Alternariaq

Andrea Patriarca and Virginia Fernández Pinto, Laboratorio de Microbiología de Alimentos, Departamento de Química Orgánica,
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
© 2018 Elsevier Inc. All rights reserved.

Introduction 1
Taxonomy 1
Morphological Characteristics 1
Molecular Analysis 2
Chemical Segregation and Polyphasic Approach 4
Secondary Metabolite Production by Alternaria 4
Mycotoxins 4
Host-Specific Toxins 4
Secondary Metabolite Profiles 5
Ecophysiology 5
Occurrence of Alternaria and Alternaria Mycotoxins in Foods 6
Citrus Fruits 6
Tomatoes 6
Apples 7
Small-Grain Cereals 7
Other Foods 7
Uncited References 8
References 8
Further Reading 8

Introduction

Alternaria is a ubiquitous fungal genus with numerous species that cause pre- and post-harvest damage to agricultural products
including cereal grains, fruits and vegetables. The genus Alternaria is widely distributed in the environment and its spores can
frequently occur in a range of different habitats. They are normal components of the soil mycota and the air worldwide. Exposure
to the spores can cause allergy and severe asthma symptoms in susceptible people. Alternaria species naturally contaminate the aerial
parts of plants and are easily isolated from decay matter. Some species are phytopathogens that cause plant diseases in the field, and
others are able to colonize ripening crops as opportunistic saprophytes causing spoilage of crops after harvest and during storage.
Since these fungi grow well at low temperatures, they are responsible for spoilage of fruits and vegetables in refrigerated storage.
A short life cycle, easily detachable spores dispersed by wind, dark mycelium and conidia are some of the properties of
pathogenic species. The presence of melanin in spores and mycelial walls protect the structures against radiation effects and adverse
environmental conditions, determining resistance. All these characteristics are advantageous for disease establishment and
dispersal, both attributes of an effective pathogen.
In addition to spoiling fruits and vegetables, many Alternaria species are also capable of producing a wide range of secondary
metabolites. Most of these metabolites are phytotoxins that play an important role in the pathogenesis of plants. Others can be
considered mycotoxins and are harmful to humans and animals that consume the contaminated vegetable foods. Relatively little
is known about the toxicity of Alternaria toxins in comparison with mycotoxins produced by other fungi such as Aspergillus,
Penicillium and Fusarium.
A correct identification of Alternaria species combined with wider surveys on susceptible crops is needed in order to establish the
toxicological risk related to Alternaria contamination of agricultural products. The taxonomy of the genus is not well defined yet,
which makes it difficult to establish an accurate relationship between the contaminant species and their associated mycotoxins.

Taxonomy
Morphological Characteristics
The traditional methods for identification of Alternaria are primarily based on morphological characteristics of the reproductive
structures. Alternaria produces large brown conidia with both longitudinal and transverse septa, borne from inconspicuous
conidiophores, and with a distinct conical narrowing or ‘‘beak’’ at the apical end. These structures can be solitary or produced in
various patterns of chains.

