Fusarium: Historical and Continued Importance

Abstract

Historically, Fusarium has been important because: (i) taxonomy of Fusarium species has been a controversial issue, (ii) Fusarium species are among the most important plant pathogens in the world, and (iii) many Fusarium species produce mycotoxins that cause animal and human diseases. The genus Fusarium was introduced by Link in 1809. “Die Fusarien” was published by Wollenweber and Reinking in 1935, described 65 species, 55 varieties, and 22 forms of Fusarium. In 1945, Snyder and Hansen reduced number of species of Fusarium to nine. In 1990s, the application of phylogenic species concept based on the DNA sequencing resulted in introducing new species of Fusarium that cannot be distinguished morphologically. In 2006, Leslie and Summerell integrated the morphological, biological, and phylogenic species concepts and published “The Fusarium Laboratory Manual,” which provides details of identification of 70 Fusarium species. Although considerable research studies on Fusarium have been accomplished in the past 200 years, yet Fusarium diseases continue to be among the most important plant diseases. Fusarium fungi are the most widespread in cereal-growing areas of the world and produce a diversity of mycotoxins, including zearalenone, fumonisin, moniliformin, and trichothecenes, which cause various disorders, including cancer, in animals and humans.

1. Introduction

The genus Fusarium was introduced by Link in 1809 [1]. However, Fusarium received more attention when “Die Fusarien” was published by Wollenweber and Reinking in 1935 [2]. In the past 80 years, tremendous investigations have been carried out on the taxonomy, biology, and mycotoxins of Fusarium species [3, 4, 5]. Although Wollenweber and Reinking described 65 species, 55 varieties, and 22 forms of Fusarium in 1935 [2], Snyder and Hansen reduced number of species of Fusarium to nine [6]. During 1940–1980, several mycologists developed different taxonomy of Fusarium, but none of them received a global agreement. During 1980s, Fusarium taxonomists in the world collaborated to offer a unique agreement on Fusarium taxonomy. In 1990s, however, the application of phylogenic species concept based on the DNA sequencing resulted in introducing new species of Fusarium that often cannot be distinguished morphologically. In 2006, Leslie and Summerell published “The Fusarium Laboratory Manual” and described 70 Fusarium species [3].

Fusarium species are among the most common and widespread plant pathogens in the world and are of great economic importance [4]. Every plant pathologist, mycologist, agronomist, and horticulturist encounters them in the course of work. They are serious pathogens on a wide range of crops. In spite of worldwide investigations on Fusarium in the past 200 years, Fusarium diseases continue to be among most important plant diseases and cause widespread crop losses throughout the world [4, 7].

Several Fusarium species produce mycotoxins, which cause various disorders, including cancer in animals and humans [5]. Zearalenone, fumonisin, moniliformin, and trichothecenes are among most important Fusarium mycotoxins, especially in grains [5]. The objective of this chapter is to provide details of Fusarium taxonomy, pathology, and mycotoxins.

2. Taxonomy

The genus Fusarium was introduced in 1809 [1]. During 1809–1935, much of the works on Fusarium were focused on identification of Fusarium species and diagnosis of Fusarium diseases. In the past 100 years, the taxonomy of Fusarium has undergone a number of changes, which is adapted and “The Fusarium Laboratory Manual” [3].

2.1. Wollenweber and Reinking

The basis for all modern taxonomic systems of Fusarium species is the work of Wollenweber and Reinking, which was published in “Die Fusarien” in Germany. In this publication, 16 sections, 65 species, 55 varieties, and 22 forms of Fusarium were introduced, which were separated based on the morphological differences [2]. Prior to this publication, about a thousand Fusarium species had been described, often a different species for every host. Wollenweber and Reinking offered an order to a chaotic situation of Fusarium taxonomy. In their taxonomic system, each section contained species that were united by critical morphological characteristics (e.g., macroconidia morphology and pigment). Each section contained only a few species. Other taxonomists used the sections created by Wollenweber and Reinking to develop their taxonomic systems.

2.2. Snyder and Hansen

During 1940s and 1950s, Snyder and Hansen in the United Sates (US) developed a new taxonomy system and reduced number of species of Fusarium to nine [6, 8, 9]. Their identification was based on using cultures derived from single spores. The Snyder and Hansen species taxonomy was easy to use and identify any Fusarium isolate to species level.

