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Phytoprotection

Fusarium head blight : a re-emerging disease T.C. Paulitz

Volume 80, Number 2, 1999

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Publisher(s) Société de protection des plantes du Québec (SPPQ)l

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Cite this article Paulitz, T. (1999). head blight : a re-emerging disease. Phytoprotection, 80(2), 127–133. https://doi.org/10.7202/706188ar

La société de protection des plantes du Québec, 1999 This document is protected by copyright law. Use of the services of Érudit (including reproduction) is subject to its terms and conditions, which can be viewed online. https://apropos.erudit.org/en/users/policy-on-use/

This article is disseminated and preserved by Érudit. Érudit is a non-profit inter-university consortium of the Université de Montréal, Université Laval, and the Université du Québec à Montréal. Its mission is to promote and disseminate research. https://www.erudit.org/en/ Colloque / Colloquium - Saint-Jean-sur-Richelieu (Québec), Canada 9 juin / 9 June 1999 Nouveaux problèmes de phytoprotection au Québec / New plant protection problems in Québec

Fusarium head blight: a re-emerging disease

Timothy C. Paulitz Dept. of Plant Science, McGill University, 21111 Lakeshore, Ste. Anne de Bellevue, Québec, Canada H9X 3V9 PHYTOPROTECTION 80: 127-133

Fusarium head blight (scab) of is to the spikelets, glumes, and rachis of endémie in Eastern Canada and is con- the head. Two to three weeks after sidered to be one of the most important anthesis, the first symptoms appear. disease on this crop, in terms of the Infected spikelets turn brown and sporo- potential losses and harm to consum- dochia form on the glumes. Thèse ers. The disease is caused by Fusarium orange-pink colored sporodochia con- graminearum Schwabe [teleomorph = tain masses of three to seven septate (Schwein.) Petch]. The macroconidia of F. graminearum, and same pathogen also attacks other small may cause infection on secondary tillers grains such as oats and ; and that flower later. However, the disease causes an ear rot of . The epide- is considered to be monocyclic, since miology of this disease hâve been re- the secondary inoculum is formed when viewed bySutton (1982) and Parry étal. the susceptibility of the host is low, and (1995). This pathogen survives over there is little plant to plant spread from the winter on wheat and maize débris. this inoculum. At harvest, seeds infect­ The following spring, purple-black per- ed at anthesis are small, whitish col­ ithecia are formed. Thèse are the fruit- ored, and wrinkled. Other seeds can ing bodies of the sexual stage of the also be infected, although they hâve a , Gibberella zeae. Asci and 4- normal appearance. The infected de- celled ascospores are formed and forc- bris is often left on the ground over the ibly ejected around the time of anthesis winter, especially in no-till or reduced of the wheat crop. In Québec, anthesis tillage situations. Perithecia can also of spring wheat occurs in late June to form in the fall, although it is unclear early July and this is when the wheat is what rôle they play in the epidemiology most susceptible to this pathogen. of the disease the following spring. G. Ascospores are considered to be the zeae is homothallic, meaning it can form most important primary inoculum of this the sexual stage by selfing. PCR-RAPD disease in eastern North America. Thèse markers and vegetable compatibility ascopores are deposited on the heads group studies show a large amount of of wheat, germinate, and infect into the genetic diversity among strains (Dusa- developing seed. Compounds in the benyagasani et al. 1999; Bowden and anthers such as choline and betaine are Leslie 1992). Perithecia are readily thought to stimulate the germination of formed in culture and in the field in the (Strange et al. 1978). After areas with adéquate summer rainfall, infection, the fungus continues to spread such as eastern Canada. The pathogen

Note du rédacteur : le texte ci-dessus est présenté tel que soumis/Editor's note : the above text is presented as submitted.

