ter and contaminated farm equipment, and over long distances pri-marily in infected transplants or in the soil carried with them. Usually, once an area b e c o m es infested with Fusarium, it remains so indefi-nitely.
Whe n healthy plants grow in contaminated soil, the germ tubes of spores or the mycelium penetrate root tips directly, or enter the roots through wounds or at the point of formation of lateral roots. T h e myce-lium advances through the root cortex intercellularly, and when it reaches the xylem vessels enters them through the pits. T h e myce-lium then remains exclusively in the vessels and travels through them, mostly upward, toward the stem and crown of the plant. While in the vessels, the mycelium branches and produces microconidia which are detached and carried upward in the sap stream. T h e micro-conidia germinate at the point where their upward movement is stopped, the mycelium penetrates the upper wall of the vessel, and more microconidia are produced in the next vessel. T h e mycelium also advances laterally into the adjacent vessels penetrating them through the pits.
T h e mechanism by which wilting of Fusarium-infected tomato plants is brought about has b e e n studied extensively and several im-portant features of the wilt syndrome have b e e n elucidated.
In the lower internodes of infected plants, fungal hyphae may b e present in one or all of the vascular bundles and may cause occlusion of individual vessels varying from less than 1 0 % to over 9 0 %, e s p e-cially below the simple perforation plates in the e n d walls of the ves-sel elements. Spores produced by the pathogen in the vesves-sels may also add to the occlusion c a u s ed by the mycelium. Considering, how-ever, that a relatively small proportion of the vessels are severely oc-c l u d ed by hyphal growth and spores, it is generally aoc-coc-cepted that plugging of vessels by mycelium contributes to, but is not the only cause of, d e c r e a s ed water flow through the vessels and of wilt.
E v en before wilt symptoms appear on infected plants, v e s s el walls throughout the primary and secondary xylem show a light brown dis-coloration, and shortly after, small patches of brownish material can b e seen in the intercellular spaces around the vessels. This material s e e ms to coat the outer surface of the v e s s el walls and probably plugs the pits of the vessel. Subsequently, much darker brown substances are deposited in the parenchymatous cells adjacent to discolored ves-sels and may even fill some of the vesves-sels, but plugs of this nature are infrequent and cannot by themselves cause wilt. T h e brown discolora-tion is c a u s ed by brown to black melanoid pigments p r o d u c ed by the
Fusarium Wilt of Tomato 293
oxidation of polyphenols to quinones by the e n z y me polyphenol oxi-dase, and s u b s e q u e nt polymerization of quinones to dark-colored melanins. Polyphenols exist in the cells as such or are produced upon breakdown of phenolic glucosides to glucose and phenols by the en-zyme â-glucosidase. It is also possible that phenolic metabolites are oxidized by polyphenol oxidase before they reach their final site of incorporation (i.e., in the lignin of lignified cells), as is e v i d e n c ed by the thinner and less rigid walls of vessels p r o d u c ed after infection.
Vessels differentiated in stems and petioles just before or after infection of the plant with the fungus frequently collapse or b e c o me distorted before or after invasion by the pathogen. Their walls are slightly thinner than those of healthy vessels and their shape is irregu-lar, in severe cases the opposing walls coming in contact and constrict-ing the cell lumen. In advanced stages of the d i s e a s e, proliferation of xylem parenchyma cells appears to occur around infected b u n d l e s, and, by the unusually high pressures they may exert on the adjacent tissues, they probably contribute to the collapse of the inadequately lignified vessel walls. Both vessel collapse, which can also b e induced by growing tomato plants in solutions containing the auxin indole-3-acetic acid (IAA), and cell proliferation s e em to result from increased auxin activity in the affected tissues. Furthermore the leaf epinasty symptom produced early in the d i s e a se s e e ms to b e induced also by the c o m b i n ed effects of ethylene, excess of auxin, and fusaric acid, all three substances known to b e p r o d u c ed by the pathogen.