2.3. Gordon

Gordon published a number of papers on Fusarium species collected from Canada [10, 11, 12]. He used Fusarium taxonomy system developed by Wollenweber and Reinking with some concepts of Snyder and Hansen system.

2.4. Messiaen and Cassini

These French scientists developed a Fusarium taxonomy system based on Snyder and Hansen system [13]. They used varieties for the subspecific level instead of cultivars, which was used by Snyder and Hanson.

2.5. Matuo

Matuo was a Japanese scientist who used the system developed by Snyder and Hanson and introduced a new Fusarium taxonomy system with 10 species [14].

2.6. Raillo

Raillo, a Russian scientist, published a taxonomic system based on the shape of macroconidia, and the presence of microconidia and chlamydospores [15].

2.7. Bilai

Bilai, a Ukrainian scientist, studied variability in characteristics related to temperature, moisture, and culture media composition and offered her own revision of the taxonomy of the genus Fusarium and recommended combining some sections suggested by Wollenweber and Reinking [16, 17].

2.8. Booth

A significant development in the taxonomy of Fusarium was made by Booth from England during 1960s and 1970s. He published a monograph “The Genus Fusarium” [18], which was a revision of the Wollenweber and Reinking’s system. Booth introduced the use of the morphology of the conidiogenous cells, especially those producing the macroconidia.

2.9. Gerlach and Nirenberg

Based on the taxonomy published in “Die Fusarien,” Gerlach and Nirenberg published their own Fusarium taxonomy system in Germany in 1982 [19]. In spite of the criticism of their taxonomic system, their work was a significant step forward in understanding of Fusarium taxonomy and many of the suggested species in their system are now accepted.

2.10. Joffe

Joffe, originally a Russian scientist and then in Israel, began his studies on Fusarium in Russia in 1940s. He included Fusarium isolates collected from Russia, Israel, and some other countries in his studies and evaluated their taxonomic and mycotoxicological issues. His work was published as a monograph “Fusarium Species: Their Biology and Toxicology” [20]. His taxonomic approach was based on the taxonomic systems of Wollenweber and Reinking [2] and Gerlach and Nirenberg [19].

2.11. Nelson, Toussoun and Marasas

Toussoun and Nelson from the United States published a pictorial guide for identification of Fusarium species, in which 9 species and 10 cultivars were described [21]. In 1983, Nelson and Toussoun together with W. F. O. Marasas from South Africa published an illustrated manual of Fusarium species and described 46 species [22]. Their taxonomic approach began a definitive shift toward a more complicated taxonomy and a larger set of recognized species and away from the nine species of Snyder and Hansen system. This manual has been widely used by scientists.

2.12. 1980s and 1990s

During 1980s, Fusarium taxonomists, including Burgess and Summerell from Australia, Gerlach and Nirenberg from Germany, Marasas from South Africa, and Nelson and Toussoun from the US collaborated to offer a unique agreement on Fusarium taxonomy based on fungal morphological characteristics. In 1990s, however, the application of phylogenic species concept to DNA sequencing resulted in introducing new species of Fusarium that often cannot be distinguished morphologically. Thus, the relatively unique uniformity of 1980s shifted toward another chaos on Fusarium taxonomy.

2.13. Leslie and Summerell

In 2006, Leslie from the United States and Summerell from Australia integrated the morphological, biological, and phylogenic species concepts and published “The Fusarium Laboratory Manual” with 70 species [3]. This manual, which is based on the outcomes of workshops conducted at the Kansas State University, is widely used by mycologists and plant pathologists to identify Fusarium isolates.

Although taxonomy of Fusarium species has been historically a complex issue, and no unanimous agreement available among the Fusarium taxonomists, using morphological characteristics combined by the molecular data minimizes differences in identification of Fusarium isolates. As more information is generated, more accurate taxonomic systems are expected to be developed for the identification of species of Fusarium.

3. Pathology

The members of genus Fusarium can incite diseases in plants, animals, and humans [23]. The mortality rate for human patients with systemic Fusarium infection is reported to be greater than 70% [24]. In addition, Fusarium species produce secondary metabolites that are associated with plant diseases, as well as with diseases of animals and humans [25, 26]. In this chapter, only Fusarium diseases in plants will be discussed.