127 has also been divided into two ecotypes, 10 years, bemg replaced by corn and Group I and II. Group I is found in arid soybeans. In the main wheat growing areas such as Australia and Eastern areas of the mid continent, Fusarium Washington and primarily causes root, head blight was considered to be a seedling, and stalk rots. It does not minor problem, surpassed by foliar form the sexual stage in culture or in diseases such as rust and Septoria. But nature, and thus does not attack the in 1993, an épidémie swept through head. Group I has recently been reclas- thèse areas and has continued for the sified as a new species F. pseudo- last 6 years. This disease has caused graminearum, based on molecular év­ over three billion dollars US in losses idence and subtle différences in the and is considered to be the most costly septatron of the macroconidia (Aoki and plant disease épidémie of the last half O'Donnell 1999). of the 20th century. This subject has been reviewed by Bai and Shaner (1994) Why is this disease so important? and McMullen et al. (1997). The impact Because the fungus produces mycotox- of this disease, along with the low grain ins in the grain which can harm animais priées of the last 2 years, has lead to and humans. The two most important numerousforeclosuresof farms in Min­ are deoxynivalenol (DON, vomitoxin) nesota, North Dakota, Manitoba and and . A number of other Saskatchewan. There is also concern trichothecenescan also beformed. This that the disease is moving to dryer areas subject is reviewed in a book by Miller of Alberta and Saskatchewan, where it andTrenholm (1994). DON causes feed- has not been previously a problem ing refusai in animais, especially non- (Gilbert 1998). ruminant swine. Zearalenone is an estrogen-like compound that causes Why has the disease re-emerged as reproductive disorders in swine. At the a problem in thèse areas? One reason présent time, the maximum allowable is the increased summer précipitation limit of DON in grain in Canada is 1 that thèse areas hâve received since ppm for human consumption, 2 ppm 1993. Some areas hâve received dou­ for animal consumption. Levels in the ble their normal summer rainfall. Like grain are heavily monitored by eleva- most diseases, free water or moisture tors, millers, and government agencies is needed for infection. Secondly, the both in Canada and the United States. prevalence of no-till and low-till agri­ culture over the last 15-20 years has Why is this called a re-emerging dis­ increased the inoculum load of the fun­ ease? It is already endémie on wheat gus. The adoption of this technology and corn in eastern Canada, because of has been widespread, and has several the high probability of rain during the intrinsic benefits, such as réduction in susceptible period of anthesis. For soil érosion and reduced energy and example, in 1996, 85% of the winter labor costs. However, since much of wheat crop of southern Ontario was the residue is left on the surface, the destroyed by the disease, resulting in inoculum can overwinter. Many stud- losses of over $100 million (Schaafsma ies hâve shown a réduction in survival et al. 1998) During anthesis, rain show- of the pathogen if the residue is buried ers came in off of Lake Ontario and set (Khonga and Sutton 1988; Teich and the stage for the épidémie. Obviously, Hamilton 1985). However a return to there was adéquate inoculum présent, the moldboard plow is unlikely. There even though the growers practiced strip may hâve also been a loss of genetic rotation with soybeans and corn. A résistance in modem cultivars, since major épidémie on maize also occurred they were not selected against this dis­ in 1990 (Charmley et al. 1994). Howev- ease. At the présent time, cultivars are er, Québec and eastern Ontario are moderately to highly susceptible. Fi- minor producers of wheat, compared nally, there has been some spéculation to the upper Midwest of the US and that the disease has increased because prairie provinces. Most of the wheat in of the movement of corn production Québec is grown for animal feed and westward into new areas previously production has declined over the last cropped with wheat. This pathogen

128 PAULITZ : FUSARIUM HEAD BLIGHT attacks both corn and wheat, so this likely to be widely practiced because of may lead to a buildup of inoculum. the energy costs, dégradation of soil structure and érosion. In addition, if inoculum can travel a iDng distance, as MANAGEMENT suggested by Francl et al. (1999) who trapped spores at sites remote from STRATEGIES fields, then tillage may not hâve a sig­ nifiant effect. Crop rotation is another How can this devastating disease be cultural practice that could reduce dis­ managed or controlled? There are a ease. The recommendation is not to number of différent stratégies, howev- plant wheat where the previous crop er as consistent with the principles of wascorn or wheat (Martin and Johnston integrated pest management (IPM), 1982), since wheat following corn has none alone will be sufficient to provide higher levels of disease (Teich and a consistent and stable réduction of this Nelson 1984), and soybean-corn rota­ disease. tion gave less disease than corn-corn (Lipps and Deep 1991). Résistant cultîvars In the long term, this is the most eco- Chemical control nomically and environmentallyfeasible Chemical control is another option, but method of managing this disease. At until recently, most of the présent, most of the commercial culti- gave only moderate control (Mesterhàzy vars are moderately to highly suscepti­ 1995). Thèse products hâve to be ap- ble. However, since 1993, huge efforts plied to the heads to protect against hâve been put into finding résistance. infection. However, new classes of Most of the work has been to incorpo- fungicides such as tebuconazole (Foli- rate résistance from Chinese lines such cur) and propiconazole (Tilt) hâve given as Sumai 3 and Ning or from the Bra- better performance (Mesterhàzy and zilian line Frontana (Dubin et al. 1997). Barlok 1996; McMullen 1998) In 1998 Résistance can be expressed in a num­ and 1999, Folicur was given an emer- ber of ways. Type I résistance is résis­ gency registration in the US on wheat tance to initial infection, Type II is résis­ and barley with a pre-harvest interval tance to spread of the hyphae within of 30 days. Tilt has full registration in the host, and type III is résistance to the US up through early flag leaf émer­ kernel symptoms, or the genetic ability gence, but certain states hâve labels to of wheat to dégrade DON (Mesterhàzy apply through heading. In 1998 and 1995). Résistance is quantitative and 1999, approximately 1 million acres may involve 3-5 gènes. A number of were treated in North Dakota and Min­ groups are attempting to map the résis­ nesota (Marcia McMullen, personal tance gènes with the goal of using communication). In 1998 and 1999, marker assisted sélection to speed up trials were conducted in both the breeding process (Anderson et al. Ontario and Québec, with the purpose 1998). Other groups are attempting to of obtaining registration in Canada. transform wheat plants using biolistic However, the économie cost and envi- techniques to insert gènes for PR pro­ ronmental concerns may limit the use teins such as thaumatin-like proteins of this strategy. In addition, new spray into wheat plants (Skadsen et al. 1998). technologies must be developed, since existing techniques are geared toward Cultural practices coverage of leaves, not a vertically Since the pathogen survives on the crop placed head. débris, burying the débris results in faster décomposition than if the débris Biological control is left on the soil (Dill-Macky et al. 1998; Biological control of this disease is still Khonga and Sutton 1988; Teich and in its infancy. There are three straté­ Hamilton 1985). Therefore, cultural prac­ gies for biological control of this dis­ tices such as conventional tillage may ease. The first is to apply the biopro- reduce disease, compared to low till. tectant to the seed, to prevent seedling However, conventional tillage is not infection (Huang and Wong 1998). The

