SMU 1
infected branches before the fungus reaches the trunk.
As with white pine blister rust, and perhaps even
more so, the control of fusiform rust is obtained
through selection and breeding of resistant trees, with
emphasis on trees possessing general rather than
specific resistance.
Selected References
Alexopoulos, C. J., Mims, C. W., and Blackwell, M. (1996). “Intro-
ductory Mycology,” 4th Ed. Wiley, New York.
Allen, R. F. (1930). A cytological study of heterothallism in Puccinia
graminis. J. Agric. Res. (Washington, DC) 40, 585–614.
Anguelova-Methar, V. S., Van Der Westhuizen, A. J., and Pretorius,
Z. A. (2001). b-1,3-Glucanase and chitinase activities and the
resistance response of wheat to leaf rust. J. Phytopathol. 149,
381–384.
Anonymous (1981). Stakman-Craigie symposium on rust diseases.
Phytopathology 71, 967–1000.
Bromfield, K. R. (1984). “Soybean Rust.” Monograph 11. The Amer-
ican Phytopathological Society, St. Paul, MN.
Browning, J. A., and Frey, K. J. (1969). Multiline cultivars as a means
of disease control. Annu. Rev. Phytopathol. 7, 355–382.
Crowell, I. H. (1934). The hosts, life history, and control of the
cedar- apple rust fungus Gymnosporangium juniperi-virginianae.
J. Arnold Arbor. Harv. Univ. 15, 163–232.
Cummins, G. B. (1959). “Illustrated Genera of Rust Fungi.” Burgess,
Minneapolis, MN.
De Jesus, W. C., Jr., do Vale, F. X. R., Coelho, R. R., et al. (2001).
Effects of angular leaf spot and rust on yield loss of Phaseolus
vul- garis. Phytopathology 91, 1045–1053.
Ellis, J., Lawrence, G., Ayliffe, M., et al. (1997). Advances in the
molecular genetic analysis of the flax-flax rust interaction. Annu.
Rev. Phytopathol. 35, 271–291.
Eversmeyer, M. G., and Kramer, C. L. (2000). Epidemiology of
wheat leaf and stem rust in the central Great Plains of the USA.
Annu. Rev. Phytopathol. 38, 491–513.
Eversmeyer, M. G., Kramer, C. L., and Browder, L. E. (1984). Pres-
ence, viability, and movement of Puccinia recondita and P. graminis
inoculum in the Great Plains. Plant Dis. 68, 392–395.
Everts, K. L., Leath, S., and Finney, P. L. (2001). Impact of powdery
mildew and leaf rust on milling and baking quality of soft red
winter wheat. Plant Dis. 85, 423–429.
Frederick, R. D., Snyder, C. L., Peterson, G. L., et al. (2002). Poly-
merase chain reaction assays for the detection and discrimination
of the soybean rust pathogens Phakopsora pachyrhizi and P. mei-
bomiae. Phytopathology 92, 217–227.
Gross, P. L., and Venette, J. R. (2000). Overwinter survival of bean
rust urediniospores in North Dakota. Plant Dis. 85, 226–227.
Hamelin, R. C., Dusabenyagasani, M. and Et-touil, K. (1998). Fine-
level genetic structure of white pine blister rust populations. Phy-
topathology 88, 1187–1191.
Hart, H. (1931). Morphologic and physiologic studies on stem-rust
resistance in cereals. Minn. Agric. Exp. Stn. Tech. Bull. 266, 1–75.
Hartman, G., Sinclair, J., and Rupe, J. (1999). “Compendium of
Soybean Diseases.” APS Press, St. Paul, MN.
Hooker, A. L. (1967). The genetics and expression of resistance in
plants to rusts of the genus Puccinia. Annu. Rev. Phytopathol. 5,
163–182.
Hovmøller, M. S., Justesen, A. F., and Brown, J. K. M. (2002). Clon-
ality and long-distance migration of Puccinia striiformis f. sp. tritici
in northwest Europe. Plant Pathol. 51, 24–32.
Hunt, R. (1997). White pine blister rust. In “Compendium of Conifer
Diseases” (E. M. Hansen and K. J. Lewis, eds.), pp. 26–27. Amer-
ican Phytopathological Society, St. Paul, MN.
Johnson, T., Green, G. J., and Samborski, D. J. (1967). The world sit-
uation of the cereal rusts. Annu. Rev. Phytopathol. 5, 183–200.
Khan, M. A., Trevathan, L. E., and Robbins, J. T. (1997). Quantita-
tive relationship between leaf rust and wheat yield in Mississippi.
Plant Dis. 81, 769–772.
Kinloch, B. B., Jr., and Dupper, G. E. (2002). Genetic specificity in the
white pine-blister rust pathosystem. Phytopathology 92, 278–280.
Kuchler, F., Duffy, M., Shrum, R. D., and Dowler, W. M. (1984).
Potential economic consequences of the entry of an exotic fungal
pest: The case of soybean rust. Phytopathology 74, 916–920.
Kushalappa, A., and Eskes, A. B. (1989). Advances in coffee rust
research. Annu. Rev. Phytopathol. 27, 503–531.
Littlefield, L. J., and Heath, M. C. (1979). “Ultrastructure of Rust
Fungi.” Academic Press, New York.
Lopes, D. B., and Berger, R. D. (2001). The effects of rust and
anthrac- nose on the photosynthetic competence of diseased bean
leaves. Phytopathology 91, 212–220.
Malloy, O. C. (1997). White pine blister rust control in North
America: A case history. Annu. Rev. Phytopathol. 35, 87–109.
McIntosh, R. A., and Brown, G. N. (1997). Anticipatory breeding for
resistance to rust diseases in wheat. Annu. Rev. Phytopathol. 35,
311–326.
Nagarajan, S., and Singh, D. V. (1990). Long-distance dispersion of
rust pathogens. Annu. Rev. Phytopathol. 28, 139–153.
Peterson, R. S., and Jewell, F. F. (1968). Status of American stem rusts
of pine. Annu. Rev. Phytopathol. 6, 23–40.
Powers, H. R., Schmidt, R. A., and Snow, G. A. (1981). Current status
and management of fusiform rust on southern pines. Annu. Rev.
Phytopathol. 19, 353–371.
Rapilly, F. (1979). Yellow rust epidemiology. Annu. Rev. Phytopathol.
17, 59–73.
Roelfs, A. P. (1989). Epidemiology of cereal rusts in North America.
Can. J. Plant Pathol. 11, 86–90.
Roelfs, A. P., and Bushnell, W. R., eds. (1985). “The Cereal Rusts,”
Vols. 1 and 2. Academic Press, Orlando, FL.
Scott, K. J., and Chakravorty, A. K., eds. (1982). “The Rust Fungi.”
Academic Press, New York.
Sillero, J. C., and Rubiales, D. (2002). Histological characterization
of resistance to Uromyces viciae-fabae in fava bean. Phytopathol-
ogy 92, 294–299.
Silva, M. C., Nicole, M., Guerra-GuimarA˘ es, L., et al. (2002). Hyper-
sensitive cell death and posthaustorial defense responses arrest the
orange rust (Hemileia vastatrix) growth in resistant coffee leaves.
Physiol. Mol. Plant Pathol. 60, 169–183.
Subrahamanyam, P., Reddy, L. I., Gibbons, R. W., and McDonald, D.
