U p on germination the secondary sporidia produce dikaryotic myce-lium which can penetrate the plants and cause infection. After sys-temic d e v e l o p m e nt through the plant, the mycelium again forms telio-spores.
Development of Disease
T h e pathogen overwinters as teliospores on contaminated wheat kernels and in drier areas, in which winter wheat is grown, in the soil.
T h e teliospores of the common bunt fungi are short-lived in wet areas, but those of the dwarf bunt fungus may remain viable in any soil for many years.
Whe n contaminated s e ed is sown or healthy s e ed is sown in bunt-infested fields, approximately the s a me conditions that favor germina-tion of seeds favor germinagermina-tion of teliospores, although infecgermina-tion is favored by cool temperatures (6-12°C), and low soil moisture follow-ing sowfollow-ing. As the young seedlfollow-ing e m e r g e s from the kernel, the telio-spore on the kernel or near the seedling also germinates through pro-duction of the basidium, primary sporidia, and secondary sporidia (Fig. 52). T h e secondary sporidia then germinate, and the dikaryotic mycelium they produce penetrates the young seedling directly. After penetration the mycelium grows intercellularly and invades the de-veloping leaves and the terminal meristematic tissue at the growing point of the plant. T h e mycelium remains dormant in the seedling during the winter, but when the seedling begins to grow again in the spring, the mycelium r e s u m es its growth and grows with the growing point. Whe n the plant forms the head of the grain, the mycelium in-vades all parts of it even before the head e m e r g e s out of the " b o o t ." As the head fills and b e c o m es mature, the mycelial threads increase in numbers and soon take over and c o n s u me the contents of the kernel cells. T h e mycelium, however, does not affect the tissues of the peri-carp of the kernel which form a rather sturdy covering for the smutted mass they contain. At the s a me time the binucleate hypha branches are transformed into round, thick-walled, binucleate teliospores, while part of the older mycelium remains vacuolated. Certain hyaline, sporelike cells, usually called sterile cells, are also present in mixture with the teliospores.
Smutted kernels are usually kept intact while on the plant, but break and release their spores upon harvest or threshing. T h e liber-ated spores contaminate the healthy kernels and are also blown away by air currents, thus contaminating the soil.
Bunt, or Stinking Smut, of Wheat
Control
Bunt can b e controlled effectively in most areas by using smut-free s e ed of a resistant variety properly treated with an appropriate fungi-cide. Whe n the s e ed to b e sown is not known to b e free of smut-spore contamination, it should b e well c l e a n ed to remove any unbroken kernels and as many of the smut spores on the s e ed as possible. T h e s e ed is then treated with the fungicide hexachlorobenzene ( H C B ), al-though other fungicides, including C e r e s an M, N ew Improved Cere-san, AraCere-san, and Spergon, give good control of the disease. T h e fungi-cides are a p p l i ed to the s e ed at the rate of 1-2 ounces per bushel either as dusts or, more commonly, by making a concentrated water suspension or slurry of the chemical that sticks to the s e ed without wetting the s e ed appreciably. In dwarf bunt, and in c o m m on bunt in drier areas, the spores survive in the soil for long periods and can cause infection of seedlings. Therefore, neither can b e completely controlled by s e ed treatment, although s e ed treatment reduces the proportion of infected plants considerably. Wher e economically possi-ble, application of hexachlorobenzene to the soil surface after plant e m e r g e n c e helps reduce dwarf bunt infection.
Many wheat varieties showing various d e g r e es of resistance to bunt have b e e n d e v e l o p ed and are u s ed commercially, e.g., Omar and Gaines, which are resistant to both common and dwarf bunts, while the varieties Brevor and Burt and most spring wheat varieties are re-sistant to dwarf bunt. E v en the s e ed of rere-sistant varieties, however, should b e treated with hexachlorobenzene before sowing.
Selected References
Purdy, L. H. 1965. C o m m on a nd dwarf bunts, their chemical control in the Pacific Northwest. Plant. Disease Reptr. 49 : 4 2 - 4 6 .
Purdy, L. H., a nd E. L. Kendrick. 1963. Influence of environmental factors on the devel-o p m e nt devel-of w h e at b u nt in the Pacific Ndevel-orthwest. IV. Effect devel-of sdevel-oil temperature a nd soil moisture on infection by soil-borne spores. Phytopathology 53: 4 1 6 - 4 1 8 . R o d e n h e i s e r, Ç . Á., a nd C. S. Holton. 1945. Distribution of races of Tilletia caries a nd T.
foetida a nd their relative virulence on certain varieties a nd selections of wheat.