1
2 Alternaria

The first attempts to organize the diverse taxa were based exclusively on conidium morphology in regard to shape, color, size,
septation, ornamentation, and so on. However, these structures can be quite complex and present a considerable diversity within
the genus, even between close-related taxa. The classification based on these principles may be laborious, time-consuming and is
often restricted to experts in this field.
According to conidia size, a subgeneric classification was made establishing two groups, the “large-spored” (conidia size in
a range of 60–100 m) and “small-spored” (conidia size less than 60 m) Alternaria. The small-spored species are cosmopolitan
saprotrophs, plant pathogens, allergens and mycotoxin producers, being the most commonly group reported in foods. Its taxonomy
is still under revision and there is a need for their accurate identification in a broad range of disciplines.
In addition to morphology, Alternaria taxa have been classified according to host specificity, such as Alternaria mali as host
specific in apple, Alternaria gaisen in pear, Alternaria longipes on tobacco, Alternaria citri in citrus, Alternaria arborescens (syn. Alternaria
alternata sp. lycopersici) in tomato, and so forth. As many morphological characteristics of these small-spored host-specific taxa
overlap those of A. alternata, it has been suggested that they should be referred to as pathotypes of A. alternata until further stable
genetic or physiological data can be produced to differentiate them. Based on the production of host specific toxins (HSTs), a system
of naming isolates as pathotypes of A. alternata was adopted, and it was particularly applied in phytopathological studies. However,
the horizontal transfer of HSTs genes was recently demonstrated, as well as the fact that HSTs production is not species-restricted,
thus the pathotype naming system would not be taxonomically robust.
Both, the traditional classification based on spore characteristics or on production of HSTs have led to the belief that the
morphospecies A. alternata is the most abundant small-spore taxon in nature. This concept prevailed for several years in scientific
works, until later taxonomic systems proved otherwise.
Since the 1960s, Emory G. Simmons dedicated his research work to organize the genus and revise all taxa through numerous
publications and can be considered a leading figure in Alternaria taxonomy. Among his substantial contributions to the genus,
he declared A. alternata as the type for the genus and developed the species-group concept by referring to certain groups using
a representative species, for instance, the Alternaria infectoria, Alternaria brassicicola, Alternaria radicina, Alternaria tenuissima or
A. alternata species-group. This sub-generic level organization is a helpful tool to classify the morphologically diverse assemblage
of Alternaria spp. and permits the generalized discussion of closely related species. This concept has been particularly valuable
between the small-spored catenulate species, which represent the most challenging in terms of accurate diagnostics.
In 2007, Simmons published an identification manual describing 276 Alternaria species based upon diagnostic characteristics of
conidia and chain formation, in particular, of the complex three-dimensional sporulation apparatus obtained under optimal
standardized culture conditions. The main factors determining the sporulation pattern are length of primary conidiophores,
branching patterns, presence, length and origin of secondary conidiophores, branching angles, degree of catenation, and size
and shapes of conidia. To summarize the morphological features of the most common species-groups reported in foods, the
A. alternata, A. tenuissima, A. arborescens and A. infectoria group characteristics are described below.
The A. alternata species-group is characterized by a single suberect, short primary conidiophore that bears a cluster of branching
or unbranched chains of 5–15 small conidia. The branching of chains originates both from the elongation of short secondary
conidiophores following terminal conidium formation and developing a series of conidiogenous loci; or from lateral secondary
conidiophores emerging from one or more conidium cells, resulting in a quite complex sporulation structure composed of
secondary, tertiary and even quaternary branching (Fig. 1).
The A. tenuissima species-group can be diagnosed by its long and single chains originating from usually short and simple primary
conidiophores. Branching is scarce and when it occurs it originates from a lateral secondary conidiophore parting from the
conidium body. This group has a pattern of moderate to long chains of 10–15 or more long-narrow conidia with or without short
lateral branches of usually 1–3 conidia.
The A. arborescens species-group is recognized by the presence of distinct long, well-defined primary conidiophores, occasionally
with a few subterminal branches, and a terminal cluster of branching conidial chains of an arborescent appearance. Branching
pattern is defined mostly by the presence of a geniculate secondary conidiophore that can originate both from the conidial apex
(most frequently) or body.
The A. infectoria species-group is characterized by chains of small conidia that branch due to the formation of long septated
secondary conidiophores between conidia arising from the apex or conidial body; the apical ones are often geniculate and have
several conidiogenous loci. Secondary conidiophores are conspicuous and determinant elements of the branched architecture.
This type of pattern results in an uncrowded set of organized branching chains with a terminal cluster that is loose in density.