(1985). Peanut rust: A major threat to peanut production in the
semiarid tropics. Plant Dis. 69, 813–819.
Ward, H. M. (1882). Researches on the life history of Hemileia vas-
tatrix, the fungus of the “coffee leaf disease.” Linn. Soc. J. (Bot.)
19, 229–335.
Zadoks, J. C. (1965). Epidemiology of wheat rusts in Europe. FAO
Plant Prot. Bull. 13, 97–108.
Zhang, L., and Dickinson, M. (2001). Fluorescence from rust fungi:
A simple and effective method to monitor the dynamics of fungal
growth in planta. Physiol. Mol. Plant Pathol. 59, 137–141.
SMUTS
Plant smuts, caused by Basidiomycetes of the order
Ustilaginales, occur throughout the world. There are
2 11. PLANT DI SEA SES CAUSED BY FUNGI
approximately 1,200 species of smut fungi. Until the
20th century, smuts were the causes of serious grain
losses that were equal to, or second only to, losses
caused by the rusts. In some respects, the smuts of
cereals were dreaded by farmers even more than rusts
because many smuts attack the grain kernels
themselves and replace the kernel contents with the
black, dusty spore masses that resemble soot or smut.
Thus, the reduction in yield is conspicuous and direct
and the quality of the remaining yield is reduced
drastically by the presence of the black smut spores on
the surface of healthy kernels. In addition to the various
cereals, smuts also affect sugarcane, onions, and some
ornamentals such as carnation.
Most smut fungi attack the ovaries of grains and
grasses and develop in them and in the fruit, i.e., the
kernels of grain crops, which they destroy completely
(Fig. 11-129). Several smuts, however, attack the leaves,
stems, or floral parts. Some smuts infect seeds or
seedlings before they emerge from the ground, and they
grow internally in the seedling until they reach the inflo-
rescence; others cause only local infections on leaves,
stems, and so on. Cells in affected tissues are either
destroyed and replaced by black smut spores or they
are first stimulated to divide and enlarge to produce a
swelling or gall of varying size and are then destroyed
and replaced by the black smut spores. The spores
are present in masses that may be held together only
temporarily by a thin, flimsy membrane or by a more
or less durable one. Smut fungi seldom kill their hosts,
but in some cases infected plants may be severely
stunted.
Most smut fungi produce only two kinds of spores:
teliospores and basidiospores (Fig. 11-127). Teliospores
are usually formed from mycelial cells along the length
of the mycelium within the smut galls, and
basidiospores either bud off laterally from the basidium
cells or are produced as a cluster at the tip of a
nonseptate basid- ium. Basidiospores of the smuts are
not borne on sterig- mata. When basidiospores
germinate, the germ tubes either unite with compatible
ones while still on the basidium and then infect or they
penetrate tissues directly. Their haploid mycelium,
however, cannot invade tissues extensively and does
not cause typical infections until two compatible
mycelia unite to produce dikaryotic mycelium. The
latter then invades tissues inter- or intracellularly and
produces the typical symp- toms and the teliospores.
Smut fungi also exist in many races; however, races of
smut fungi are not as stable as rusts, as each generation
of smut fungi on the host plant involves meiosis, i.e.,
genetic recombination, and this results in new races
appearing constantly. The most common smut fungi and
the diseases they cause are the following.
Ustilago, causing corn smut [U. zeae (maydis)],
loose smut of cereals (U. avenae, U. nuda, and U.
tritici), and sugarcane smut (U. scitaminea)
Tilletia, causing covered smut or bunt of wheat [T.
caries (= T. tritici) and T. laevis (= T. foetida)],
dwarf bunt of wheat (T. controversa), and Karnal
bunt of wheat (T. indica)
Sphacelotheca, causing the sorghum smuts (S. sorghi,
S. cruenta, and S. reiliana)
Urocystis, causing onion smut (U. cepulae)
Neovossia, causing kernel smut of rice (N. bar-
clayana)
Entyloma, causing leaf smut of rice (E. oryzae)
Smuts generally overwinter as teliospores on con-
taminated seed, in plant debris, or in the soil. However,
some smuts overwinter as mycelium inside infected
kernels or in infected plants. The teliospores are not
infectious but produce basidiospores, which on germi-
nation either fuse with compatible ones and then infect
or penetrate the tissue and then fuse to produce dikary-
otic mycelium and the typical infection. Smut fungi have
only one generation per year, each infection resulting in
one crop of teliospores per growing season.
The control of smuts is primarily by use of resistant
varieties and seed treatment. The latter may involve
either chemical dusting or dipping, if the fungus is
present as teliospores on the seed surface or in the soil,
or hot water if the fungus is present as mycelium inside
the seed. The discovery of carboxin, thiabendazole, eta-
conazole, and other fungicides that are absorbed and
translocated systemically by seeds and seedlings allows
chemical control by seed treatment of even those smuts
present as mycelium inside the seeds. Soil treatments
with these and other chemicals are also useful in the
control of smut diseases.
CORN SMUT
Corn smut occurs wherever corn is grown. It is more
prevalent, however, in warm and moderately dry areas.
Corn smut damages plants and reduces yields by
forming galls on the aboveground parts of plants,
including ears, tassels, stalks, and leaves. The number,
size, and location of smut galls on the plant affect the
amount of yield loss. Galls on the ear usually destroy it
to a large extent, whereas large galls above the ear cause
much greater reduction in yield than galls below the ear.
Losses from corn smut range from a trace up to 10%
or more in localized areas. Some individual fields of
sweet corn may show losses approaching 100% from
corn smut. Generally, however, over large areas and
with the use of resistant varieties, losses in grain yields
average about 2%.