Fusarium has been known for over 200 years. Despite universal effort on developing effective management of Fusarium in plants, Fusarium diseases continue to be among the most important plant diseases. Fusarium species are among the most widespread fungi in the world and are of great economic importance. Many plant species are affected with at least one Fusarium disease [3, 4]. The American Phytopathological Society reported that 81 of 101 economically important plants have at least one Fusarium disease (www.apsnet.or/online/common/search.asp). To understand importance of Fusarium diseases in plants, Table 1 was prepared that shows Fusarium species, their host plants, and geographical distributions.

Fusarium species	Host plants	Geographic distribution
F. acuminatum	Legumes	Temperate regions
F. andiyazi	Sorghum	Africa, Australia, US
F. anthophilum	Many plant species	Temperate regions
F. avenaceum	Carnations, cereals, legumes	Temperate regions
F. aywerte	Grasses	Australia
F. babinda	Soil	Australia
F. begoniae	Begonia species	Germany
F. brevicatenulatum	Millet, Striga asiatica	Africa
F. bulbicola	Bulb plant species	Europe
F. camptoceras	Banana, cacao	Tropical and subtropical regions
F. circinatum	Conifers	Chile, Japan, Mexico, South Africa, US
F. concentricum	Musa species	Central America
F. crookwellense	Potato, cereals	Temperate regions
F. culmorum	Cereals	Temperate regions
F. decemcellulare	Trees	Tropical regions
F. denticulatum	Sweet potato	Brazil, Cuba, Indonesia, US, Zambia
F. foetens	Begonia species	Germany, Netherlands
F. fujikuroi	Rice	Rice-growing areas
F. globosum	Corn, wheat	Africa, Japan
F. graminearum	Barley, corn, wheat	Worldwide
F. guttiforme	Pineapple	Cuba, South America
F. heterosporum	Millet, other grasses	Africa
F. hostae	Hosta species	South Africa, US
F. konzum	Grasses	US
F. lactis	Fig	US
F. lateritium	Woody plants	Worldwide
F. mangiferae	Mango	Africa, Asia, US
F. musarum	Banana	Panama
F. napiforme	Millet, sorghum	Africa, Argentina, Australia
F. nelsonii	Alfalfa, sorghum	South Africa
F. nisikadoi	Bamboo, wheat	Japan
F. nygamai	Sorghum	Arid regions
F. oxysporum	Many plant species	Worldwide
F. phyllophilum	Dracaena and Sansevieria species	Europe, Japan
F. poae	Cereal	Worldwide
F. polyphialidicum	Sorghum grain	Australia, Italy, South Africa
F. proliferatum	Asparagus, corn, mango, sorghum	Worldwide
F. pseudoanthophilum	Corn	Southern Africa
F. pseudograminearum	Barley, triticale, wheat	Drier areas worldwide
F. pseudonygamai	Pearl millet	Africa, US
F. ramigenum	Ficus carica	US
F. redolens	Many hosts	Temperate regions
F. sacchari	Corn, sugarcane	Mexico, Philippines
F. semitectum	Banana	Subtropical regions
F. solani	Many plant species	Worldwide
F. sterilihyphosum	Mango	South Africa
F. subglutinans	Corn	Cooler corn-growing areas
F. succisae	Succisa pratensis	Europe
F. thapsinum	Sorghum	All sorghum-growing areas
F. torulosum	Several plant species	Temperate regions
F. udum	Pigeon pea	Southern Asia, sub-Saharan of Africa
F. venenatum	Several plant species	Europe
F. verticillioides	Corn	Worldwide

Table 1.

Plant pathogen Fusarium species, their host, and geographic distribution.

Source: The Fusarium Laboratory Manual [3].

4. Fusarium toxins

Mycotoxins are toxic secondary metabolites produced by fungi and are capable of causing diseases in both animals and humans. Mycotoxins may produce birth defects, abortion, tremors, and cancers [27, 28, 29, 30]. Among the major mycotoxin-producing fungi are Aspergillus, Claviceps, Fusarium, and Penicillium species [27, 28]. Fusarium fungi are the most widespread in cereal-growing areas of the world and produce a diversity of mycotoxin types. The most prevalent Fusarium toxins are zearalenone, fumonisin, moniliformin, and trichothecenes (T-2/HT-2 toxin, deoxynivalenol, diacetoxyscirpenol, nivalenol) [5, 28, 30, 31].

