21st Century Guidebook to Fungi, SECOND EDITION, by David Moore, Geoffrey D. Robson and Anthony P. J. Trinci

Table of Contents

1. Chapter 13: Ecosystem mycology: saprotrophs, and mutualisms between plants and fungi
2. Chapter 14: Fungi as pathogens of plants
   1. Fungal diseases and loss of world agricultural production
   2. A few examples of headline crop diseases
   3. The Rice Blast fungus Magnaporthe grisea (Ascomycota)
   4. Armillaria (Basidiomycota)
   5. Pathogens that produce haustoria (Ascomycota and Basidiomycota)
   6. Cercospora (Ascomycota)
   7. Ophiostoma (Ceratocystis) novo-ulmi (Dutch Elm disease or DED) (Ascomycota)
   8. Black stem rust (Puccinia graminis f. sp. tritici) threatens global wheat harvest
   9. Plant disease basics: the disease triangle
   10. Necrotrophic and biotrophic pathogens of plants
   11. The effects of pathogens on their hosts
   12. How pathogens attack plants
   13. Host penetration through stomatal openings
   14. Direct penetration of the host cell wall
   15. Enzymatic penetration of the host
   16. Pre-formed and induced defence mechanisms in plants
   17. Genetic variation in pathogens and their hosts: co-evolution of disease systems
   18. Chapter 14 References and further reading
   19. Buy a PDF of Chapter 14
3. Chapter 15: Fungi as symbionts and predators of animals

14.7 Ophiostoma (Ceratocystis) novo-ulmi (Dutch Elm disease or DED) (Ascomycota)

Ophiostoma novo-ulmi destroyed most (estimated 25 million) mature elm trees in the UK and was responsible for similarly devastating diseases around the world throughout the 20th century; an epidemic which still rages on today (Anonymous, 2018). The story illustrates several features:

• disease vectors;
• geographic isolation, and the creation of ‘new’ diseases when geographical barriers are beached by accidental introductions through intercontinental trade and commerce; and
• the importance of ‘amenity’ plants.

This tree disease first came to notice in Holland in 1918 and 1919. Elms died soon after first showing symptoms and mature trees were lost in large numbers. It came to be called Dutch Elm Disease because its true cause was established in the 1920s by Dutch scientists. They found it was caused by a fungus first called Ceratocystis. Today we know the fungus as Ophiostoma and recognise three species: O. ulmi, which caused the infection in Europe in 1910 and which reached North America on imported timber in 1928, O. himal-ulmi, found naturally in the western Himalaya, and the most virulent O. novo-ulmi, which was first described in Europe and North America in the 1940s and was responsible for devastating infections of elms in both regions from the late 1960s onwards. O. novo-ulmi could be a hybrid between O. ulmi and O. himal-ulmi. O. ulmi seems to have been brought to Europe accidentally from the Dutch East Indies in Southeast Asia during the late nineteenth century.

Symptoms of Dutch elm disease are symptoms of lack of water and nutrients; described as wilting. Leaves first droop and then turn yellow. In a few days to weeks, the leaves are brown and dead, then larger branches begin to die, and most trees are completely dead within two years. The reason for this progression is that the plant reacts to the fungus by plugging its own xylem tissue with gum and tyloses (bubble-like plugs in the xylem cavity formed when adjacent parenchyma cells grow into the conducting cells of the xylem) in a vain attempt to stop the spread of the fungus. As more and more channels are plugged the diseased tree is starved of nutrients and water. The rate of progression of Dutch elm disease in the infected tree can be continuously and quantitatively estimated from sap flow measurements using non-invasive monitoring (Urban & Milon, 2014).

But there is more than a fungus involved. Left to itself, the fungus has difficulty passing from tree to tree. In this case, what turns a disease into a raging epidemic is a relationship between the fungus and several species of elm bark beetles. Adult females of these insects lay eggs in recently dead elms. Their eggs hatch and young larvae tunnel into the inner bark and outer wood to feed on it. If the tree has been killed by Dutch elm disease, the fungus sporulates in the beetle tunnels so the adult beetles that emerge are covered with fungus spores. These are transported to the first tender, young, healthy elm twigs that the young beetles bite into. Elm bark beetles, therefore (Scolytus multistriatus in Europe) are vectors of Dutch elm disease. Indeed, the fungal pathogen makes the host trees attract insect vectors, thereby manipulating its host tree to enhance their appeal to foraging beetles (McLeod et al., 2005; Raffa et al., 2015).