Symptoms
When young corn seedlings are infected, minute galls
form on the leaves and stems, and the seedling may
remain stunted or may be killed. On older plants, infec-
tions occur on the young, actively growing tissues of
axillary buds, individual flowers of the ear and tassel,
leaves, and stalks (Fig. 11-144).
Infected areas are permeated by the fungus
mycelium, which stimulates the host cells to divide and
enlarge, thus forming galls. Galls are first covered with a
green- ish white membrane. Later, as the galls mature,
they reach a size from 1 to 15 centimeters in diameter,
and their interior darkens and turns into a mass of
powdery, dark olive-brown spores. The silvery gray
membrane then ruptures and exposes the millions of
sooty teliospores, which are released into the air. Galls
on leaves frequently remain very small (about 1–2 cm in
diameter), hard, dry, and do not rupture.
The Pathogen: Ustilago zeae
The fungus produces dikaryotic mycelium, the cells
of which are transformed into black, spherical, or ellip-
soidal teliospores. Teliospores germinate by producing
a four-celled basidium (promycelium) from each cell
of which a basidiospore (sporidium) develops (Fig. 11-
145).
Development of Disease
The fungus overwinters as teliospores in crop debris
and in the soil, where it can remain viable for several
years. In the spring and summer, teliospores germinate
and produce basidiospores, which are carried by air cur-
rents or are splashed by water to young, developing
tissues of corn plants. Basidiospores germinate and
produce a fine hypha, which can enter epidermal cells
directly. After an initial development, however, its
growth stops and the hypha usually withers and some-
times dies, unless it contacts and fuses with a haploid
hypha derived from a basidiospore of the compatible
mating type. If fusion takes place, the resulting hypha
becomes dikaryotic, enlarges in diameter, and grows
into the plant tissues mostly intercellularly (Fig. 11-
145). Cells surrounding the hypha are stimulated to
enlarge and divide, and galls begin to form even before
the fungus actually gets there.
Galls in older plants seem always to be the result of
local infections. Systemic infections occur occasionally
in very young seedlings. Frequently, however, only a
small number of the actual local infections develop into
typical, large galls, with the others remaining too small
to be visible.
SMU 3
The mycelium in the gall remains intercellular during
most of gall formation, but before sporulation, the
enlarged corn cells are invaded by the mycelium, col-
lapse, and die. The mycelium utilizes the cell contents
for its further growth, and the gall then consists pri-
marily of dikaryotic mycelium and plant cell remains.
Most of the dikaryotic cells subsequently develop into
teliospores and, in the process, seem to absorb and
utilize the protoplasm of the other mycelial cells, which
remain empty. Only the membrane covering the gall is
not affected by the fungus, but finally the membrane
breaks and the teliospores are released. Some of the
released teliospores, if they land on young, meristematic
corn tissues, may cause new infections and new galls
during the same season, but most of them fall to the
ground or remain in the corn debris, where they can
survive for several years.
Control
No corn varieties or hybrids completely resistant to
smut are known, but several corn hybrids show moder-
ate resistance to the fungus. New pathogen races appear
constantly, however; therefore partial resistance is the
major type of resistance selected for in breeding pro-
grams. Sanitation measures, such as removal of smut
galls before they break open, and crop rotation help
where corn is grown in small, rather isolated plots but
is impractical and impossible in large corn-growing
areas. In some countries, e.g., Mexico, corn smuts are
collected and used as food delicacies, not unlike the
edible mushrooms consumed elsewhere.
LOOSE SMUT OF CEREALS
Loose smut of cereals occurs worldwide but is more
abundant and serious in humid and subhumid regions.
Loose smut causes damage by destroying the kernels
(Fig. 11-146) of the infected plants and by smearing and
thus reducing the quality of the grain of the noninfected
plants on harvest. Losses from loose smut may be up to
10 or 40% in certain localities in a given year, but the
overall losses in the United States are approximately 1%
per year.
Symptoms
Loose smut generally does not produce discernible
symptoms until the plant has produced a head. Smutted
plants sometimes head earlier than healthy ones, and
smutted heads are often elevated above those of healthy
plants (Fig. 11-146). In an infected plant, usually all the
heads and all the spikelets and kernels of each head are
4 11. PLANT DI SEA SES CAUSED BY FUNGI