Molecular Analysis
With the advancement of molecular techniques, several studies have examined taxonomic relationships among small-spored
catenulate Alternaria spp. using a variety of methods in an attempt to establish consensus with contemporary morphological-
based species.
Molecular studies have been made with special interest in the classification of small-spored Alternaria, which show little
resolution in their molecular phylogeny. Sequencing of “housekeeping genes”, such as internal transcribed spacer region (ITS),
mitochondrial small subunit (SSU), and mitochondrial large subunit (MtLSU), which have been used with success in other genera,
has not yielded any segregation among the small-spored Alternaria pathogens, except for the A. infectoria species-group which
constitutes a quite distinct clade. However, MtLSU sequence data was variable enough to satisfactorily differentiate some
 Alternaria 3

A E

B F

C G

D H

Figure 1 (A)–(D) Sporulation pattern on 7-day old PCA cultures of representative strains of: (A) A. alternata, (B) A. tenuissima, (C) A. arborescens,
and (D) A. infectoria species-group. (E)–(H) Conidiophores and conidia from (E) A. alternata, (F) A. tenuissima, (G) A. arborescens, and (H) A. infectoria
species-group. (A)–(D) Images from Petri dishes using a stereo microscope under low magnification. (E)–(H) Image from a prepared slide mount
using a compound microscope under high magnification.

large-spored species of Alternaria among themselves as well as large-spored from small-spored ones. Some sequences
from functional genes, such as b-tubulin, translation elongation factor a, calmodulin, actin, chitin synthetase, and
1,3,8-trihydroxynaphthalene reductase, also failed to differentiate the small-spored Alternaria pathogens. More recent molecular
studies proved the inability of ITS to resolve among Alternaria isolates, despite being considered an almost universal barcoding
gene for fungi, due to the high level of similarity between several morphological species. These studies pointed out the plasma
4 Alternaria

membrane ATPase and calmodulin loci as the most suitable genetic markers for the genus. Among the small-spored species closely
related to A. alternata, OPA10–2 and endoPG were the gene regions that showed the highest variability.
Several taxonomic revisions based on molecular data have been recently made. Particularly, a series of works based on
a phylogenetic approach for systematic resolution using nuclear protein-coding loci, have proposed significant changes in Alternaria
taxonomy. Several phylogenetic species-groups were elevated to the taxonomic status of section in order to provide an accurate
identification of a taxon or group of taxa. A total of 27 sections, each represented by a type specimen, were proposed to organize
the taxonomical diversity of the genus. The Alternaria section Alternaria includes the type for the genus and contains most of the
small-spored Alternaria species that constitutes the most relevant food pathogens (A. alternata, A. arborescens, A. tenuissima, and
others). The A. infectoria species-group belongs to the section Infectoriae in this new classification.

Chemical Segregation and Polyphasic Approach

In addition to morphology and molecular analysis, the production of secondary metabolites has been used as a mean of
identification and classification. Profiles of metabolites produced on standardized laboratory media have been utilized to
distinguish between Alternaria species-groups taking advantage of the enormous potential to biosynthesize different secondary
metabolites of this genus.
A profile of secondary metabolites can be visualized using chromatographic methods such as thin layer chromatography and
ultra-violet light, high performance liquid chromatography and diode array detection (HPLC-DAD) or combined with mass
spectrometry (HPLC-MS). A technique based on electrospray ionization (ESI) with negative ion detection and MS–MS has
overcome previous limitations of other analytical methods in terms of sensitivity and specificity. Extraction methods are easy,
less time consuming than morphological characterization and relatively economic and it have been successfully used in
differentiating between species in other genera such as Aspergillus, Fusarium and Penicillium. Secondary metabolite data can be
statistically analyzed to determine a characteristic profile for a species or species-group, or they can be used to determine
species-specific metabolites that could be adopted as chemotaxonomic markers in taxon identification.
The most recent tendency to achieve accurate identification of Alternaria species is a polyphasic approach which integrates the
three aspects, morphological characteristics, molecular analysis and secondary metabolite profiling. The combination of all the
information provided by different perspectives represents a powerful tool for classification of this complex genus. The inclusion
of additional data, such as ecology or plant pathogenicity could be a future trend that might lead to an unequivocal classification
and systematic placement of Alternaria strains into species.

