0274-B1
Danny Rioux[1]
Dutch elm disease (DED), caused by Ophiostoma ulmi, is probably the best known tree disease in the world. DED is very destructive and can affect most elm species. When DED was introduced into Canada around 1944, the very susceptible white elm (Ulmus americana) was abundant and beetle vectors were already present. Together with the strong likelihood that infected elm wood could be easily transported, for instance as firewood, all the conditions were in place for disaster. Efforts were rapidly made to eradicate DED but to no avail. By 1981, DED covered almost 100% of the natural range of U. americana in Canada. The disease’s economic impact has been enormous in many municipalities where the elm was often the main shade tree lining the streets. Vigorous integrated control systems implemented in many municipalities have however enabled them to save most of their elms. Considerable research has been done to better understand and control this serious disease. Chemical pesticides were developed as well as novel biological control agents. For example, by injecting into trees a glycopeptide isolated from non-aggressive O. ulmi isolates, some protection comparable to a vaccine reaction was obtained. Numerous studies were also conducted to assess the significance of a toxin, cerato-ulmin, produced by O. ulmi. Using molecular biology techniques, a pathogenicity gene was identified for the first time in 1999. Numerous Canadian researchers have also played a leading role in studying the defense mechanisms in response to DED infection. In this respect, phytoalexin accumulation and compartmentalization processes were considered significant when some level of resistance was observed.
Elm trees are highly regarded as ornamentals. They have pleasant forms, are fast-growing, are easily transplanted and most of them are well adapted to the numerous stressful conditions found in cities. Of the three native elm species in Canada, the most beautiful and most widely distributed one is U. americana. Unfortunately, this species is the most susceptible to DED and this has not only had major repercussions on cities but also on the hardwood industry (Huntley 1982). The first wave of DED, which ended in the 1940s, was caused by O. ulmi, while the prevalent aggressive O. novo-ulmi is responsible for the current epidemic (Brasier 1991). In this paper, the pathogenic agent will be denoted as O. ulmi. The fungus is transmitted from tree to tree by beetle vectors and occasionally through root grafts. Infected wood, such as firewood, carried by humans has also been key in the dissemination of DED. This is an overview of what has happened in Canada since the disease was first observed in 1944. Unfortunately, it is impossible to report here on all of the pertinent literature on this subject.
DED was first observed in Canada at Saint-Ours (near Sorel in the Province of Quebec) in 1944 (Pomerleau 1945). The pathogen was probably introduced through crates made of infected elm wood coming by ship from Europe (Pomerleau 1964). Efforts were made to detect and destroy all infected trees from 1945 to 1949 but in 1950 the program was abandoned because DED was deemed to be too well established in this province (Pomerleau 1953). Nevertheless, the presence of DED was still monitored between 1950 and 1959, when it was estimated that DED had progressed at an average rate of 3100 km2/year (Pomerleau 1961). The epidemic by then covered more than half the range of U. americana in Quebec and around 650 000 elms were killed (Pomerleau 1961).
In Ontario, the disease was first found at Saint-Isidore in 1946; likely it had spread from the outbreak occurring in Quebec (Pomerleau 1964). In 1950, DED reached the Niagara Peninsula apparently as an extension from New York State (Pomerleau 1964). By 1952, a third infected area was noted in the Windsor region, likely as an introduction from Ohio or Michigan (Campana and Stipes 1981). DED at that time occurred in 46 counties and already covered 165 760 km2 in Ontario (Dance and Lynn 1952; Pomerleau 1964).
DED was first observed in New Brunswick at Woodstock in 1957 (Anonymous 1957). In Nova Scotia, it was first found in two trees in Liverpool in 1969 (Forbes et al. 1969) and the disease was first confirmed in 1979 in Prince Edward Island (Magasi 1982).
In western Canada, DED was first identified in Manitoba in 1975 (Ives and Petty 1976) and in Saskatchewan in 1981 (Sterner and Davidson 1982). In Alberta, so far, only one diseased tree has been found in 1998 (Feddes-Calpas 2000).
