Puccinia gramnis Biology
Stem or black rust of wheat is caused by P. graminis f. sp. tritici. At one time, it was a feared disease in most wheat regions of the world. The fear of stem rust was under-standable because an apparently healthy crop three weeks before harvest could be reduced to a black tangle of broken stems and shrivelled grain by harvest. In Europe and North America, the removal of the alternate host reduced the number of combinations of virulence and the amount of locally produced inoculum (aeciospores). In addition, in some areas early maturing cultivars were introduced to permit a second crop or to avoid flowering and grain-filling during hot weather. Early maturing cultivars escape much of the damage caused by stem rust by avoiding the growth period of the fungus. The widespread use of resistant cultivars worldwide has reduced the disease as a significant factor in production. Although changes in pathogen virulence have rendered some resistances ineffective, resistant cultivars have generally been developed ahead of the pathogen. The spectacular epidemics that developed on Eureka (Sr6 in Australia) in the 1940s and on Lee (Sr9g, Sr11, Sr16), Langdon (Sr9e, +) and Yuma (Sr9e, +) in the United States in the mid-1950s really have been the exceptions in the past. The experience in other parts of the world has been similar (Luig and Watson, 1972; Roelfs, 1986; Saari and Prescott, 1985). Today, stem rust is largely under control worldwide.
The epidemiology of P. graminis is similar to P. triticina. The minimum, optimum and maximum temperatures for spore germination are 2°, 15° to 24°, and 30°C, respectively (Hogg et al., 1969) and for sporulation, 5°, 30° and 40°C, respectively, which is about 5.5°C higher in each category than for P. triticina. Stem rust is more important late in the growing period, on late-sown and maturing wheat cultivars, and at lower altitudes. Spring-sown wheat is particularly vulnerable in the higher latitudes if sources of inoculum are located downwind. Large areas of autumn-sown wheat occur in the southern Great Plains of North America, providing inoculum for the northern spring-sown wheat crop. In warm humid climates, stem rust can be especially severe due to the long period of favourable conditions for disease development when a local inoculum source is available.
Stem rust differs from leaf rust in requiring a longer dew period (six to eight hours are necessary). In addition, many penetration pegs fail to develop from the appressorium unless stimulated by at least 10 000 lux of light for a three-hour period while the plant slowly dries after the dew period. Maximum infection is obtained with 8 to 12 hours of dew at 18°C followed by 10 000+ lux of light while the dew slowly dries and the temperature rises to 30°C (Rowell, 1984). Light is seldom limiting in the field as dews often occur in the morning. However, little infection results when evening dews and/or rains are followed by winds causing a dry-off prior to sunrise. In the greenhouse, reduced light is often the reason for poor infection rates. The effect of light probably is an effect on the plant rather than the fungus system as urediniospores injected inside the leaf whorl result in successful fungal penetrations without light striking the fungus. Stem rust uredinia occur on both leaf and stem surfaces as well as on the leaf sheaths, spikes, glumes, awns and even grains.
A stem rust pustule (uredinium) can produce 10 000 urediniospores per day (Katsuya and Green, 1967; Mont, 1970). This is more than leaf rust, but the infectability is lower with only about one germling in ten resulting in a successful infection. Stem rust uredinia, being mostly on stem and leaf sheath tissues, often survive longer than those of leaf rust, which are confined more often to the leaf blades. The rate of disease increase for the two diseases is very similar.
Stem rust urediniospores are rather resistant to atmospheric conditions if their moisture content is moderate (20 to 30 percent). Long-distance transport occurs annually (800 km) across the North American Great Plains (Roelfs, 1985a), nearly annually (2000 km) from Australia to New Zealand (Luig, 1985) and at least three times in the past 75 years (8 000 km) from East Africa to Australia (Watson and de Sousa, 1983).
Aeciospores can also be a source of inoculum of wheat stem rust. Historically, this was important in North America and northern and eastern Europe. This source of inoculum has generally been eliminated or greatly reduced by removal of the common or European barberry (Berberis vulgaris) from the proximity of wheat fields. Aeciospores infect wheat similarly to urediniospores.