Secondary Metabolite Production by Alternaria

Mycotoxins
Alternaria spp. can produce a wide variety of toxic metabolites that play an important role in plant pathogenesis. Many of these
metabolites, under determined environmental conditions, could accumulate in vegetable foods and be harmful to humans and
animals. These compounds belong principally to three different structural groups: (i) the dibenzopyrone derivatives, alternariol
(AOH), alternariol monomethyl ether (AME), and altenuene (ALT); (ii) the perylene derivatives altertoxins (ATX-I, ATX-II and
ATX II); and (iii) the tetramic acid derivative, tenuazonic acid (TA). Another metabolite of miscellaneous structure, tentoxin
(TEN), has been recently considered a relevant mycotoxin by international food safety authorities, although toxicological data
available are limited and only its phytotoxic effects have been confirmed up to now.
TA, AOH, AME and ATX-I are the main Alternaria mycotoxins that can contaminate foods. Of particular health concern is the
association found between Alternaria contamination in cereal grains and the high levels of human esophageal cancer in China.
The toxicity of TA has been reported in plants, in chick embryos and several animal species, including guinea pigs, mice, rabbits,
dogs, and rhesus monkeys. In dogs, it has caused hemorrhages in several organs and in chickens, subacute toxicity has been
observed. Precancerous changes have been reported in the esophageal mucosa of mice. The possible involvement of TA in the
etiology of onyalai, a human hematological disorder occurring in Africa, has been suggested. AME and AOH have been found
to be mutagenic in microbial and mammalian cell systems. There is also some evidence of carcinogenic properties as they induce
squamous cell carcinoma in mice. Recently reported are the estrogenic potential of AOH, its inhibitory effects on cell proliferation,
and its genotoxic effect in cultured mammalian cells. ATX-I and related compounds may cause acute toxicity in mice and have been
reported to be more potent mutagens than AOH and AME.

Host-Specific Toxins
Certain species in the genus Alternaria produce low-molecular-weight compounds known as HSTs that determine their host range
and contribute to their virulence or pathogenicity. These host-specific forms were earlier designated as pathotypes of A. alternata but
they were subsequently assigned to other species, as is shown in Table 1.
From the seven described pathotypes of A. alternata, the new taxonomic division based on phylogenetic studies, recognized two,
namely A. gaisen and A. longipes, as separate species in the section Alternaria. The tomato pathotype would belong to an A. arborescens
species complex, belonging to the same section. There is a recent proposal of regaining the forma specialis designation for those
pathotypes producing HSTs which cannot be considered different phylogenetic species from A. alternata.
 Alternaria 5

Table 1 Host specific toxins of plant pathogen Alternaria species

Species Synonym Pathotype Disease Toxin

Alternaria gaisen Nagano A. kikuchiana Tanaka A. alternata Japanese pear Black spot of Japanese pear AK toxins
A. limoniasperae Simmons A. citri rough lemon pathotype A. alternata rough lemon Brown spot of rough lemon ACRL toxin
A. toxicogenica Simmons A. citri tangerine pathotype A. alternata tangerine Brown spot of tangerine ACTG toxins
A. longipes Mason – A. alternata tobacco Brown spot of tobacco AT toxin
A. mali Roberts – A. alternata apple Alternaria blotch of apple AM toxins
A. arborescens Simmons A. alternata f. sp. lycopersici A. alternata tomato Stem canker of tomato AAL toxins
– – A. alternata strawberry Black spot of strawberries AF toxins

The virulence of the several “pathotypes” to different host can be explained as an evolutionary adaptation based on the ability to
produce HSTs. Their characterization has been useful in the investigation of evolution and phylogenetic relationships among
small-spored Alternaria. These toxins act by inducing susceptibility of host cells by suppressing their defense reactions. Among
the several HSTs produced by this genus, the AAL toxins are of concern because of their structural and toxicological similarities
to the fumonisins, the carcinogenic mycotoxins produced by Fusarium species.