T h e tomato wilt Fusarium is known to produce at least three toxins:
fusaric acid, dehydrofusaric acid, and lycomarasmin, all of which are b e l i e v ed to play a role in wilt production. T h e y s e em to affect the permeability of parenchymatous cells to water and to cause respiratory disturbances in d i s e a s ed plants. T h e toxins are also known to che -late heavy metals such as iron and copper, which may thus b e c o me limiting in the function of the cofactor-requiring e n z y m es and in other metabolic functions of the plant cells. T h e role of the toxins, however, although of some importance, does not s e em to b e the primary factor in the d e v e l o p m e nt of wilt.
T h e main event in infected plants is that d i s e a s ed plants lose more water than they gain over a period of time. This does not s e em to b e d ue to inability of the roots to absorb water, but to the increasing re-sistance to the flow of water in the vascular system of the stem and pet-ioles. Part of the resistance is d u e, of course, to the presence of the fungus in the vessels and to the r e d u c ed diameter of the distorted or collapsed vessels. In addition to these, however, degradation products
of pectin and cellulose breakdown are released from surrounding tis-sues into the vessels. T h e se not only increase the viscosity, and there-fore decrease the rate of m o v e m e nt of water in the vessels, but they also form gels and, following oxidation, gums which may form plugs on the vertical or lateral perforations of the vessels and further inhibit the movement of water. T h e fungus is known to produce both pecto-lytic and cellulopecto-lytic enzymes. T h e enzymes may also play a role in weakening the walls of the vessels, which collapse under the influ-enc e of the increased tension in the water-conducting columns as a result of a growing water shortage in leaves.
Fwsanwra-infected tomato plants commonly d e v e l op tyloses. Ty-loses are protrusions of the ray parenchyma cells into the xylem through the pits and appear when the xylem vessels b e c o me inactive or are injured. T h e internal tension in the vessels of d i s e a s ed plants, however, c o m b i n ed with the weakening of the pit m e m b r a ne and to-rus by the pectolytic enzymes, s e em to facilitate formation of tyloses and may b e responsible for the more frequent appearance of tyloses in vessels of d i s e a s ed than of healthy plants. Extensive formation of ty-loses, of course, may completely block or greatly retard the movement of water through the vessels. Furthermore, the pectolytic enzymes of the fungus may rupture the wall of s o me tyloses, resulting in release of the contents of the parenchyma cell into the vessel lumen which may add to the blockage already c a u s ed by the gels and gums present in the vessel.
Presumably a combination of the above-outlined processes is re-sponsible for the breakdown of the water economy of the infected plant, and when the amount of water available to the leaves is below the required m i n i m um for their function, the stomata close, the leaves wilt and finally die, followed in death by the rest of the plant. T h e fungus then invades the parenchymatous tissues of the plant exten-sively, reaches the surface of the d e ad tissues, and there it sporulates extensively. T h e spores may b e disseminated to ne w plants or areas by wind, water, etc.
Occasionally, the fungus may reach the fruit of infected plants and penetrate or contaminate the seed. This happens primarily w h en the soil moisture is high and the temperature relatively low, conditions that allow plants to produce good yields although infected with the fungus. Usually, however, infected fruits decay and drop, and, e v en if harvested, infected s e e ds are so light that they are eliminated in the procedures of extraction and cleaning of the s e ed and therefore play little role in the spread of the fungus.
Fusarium Wilt of Tomato 295
Control
U se of tomato varieties resistant to the fungus is the only practical m e a s u re for controlling the d i s e a se in the field. Several such varieties, e.g., C a m p b e ll 146, H o m e s t e a d, Kokomo, Manalucie, C P C - 2, Pearson VF-6 , Ohio W-R7, Ohio W-R25, T i p p e c a n o e, are available today, al-though most of them are not completely resistant, b ut under condi-tions suboptimal for infection will produce good yields e v en in heav-ily infested soils. T h e fungus is so w i d e s p r e ad and so persistent in soils that neither s e e d b ed sterilization nor crop rotation is of m u ch value. Soil sterilization is too expensive for field application, but should b e always practiced for greenhouse-grown tomato plants. U se of healthy s e ed and transplants is of course mandatory, and hot-water treatment of s e ed s u s p e c t ed of b e i ng infected should p r e c e de Fusarium oxysporum F. lycopersici. Phytopathology 50: 3 2 9 - 3 3 1 .