Wheat, barley, triticale and a few related species are the primary hosts for P. graminis f. sp. tritici. However, the closely related pathogen, P. graminis f. sp. secalis, is virulent on most barleys and some wheats (e.g. Line E). Puccinia graminis f. sp. secalis can attack Sr6 and Sr11 in a Line E host background (Luig, 1985). The primary alternate host in nature has been B. vulgaris L., a species native to Europe, although other species have been susceptible in greenhouse tests. The alternate hosts are usually susceptible to all or none of the formae speciales of P. graminis.
The main alternate host for P. graminis is B. vulgaris, which was spread by humans across the northern latitudes of the Northern Hemisphere. Because of its upright, bushy growth with many sharp thorns, it made an excellent hedge along field borders. The wood was useful for making tool handles, the bark provided a dye and the fruit was used for making jams. Settlers coming to North America from Europe brought the barberry with them. The barberry spread westward with humans and became established as a naturalized plant from Pennsylvania through the eastern Dakotas and southward into north-eastern Kansas. Many species of Berberis, Mahonia and Mahoberberis are susceptible to P. graminis (Roelfs, 1985b). The Canadian or Allegheny barberry, B. canadensis, should be added to this list.
The alternate host was a major source of new combinations of genes for virulence and aggressiveness in the pathogen (Groth and Roelfs, 1982). The amount of variation in the pathogen made breeding for resistance difficult, if not impossible. Of the virulence combinations present one year, many would not reoccur the following year, but many new ones would appear (Roelfs, 1982). The barberry was the source of inoculum (aeciospores) early in the season. Generally, infected bushes were close to cereal fields of the previous season, so inoculum travelled short distances without the loss in numbers and viability associated with long-distance transport. A single large barberry bush can produce about 64 x 109 aeciospores in a few weeks (Stakman, 1923). This is the equivalent of the daily output of 20 million uredinia, in an area of 400 m2.
Barberry was a major source of stem rust inoculum in Denmark (Hermansen, 1968) and North America (Roelfs, 1982). The success of reducing stem rust epidemics in northern Europe and North America following the removal of barberry near wheat fields has probably led to an overemphasis of the role of this alternate host in generating annual epidemics elsewhere.
Resistance to P. graminis in Berberis is reported to result from the inability of the pathogen to directly penetrate the tough cuticle (Melander and Craigie, 1927). Berberis vulgaris becomes resistant to infection about 14 days after the leaves unfold. However, infections occur on the berries, thorns and stems, which suggests the toughening of the cuticle may not be as important as originally thought. In recent testing of alternate host cultivars, a hypersensitive response has been observed particularly with Berberis spp. (Mahonia).
In most areas of the world, the life cycle (see scematic above) of P. graminis f. sp. tritici consists of continual uredinial generations. The fungus spreads by airborne urediniospores from one wheat plant to another and from field to field. Primary inoculum may originate locally (endemic) from volunteer plants or be carried long distances (exodemic) by wind and deposited by rain. In North America, P. graminis annually moves 2 000 km from the southern winter wheats to the most northern spring wheats in 90 days or less and in the uredinial cycle can survive the winter at sea level to at least 35°N. Snow can provide cover that occasionally permits P. graminis to survive as infections on winter wheat even at severe sub-freezing temperatures experienced at 45°N (Roelfs and Long, 1987). The sexual cycle seldom occurs except in the Pacific Northwest of the United States (Roelfs and Groth, 1980) and in local areas of Europe (Spehar, 1975; Zadoks and Bouwman, 1985). Although the sexual cycle produces a great genetic diversity (Roelfs and Groth, 1980), it also produces a large number of individuals that are less fit due to frequent recessive virulence genes (Roelfs and Groth, 1988) and to reassortment of genes for aggressiveness. Puccinia graminis has successfully developed an asexual reproduction strategy that apparently allows the fungus to maintain necessary genes in blocks that are occasionally modified by mutation and selection.