The numerous headlines found for instance in the printed media (Jorgensen 1982) show that DED has always been an emotional subject in Canada. This is understandable as the elm constitutes as much as 50-80% of the shade trees in many cities (Sterner and Davidson 1982). Municipal programs to suppress Dutch elm disease have had highly variable results. In Fredericton, the “City of the Stately Elms”, where the disease appeared in 1961, 30% of the elms were lost to the disease over 30 years but thanks to a vigorous planting program, about 3000 elms are still present within the city center (Magasi et al. 1993; Don Murray, personal communication). Winnipeg, with the active involvement of its citizens, has so far been a success story in keeping its elm population at over 200 000 individuals (Allen 2002). In 1992, the “Coalition to Save the Elms” was created from 27 different community groups and this organization now has a membership of over 2000 (Allen 2002). The disease that was first noticed in this city in 1975 (Ives and Petty 1976) continues to be a serious problem but 90% of the losses occur along river banks rather than on residential streets (Allen 2002). DED was recorded in Regina in 1981 and this city has done remarkably well in protecting its 100 000 U. americana trees, as only 28 trees have been killed by the disease so far (Gustafson 2002). In Quebec City, the situation is also encouraging as the disease incidence is around 2%, which is considered an acceptable level (Pierre Côté, personal communication). The elm population is about 3500 in the central part of this municipality.
In Montreal and Toronto, the situation has been rather catastrophic and this is probably partly because of the presence of high populations of the European beetle (Scolytus multistriatus). Montreal had a population of 50 000 elms in the early 1970s but between 1970-1980, 90% of these trees were “harvested” by DED (Pierre Jutras, personal communication). Only around 1400 elms can now be found along the streets in Montreal. By 1976 in Toronto, the original population of 35 000 elms had been reduced by 80% (Huntley 1982) and a recrudescence of DED has recently been noted in the new amalgamated city (Jozef Ric, personal communication).
Control methods
As reported worldwide, it was clear that the best method to control DED was to develop integrated programs aimed mainly at detecting infected trees, removing and destroying trees or infected branches, reducing beetle populations and preventing or treating trees by the injection of fungicides. Such programs are partially or entirely described in numerous documents published in Canada (i.e. Smith and Forbes 1968; Magasi et al. 1993). It was shown in the United States that these programs were at least 35% less expensive compared to areas without programs where dead trees had to be removed and replaced all the same, which are two costly operations (Cannon and Worley 1980).
As for fungicides, efforts were made to increase the solubility of MBC (methyl-2-benzimidazole carbamate), the active ingredient of benomyl, by obtaining various salts of this compound (Kondo et al. 1973). Thus, MBC-phosphate, at a concentration that limited the development of O. ulmi, was also well distributed throughout the tree. In addition, all MBC-salts produced were less phytotoxic than MBC alone. The distribution of MBC-phosphate was later shown to be more erratic in a study where a new bio-assay was also developed to assess the phytotoxicity of this fungicide as well as that of various insecticides (Roy et al. 1980).
A biological control measure was envisaged after the isolation of a Deuteromycotina fungus from elm wood that showed antagonistic properties against O. ulmi. This fungus was identified as being Phaeotheca dimorphospora (DesRochers and Ouellette 1994) and it was also assessed against O. ulmi and many other tree pathogens (Yang et al. 1993).
One promising control measure recently developed is in the field of induced resistance. It was shown that inoculation of nonaggressive isolates of O. ulmi in U. americana seedlings could stimulate resistance to subsequent inoculation with aggressive isolates (Hubbes and Jeng 1981). Injection of a glycoprotein isolated from nonaggressive isolates by these workers similarly significantly protected elms by seemingly eliciting and intensifying their natural defense mechanisms.