Phytopathology 35 : 9 5 5 - 9 6 9 .
Stem rust of wheat is worldwide in distribution and attacks wheat wherever it is grown. Similar rust diseases attack the other cultivated cereals and probably most wild grass species. T wo other rusts, leaf rust and stripe rust also attack wheat and cause symptoms and losses similar to those c a u s ed by stem rust.
Stem rust attacks all the aboveground parts of the wheat plant on which it produces small, elongate, brick-red or black pustules (Fig.
53). Stem rust causes losses by reducing yield and quality of grain (Fig. 54). Infected plants usually produce fewer tillers, set fewer seeds per head, and the kernels are smaller in size, generally shriveled and of poor milling quality and food value. U n d er extreme situations, heavily infected plants may die. Wher e wheat is u s ed for pasture, the shorter, low-tillering infected plants represent a lower forage yield and quality. H e a vy seedling infection of winter wheat also w e a k e ns the plants and makes them susceptible to winter injury and to attack by other pathogens. T h e amount of losses c a u s ed by stem rust may vary from slight to complete destruction of wheat fields over rather large areas, sometimes e n c o m p a s s i ng several states. T e n s of millions of bushels of wheat are lost to stem rust in the United States annually, and during years of severe stem rust e p i d e m i cs the losses are in the hundreds of millions of bushels.
Symptoms
T h e pathogen causing stem rust of wheat attacks and produces symptoms on two distinctly different kinds of host plants. T h e most serious, and economically important, symptoms are produced on
Stem Rust of Wheat 313
F i g. 53. (A) S y m p t o ms of s t em rust of w h e at as it a p p e a rs on w h e at stems a nd l e a v es in the field. (B) C l o s e - up of stem rust s y m p t o ms on grain stems. (Photos by courtesy of U.S. D e p t. Agr.)
wheat and certain related cereals (e.g., barley, rye) and grasses. Symp-toms, however, although economically unimportant, are also pro-d u c epro-d on plants of common barberry (Berberis vulgaris) anpro-d certain other wild native species of barberry.
T h e symptoms on wheat appear at first as long, narrow, elliptical blisters, parallel with the long axis of the stem, leaf, or leaf sheath of young seedlings or of plants at any stage of growth (Fig. 53). In later stages of wheat plant growth, blisters may appear on the glumes, and even the beards. Within a few days, the epidermis covering the pus-tules is ruptured irregularly and is p u s h ed back revealing a powdery mass of reddish or rust-colored spores, called uredospores. T h e pus-tules, called uredia, vary in size from very small to about 3 m m w i de by 10 m m long. Later in the season, as the grass plant approaches ma-turity, the rusty color of the pustules turns black b e c a u se the fungus produces teliospores instead of uredospores and uredia are
trans-F i g. 54. C o m p a r i s on of kernels from healthy a nd stem rust-infected w h e at plant. Left:
P l u mp wheat. Right: Wheat shriveled by stem rust. (Photo by courtesy of U . S.
D e p t. Agr.)
formed into black, smooth rather than powdery, telia. Sometimes telia may d e v e l op i n d e p e n d e nt of uredia. Although the size of uredia or te-lia is rather small, either fruiting structure may exist on wheat plants in such great numbers that large parts of the plant appear to be cov-ere d with the ruptured areas which are filled with either the rusty-red uredospores or the black teliospores or both.
On barberry, the symptoms appear as yellowish to orange-colored spots on the leaves and sometimes on young twigs and fruits. Within the spots, and in leaves generally on the upper side, appear a few minute dark-colored bodies called pycnia (or spermagonia), usually bearing a small droplet of liquid. On the lower side of the leaf, be-neath the pycnia, and occasionally on the u p p er surface, or next to the pycnia on twigs, fruit, petioles, etc., groups of orange-yellow horn- or cuplike projections, called aecia, appear. T h e host tissue bearing the aecia is frequently hypertrophied. T h e aecial wall, called a peridium, usually protrudes at the margin of the cups and its light, whitish color is contrasted with the orange-colored aeciospores contained in the aecia.