Urediniospore germination starts in one to three hours at optimum temperatures (Table 13.2) in the presence of free water. The moisture or dew period must last six to eight hours at favourable temperatures for the spores to germinate and produce a germ tube and an appressorium. Visible development will stop at the appressorium stage until at least 10 000 lux (16 000 being optimum) of light are provided. Light stimulates the formation of a penetration peg that enters a closed stoma. If the germling dries out during the germination period, the process is irreversibly stopped. The penetration process takes about three hours as the temperature rises from 18° to 30°C (Rowell, 1984). The light requirement for infection makes P. graminis much more difficult to work with in the greenhouse than P. recondita. Most likely, light seldom has an effect in the field except when dew periods dissipate before daybreak.
Urediniospores develop in pustules (uredinia) that rupture the epidermis and expose masses of reddish-brown spores. The uredinia are larger than those of leaf rust and are oval-shaped or elongated, with loose or torn epidermal tissue along the margins (Plate 16). The urediniospores are reddish-brown, elliptical to egg-shaped, echinulate structures measuring 24 to 32 µm x 18 to 22 µm (Plate 17).
As the host matures, telia (Plate 18) are produced directly from urediniospore infections or teliospores can be produced in a mature uredinial pustule. The teliospores are dark brown two-celled and somewhat wedge-shaped. They have thick walls, and measure 40 to 60 µm x 18 to 26 µm. The apical cell is rounded or slightly pointed (Plate 19). The teliospores are dicaryotic (n + n) and remain with the straw until spring. During this time, karyogamy occurs and the teliospores become diploid (2n). With spring rains and favourable temperatures, the teliospore germinates, un-dergoes meiosis and produces a four-celled basidium. Each cell produces a stigma with a single haploid basidiospore (1n). The hyaline basidiospore is windborne short distances (metres) to the barberry bush. Basidiospores germinate and penetrate directly. For maximum infection, the barberry leaf tissue should be less than two weeks old. Infection by a basidiospore results in the production of a pycnium (1n). The pycnium produces receptive hyphae and pycniospores of a single mating type (+ or -) that serve as female and male gametes for the fungus. Pycniospores of one mating type must be transferred to the receptive hyphae of the opposite mating type to initiate aeciospore development. The transfer of pycniospores is frequently done by insects, which are attracted to the oozing pycnial nectar produced by the pycnium. Mating of + and - types can also be facilitated by splashing rain, brushing of leaves, larger animals and neighbouring infections that coalesce. Aeciospores are dicaryotic (n + n) and are produced in aecia generally on the lower surface of the barberry leaves seven to ten days following fertilization. The aeciospores are the products of genetic recombination and may differ in their virulence and aggressiveness. The extent of variation depends on the differences between the parental isolates. Puccinia graminis f. sp. tritici has been crossed with other formae speciales, and crosses with P. graminis f. sp. secalis were relatively fertile (Johnson, 1949). In Australia, evidence points to recombination of wheat stem rust and the scabrum rust (P. graminis f. sp. secalis) (Burdon et al., 1981; Luig and Watson, 1972).
Aeciospores are hydroscopically released from the aecia and are airborne to wheat over distances of metres to perhaps a few kilometres. Aeciospores require similar conditions for infection to those of urediniospores. Infection by aeciospores results in the production of dicaryotic (n + n) uredinia with urediniospores. The repeating asexual cycle then involves urediniospores producing uredinia in about a 14-day cycle with optimum conditions. Under field conditions, where temperatures vary greatly, the cycle can be either lengthened or shortened. Generally, lower temperatures in the field, at least in the early stages of the crop cycle, tend to lengthen the latent period. In northern India, a latent period of 31 days was recorded for stem rust (Joshi and Palmer, 1973).
Source: The wheat rusts: R.P. Singh, J. Huerta-Espino, A.P. Roelfs