Kendrick, J. B. 1944. Fruit invasion and s e ed carriage of tomato Fusarium wilt.
Phytopathology 34: 1005-1006.
Kuo, M. S., a nd R. P. Scheffer. 1964. E v a l u a t i on of fusaric acid as a factor in d e v e l o p-m e n t of Fusariup-m wilt. Phytopathology^: 1041-1044.
L u d w i g, R. A. 1952. S t u d i es on the p h y s i o l o gy of hydromycotic wilting in the tomato sin-gle-spore isolates of the tomato wilt Fusarium. Phytopathology 31: 103-120.
Corn Smut
Occurrence and Importance
Corn smut occurs wherever corn is grown. It is more prevalent, however, in warm and moderately dry areas, where it causes serious d a m a ge to susceptible varieties.
Corn smut damages plants and reduces yields by forming galls on any of the aboveground parts of plants, including ears, tassels, stalks, and leaves. T h e number, size, and location of smut galls on the plant affect the amount of yield loss. Galls on the ear usually destroy it com-pletely, while large galls above the ear cause much greater reduction in yield than do galls below the ear. L o s s es from corn smut are highly variable from one location to another and may range from a trace up to 1 0 % or more in localized areas. S o me individual fields of sweet corn may show losses approaching 1 0 0 % from corn smut. Generally, how-ever, over large areas and with the use of resistant varieties, losses in grain yields seldom e x c e e d 2 %.
Symptoms
Whe n young corn seedlings are infected, minute galls are formed on the leaves and stem, and the seedling may remain stunted or may b e killed by the pathogen. S e e d l i ng infection, however, is rather rare in the field.
On older plants, infections occur on the young, actively growing or embryonic tissues of axillary b u d s, individual flowers of ear and tas-sel, leaves and stalks (Fig. 46). T h e infected areas are permeated by the fungus mycelium which stimulates the host cells to divide and enlarge, thus forming overgrowths or galls. Galls are first covered with a glistening, greenish or silvery-white m e m b r a ne enclosing the en-larged host cells and the fungus mycelium. Later as the galls mature, they reach a size from 1 to 15 cm in diameter, their interior darkens, and is turned into a mass of powdery, dark olive brown spores. T h e silvery gray m e m b r a ne then ruptures and exposes the millions of the sooty teliospores, which are released into the air. Galls on leaves fre-quently remain very small (about 1-2 cm in diameter); they b e c o me hard and dry and do not rupture.
The Pathogen: Ustilago maydis
T h e pathogen causing corn smut is a basidiomycete. T h e mycelium is colorless and septate, each cell containing two separate nuclei
Corn Smut 297
F i g. 46. Corn smut s y m p t o ms on y o u ng s t em of corn plant (A), on ear of corn (B), and on m a le inflorescence (C). (Photos by courtesy of the D e p a r t m e nt of Plant Patholo-gy, Cornell University.)
(dikaryotic mycelium). In infected plant tissues the mycelial cells are transformed into dikaryotic teliospores which form inside the myce-lial wall. T h e teliospores are spherical to ellipsoidal, 7-12 μ in diam-eter, black, with prominent spinelike echinulations. Teliospores un-dergo meiosis and germinate by producing a 4-celled b a s i d i um (promycelium), from each cell of which an ovate, hyaline, uninucleate basidiospore (sporidium) develops (Fig. 47). Usually two of the basid-iospores are of one mating type and the other two of the opposite, compatible type. In culture, basidiospores may increase in numbers by budding. U p on germination basidiospores produce a fine, haploid hypha which grows well saprophytically, but is weekly parasitic and requires fusion with a haploid compatible hypha in order to cause typ-ical infection of the host.