A B

C D
FIGURE 11-144 Corn smut caused by Ustilago maydis. Smut in younger (A) and older (B) ears of corn in which
individual corn kernels have enlarged greatly and filled with smut spores. (C) Smut on a corn tassel and (D) smut galls
on corn stem. [Photographs courtesy of (A) P. E. Lipps, Ohio State University, (B) D. Ormrod, WCPP, and (C and D)
K. Mohan, University of Idaho.]
 SMU 5

Compatible
basidiospores
Basidiospores infect young
plants or growing tissues of older plants Dikaryotic mycelium
infects kernel through silk

Ears of corn
are infected through the silk
Infected kernel
enlarges and forms gall
Basidiospores

Leaf or stem
infection

Basidium

Galls on leaf

Corn plant with galls

Greminating
teliospore
Mycelium
in gall

Zygote

Teliospores
overwintering on soil
Dikaryotic cells
of mycelium become teliospores in gall
Galls full of teliospores

FIGURE 11-145 Disease cycle of corn smut caused by Ustilago maydis.

smutted, i.e., they are each transformed into a smut
mass consisting of olive-green spores (Fig. 11-146).
Smutted kernels are at first covered by a delicate
grayish membrane, which soon bursts and sets the
powdery spores free. The spores are then blown off by
the wind and leave the rachis a naked stalk.
The Pathogens: Ustilago nuda and Ustilago tritici
The mycelium is hyaline during its growth through
the plant, and it is hyaline changing to brown near
maturity. The mycelial cells are transformed into brown,
spherical teliospores, which germinate readily and
produce a basidium consisting of one to four cells. The
basidium produces no basidiospores, but its cells ger-
minate and produce short, uninucleate hyphae that fuse
in pairs and produce dikaryotic mycelium, which is
capable of infection (Figs. 11-146 and 11-147).
Development of Disease
The pathogens overwinter as dormant mycelium in
the scutellum of the cotyledon of infected kernels. When
planted, infected kernels begin to germinate, and the
mycelium resumes its activity and grows intercellularly
through the tissues of the young seedling until it reaches
the growing point of the plant (Fig. 11-147). The
mycelium then follows closely the growing point of the
plant, while the hyphae in the tissues of the lower stem
frequently disappear. When the plant forms the head,
the mycelium invades all the young spikelets, where it
grows intracellularly and destroys most of the tissues of
the spike, except the rachis. By this time, most infected
plants are slightly taller than most healthy plants due to
the stimulatory action of the pathogen. The mycelium in
the infected kernels is soon transformed into
teliospores, which are contained only by a delicate
outer membrane
6 11. PLANT DI SEA SES CAUSED BY FUNGI

