Loline alkaloid

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Figure 1. General structure of the loline alkaloids produced in grasses infected by fungi of the Epichloe/Neotyphodium complex (epichloae endophytes); R' and R'' denote variable substituents that can include methyl, formyl, and acetyl groups giving rise to different loline species. Loline core structure.svg
Figure 1. General structure of the loline alkaloids produced in grasses infected by fungi of the Epichloë/Neotyphodium complex (epichloae endophytes); R' and R'' denote variable substituents that can include methyl, formyl, and acetyl groups giving rise to different loline species.

A loline alkaloid is a member of the 1-aminopyrrolizidines (often referred to as lolines), which are bioactive natural products with several distinct biological and chemical features. The lolines are insecticidal and insect-deterrent compounds that are produced in grasses infected by endophytic fungal symbionts of the genus Epichloë (anamorph species: Neotyphodium ). Lolines increase resistance of endophyte-infected grasses to insect herbivores, and may also protect the infected plants from environmental stresses such as drought and spatial competition. They are alkaloids, organic compounds containing basic nitrogen atoms. The basic chemical structure of the lolines comprises a saturated pyrrolizidine ring, a primary amine at the C-1 carbon, and an internal ether bridge—a hallmark feature of the lolines, which is uncommon in organic compounds—joining two distant ring (C-2 and C-7) carbons (see Fig. 1). Different substituents at the C-1 amine, such as methyl, formyl, and acetyl groups, yield loline species that have variable bioactivity against insects. Besides endophyte–grass symbionts, loline alkaloids have also been identified in some other plant species; namely, Adenocarpus species (family Fabaceae) and Argyreia mollis (family Convolvulaceae).

Contents

Discovery

A member of the loline alkaloids was first isolated from the grass Lolium temulentum and its elemental composition determined in 1892. It was initially named temuline and later renamed norloline. (Reviewed by Schardl et al. (2007).) [1] Studies in the 1950s and 1960s by Russian researchers established the name loline and identified the characteristic 2,7 ether bridge in its molecular structure. [1] Since then the analytical methods for purification and analysis of the lolines have been refined and several different loline species have been identified in many Lolium and related grasses infected by the Epichloë/Neotyphodium (epichloae) endophytes. [2] [3] Lolines are absent in grass plants that do not harbor the epichloae endophytes, and not all epichloae produce the lolines. [1] Because of the very intimate association of plant and endophyte and difficulties to reproduce the symbiotic conditions in vitro, it was long unknown if the fungus was the producer of the lolines, or if they were synthesized by the plant in response to endophyte infection. In 2001, it was demonstrated that the endophyte Neotyphodium uncinatum produces lolines in some chemically defined growth media, [4] which suggests that the endophyte is also the producer of the lolines in the grass plant. The lolines have also been reported from some plants in several plant families, [5] [6] suggesting a more widespread occurrence of these compounds in nature.

Mechanism of action

Lolines are insecticidal and deterrent to a broad range of insects, including species in the Hemiptera, Coleoptera, Hymenoptera, Lepidoptera, and Blattodea, such as the bird cherry-oat aphid (genus Rhopalosiphum ), large milkweed bug (Oncopeltus fasciatus), and American cockroach (Periplaneta americana). [1] [7] LC50 values of N-formylloline or N-acetylloline from grass seed extracts are 1-20 μg/ml for aphids and milkweed bugs and impair insect development and fecundity and cause avoidance of loline-containing grass tissues. [7] However, results of feeding tests with grass extracts are occasionally difficult to interpret due to the presence of other endophyte alkaloids in these extracts, [1] and the exact mechanisms of the insecticidal actions of the lolines are unknown. The lolines may be neurotoxic to the insects, and differences in the chemical groups at the C-1-amine result in different levels of insect toxicity; for example, N-formylloline (see Fig. 2), which occurs in higher concentrations in endophyte-infected grass plants, [7] has greater insect toxicity than some other lolines, which occur at lower concentrations in the grass plant. [1]

Figure 2. N-formylloline, one of the most abundant lolines in endophyte-infected grasses. N-formylloline.svg
Figure 2. N-formylloline, one of the most abundant lolines in endophyte-infected grasses.

Loline bioactivities show some unexpected variability with variation in their concentration in grass tissues. For example, the tall fescue endophyte, N. coenophialum , has been associated with enhanced resistance to the migratory root-endoparasitic nematode, Pratylenchus scribneri . At low concentrations, N-formylloline serves as a chemoattractant for P. scribneri, but acts as a repellant at higher concentrations. [8] However, ergot alkaloids also have repellent and immobilizing effects on P. scribneri, [8] and an endophyte of perennial ryegrass lacking lolines, and genetically engineered to produce no ergot alkaloids, exhibits resistance to this nematode. [9] Therefore, the relative importance of the loline and ergot alkaloids to nematode resistance remains unclear.