Secondary Metabolite Profiles

The production of secondary metabolites has been successfully used for identification and classification of similar species within the
genus, especially between the small-spored species-groups.
Isolates belonging to the A. alternata, A. tenuissima and A. arborescens species-groups have been reported to produce most of the
known metabolites and are the major responsible for the accumulation of Alternaria mycotoxins in foods. The three groups contain
a high percentage of isolates producing AOH, AME and several compounds from the same biosynthetic pathway, such as ALT. TA is
also a metabolite frequently produced by these groups and is usually synthesized in high amounts by many of their isolates. The
production of ATXs has also been reported for these small-spored species-groups although less frequently. The only specific
metabolites from the A. arborescens species-group are the AAL toxins, but they are rarely produced in vitro; therefore they are not
a reliable chemical taxonomic marker for this group. Many isolates within all these Alternaria species-groups are also able to produce
TEN, a cyclic tetrapeptide that causes chlorosis in several sensitive plants.
The species belonging to the A. infectoria species-group show a metabolite profile very different from the ones mentioned above.
None of the isolates within this group produces any of the most common metabolites reported for the genus; on the contrary they
produce infectopyrones, novae-zelandins and phomapyrones, which are metabolites never found in other Alternaria species-group.
Only perylene derivatives, such as ATXs, and other structurally related compounds were found in common with the rest of the
small-spored alternarias.
Among the large-spored groups the most common metabolites produced are altersolanols. Zinniol is produced by Alternaria
dauci, Alternaria porri and Alternaria solani. On the other hand, A. porri, Alternaria tomatophila and A. solani have in common the
production of altersolanol and macrosporin. A porri and A. solani shared the production of alterporriols and TEN. ATX-I is produced
by A. solani and A. tomatophila. AME has only been reported from A. dauci, erythroglaucin and other anthraquinones from A. porri,
and alternaric acid, alternariol, solanapyrones and zinnolide from A. solani.
The diversity in metabolite profiles turns chemical data a valuable tool to complement morphological and molecular analysis in
the characterization of Alternaria species groups. Even though the boundaries between metabolite production capacity from the
small-spored species are not sharp, they are consistent with the new classification based on phylogenetic data and can be utilized
to segregate species or groups belonging to sect. Alternaria from sect. Infectoriae.

Ecophysiology

Few studies have determined the optimal and limiting conditions responsible for germination, growth and mycotoxin production
in Alternaria spp. The optimal temperature range for Alternaria growth is 22–28  C, with the minimal reported as 3  C and
enabling the fungus to grow under cold storage. Alternaria spp. continue to develop in several vegetables stored at refrigeration
temperatures or in certain apple cultivars stored at 0  C or below. Fruits and vegetables subjected to cold stress are more sensitive
to disease initiation. Optimal Alternaria growth occurs at pH 4–5.4. A. alternata is able to grow in oxygen concentrations as low as
0.25%, with growth rates being proportional to oxygen concentration. The minimum water activity (aw) for growth at 25  C is 0.86.
Faster growth was registered at aw 0.98.
Optimal environmental conditions for Alternaria mycotoxins production reported by several researchers differ according to the
strains and the substrates considered. Two strains isolated from soya bean produced maximum amount of AOH on irradiated soya
beans at aw 0.98 and different temperature (15 and 25  C) depending on the strain. The maximum amount of AME was produced
by both strains at aw 0.98 and 30  C. No significant production of either toxin was registered at aw 0.90. Other authors reported that
alternariol, its monomethyl ether and altenuene were produced optimally on autoclaved wheat grains at 25  C and 0.98 aw. Another
study was carried out with a mixed inoculum of five strains of A. alternata isolated from tomato fruits affected by “black mould” and
6 Alternaria