Zearalenone is a group of estrogenic metabolites produced by several species of Fusarium, the most known of which is F. graminearum [5, 28]. Zearalenone is the generic name for a complex macrocyclic molecule and is derived from the perfect stage of the fungus F. graminearum (Gibberella zeae) [28]. Fusarium infection and zearalenone production are most notable on barley, corn, oat, sorghum, and wheat. Fusarium causes crown rot of corn, and scab of barley, oat, and wheat. Zearalenone is produced in infected plants in the field and in stored food and feed stuffs including cereal grains [5, 28].

Zearalenone is frequently implicated in reproductive disorders of farm animals and occasionally in hyperoestrogenic syndromes in humans [28, 32]. It has been reported that zearalenone possess estrogenic activity in cattle, pigs, and sheep. The biotransformation for zearalenone in animals involves the formation of two metabolites α-zearalenol and β-zearalenol, which are subsequently conjugated with glucuronic acid [32]. Moreover, zearalenone has also been shown to be hepatotoxic, hematotoxic, immunotoxic, and genotoxic.

Fumonisins are hydroxylated long-chain alkylamines esterified with propanetricarboxylic acid moieties produced by Fusarium moniliforme worldwide [33, 34]. The fumonisins have been reported carcinogenic in laboratory rats. It has also been reported that consumption of corn contaminated with Fusarium moniliforme is associated with higher than average incidence of esophageal cancer, and fumonisins may be responsible. Fumonisins are structurally similar to sphingosine and may exert their biological activity through their ability to block key enzymes (sphinganine- and sphingosine-N-acyltransferases) involved in sphingolipid biosynthesis.

Moniliformin is produced by several Fusarium species on cereals worldwide [31, 35]. Moniliformin is a small and ionic molecule that forms only a single sensitive fragment ion in the collision cell of a tandem mass spectrometer. There is great variability in the moniliformin synthesized by Fusarium spp. [35]. It has been reported that moniliformin in large amounts acts at the level of sugar metabolism and is cytotoxic at high concentrations in mammalian cells [35]. In addition, this toxin causes intoxication, and the lesions include intestinal hemorrhage, muscle weakness, breathing difficulty, cyanosis, coma, and death.

Trichothecenes are a very large group of mycotoxins produced by various species of Fusarium, Cephalosporium, Myrothecium, Stachybotrys, Trichoderma, Trichothecium, and Verticimonosporium. The generic name “trichothecene” has been derived from a Trichothecium species from which the first of these related compounds was isolated [28]. Trichothecenes belong to sesquiterpene compounds. They are produced on many different grains, e.g., corn, oats, and wheat by various Fusarium species such as F. graminearum, F. poae, and F. sporotrichioides [28, 36, 37].

There are several types of trichothecene mycotoxins, including deoxynivalenol, diacetoxyscirpenol, HT-2 mycotoxins, neosolaniol, nivalenol, satratoxin-H, T-2 mycotoxins, verrucarin A, and vomitoxin. Exposure to trichothecene mycotoxins can cause different symptoms in people such as dry eyes, tiredness, fatigue, vomiting, diarrhea, abdominal pain, mental impairment, rash, and bleeding [28]. In addition, T-2 mycotoxins are also substances for biological warfare that can be absorbed through a person’s skin [37].

Trichothecenes are typically found in plants when the autumn is cool and wet that delays harvest of grains such as corn. The toxins are also found in animal feeds that contain contaminated grain with Fusarium. Joffe [39] reported that trichothecenes are among the most toxic mycotoxins. He found that the LD50 rate for laboratory mice given trichothecene mycotoxins is between 1 and 7 mg/kg, depending on the specific type of trichothecene and the method of exposure [38, 39]. Toxicity of trichothecene in human is documented since 1913 when people in Russia consumed cereals that overwintered in the field [38, 39].

5. Conclusions

After about 200 years from the first introduction of Fusarium, there is not a universal agreement on the taxonomy of Fusarium species yet. However, considerable efforts are underway to use the available information to develop a uniform taxonomy system for Fusarium. Fusarium species infect most of plant species and cause substantial crop and yield losses. Effective management of Fusarium diseases in crops is not only essential for preventing crop losses but also needed to minimize mycotoxin production in food and feed products. Major strategies for preventing/minimizing mycotoxin production should be based on preventing growth of Fusarium in plants and therefore mycotoxin formation, reducing or eliminating mycotoxins from contaminated food and feed stuffs, or diverting contaminated products to low risk uses.