help clarify that relationship.
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FOOTNOTES |
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Accepted for publication July 9, 2002.
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LITERATURE CITED |
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