grown on a synthetic tomato medium of aw adjusted with glycerol. Optimal conditions were aw 0.95 and 21  C for AOH, aw 0.95
and 35  C for AME and aw 0.98 and 21  C for TA. aw 0.90 was found to be limiting for the production of these Alternaria
mycotoxins. None of the toxins were detected at a temperature of 6  C, although other studies on different substrates reported
mycotoxin production at lower temperatures. According to these results, a storage temperature of 6  C or below could be considered
safe for tomato fruits and high moisture tomato products (aw > 0.95) in relation with Alternaria toxins. Even though the
biosynthesis of AOH and AME is affected differently than TA by environmental factors, a low storage temperature would be effective
in controlling production of all three toxins in tomato products.

Occurrence of Alternaria and Alternaria Mycotoxins in Foods

Alternaria species are commonly associated with plant diseases causing spoilage of agricultural commodities with consequent
economic losses. Moreover, as a result of Alternaria growth, several mycotoxins have been detected as natural contaminants in these
products. Mycotoxin accumulation in fruits and vegetables may occur in the field and during harvest, post-harvest and storage.
Vegetable foods infected by Alternaria rot are obviously not suitable for consumption. Since consumers will reject fruit that is visibly
moldy or rotten, whole fresh fruits are not believed to contribute significantly with Alternaria toxins to human exposure. However,
processed vegetable products may introduce high amounts of these toxins to the human diet if decayed or moldy fruit is not
removed before processing.
Several crops of agricultural value are susceptible to infection by different Alternaria species and can contribute to the entry of
Alternaria mycotoxins in the food chain.

Citrus Fruits
Alternaria brown spot is a disease of mandarins, tangerines and various tangerine hybrids. The pathogen causes necrotic lesions in
mature fruit that are unacceptable to consumers. Although the relationship between the presence of lesions and mycotoxins in citrus
products is not currently known, fruit with these defects should not be used to produce juice.
Black center rot (or “black heart rot”) of oranges and lemons caused by an Alternaria species generally known as A. citri appears as
internal blackening of the fruit. Two kinds of Alternaria heart rot are distinguished in mandarins based on the color of the affected
tissues (grey or black). The grey color is associated with felty gray mycelium and the black color with sporulation (Fig. 2C).
Investigations carried out on the natural occurrence of mycotoxins in infected fruits showed that the two kinds of mandarin heart
rot contain different mycotoxin profiles: TA, AME and AOH were found in black rot samples, whereas TA was the only toxin
detectable in grey rot samples. Besides the three main toxins, ALT and altenuic acid-III were detected in citrus fruit juices.

Tomatoes
As is common for many soft-skinned fruits, tomatoes are especially susceptible to fungal decay. Alternaria is the most frequent
fungus on moldy tomatoes and is responsible for the disease known as “black mould of tomato” (Fig. 2A). It appears as dark brown
to black typical lesions, which are of firm texture and can become several centimeters in diameter, with abundant sporulation of the
fungus. Fruits become increasingly susceptible to fungal invasion during ripening. The disease is favored by warm rainy weather.
Infection can occur at the stem end of the fruit or through mechanical injury, cracking from excessive moisture during growth,
or chilling. Some investigations have demonstrated that Alternaria rot can develop at all acceptable handling temperatures and
can be avoided only by rapid marketing. Fungal decay of fresh tomatoes is very rapid at 25  C.
A. alternata has been mentioned as the dominant fungal species occurring on naturally infected tomato fruits, but after the
changes in the taxonomy of this genus introduced by Simmons, other species such as A. tenuissima, A. arborescens and A. longipes
were also found to be associated with postharvest spoilage of tomatoes.