Stem Rust of Wheat 315
The Pathogen: Puccinia graminis tritici
T h e wheat stem rust pathogen is a basidiomycete. Its mycelium is colorless and produces several different kinds of spores (Fig. 55). Four haploid basidiospores belonging to two different mating types are produced by each of the two cells of the overwintering teliospore. T h e basidiospores produce haploid mycelium which can infect and grow only on barberry, on which they produce flask-shaped pycnia. T h e pycnia are of two mating types and produce small, haploid pycnio-spores (spermatia) which ooze out, and long, haploid hyphae which protrude on the leaf surface through the openings of the pycnia. T h e protruding hyphae are called receptive hyphae b e c a u se they b e h a ve as female gametes and can b e fertilized by pycniospores from another pycnium of the compatible mating type. T h e fertilized hypha be -comes dikaryotic and grows as such into the tissues surrounding the pycnia on petioles, blossoms, etc., or toward the opposite side of the leaf, where it usually produces aecia. T h e aecia, produced on barber-ry, contain rows of dikaryotic aeciospores that can no longer infect barberry, but can infect only wheat. T h e dikaryotic mycelium pro-d u c epro-d from the germinating aeciospores grows into the wheat tissues intercellularly and, just b e l ow the epidermis, forms uredia which pro-d u ce the brick-repro-d or rusty colorepro-d urepro-dospores. Urepro-dospores can then reinfect wheat (secondary infection). T h e y are the only kind of stem rust spores that can infect the host on which they are produced, and produce more uredia and uredospores. Later on in the season, uredia also produce teliospores along with, or instead of, uredospores, or late uredospore infections on wheat may result in direct production of telia which, in turn, produce only teliospores. T h e teliospores are still dikaryotic, but just before they germinate the two nuclei in each cell fuse to produce a true diploid nucleus. Upon germination of the teliospore a basidium is produced, and the diploid nucleus undergoes meiosis. T h e resulting nuclei divide once mitotically and m o ve into the basidium, and each of the four haploid nuclei m o v es into one of the four basidiospores formed laterally on the b a s i d i u m . T he basidio-spores are again of two mating types and can infect only barberry.
Development of Disease
In the cooler, northern regions the fungus overwinters as telio-spores attached to the telia of infected wheat debris or scattered on the soil. Teliospores germinate in the spring only after they have b e e n subjected to low temperatures, such as freezing and thawing,
occur-ring naturally in northern areas duoccur-ring the winter. T h e basidiospores produced by each teliospore are carried by air currents for rather short distances, probably no more than a few hundred meters. If barberry plants are growing nearby and the basidiospores land on young bar-berry leaves, petioles, blossoms, or fruit, the basidiospores germinate and penetrate the epidermal cells directly, but after that, the myce-lium grows mostly intercellularly with the formation of simple or branched haustoria which enter the cells. Within 3 or 4 days the hy-phal branches converge toward a point just below the epidermis, where they form a mat of mycelium d e v e l o p i ng into a pycnium (Fig.
55). T h e outward pressure of the pycnium finally breaks the epider-mis, and the ostiole of the pycnium e m e r g e s on the surface of the plant tissue. Receptive hyphae originating in the pycnium extend beyond the lips of the ostiole, and at the same time pycniospores e m b e d d ed in a sticky liquid are e x u d ed through the ostiole. Insects visiting the in-fected barberry leaves b e c o me smeared with pycniospores and carry them to other, possibly sexually compatible pycnia. Pycniospores may also b e carried to compatible pycnia by rainwater or d e w running off the plant surface. Whe n a pycniospore is brought into contact with a receptive hypha of a compatible pycnium, fertilization takes place.
T h e nucleus of the pycniospore p a s s es into the receptive hypha, but it does not unite with the nucleus already present in the latter. Instead, it divides mitotically and one of its two nuclei remains in the cell, while the other moves to the n e x t t e ll of the receptive hypha, where it divides again and so on, so that the cells of the receptive hypha and of all the branches produced subsequently from it contain two separate nuclei, thus forming a dikaryotic mycelium. This mycelium then grows intercellularly toward the periphery of the pycnia, present on petioles, fruit, etc., or usually toward the lower side of the leaf bearing the pycnium, where it forms thick mycelial mats that will d e v e l op into aecia. In the meantime, the host cells surrounding the mycelium are stimulated to enlarge, and along with the increased v o l u me of the fungus, result in a swelling of the infected area on the lower surface of the leaf.
T h e aecia form in groups and protrude considerably b e y o nd the leaf or other tissue surface of the barberry plant. T h e aeciospores are pro-d u c epro-d in chains on short hyphae insipro-de the aecium, anpro-d each spore contains two separate nuclei. Aeciospores are released in the late spring or early summer and are carried by wind to nearby wheat plants on which they germinate. T h e germ tube penetrates wheat stems, leaves or sheaths through stomata and after the mycelium grows intercellularly for a while, it then grows more profusely toward,
Fig. 55. Disease cycle of stem rust of wheat caused by Puccinia graminis tritici.
