Plant of the Week – 26th October – Ergot (Claviceps purpurea) – a fungal parasite of wild and cultivated grasses

We all know that fungi are not plants, but the Botanical Society of Scotland promotes the study of cryptogams, and so fungi as our honorary plants are very much within our remit.

Autumn is the time of year to look out for ergot, a fungal parasite of wild and cultivated grasses; its effect on humans and other animals has a long and fascinating history. The photographs below show the hard, weather-resistant purple black sclerotia on the flower spikes of Dactylis glomerata, Ammophila arenaria, Leymus arenarius and Lolium perenne.

Clearly the parasite is not fussy about which species of wild grass it chooses to inhabit. Of the cultivated grasses wheat, triticale and barley can suffer from the disease, but it is rye which is most susceptible. It is therefore those areas of Europe where rye is grown as the staple crop, which have been most affected in the long history of ergotism. The sclerotia, which are composed of tightly compacted hyphae, are filled with highly toxic alkaloids which elicit various neuropsychiatric and vascular responses. Problems arise when the sclerotia from cultivated grasses are reaped together with the grain, and subsequently milled to make flour. In the Middle Ages ergotism was commonplace throughout Europe, but not the knowledge of what caused the symptoms. It was referred to as St Anthony’s Fire – named after a third century saint who had hallucinatory bouts – supposedly from conniving with the devil. Abortions, convulsions, hallucinations, and gangrene of hands and feet associated with a burning sensation (hence the term ‘Fire’), are some of the symptoms associated with ingestion of the sclerotia. 100g of sclerotia over several days constituted a lethal dose (Chu, 2003), while 3 (about 1.5g) would induce contractions in childbirth (Lee, 2009), and probably abortions at an earlier stage too. 100g may seem like quite a lot of sclerotia (each sclerotium weighs about 0.5g), but according to Chu (2003) in some areas of France, grain contains as much as 25% sclerotia, which once milled, become invisible in a dark rye loaf. Livestock and poultry suffer from similar serious veterinary problems (Wakenell, 2016; Evans et al., 2012), and for them consumption of ergot from pasture grasses can cause serious problems. 

The first definitive identification of ergotism comes from 600 BC from an Assyrian cuneiform tablet on which it is described as a ‘noxious pustule in the ear of grain’. It was the Roman historian Lucretius (98-55 BC) who first called it ‘Ignis sacer’, Holy Fire.  In one of the holy books of the Parsecs in the 7th century the origin of ergotism was considered to be ‘noxious grasses that cause pregnant women to drop the womb and die in childbed’ (van Dongen and de Groot, 1995).  The hallucinogenic effects of convulsive ergotism have been implicated in witchery and even the emergence of mystic cults. In Massachusetts in 1692 the village of Salem (later Danvers) was the site of famous witch trials after a group of young girls, who exhibited strange symptoms of hallucinations, delirium, violent convulsions, incomprehensible speech, trance like states and odd skin sensations, were accused of witchcraft and being inhabited by the devil. Ergot has been suggested as a possible cause of this strange satanic witchcraft ‘epidemic’ (Caporael, 1976). In Central Europe ergot has also been held responsible for Sabbateanism and Chasidism (Packer, 1998).

Historical researchers have found that there were two distinct forms of ergotism in Medieval human societies, one gangrenous, and the other convulsive. The two types are determined by geography. In Europe, the river Rhine seems to form a decisive boundary, with cases West of the Rhine presenting as gangrenous and those on the East side of the Rhine as convulsive. Since rye is the host plant in all cases, the suggestion has been made that different growing conditions may affect the exact composition of the alkaloid cocktail, and hence elicit different symptoms (Hagan, 2018).

Mycologically speaking, Claviceps purpurea has an equally bewitching life cycle history. Before winter the sclerotia will fall to the ground and lie there on top of the soil or half buried in leaf litter. Here they will lie dormant for a while; indeed, a period of vernalisation is required, before they can absorb water and germinate to form several fruiting bodies. If you are lucky to catch the moment of germination, you will see that bumps develop on the sclerotium from which will grow 6-60 little drumsticks called stromata.  Each is 15-30 mm long, has a rounded head – yellow or reddish or purple. Inside each head are numerous pear-shaped cavities called perithecia, and inside the perithecia are the flask shaped asci, each with 8 needle-like ascospores (2 x 60-70 µm). The ascospores are the result of a meiotic division (yielding 4) followed by one mitosis (yielding 8).  When ripe, the ascospores are shot out, as in most Ascomycetes, and are then transported by the wind to the open flowers of other hosts. When the ascospore lands on the stigma of a flowering grass, it germinates, sending a hypha down the style towards the ovary. The fungus is homothallic, which means that a single homokaryotic spore is sufficient for completion of the sexual life cycle (Esser and Tudzynki, 1978). Within the ovary it settles down to a mycelial stage, and proceeds to multiply itself asexually, producing thousands of genetically identical conidia in a sticky honeydew. The honeydew attracts insects which spread the fungus further, initiating new rounds of infection. Later in the summer conidial production ceases. While the healthy fertilised ovaries develop into seeds, the compacted interwoven mycelium in infected ovaries hardens to become the sclerotium.