A B C

Figure 2 Fruits infected by Alternaria spp. (A) Black mould of tomato fruit, (B) moldy core-rot of apple, (C) black heart rot of mandarin.
 Alternaria 7

Alternaria mycotoxin occurrence has been reported in tomatoes. TA was the major toxin produced in naturally infected fruits.
Lower levels of AOH and AME were also recorded. TEN has also been isolated from tomato lesions.
Temperature is one of the major environmental factors affecting the shelf life of tomato fruits and their rate of deterioration by
Alternaria. To control toxin production in tomato fruits, temperature below 6  C should be maintained, and the storage period
should not exceed 10 days.
Direct consumption of moldy tomatoes by consumers is unlikely, but these tomatoes may possibly be used for processed tomato
products. In fact, tenuazonic acid and the alternariols were detected in tomato paste, pulp, concentrate, juice, sauces and tomato
puree samples, occasionally in very high amounts. TEN and ALT were also found in several of these tomato products. To prevent
mycotoxin contamination of processed tomato products, moldy or damaged tomatoes should not be used. Few studies have been
carried out on the stability of Alternaria mycotoxins, although like other mycotoxins they are probably quite stable. A major
proportion of the toxins survived the autoclaving of tomatoes in producing tomato paste.

Apples
Core rot of apples is a well-known post-harvest disease that mainly infects the Red Delicious varieties (Fig. 2B). Moldy core rot
reduces apple fruit quality and is a worldwide problem occurring in most countries where apples are grown. The disease has
been linked in the past to the single species A. alternata, whereas later studies concluded that representatives of several species
groups, including A. arborescens, A. infectoria and A. tenuissima, were involved.
Newly harvested, undamaged apples are usually free of fungal infection. Fungal spores, which are generally present on the fruit
surface, preferably enter through wounds formed during harvesting and handling. Sometimes, the fungus can also penetrate the
fruit via open calyces, into the core or carpel regions, during fruit development and storage.
Most of the Alternaria strains isolated from rotten apples produced AOH and AME in the whole fruits after inoculation. Studies
on the possible transfer of Alternaria mycotoxins from the rotten part of an inoculated fruit to the surrounding sound tissues
indicated that toxins were not restricted to the rotted area, which was characterized by abundant fungal hyphae. They could also
be isolated from the sound tissues, although the toxin levels were lower. Apples with moldy cores may be used in producing apple
juice, resulting in high levels of Alternaria toxins in processed apple products. The natural occurrence of AOH, AME, and TA in
samples of commercial apple juice and apple juice concentrate was reported in several countries. TEN was also found, but at traces
levels and in a lower number of commercial apple juice samples.

Small-Grain Cereals
Alternaria is the most common genus found in cereal grains in several regions of the world. References from many countries about
the prevalence of this fungus in cereals indicate a very high incidence, with more than 90% of the grains affected. Infected grains
develop a disease called black point, which consists of a discoloration of the germ and the seed due to mycelial and conidial masses.
Small-grain cereals such as wheat, triticale, barley and oats are frequently infected, whereas rice and maize are less susceptible. Black
point is known to affect grain quality adversely, impairing flour, semolina and their products. The presence of dark specks in pasta
and discoloration in noodles results in downgrading with heavy financial losses. Several Alternaria species have been involved,
mainly A. alternata, A. tenuissima and also Alternaria triticina, which is an important pathogen of wheat considered the major cause
of leaf blight. The A. infectoria species-group was found as responsible of black point observed in certain wheat cultivars in
Argentina, Australia, North America and several European countries. As a consequence of the disease, small-grain cereals are
frequently contaminated with Alternaria mycotoxins. Natural occurrence of AOH, AME and TA has been reported worldwide in
wheat, barley and oats, and several cereal-based processed foods. High concentrations of TA and AME and lower levels of ALT
were found in sorghum in India. TEN was found in cereal grains, bakery products, and rice based cereal foodstuff. Of particular
concern is the presence of TA at high levels in sorghum-based infant food reported in Germany.