Development of Disease
T h e fungus overwinters as teliospores in crop debris and in the soil, where it can remain viable for several years. In the spring and s u m m er teliospores germinate and produce basidiospores which are carried by air currents or are splashed by water to young, d e v e l o p i ng tissues of corn plants. T h e basidiospores germinate on the host surface and pro-d u ce a fine hypha which can enter epipro-dermal cells by pro-direct penetra-tion. After an initial d e v e l o p m e nt however, its growth stops and the hypha usually withers and sometimes dies, unless it comes in contact and fuses with a haploid hypha derived from a basidiospore of the compatible mating type. If fusion takes place, the resulting hypha en -larges in diameter and is either dikaryotic or multinucleate, the latter b e c o m i ng dikaryotic later on. T h e dikaryotic hypha grows into the plant tissues mostly intercellularly (Fig. 47). T h e cells surrounding the hypha are stimulated to hypertrophy and hyperplasia, and galls begin to form. Hyperplasia may even appear in advance of the actual invasion of the tissues by the fungus, and galls may b e g in to form even before the fungus is actually present.
Galls in d e v e l o p ed plants s e em to b e always the result of local infections of plant tissues. Systemic infections s e l d om occur and only in very young seedlings. Frequently, however, only a small number of the actual local infections d e v e l op into typical, large galls, the others remaining too small to b e visible.
T h e mycelium in the gall remains intercellular during most of gall formation, but before sporulation, the enlarged corn cells are invaded by the mycelium, collapse, and die. T h e mycelium utilizes the cell
* Galls full of teliosDores Fig. 47. Disease cycle of corn smut caused by Ustilago maydis.
Dikaryotic cells of mycelium become teliospores in gall Mycelium
in nnl l
Infected kernel enlarges and ^ forms gall
Dikaryotic mycelium infects kernel ^through silk
Compatible .basidiospores Ears of corn are infected through the silk Leaf or stem infection Corn plant with galls Teliospores j overwintering 1 on soil
Zygote
Germi- nating telio- spore
Basidium
Basidiospores
Basidiospores infect young plants or growing tissues of older plants Galls on leaf .
contents for its further growth and the gall then consists primarily of dikaryotic mycelium and cell remnants. Most of the dikaryotic cells subsequently d e v e l op into teliospores, and in the process s e em to absorb and utilize the protoplasm of the other mycelial cells which remain empty. Only the m e m b r a ne covering the gall is not affected by the fungus, but finally the m e m b r a ne breaks and the teliospores are released. S o me of the released teliospores, if they land on young, meristematic corn tissues may cause ne w infections and ne w galls during the s a me season, but most of them fall to the ground or remain in the corn debris where they can survive for several years.
Control
Corn smut may b e controlled to a degree through the use of corn hybrids with some resistance to the fungus. No corn varieties or hy-brids completely resistant to smut are known. T h e pathogen, howev-er, shows extreme variability in its pathogenicity and ne w races ap-pear constantly, making control through resistance difficult. Control through sanitation measures, such as removal of smut galls before they break open, and through crop rotation is possible only where corn is grown in small, rather isolated plots, but is impractical and impossible in large corn-growing areas.
Selected References
C h r i s t e n s e n, J. J. 1963. Corn s m ut c a u s ed by Ustilago maydis. Am. Phytopathol. Soc.
Monograph 2: 4 1 p p.
D a v i s, G. N. 1936. S o me of the factors influencing the infection a nd pathogenicity of Ustilago zeae (Backm.) U n g er on Zea mays L. Iowa Agr. Expt. Sta. Res. Bull. 199:
2 4 7 - 2 7 8 .
Dietrich, S. 1959. U n t e r s u c h u n g en zur B i o l o g ie a nd B e k a m p f u ng v on Ustilago zeae (Beckm.) Unger. Phytopathol. Z. 35 : 3 0 1 - 3 2 2 .