A B

C
FIGURE 11-146 Loose smut of cereals. (A) Field with heads of barley infected with loose smut caused by
Ustilago nuda. (B) Close-up of a healthy (right) and several heads of barley infected with loose smut. (C) Microscopic
view of smut fungus mycelium and spores in an infected barley embryo. [Photographs courtesy of (A) P. Thomas, (B)
I.R. Evans, WCPD, and (C) V. Pederson, North Dakota State University.]

of host tissue. The membranes burst open soon after
maturation of the teliospores, and the spores are released
and blown off by air currents to nearby healthy plants.
Spore release coincides with the opening of the flowers
of healthy plants. Teliospores landing on flowers germi-
nate through formation of a basidium on which the
haploid hyphae are produced. After fusion of sexually
compatible haploid hyphae, the resulting dikaryotic
mycelium penetrates the flower through the stigma or
through the young ovary walls and becomes established
in the pericarp and in the tissues of the embryo before
the kernels become mature. The mycelium then
becomes inactive and remains dormant, primarily in the
scutel- lum, until the infected kernel germinates.
Control
Loose smut is now controlled by treating infected
seeds with carboxin and its carboxanilide derivatives
before planting. These chemicals are absorbed and act
systemically in the seed or in the growing plant.
Although some barley and wheat varieties are quite
resistant to loose smut, most of the commercial varieties
are very susceptible to it.
The best means of controlling loose smut is through
the use of certified smut-free seed. Until the discovery
of systemic fungicides, when seed was known to be
infected with loose smut mycelium, the best way of dis-
infecting it was by treating it with hot water. Usually
small lots of seed are treated with hot water and planted
in isolated fields to produce smut-free seed to be used
during the next season. The hot-water treatment con-
sists of soaking the seed, contained in half-filled burlap
bags, in 20°C water for five hours, draining it for one
minute, dipping it in 49°C water for about one minute
and then in 52°C water for exactly 11 minutes, and
immediately afterward placing it in cold water for the
seed to cool off. The seed is then allowed to dry so that
it can be sown. Because some of the seed may be killed
by the hot-water treatment, a higher seeding rate may
be employed to offset the reduced germinability of the
treated seed.
 SMU
Mycelium follows
growth of growing point of plant intercellularly
Mycelium invades
young seedlings intracellularly
Mycelium overwinters
in the embryo of infected cereal kernels
Mycelium invades
parts of embryo in seed
FIGURE 11-147 Disease cycle of loose smuts of barley and wheat caused by Ustilago nuda and U. tritici.
COVERED SMUT, OR BUNT, OF WHEAT
Covered smut, or bunt, or stinking smut of wheat occurs
in all wheat-growing areas of the world. There are actu-
ally three kinds of bunt caused by related but different
fungi: common bunt, which now is controlled easily by
treating the seed with fungicides and therefore causes
few losses in most developed countries; dwarf bunt,
which still cannot be controlled and therefore continues
to cause severe losses in many parts of the world,
includ- ing the Pacific Northwest of the United States;
and Karnal bunt, which, so far, occurs only in India and
some other Asian countries, Mexico, and a few locations
in the southwestern United States.
Bunt destroys the contents of infected kernels and
replaces them with the spores of the fungus (Figs. 11-
7
Mycelium invades the spike
and young kernels intercellularly
Mycelial cells in kernels
become teliospores
Kernels of infected
plants are filled with teliospores
Teliospore germinates
on flower. Dikaryotic mycelium infects ovary
Kernel membrane breaks.
Teliospores blown away by air currents
on flowers of
healthy plants
148A–11-148C). Bunt also causes slight to severe stunt-
ing of infected plants, depending on the species of
bunt fungus involved. Infected plants are usually
more susceptible than healthy plants to certain other
dis- eases and to winter injury. When bunt is not
controlled, it may cause devastating losses, but even
with the effec- tive control measures practiced in the
United States today, the disease continues to cause
severe losses. In addition, bunt causes market losses by
reducing the quality, and the price, of wheat
contaminated with smutted kernels or smut spores.
Such wheat is discolored, has a foul odor, and is suitable
for feed uses only. Bunt, moreover, results in explosions
in combines and elevators during threshing or handling
of smutted wheat because of the extreme combustibility
of the oily smut spores in the presence of sparks from
machinery (Fig. 11-148D).
8 11. PLANT DI SEA SES CAUSED BY FUNGI

A1

G F
FIGURE 11-148 Bunt, stinking smut, or covered smut of wheat caused by Tilletia tritici and T. laevis. (A) Field
with stunted, covered smut-infected wheat plants and close-up of a single infected plant (A1). (B) Healthy (left) and
infected (right) wheat heads showing size and direction of growth of infected kernels. (C) Healthy wheat kernels
(golden yellow) mixed with black kernels filled with smut spores (teliospores). (D) Cloud of smut spore dust produced
by a combine harvesting a heavily infected field. (E and F) Teliospores (smut spores) of Tilletia tritici and T. laevis. (G) A
covered smut teliospore germinates by producing a basidium and eight primary sporidia that fuse and produce H-
shaped structures. [Photographs courtesy of (A) R. Johnston, USDA, (B and D) L.J. Duczek, WCPD, (C) P.E. Lipps,
Ohio State University, (E and F) M. Babadoost, University of Illinois, and (G) M.F. Brown and H.G. Brotzman.]