Other Foods
Olives are often affected by Alternaria, particularly if the fruits remain in the soil for a long time after ripening. Several Alternaria
toxins were detected in molded or damaged olives and were also found in olive oil as well as in other edible oils (rapeseed, sesame
and sunflower).
Although A. alternata and A. radicina are associated to black rot of carrots, no Alternaria toxins were found in carrot roots or in
commercial carrot products, with the exception of ALT in carrot juice, but in low frequency and levels. In contrast, AOH and AME
were detected in several fruit beverages such as grape, apricot, grapefruit, and raspberry juice, cranberry and prune nectar, and
different wines.
Alternaria mycotoxins have been reported in many other vegetable foods that are frequently infected by the fungus, such as
peppers, melons, mangoes, sunflower, raspberries, pecans and Japanese pears. It has been reported that Alternaria mycotoxins
were not a major problem in strawberries because of the presence of fast-growing molds such as Rhizopus and Botrytis, which
outgrow Alternaria and inhibits its growth.
At present, there are no specific regulations for any of the Alternaria toxins in foods. However, these mycotoxins should not be
underestimated since they are produced by several Alternaria species frequently associated with a wide range of agricultural products
8 Alternaria

and processed plant foods of relevant value in the human diet. More investigations on the toxic potential of these toxins and their
hazard for human consumption are needed to make a reliable risk assessment of dietary exposure and better define guidelines on
Alternaria mycotoxin limits in foods.

Uncited References

Andersen and Thrane, 1996; Andersen et al., 2002; Andersen et al., 2009; Andersen et al., 2015; Andrew et al., 2009; Asam and
Rychlik, 2013; Barkai-Golan and Paster, 2008; Lawrence et al., 2013; Lawrence et al., 2016; Logrieco et al., 2009; Ostry, 2008;
Oviedo et al., 2011; Patriarca, 2016; Pitt and Hocking, 2009; Polizzotto et al., 2012; Pose et al., 2010; Pryor and Michailides,
2002; Scott, 2004; Simmons, 1999; Taralova et al., 2011; Tsuge et al., 2013; Woudenberg et al., 2015.

References

Andersen, B., Thrane, U., 1996. Differentiation of Alternaria infectoria and Alternaria alternata based on morphology, metabolite profiles, and cultural characteristics. Can. J.
Microbiol. 42, 685–689.
Andersen, B., Kroger, E., Roberts, R., 2002. Chemical and morphological segregation of Alternaria arborescens, A. infectoria and A. tenuissima species-group. Mycol. Res. 106 (2),
170–182.
Andersen, B., Sørensen, J.L., Nielsen, K.F., van den Ende, B.G., de Hoog, S., 2009. A polyphasic approach to the taxonomy of the Alternaria infectoria species–group. Fungal Genet.
Biol. 46, 642–656.
Andersen, B., Nielsen, K.F., Fernández Pinto, V., Patriarca, A., 2015. Characterization of Alternaria strains from Argentinean blueberry, tomato, walnut and wheat. Int. J. Food
Microbiol. 196, 1–10.
Andrew, M., Peever, T.I., Pryor, B.M., 2009. An expanded multilocus phylogeny does not resolve morphological species within the small–spored Alternaria species complex.
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Further Reading

Barkai-Golan, R., 2001. Post-harvest Diseases of Fruits and Vegetables, Development and Control. Elsevier, Amsterdam, The Netherlands.
Barkai-Golan, R., Paster, N., 2008. Mycotoxins in fruits and vegetables. San Diego, USA: Elsevier.
Lawrence, D.P., Rotondo, F., Gannibal, P.B., 2016. Biodiversity and taxonomy of the pleomorphic genus Alternaria. Mycological Progress 15 (3), 1–22.
Simmons, E.G., 2007. Alternaria an Identification Manual. Centraalbureau voor Schimmelcultures, Utrecht, Netherlands.

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Change History: March 2018. A. Patriarca and V. Fernández Pinto updated the text and further readings to this entire article, and replaced one of the keywords.