129 second strategy, also protectant, is to EPIDEMIOLOGY OF apply bacteria, yeasts, or fungi to the FUSARIUM HEAD BLIGHT head of wheat at the time of flowering, when it is most susceptible. For exam­ CAUSED BY THE SEXUAL ple, Sporobolomyces roseusand Paeni- STAGE GIBBERELLA ZEAE bacillus maceranssuppressed infection of wheat when applied in the green- In the past 8-9 years, my laboratory has house (Stockwell et al. 1997). A récent been investigating the epidemiology of program is selecting bacteria for their this disease in Québec. This research ability to utilize choline, a component was possible because of the develop- of pollen that stimulâtes the germina­ ment of a method to produce ascospore tion of Fusarium graminearum, with the inoculum in the field which mimicked idea that thèse bacteria will compete natural inoculum. Corn kernels are with the fungus for thèse compounds soaked in water, placed in glass jars or (Khan et al. 1998). This strategy has aluminum pans, autoclaved twice, and several obstacles, among which are inoculated with macroconidia of F. survival of the microorganisms on the graminearum. After 3 weeks, the corn head in the field, obtaining complète kernels are colonized with mycélium, coverage, and the timing of application are dried and spread on the ground in (da Luz et al. 1999). F. graminearum can field plots of wheat. After 10-14 days, infect after anthesis, although the sus- perithecia are formed and ascospores ceptibility is lower, thus one applica­ are ejected. This enabled us to look at tion of the biocontrol agent may not be questions such as : When are as­ sufficient. The third strategy is to apply cospores released during the day and biocontrol agents to the crop residue, season? What environmental conditions to décompose the débris and interfère are associated with ascospore release? with the production of perithecia in the How far can inoculum be dispersed? débris. However, little work has been What do disease foci and gradients look done in this area. Fernandez (1992) like? When is wheat most susceptible showed that inoculation of wheat straw to infection? with Trichoderma harzianum reduced the incidence of colonization of Fusar­ Ascospores are primarily released, ium graminearum, but no measure was beginning in the early evening, around made of severity of colonization or ef- 16:00-20:00 (Paulitz 1996). Release be- fecton inoculum production. This strat­ gins around the same time as the rel­ egy has been successful with interfer- ative humidity in the canopy increases ing with the overwintering and primary as the température decreases. This inoculum production of Venturia could be coincidental, or it could mean inaequalis, an Ascomycete that over- that asci must dry out during the day, winters in apple leaves (Carisse et al. and re-hydrate in the evening by taking 1999; Heye and Andrews 1983). Mi- up moisture from the air, leading to crosphaeropsis sp., the Coelomycete swelling and bursting of the asci or used in the study by Carisse et al. (1999), ascus attachment in the perithecia. is also being tested as a biocontrol agent Ascospores are released on days with- against G. zeae, both in the field and lab out rainfall, contrary to other reports (Bujold et al. 1999). It has been applied that say rainfall is required for release. in the fall and spring to the residue of In fact, on wet days, we did not see field microplots that were inoculated ascospore release. Ascospores were with macroconidia at the flowering stage typically released 2-4 days after a major and has changed the dynamics and tim­ rain event, indicating the importance of ing of perithecia formation (Bujold, moisture in the maturation of the per­ Carisse, and Paulitz, unpublished). ithecia and asci, but not their release. Another possibility is to apply nutrients This same timing has been corroborat- to hasten the décomposition of the ed in other subséquent studies. Dis­ débris. Khonga and Sutton (1991)found ease from small area sources of inocu­ that urea, acetic acid and propionic acid lum (1 m2) are asymmetrical, steeper inhibited the formation of perithecia on on the upwind than downwind side of artificially infested corn stems, the gradient (Fernando et al. 1997b).