Symptoms
Plants infected with the common bunt fungi are
usually a few to several centimeters shorter than
healthy plants and may sometimes be only half as tall.
Plants infected with the dwarf bunt fungus may be only
one- fourth as tall as healthy plants and may show an
increase in the number of tillers. Infected plants may
appear slightly bluish green to grayish green in color,
but this is not easily distinguishable.
Distinct bunt symptoms, however, are shown by the
heads of infected plants. Infected heads are slimmer and
are usually bluish green rather than the normal yellow-
ish green, and their glumes seem to spread apart and
form a greater angle with the main axis (Fig. 11-148B).
Infected kernels are shorter and thicker than healthy
ones and are grayish brown rather than the normal
golden yellow or red (Figs. 11-148B and 11-148C).
When mature kernels are broken, they are found to be
full of a sooty, black, powdery mass of fungus spores
(Figs. 11-148E and 11-148F) that give off a distinctive
odor resembling that of decaying fish. During the
harvest of infected fields, large clouds of spores may be
released in the air (Fig. 11-148D).
The Pathogens
Tilletia caries (= T. tritici) and T. laevis (= T. foetida)
cause the common bunt, whereas T. controversa causes
dwarf bunt and T. indica causes Karnal bunt (see later).
The first two species are similar in their life histories
and disease development. The biology of T. controversa
is different and somewhat similar to that of T. indica.
The pathogens produce teliospores with different sets of
wall markings.
The mycelium is hyaline. During sporulation,
most cells are transformed into spherical, brownish
teliospores, while the rest of the mycelial cells remain
hyaline and sterile. On germination of a teliospore a
basidium is produced, at the end of which 8 to 16
basidiospores develop in T. caries and T. laevis, whereas
14 to 30 basidiospores develop in the dwarf bunt fungus
T. controversa and 32 to 128 in T. indica. Basidiospores,
usually called primary sporidia, fuse in pairs through
the production of lateral branches between compatible
mating types and appear as H-shaped structures (Figs.
11-148G and 11-149). The nucleus of each primary
sporidium divides, and through exchange of one of the
nuclei the two fused primary sporidia become dikary-
otic. When the primary sporidia germinate, they
produce dikaryotic secondary sporidia. These produce
dikaryotic mycelium, which can penetrate the plants
and cause infection. After systemic development
through the plant, the mycelium again forms teliospores
in the kernels.
SMU 9
Development of Disease
The pathogens of common bunt overwinter as
teliospores on contaminated wheat kernels and less
frequently in the soil. Teliospores of the common bunt
fungi are short lived in wet areas, losing viability within
two years, whereas those of the dwarf bunt and Karnal
bunt fungi may remain viable in any soil for at least
three years and often for as long as 10 years.
When contaminated seed or healthy seed is sown
in bunt-infested fields, approximately the same condi-
tions that favor the germination of seeds favor the
germination of common bunt teliospores. Teliospores of
the common bunt fungi germinate readily, and as the
young seedling emerges from the kernel, the teliospore
on the kernel or near the seedling also germinates
through the production of the basidium, primary
sporidia, and secondary sporidia (Figs. 11-148 and 11-
149). The secondary sporidia then germinate, and the
dikaryotic mycelium they produce infects the young
seedling.
Teliospores of the dwarf bunt fungus, however,
germinate slowly even under optimum conditions of
temperature (3–8°C) and moisture, requiring from 3 to
10 weeks for maximum germination. Persistent snow
cover, providing soil surface temperatures of -2 to 2°C,
is consistently correlated with high dwarf bunt inci-
dence. Dwarf bunt infections apparently originate from
teliospores germinating at or near the soil surface from
December through early April. Germinating secondary
sporidia penetrate the tiller initials of wheat seedlings
after seedling emergence. The more tiller initials formed
during the infection period, the greater the incidence of
bunted plants and of bunted heads per plant. Germi-
nating seedlings and older tillers apparently are not sus-
ceptible to infection by the dwarf bunt fungus.
After penetration, the mycelium grows intercellularly
and invades the developing leaves and the meristematic
tissue at the growing point of the plant. The mycelium
remains dormant in the seedling during the winter;
however, when the seedling begins to grow again in the
spring, the mycelium resumes its growth and grows
with the growing point. When the plant forms the
head of the grain, the mycelium invades all parts of it
even before the head emerges. As the head fills and
becomes mature, the mycelial threads increase in
number and soon take over and consume the contents
of the kernel cells. The mycelium, however, does not
affect the tissues of the pericarp of the kernel, which
form a rather sturdy covering for the smutted mass they
contain. At the same time, most hyphal cells are trans-
formed into teliospores.
Smutted kernels are usually kept intact while on the
plant, but break and release their spores on harvest or
10 11. PLANT DI SEA SES CAUSED BY FUNGI