Aeciospore infects wheat stem or leaf through stomata
A Wheat plants
Aeciospores Clusters of aecia on under side of barberry leaf Uredospores Uredospore reinfects wheat through stomata
/ Teliospores ^^Telia on wheat 'at the end of season vv^More /uredia on wheat ^v^uredium V on wheat
Aecium V: primordiumV
^ Fertilized receptive
L
hypha/ ,
Pycniospores fertilize compatible receptive hypha Pycniospores Pycnia on barberry leaf Telia and uredia on wheat stem or leaf
^-Basidiospores Basidium Overwintering teliospore ,
Barberry stem and leaves y Basidiospores mtect ' barberry leaf directly
Receptive X hypha J Germinating teliospore
but below the surface of, the wheat tissue and forms a mat of myce-lium just below the epidermis. Many short hyphae arise from the mycelium, and at the tip of each forms one uredospore. T h e growth of the sporophores and of the uredospores exert pressure on the epider-mis which is p u s h ed outward and forms a pustule manifesting the presence of the uredium. Finally the epidermis is broken irregularly and flaps back revealing several hundred thousand rusty-colored ure-dospores which are easily detached from the sporophores and give a powdery appearance to the uredium.
T h e uredospores are easily blown away by air currents, and stronger winds may carry them many miles, even hundreds of miles, from the point of their origin. T h e uredospores can reinfect wheat plants. Whe n they land on wheat plants, in the p r e s e n ce of dew, a film of water or relative humidities near the saturation point, they germinate and en-ter the plant through stomata. T h e mycelium grows inen-tercellularly again, sends haustoria into the plant cells, and within 8 to 10 days from inoculation it produces a ne w uredium and more uredospores. Many successive infections of wheat plants by uredospores may take place within one growing season up to the time the plant reaches full matu-rity. Most of the d a m a ge c a u s ed to wheat growth and yield results from such uredospore infections which may literally cover the stem, leaf, leaf sheaths, glumes, etc., with uredia.
T h e presence of numerous uredia on wheat plants results in an in-creased water loss by the plant b e c a u se of increases in transpiration of water by infected plants and in evaporation of water through the rup-tured epidermis. In addition to r e d u c ed amounts of water being avail-able to the d i s e a s ed plant, the fungus itself removes much of the nutri-ents, and water, that would normally b e u s ed by the plant. T h e respiration of infected plants increases rapidly during the develop-men t of the uredia, but a few days after sporulation of the fungus res-piration drops to slightly below normal. Photosynthesis of d i s e a s ed plants is r e d u c ed considerably d ue to destruction of much of the pho-tosynthetic area by the fungus and to interference of the fungal secre-tions with the photosynthetic activity of the remaining green areas on the plant. T h e fungus also s e e ms to interfere with normal root devel-opment and uptake of nutrients by the roots. All these effects reduce the amount of nutrients available for the production of the normal number and size of s e e ds on the plant, which are further accentuated by fungus-induced earlier maturity of the plant, resulting in d e c r e a s ed time available for the s e ed to fill out. T h e total amount of d a m a ge de-pends considerably on the stage of d e v e l o p m e nt of the wheat plant at the time rust infection b e c o m es heavy. T h u s, heavy rust infections
Stem Rust of Wheat 319
before or at the flower stage are extremely d a m a g i ng and may cause total yield loss (Fig. 54), whereas if heavy infections do not occur until late dough stage, the d a m a ge to yield is m u ch smaller.
Whe n the wheat plant approaches maturity, or when the plant fails b e c a u se of overwhelming infection, the uredia produce teliospores instead of uredospores, or ne w telia may d e v e l op from recen t uredo-spore infections. Teliouredo-spores do not germinate immediately and do not infect wheat, but are the overwintering stage of the fungus. Telio-spores also serve as the stage in which fusion of the two nuclei and meiosis take place and result in the production of ne w combinations of genetic characters of the fungus through genetic recombination and, upon germination, production of genetically different basidio-spores. U p on fertilization in the pycnia, the different genetic charac-ters are c o m b i n ed again in the dikaryotic mycelium of the aecium and uredium and result in the appearance of ne w races of the fungus which can possibly infect n e w or old varieties of wheat that were pre-viously i m m u ne or resistant to the existing races. Several hundred races of the stem rust fungus are known to date and ne w ones appear every year. Variability in the rust fungus can, of course, b e brought about by mutation and other m e c h a n i s ms during the production of any kind of spores. Such m e c h a n i s ms s e em to b e primarily responsible for the variability of the fungus in southern areas, where teliospores are p r o d u c ed infrequently and usually do not germinate, or in areas where the alternate host, barberry, is absent.
In southern regions the fungus usually overwinters as mycelium on
In southern regions the fungus usually overwinters as mycelium on