130 PAULITZ : FUSARIUM HEAD BLIGHT

The direction of the gradient corre­ prédictive models based on threshold sponds to the nightly wind direction. degree days and hours of critical wet- Disease gradients were derived from ness. The hope is that growers may be thèse foci, using exponential models. able to predict risk by knowing when

The D50, the distance at which disease perithecial maturity will occur and when déclines 50% from the source, was 5-10 ascosores will be released, relative to m , and the D90 value (distance at which the flowering of the crop. disease déclines 90%) was between 10- 25 m. However, more récent experi- ments with gradients from larger REFERENCES sources of overwintered inoculum sug- gests that the gradients may be longer - Anderson, J.A., B.L. Waldron, B. Moreno- declining only 50% 20-40 m from the Sevilla, R.W. Stack, and R.C. Frohberg. 1998. DNA markers for Fusarium head source (Bujold, Carisse, and Paulitz, blight résistance QTL in two wheat pop­ unpublished). Experiments are current- ulations. Page 57 in Proceedings of the ly underway this year, using longer 1998 National Fusarium Head Blight Fo­ transects of rotorod samplers (50 m) rum, Michigan State Univ, East Lansing, and 10 m X 10 m sources of overwin­ Mich. October 1998. tered inoculum. Studies with potted Aoki, T., and K. O'Donnell. 1999. Morpho- wheat plants of différent âges exposed logical and molecular characterization of to inoculum in the field showed that Fusarium pseudograminearum sp. nov., anthesis-milk stage is most suscepti­ formerly recognized as the Group I pop­ ulation of Fusarium graminearum. My- ble, but seed infection can take place cologia 91 : 597-609. from late milk through soft and hard Bai,G.,andG.Shaner. 1994. Scabofwheat: dough stage (Fernando et al. 1997a). prospects for control. Plant Dis. 78 : 760- Thèse results were corroborated in 766. experiments with field plants whose Bowden, R.L,andJ.F. Leslie. 1992. Nitrate- heads were agged before émergence nonutilizing mutants of Gibberella zeae and exposed at various stages of matu- (Fusarium graminearum) and their use in rity. Current research is dealing with determining végétative compatibility. the dynamics of perithecia formation. Exp. Mycol. 16 : 308-315. We found two cycles of perithecia for­ Bujold, I., T.C. Paulitz, M. Tremblay, and O. Carisse. 1999. Optimization of in vitro mation in 1997-1998 and 1998-1999. perithecial production of Gibberella zeae Because of the abnormally warm fall on wheat and corn débris. Phytopathol- and late snowfall in thèse two years, ogy 89 : S10 (abstract). mature perithecia were formed in Sep- Carisse, O., V. Philion, D. Rolland, and J. tember and October. The mature as- Bernier. 1999. Effect of fall application cospores were still viable in December, of fungal antagonists on spring ascospore although they took on an abnormal production of the apple scab pathogen, morphology. Instead of being straight- Venturia inaequalis. Phytopathology (in press). walled, the ascospores were constrict- Charmley, L.L., A. Rosenberg, and H.L. Tren- ed at the septa, and many of them had holm. 1994. Factors responsible for éco­ fragmented. However, the fragments nomie losses due to Fusarium were still viable and capable of germi­ contamination of grains, foods and feed- nation. The rôle of perithecia and as­ stuffs. Pages 471-486 in J.D. Miller, and cospores formed in the fall is still un- H.L. Trenholm (eds.), in grain : known. Although the asci were compounds other than aflatoxin, Eagan degraded by late fall, ascospores could Press, St. Paul, MN. still be splashed dispersed the follow- da Luz, W.C., C.A. Stockwell, and G.C. ing in spring and colonize further de- Bergstrom. 1999. Présent status and theoretical aspects of biological control bris. The following May, over 70% of of Fusarium graminearum. In K. Léonard the overwintered ascospores were still and W. Bushnell (eds.), Fusarium head viable. Another crop of new perithecia blight of wheat and barley, American Phy- formed in late May - early June. At the topathological Society Press, St. Paul, same time, we hâve been recording MN. (in press). température and moisture in débris over the entire season, which may lead to

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