Binucleate Mycelium reaches and

secondary sporidium follows growing point of plant

Primary sporidia
fuse to form H-shaped structures

Mycelium penetrates
Dikaryotic mycelium seedling directly and grows between cells
from secondary sporidium attacks wheat seedling
Intercellular
Secondary mycelium
sporidium germinates

Mycelium grows
Uninucleate through spike and into wheat kernels
primary sporidia

Basidium
Mycelium becomes
Germinating teliospore intracellular in kernels
Healthy
wheat head

Zygote
Teliospores on
Mycelial cells
germinating wheat kernel Smutted kernels
break upon harvest and contaminate healthy wheat kernels are transformed into teliospores

Smutted wheat kernel full of teliospores

Smutted
wheat head
FIGURE 11-149 Disease cycle of covered smut or bunt of wheat caused by Telletia sp.

threshing. The liberated spores contaminate the healthy
kernels and are also blown away by air currents, thus
contaminating the soil.
Control
Common bunt can be controlled by using smut-free
seed of a resistant variety treated with an appropriate
fungicide. Contaminated seed should be cleaned to
remove any unbroken, infected kernels and as many of
the smut spores on the seed as possible. The seed is
then treated with appropriate fungicides. In dwarf bunt,
Karnal bunt, and in common bunt in drier areas, the
spores survive in the soil for long periods and can cause
infection of seedlings. In such cases, the most effective
control is through the use of resistant cultivars, whereas
seed treatments with certain systemic fungicides are
moderately effective.
 SMU 11

BOX 20 Karnal Bunt of Small Grains — Legitimate Concerns and Political Predicaments

Karnal bunt, named after the town
Karnal of India where it was first
observed in 1931, affects wheat and trit-
icale (a hybrid of wheat and rye) on
which it causes a covered smut (Fig. 11-
150). Karnal bunt is caused by the
fungus Tilletia indica, known previously
as Neovossia indica. Karnal bunt is also
known as partial bunt because only a
portion of the wheat kernels is affected.
The disease has now been reported from
several other countries in Asia, in the
early 1980s from Mexico, and, since
1996, from a few places in the south-
western United States. A great effort was
launched in the United States to deter-
mine the extent of the area to which the
Karnal bunt fungus had spread. These
efforts were hampered somewhat by the
fact that the teliospores of this fungus
were very similar in appearance to those
of the fungus Tilletia walkeri, the cause
of ryegrass smut. This similarity led at
first to several misdiagnoses and to
unnecessary augmentation of the area
where Karnal bunt presumably existed.
By the end of 2001, Karnal bunt was
found only in a few areas in Arizona,
California, and Texas.
Karnal bunt has a minimal effect on
yield and quality of wheat. Reported
yield losses from Karnal bunt in India
and in Mexico varied from 0.12 to
0.5%. In addition, the disease is
managed easily through the use of clean
seed treated with appropriate fungicides
and application of appropriate agricul-
tural practices. Also, the disease cannot
become established in new locations
that do not provide favorable climatic
condi- tions, which, for teliospore and
sporidia germination, include high
relative humidity or free water and
temperatures around 20°C. However,
because coun- tries presently free from
the disease do not allow importation of
Karnal bunt- infected wheat, the
inability to export wheat contaminated
with the disease has created an
emergency situation in the United
States, one of the largest exporters of
wheat. Wheat infected with the Karnal
bunt fungus is not toxic to humans or
animals.
The Karnal bunt fungus overwinters
as teliospores (Fig. 11-150D) on the soil.
In the presence of moisture, teliospores
germinate by producing a basidium

B
A

C D

FIGURE 11-150 Karnal bunt caused by Tilletia indica. (A) Head of wheat containing kernels infected with Karnal
bunt. Numerous wheat kernels infected with Karnal bunt (B) and close-up of a few infected kernels indicating the pos-
sible severity of infection (C). (D) Teliospores of Karnal bunt at various stages of maturity. (Photographs courtesy of
USDA.)
12 ROOT
11. AND
PLANT
STEM
DI SEA
ROTS
SES CAUSED
CAUSED BY
BY BA
FUNGI
SID IOM YC ET ES 593

(promycelium) that, in turn, produces as

many as 180 primary sporidia. The
primary sporidia germinate and
produce mycelia, which then produce
large numbers of secondary sporidia. At
the time of flowering, both primary and
sec- ondary sporidia are blown or
splashed upward on wheat plants and
those that reach the plant head infect
the develop- ing kernels. The fungus is
restricted to the pericarp of the kernel
and there, as the kernels mature, the
fungus produces large numbers of
teliospores and, if the kernels rupture
at harvest, the teliospores are released
on the soil. Teliospores can survive in
soil for five
years and can survive in dry wheat seed
for several years.
Karnal bunt is a disease that could, at
some point, become a serious disease of
wheat and other grains. So far, however,
the disease causes little yield loss and is
of concern only because strict interna-
tional quarantines prohibit the interna-
tional sale of Karnal bunt-contaminated
wheat. The measures and their costs
required for monitoring wheat fields in
the United States for Karnal bunt are
considerable, as are delays in processing
and shipping of wheat internationally.
This, of course, is in addition to meas-
ures taken for reducing and certifying,
for export to certain countries, wheat
as free of, or containing no more than
a low maximum number of teliospores
of the much more severe dwarf bunt
disease of wheat, caused by Tilletia con-
troversa. The cases of both diseases
point out the need for early detection,
unambiguous diagnosis, and effective
monitoring of a pathogen so that it is
kept from entering a country that, so far,
is free from it, avoiding imposing quar-
antines in areas where only look-alike
pathogens are present, and limiting the
quarantine to areas in which the real
pathogen is present.

