Neotyphodium

Neotyphodium
Neotyphodium
Neotyphodium coenophialum
Scientific classification
Kingdom: Fungi
Division: Ascomycota
Class: Ascomycetes
Subclass: Sordariomycetes
Order: Hypocreales
Family: Clavicipitaceae
Genus: Neotyphodium
Glenn, C.W. Bacon & Hanlin (1996)
Type genus
Neotyphodium coenophialum
(Morgan-Jones & W. Gams) Glenn, C.W. Bacon & Hanlin (1996)

Neotyphodium is a form genus containing species of endophytic fungi. These endophytes are asexual, seed-borne symbionts of cool-season grasses, and grow intercellularly throughout the aerial tissues of their hosts, including shoot apical meristems, leaf sheaths and blades, inflorescences, seeds and embryos. The Neotyphodium endophytes produce at least four different classes of compounds with various biological activities (toxicity or feeding deterrence) against insect and mammalian herbivores.[1]

Contents

Taxonomic considerations

Neotyphodium species (with the likely exception of N. chilense) are closely related to teleomorphic species of the genus Epichloë, from which many have evolved by processes involving interspecific hybridization.[2] Molecular phylogenetic evidence demonstrates that asexual Neotyphodium species are derived either from individual Epichloë species, or more commonly, from hybrids with at least two ancestral Epichloë species.[2][3] Hence, the form genus Neotyphodium is very closely associated with the teleomorphic genus Epichloë.[4] In keeping with the code of botanical nomenclature, the form genus refers to the asexual spore or vegetative state, and the teleomorphic genus refers to the sexual state. Because of their close relationships and shared biological properties, members of these two genera are collectively called 'epichloae' (singular = 'epichloë').

Life cycle

The taxonomic dichotomy is especially interesting in this group of symbionts, because vegetative propagation of fungal mycelium occurs by vertical transmission, i.e., fungal growth into newly developing host tillers (=individual grass plants). Importantly, all Neotyphodium and some Epichloë species infect new grass plants solely by growing into the seeds of their grass hosts, and infecting the growing seedling.[5][6] Manifestation of the sexual state — which only occurs in Epichloë species — causes choke disease, a condition in which grass inflorescences are engulfed by rapid fungal outgrowth forming a stroma. The fungal stroma suppresses host seed production and culminates in the ejection of meiospores (ascospores) that mediate horizontal (contagious) transmission of the fungus to new plants.[5] So, the two transmission modes exclude each other, although in many grass-Epichloë symbiota the fungus actually displays both transmission modes simultaneously, by choking some tillers and transmitting in seeds produced by unchoked tillers.

While being obligate symbionts in nature, most epichloae are readily culturable in the laboratory on culture media such as potato dextrose agar or a minimal salts broth supplemented with thiamine, sugars or sugar alcohols, and organic nitrogen or ammonium.[7]

Coevolution and growth synchrony with grass hosts

The epichloae display a number of central features that suggest a very strong and ancient association with their grass hosts. The symbiosis appears to have existed already during the early grass evolution that has spawned today's pooid grasses. This is suggested by phylogenetic studies indicating preponderance of codivergence of Neotyphodium/Epichloë species with the grass hosts they inhabit.[8] Growth of the fungal symbiont is very tightly regulated within its grass host, indicated by a largely unbranched mycelial morphology and remarkable synchrony of grass leaf and hyphal extension of the fungus;[9][10] the latter seems to occur via a mechanism that involves stretch-induced or intercalary elongation of the endophyte's hyphae, a process so far not found in any other fungal species, indicating specialized adaptation of the fungus to the dynamic growth environment inside its host.[11] A complex NADPH oxidase enzyme-based ROS-generating system in epichloae is indispensable for maintenance of this growth synchrony. Thus, it has been demonstrated that deletion of genes encoding these enzymes in Epichloë festucae causes severely disordered fungal growth in grass tissues and even death of the grass plant.[12][13]

Effects on the grass plant and on herbivores

It has been proposed that vertically transmitted symbionts should evolve to be mutualists since their reproductive fitness is intimately tied to that of their hosts.[14] In fact, some positive effects of epichloae on their host plants include increased growth, drought tolerance, and herbivore and pathogen resistance.[5][15] Resistance against herbivores has been attributed to alkaloids produced by the symbiotic epichloae.[16] Although grass-epichloë symbioses have been widely recognized to be mutualistic in many wild and cultivated grasses, the interactions can be highly variable and sometimes antagonistic, especially under nutrient-poor conditions in the soil.[17]

Due to the relatively large number of grass species harboring epichloae and the variety of environments in which they occur, the mechanisms underlying beneficial or antagonistic outcomes of epichloë-grass symbioses are difficult to delineate in natural and also agricultural environments.[5][18] Some studies suggest a relationship between grazing by herbivores and increased epichloë infestation of the grasses on which they feed,[19][20] whereas others indicate a complex interplay between plant species and fungal symbionts in response to herbivory or environmental conditions.[21] The strong anti-herbivore activities of several bioactive compounds produced by the epichloae [16][22] and relatively modest direct effects of the epichloae on plant growth and physiology[23][24] suggest that these compounds play a major role in the persistence of the symbiosis.

Bioactive compounds

Many Neotyphodium endophytes produce a diverse range of natural product compounds with biological activities against a broad range of herbivores.[16][25] Ergoline alkaloids (which are ergot alkaloids, named after the ergot fungus, Claviceps purpurea, a close relative of the epichloae) are characterized by a ring system derived from 4-prenyl tryptophan.[26] Among the most abundant ergot alkaloids in epichloë-symbiotic grasses is ergovaline, comprising an ergoline moiety attached to a bicyclic tripeptide containing the amino acids L-proline, L-alanine, and L-valine. Key genes and enzymes for ergot alkaloid biosynthesis have been identified in epichloae and include dmaW, encoding dimethylallyl-tryptophan synthase and lpsA, a non-ribosomal peptide synthetase.[26]

N-formylloline, an insecticidal alkaloid produced in several Neotyphodium–grass symbiota.

Another group of epichloë alkaloids are the indole-diterpenoids, such as lolitrem B, which are produced from the activity of several enzymes, including prenyltransferases and various monooxygenases.[27] Both the ergoline and indole-diterpenoid alkaloids have biological activity against mammalian herbivores, and also activity against some insects.[16] Peramine is a pyrrolopyrazine alkaloid thought to be biosynthesized from the guanidinium-group-containing amino acid L-arginine, and pyrrolidine-5-carboxylate, a precursor of L-proline,[22] and is an insect-feeding deterrent. The loline alkaloids [28] are 1-aminopyrrolizidines with an oxygen atom linking bridgehead carbons 2 and 7, and are biosynthesized from the amino acids L-proline and L-homoserine.[29] The lolines have insecticidal and insect-deterrent activities comparable to nicotine.[28] Loline accumulation is strongly induced in young growing tissues[30] or by damage to the plant-fungus symbiotum.[31] Many, but not all, epichloae produce up to three classes of these alkaloids in various combinations and amounts.[16]

Species

References

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