In North America, O. novo-ulmi relies on both the (accidentally introduced) European elm bark beetle, S. multistriatus, and the native elm bark beetle, Hylurgopinus rufipes, for transport to new host elms (H. rufipes can withstand colder winter temperatures and is the primary vector of Dutch elm disease across the North American prairies). Chinese and Siberian elms are highly resistant to the disease, but those native to Europe and North America are not. So the next step in the story is that Dutch elm disease was first found in North America in 1930 in Cincinnati, Ohio.

The evidence indicates that it was introduced on elm logs from Europe landed at ports on the US eastern seaboard. The American elm had become an important amenity tree throughout the continent, being planted in urban sites to such an extent that it’s no exaggeration to describe the plantings as urban forests. But by 1950 the disease was spreading through seventeen states (and into south-eastern Canada). Today, Dutch Elm disease occurs wherever American elms grow in North America. Countless millions of trees have been killed, with a corresponding multi-billion dollar cost of removing and disposing of them and replacing the trees that were lost with new plantings. But the story has yet another twist.

In May 1963 a shipment of American elm logs was landed in the United Kingdom. The logs were infested with both elm bark beetles and Ophiostoma, and in the course of the next few years twenty-five million elm trees died in Britain. In the 1970s, distributions of populations of two subspecies of Ophiostoma novo-ulmi, subsp. americana and subsp. novo-ulmi began to overlap in Europe, resulting in hybrid swarms. A hybrid swarm is a population of hybrids that survives beyond the initial hybrid generation; with interbreeding between hybrid individuals and backcrossing with parental types, this may enable new locally-adapted subspecies to emerge (Brasier et al., 2021).

There are hopes for biological control (biocontrol) of Dutch elm disease (Scheffer et al., 2008) and other fungal pathogens (Massart & Jijakli, 2007). The Ophiostoma novo-ulmi genome is providing insights into the phytopathogenicity of the fungus, although the study identified 1,731 proteins potentially involved in pathogen-host interactions, so it might be a long haul (Bernier et al., 2014; Comeau et al., 2015).

Joan Webber, Principal Pathologist at the UK’s Forest Research, has pointed out that in Britain:

 ‘…we probably have more elm trees now than we did before the current epidemic started in the late 1960s.  However, they tend to be relatively young elms whilst magnificent mature elms that graced much of the countryside are more of a rarity…’ (Webber, 2016).

As there is no cure yet, the key to control of Dutch elm disease is sanitation. Dead, dying, or weak elm wood must be destroyed to eradicate both fungus and beetle. It goes beyond the aerial parts of the tree, though. The roots of adjacent elms tend to fuse together over time, resulting in a shared root system between several trees. This type of root grafting can occur between elms within 15 m of one another. When a single elm tree in such a group becomes infected, the fungus can move down the diseased tree into the roots and then into the next healthy tree through root grafts. The sanitation processes must include disruption of these root grafts by digging a trench at least 60 cm deep along a line around the tree and beyond the longest branches of the diseased tree.

To control the Dutch elm disease syndrome there are several potential targets, because the biological control might depend on:

•  Developing resistant varieties of elm or techniques to induce resistance to disease-causing fungi in susceptible elm. Princeton Elms, bred for resistance to Dutch Elm Disease in the US are only mildly resistant, but the ‘resista-elm’ (sold as Ulmus ‘New Horizon’: http://www.resista-ulmen.com/en/) has a 100% resistance record up to the time of writing.
• Organisms (bacteria or fungi) to compete with Ophiostoma;
• Hyperparasites (that is, parasites of the parasites) of either Ophiostoma or the elm bark beetle;
• Processes that prevent successful breeding of the beetles.

If you want to know more about Dutch Elm Disease you could start by viewing the web pages listed in Resources Box 14.2.

Resources Box 14.2 Where to find more information about Dutch Elm Disease The following websites will introduce you to the past, present and future challenges presented by Dutch Elm Disease. Royal Horticultural Society https://www.rhs.org.uk/advice/profile?PID=154 Forestry Commission https://www.forestry.gov.uk/dutchelmdisease The American Phytopathological Society United States Department of Agriculture, National Invasive Species Information Center

 

Updated September, 2021