The alkaloids contained within the sclerotia are of considerable pharmacological value and so rye crops can be inoculated and the sclerotia harvested. However, nowadays submerged fermentation is the preferred method of biosynthesis (Moore, 2002). The main alkaloids, ergotamine (used to treat migraines), ergocryptine, ergopeptine and lysergil-amides can all be converted to D-lysergic acid (precursor to LSD) for both pharmaceutical and illicit drug use (Haarmann et al., 2009).

Present-day cereal growers rely on good management to prevent infestations. There are no genetically resistant varieties and there are no fungicides registered for this use (DEFRA, 2011). The only way to avoid the problem is to mow the field verges so as to remove the wild grasses, plough the fields deeply so as to bury any errant sclerotia, and to rotate the crops, since the sclerotia cannot survive more than one season. If all this fails it is possible to clean up contaminated grain by placing it in a brine solution; the ergot bodies float while the healthy grains sink (Wegulo and Carlson, 2011). Prevention and cleaning methods are particularly relevant at the moment, as the maximum limits of contamination in the UK are due to be lowered from harvest 2021 from the current limit of 0.05% w/w (0.5g/kg grain) to 0.02%w/w (Farmer’s Weekly, 2020).

References:

Caporael, L. R. (1976). Ergotism: The Satan loosed in Salem? Science, 192, 21-26.

Chu, F.S. (2003) Mycotoxins. Encyclopedia of Food Sciences and Nutrition (2nd edition).

van Dongen, P.W. and de Groot. A.N. (1995) History of ergot alkaloids from ergotism to ergometrine. Eur. J. Obstet. Gynecol. Reprod. Biol. 60, 109-116.

DEFRA (2002) Managing ergot in cereal crops. http://adlib.everysite.co.uk/adlib/defra/content.aspx?doc=100057&id=100058 (retrieved 22/10/2020)

Esser, K. and Tudzynski, P. (1978) Genetics of the ergot fungus Claviceps purpurea. I. Proof of a monoecious life-cycle and segregation patterns for mycelial morphology and alkaloid production. Theor. Appl. Genet. 53, 145–149.

Evans, T.J., Dennis, J., Blodgett, G. and Rottinghaus, E. (2012) Fescue toxicosis. Veterinary Toxicology, Chapter 87: 1166-117.

Farmers Weekly (2020) How to prepare for ergot limits in cereals for harvest 2021. https://www.fwi.co.uk/arable/crop-management/disease-management/how-to-prepare-for-ergot-limits-in-cereals-for-harvest-2021 (retrieved 22/10/2020).

Hagan, A. (2018) From poisoning to pharmacy. https://asm.org/Articles/2018/November/From-Poisoning-to-Pharmacy-A-Tale-of-Two-Ergots (retrieved 20/10/2020).

Haarmann, T., Rolke, Y., Giesbert, S. and Tudzynski, P. (2009) Ergot: from witchcraft to biotechnology. Molecular Plant Pathology, 10, 563- 577.

Lee, M.R. (2009) The history of ergot of rye (Claviceps purpurea) I: From antiquity to 1900. J.R. Coll. Physicians,39: 79-84.

Moore, D. (2002) The origin of drugs in current use: the ergot alkaloids story http://www.davidmoore.org.uk/Sec04_03.htm (retrieved 20/10/2020).

Packer, S. (1998) Jewish mystical movements and the European ergot epidemics. Israel J. Psychatr. Relat. Sci. 35, 227–239. https://pubmed.ncbi.nlm.nih.gov/9803689/

Wakenell, P. (2016) Management and medicine of backyard poultry. Current Therapy in Avian Medicine and Surgery ed. Brian Speer. Chapter 15, 550-565.

Wegulo, N.S. and Carlson, M.P. (2011) Ergot of Small Grain Cereals and Grasses and Its Health Effects on Humans and Livestock. University of Nebraska–Lincoln Extension. https://extensionpublications.unl.edu/assets/pdf/ec1880.pdf (retrieved 23/10/2010)

© Maria Chamberlain

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