H a n n a, W. F. 1919. S t u d i es in the physiology a nd cytology of Ustilago zeae a nd Sow-sporium reilianum. Phytopathology 19: 4 1 5 - 4 4 3 .
J o h n s o n, I. J., a nd J. J. Christensen. 1935. Relation b e t w e en n u m b e r, s i z e, a nd location of s m ut infections to reduction in y i e ld in corn. Phytopathology 2 5 : 2 2 3 - 2 3 3 . Potter, Á. Á., a nd L. E. M e l c h e r s. 1925. Study of the life history a nd ecologic relations of
the smut of m a i z e. / . Agr. Res. 30: 161-173.
Stakman, E. C , J. J. C h r i s t e n s e n, C. J. E i d e, a nd B. Peturson. 1929. Mutation a nd hy-bridization in Ustilago zeae. Minn. Agr. Expt. Sta. Tech. Bull. 65: 108 pp., illus.
Stringfield, G. H., a nd D. H. B o w m a n. 1942. B r e e d i ng corn hybrids for s m ut resistance.
/ . Am. Soc. Agron. 34: 4 8 6 - 4 9 4 .
Loose Smut of Barley and Wheat
T i s d a l e, W. H., a nd C. O. Johnston. 1926. A study of s m ut resistance in corn s e e d l i n gs g r o wn in the g r e e n h o u s e . /. Agr. Res. 32 : 6 4 9 - 6 6 8 .
L o o se Smut of Barley and Wheat Occurrence and Importance
L o o se smut of barley and wheat is worldwide in distribution. Al-though it occurs wherever barley and wheat are grown, it is more abundant and serious in h u m id and s u b h u m id regions.
L o o se smut causes d a m a ge by destroying the kernels of the infected plants and by reducing the quality of the grain of the noninfected plants upon harvest. L o s s es from loose smut may b e up to 10 or 4 0 % in certain localities in a given year, but the overall losses in the United States are approximately 2 % per year.
Symptoms
L o o se smut generally does not produce any symptoms until the plant has headed. Smutted plants as a rule h e ad earlier than the healthy ones, and smutted heads are elevated rapidly above those of the healthy plants. In an infected plant usually all the heads and all the spikelets and kernels of each h e ad are smutted, although s o me of them may sometimes e s c a pe infection. In infected heads each spike-let is entirely transformed into a smut mass consisting of olive-green spores (Fig. 48). This is at first covered by a delicate grayish m e m -brane which soon bursts and sets the powdery spores free. T h e spores are then blown off by the w i nd and leave the rachis a naked stalk. In infected barley plants small smutted galls may also d e v e l op on the leaves b e l ow the head.
The Pathogen: Ustilago nuda
T h e pathogen is a basidiomycete. T h e mycelium is hyaline during its growth through the plant, but it changes to brown near maturity.
T h e mycelial cells are dikaryotic and are finally transformed into brown, spherical, echinulate teliospores. Teliospores germinate read-ily and produce a b a s i d i um consisting of one to four cells. T h e basid-ium produces no basidiospores, but its cells germinate and produce short, uninucleate hyphae b e l o n g i ng to two different mating types.
Compatible hyphae fuse in pairs and produce dikaryotic mycelium which is capable of infection (Fig. 49).
301
F i g. 48. S y m p t o ms of loose s m ut of barley as they a p p e ar in the field (A) a nd on a sin-gle h e ad of barley (B). (Photos by courtesy of the D e p a r t m e nt of Plant Pathology, Cornell University.)
Development of Disease
T h e pathogen overwinters as dormant mycelium in the cotyledon (sometimes called the scutellum) of infected kernels. Whe n planted, infected kernels begin to germinate, the mycelium resumes its activ-ity and grows intercellularly through the tissues of the embryo and the young seedling until it reaches the growing point of the plant (Fig.