Selected References ROOT AND STEM ROTS CAUSED

Christensen, J. J. (1963). Corn smut caused by Ustilago maydis. Am.
Phytopathol. Soc. Monogr. 2, 1–41.
Bonde, M. R., Peterson, G. L., Schaad, N. W., et al. (1997). Karnal
bunt of wheat. Plant Dis. 81, 1370–1377.
Fischer, G. W., and Holton, C. S. (1957). “Biology and Control of the
Smut Fungi.” Ronald, New York.
Gogoi, R., Singh, D. V., and Srivastava, K. D. (2001). Phenois as a
biochemical basis of resistance in wheat against Karnal bunt. Plant
Pathol. 50, 470–476.
Hoffmann, J. A. (1982). Bunt of wheat. Plant Dis. 66, 979–986.
Joshi, L. M., et al. (1983). Karnal bunt: A minor disease that is now
a threat to wheat. Bot. Rev. 49, 309–330.
Mathre, D. E., ed. (1982). “Compendium of Barley Diseases.” APS
Press, St. Paul, MN.
Mathre, D. E. (1996). Dwarf bunt: Politics, identification, and biology.
Annu. Rev. Phytopathol. 34, 67–85.
Snetselaar, K. M., and Mims, C. W. (1993). Infection of maize
stigmas by Ustilago maydis: Light and electron microscopy.
Phytopathol- ogy 83, 843–850.
Thakur, R. P., Leonard, K. J., and Pataky, J. K. (1989). Smut gall
devel- opment in adult corn plants inoculated with Ustilago maydis.
Plant Dis. 73, 921–925.
Thomas, P. L. (1991). Genetics of small-grain smuts. Annu. Rev. Phy-
topathol. 29, 137–148.
Trione, E. J. (1982). Dwarf bunt of wheat and its importance in
inter- national wheat trade. Plant Dis. 66, 1083–1088.
Trione, E. J., Stockwell, W. O., and Latham, C. J. (1989). Floret devel-
opment and teliospore production in bunt-infected wheat, in plant
and in cultured spikelets. Phytopathology 79, 999–1002.
Urech, P. A. (1972). Investigations on the corn smut caused by Usti-
lago maydis. Phytopathol. Z. 73, 1–26.
Warham, E. J. (1992). Karnal bunt of wheat. In “Plant Diseases of
International Importance” (U.S. Singh, A. N. Mukhopadhyay, J.
Kumar, and H. S. Chaube, eds.), Vol. 1, pp. 1–24. Prentice-Hall,
Englewood Cliffs, NJ.
Whitaker, T. B., Wu, J., Peterson, G. L., et al. (2001). Variability asso-
ciated with the official USDA sampling plan used to inspect
export wheat shipments for Tilletia controversa spores. Plant
Pathol. 50, 755–760.
Wiese, M. V. (1987). “Compendium of Wheat Diseases,” 2nd Ed.
APS Press, St. Paul, MN.
BY BASIDIOMYCETES
Several Basidiomycetes cause serious plant losses by
attacking primarily the roots and lower stems of plants
(Fig. 11-129). Some of these fungi, e.g., Rhizoctonia
(teleomorph: Thanatephorus) and Sclerotium (teleo-
morph: Aethalium), attack primarily herbaceous plants.
Some, like Typhula, attack only grasses and some, like
Marasmius, affect primarily turfgrasses. However, some
other fungi, e.g., Armillaria, some species of Heteroba-
sidion, particularly H. annosum, and of Phellinus and
Polyporus, attack only roots and lower stems of woody
plants, primarily forest trees, and certain fruit trees.
Other fungi cause root or crown rot of tropical plants
such as banana and sugarcane, witches’-broom of cacao
(Crinipellis spp.), or wiry cord blights on the tops of
tropical trees.
ROOT AND STEM ROT DISEASES CAUSED BY
THE “STERILE FUNGI” RHIZOCTONIA AND
SCLEROTIUM
Fungi Rhizoctonia and Sclerotium are soil inhabitant
basidiomycetes and cause serious diseases on many
hosts by affecting the roots, stems, tubers, corms, and
other plant parts that develop in or on the ground.
These two fungi were known as sterile fungi because for
many years they were thought to produce only
sclerotia and to be incapable of producing spores of any
kind, either sexual or asexual. The two were
distinguished from one another by the characteristics of
their mycelium and by the fact that Rhizoctonia
sclerotia have a uniform texture throughout, whereas
Sclerotium sclerotia are internally differentiated into
three areas. It is known