The pathogen
Many metabolites produced by O. ulmi were studied but special attention was paid to two phytotoxins: a peptidorhamnomannan and a protein called cerato-ulmin. Most of the work on cerato-ulmin was conducted in Canada. It was isolated from liquid cultures of the pathogen in the form of hydrophobic microstructures (Richards and Takai 1973) shown to be specific to O. ulmi (Takai 1974). The toxin was detected in infected U. americana (Richards and Takai 1988) where it was reported to cause a reduction of transpiration and a concomitant increase in respiration (Richards and Takai 1984). Although a correlation was found between pathogen virulence and toxin production (Takai 1980), these results were not confirmed in a study where chemically induced mutants of O. ulmi were produced (Bernier 1988). The fact that an Italian team has recently been able to genetically modify O. quercus, a non-pathogenic fungus on elm, to produce cerato-ulmin and to induce DED symptoms when inoculated in elms (Del Sorbo et al. 2000) may well renew interest in this toxin.
Biotechnological techniques have also made it possible to differentiate strains and populations of O. ulmi (Bernier et al. 1983; Hintz et al. 1993). Interestingly, a pathogenicity gene has been identified for the first time when the difference in aggressiveness between O. ulmi strains was shown to be controlled by a single nuclear gene (Et-Touil et al. 1999).
Defense mechanisms
As reported for many tree diseases, two of the most important tree defense mechanisms against DED now stand out as phytoalexin accumulation and the compartmentalization of invaded tissues.
Phytoalexins
Phytoalexins are substances that are produced in response to infection and inhibit the development of plant pathogens. The accumulation of such substances, mainly known as mansonones in elm, was reported in Europe for the first time by Overeem and Elgersma (1970). It was demonstrated that the accumulation of mansonones was correlated with resistance to DED when U. americana and the resistant U. pumila were inoculated with aggressive and nonaggressive isolates of O. ulmi (Duchesne et al. 1985, 1986). Phytoalexins were particularly abundant in U. americana after inoculation with nonaggressive isolates (Hubbes and Jeng 1981; Jeng et al. 1983).
Rapid phytoalexin accumulation may be important in delaying invasion until other mechanisms of resistance, such as compartmentalization, take over. Compartmentalization might also be a way to concentrate these substances exactly where they may be in contact with the pathogenic agent.
Compartmentalization
Compartmentalization processes involve the formation of anatomical barriers that limit the extent of injured xylem tissues (Shigo 1984). The most effective defensive zone of compartmentalization is called the barrier zone which is formed by the cambium in response to damage.
While studying in light microscopy different nonhost trees artificially inoculated with O. ulmi, one of their most prominent responses was the formation of barrier zones that limited the radial spread of infection (Rioux and Ouellette 1989). Barrier zone formation was particularly spectacular in some nonhosts whereas in U. americana, barrier zones were usually absent in infected branches or when present, they appeared in later infection stages and even then, they were often discontinuous. Histochemical tests indicated that lignin and suberin were important components of barrier zones and that the intensity of their detection was correlated to the apparent resistance of the species studied (Rioux and Ouellette 1991). In transmission electron microscopy (TEM), noticeable details of xylem elements were observed in U. americana having survived DED (Ouellette 1981a, 1981b). New structures found in vessel elements and totally different from the already known tyloses were thoroughly described in TEM, as these components were apparently significant for DED development (Ouellette 1980).
The presence of DED in Canada has over the years triggered many valuable citizen initiatives as well as pertinent research projects. It is estimated that around 700 000 elm trees are still present in Canadian cities, which represents a value exceeding 2.5 billion dollars (Hubbes 1999). Keeping in mind that tree diversity should be encouraged in our cities, let us hope that we will be up to the task of maintaining the elm as a key element in our urban landscapes.
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| [1] Natural Resources Canada,
Canadian Forest Service, Laurentian Forestry Centre, 1055 du P.E.P.S., P.O.
Box 3800, Sainte-Foy, Québec, Canada G1V 4C7. Tel: 418-648-3127;
Email: [email protected] |