Many epichloae endophytes—including N. coenophialum symbiotic with Lolium arundinaceum (syn. Festuca arundinacea, tall fescue)—also produce ergot alkaloids that are toxic to mammalian herbivores. The ergot alkaloids occur at relatively low concentrations in the plant and are often difficult to detect analytically. By contrast, the lolines frequently accumulate to very high levels in grass tissues, [1] and were, therefore, initially associated also with toxicity to mammalian herbivores. [10] Specifically, the lolines were thought to be responsible for toxic symptoms called fescue toxicosis displayed by livestock grazing on grasses infected by N. coenophialum. [10] However, subsequently it was demonstrated that only the endophyte-produced ergot alkaloids are responsible for the symptoms of fescue toxicosis (or summer syndrome), [11] and not the lolines which, even at high doses, have only very small physiological effects on mammalians feeders. [12] Another group of alkaloids, the senecio-type alkaloids, are produced by various plants and like the lolines, the senecio alkaloids possess a pyrrolizidine ring structure. Unlike the lolines, however, the senecio alkaloids exhibit strong hepatotoxicity, [13] owing to a double bond between C-1 and C-2 in their ring structure. [13] This double bond is absent in the lolines, explaining the lack of hepatotoxicity of this group of compounds. The lolines have been suggested to inhibit seed germination or growth of other plants (allelopathy), [14] and to increase resistance of infected grasses against drought, but such effects have not been substantiated under more natural conditions of cultivation or in habitats. [1] [15]

Production and distribution in the grass plant

Figure 3. Neotyphodium coenophialum hyphae in tall fescue leaf tissue. Lolines commonly accumulate in the N. coenophialum-tall fescue symbiosis, providing protection from insects and other environmental stresses. Neotyphodium coenophialum.jpg
Figure 3. Neotyphodium coenophialum hyphae in tall fescue leaf tissue. Lolines commonly accumulate in the N. coenophialum–tall fescue symbiosis, providing protection from insects and other environmental stresses.

Lolines are produced by several grass–endophyte symbioses involving epichloae species, often along with other bioactive metabolites including ergot alkaloids and indole diterpenoids, and the unusual pyrrolopyrazine alkaloid, peramine, which is not found in other biological communities or organisms. The lolines are produced at levels, however, that can exceed 10 mg/g grass tissue (ranging from 2–20,000 μg/g [1] [16] ), exceeding the concentrations of the other endophyte alkaloids by >1000-fold. [7] Lolines produced in the grasses Lolium pratense (syn. Festuca pratensis, meadow fescue) and tall fescue infected by N. uncinatum and N. coenophialum (see Fig. 3), respectively, exhibit variable concentrations in grass tissues. [2] [16] Higher loline concentrations (100–1000 μg/g) are present in the seeds and in younger leaf tissues, and the lolines display seasonal changes in concentration levels throughout the plant. [16] The periodical appearance of tissues with high loline concentrations, such as flowering stems and seeds, contributes to this seasonal variation. [16] Loline concentrations often increase in grass tissues regrown after defoliation and clipping of plants, suggesting an inducible defense response mechanism, involving both symbiotic partners. However, this increase appears to be due to higher loline levels in younger leaves compared to older leaves, [17] but loline increases resembling inducible plant defenses have also been reported. [18] Variation of loline concentration with the developmental stage of specific grass tissues [16] suggests regulation of in planta loline distributions, providing greater protection of newly grown or embryonic tissues against attacks by insects. [1] Surprisingly, exogenous application of the plant signaling compound, methyl jasmonate—which commonly signals predation by insects—decreases expression of the genes for the lolines. [19] The factors that control loline production vary also among endophyte-infected grass tissues: whereas plant-supplied amino acids that are loline precursors limit accumulation of lolines in many grass tissues, [17] their production in tissues that bear external mycelial growth for fungal reproduction (stromata) is regulated by the expression of loline genes. [20]

Biosynthesis

The lolines are structurally similar to pyrrolizidine alkaloids produced by many plants, notably the necine ring containing a tertiary amine. This led to the early hypothesis that the biosynthesis of the lolines is similar to that of the plant pyrrolizidines, which are synthesized from polyamines. [21] However, feeding studies with carbon isotope–labeled amino acids or related molecules in pure cultures of the loline-producing fungus N. uncinatum recently demonstrated that the loline alkaloid pathway is fundamentally different from that of the plant pyrrolizidines. [1] The basic loline chemical structure is assembled in several biosynthetic steps from the amino acid precursors, L-proline and L-homoserine. [22] In the proposed first step in loline biosynthesis, these two amino acids are coupled in a condensation reaction linking the γ-carbon in homoserine to the secondary amine in proline in a PLP–type enzyme–catalyzed reaction to form the loline intermediate, N-(3-amino-3-carboxy)propylproline (NACPP). [23] Further steps in loline biosynthesis are thought to proceed with sequential PLP-enzyme-catalyzed and oxidative decarboxylations of the carboxy groups in the homoserine and proline moieties, respectively, cyclization to form the core loline ring structure, and oxidation of the C-2 and C-7 carbons to give the oxygen bridge spanning the two pyrrolizidine rings. [1] [24]

Genetic studies agree with the biosynthetic routes established in the precursor-feeding experiments. [1] AFLP-based studies using crosses between strains of the endophyte, Epichloë festucae, that differ in the capacity to produce lolines, show that loline production and protection of the grass, Lolium giganteum, from feeding by the aphid, Rhopalosiphum padi, segregate in a Mendelian fashion. [25] The presence of a single locus for loline production was later confirmed by the finding that loline-producing epichloae endophytes contain a gene cluster (LOL cluster) of at least eleven genes. [20] [26] The LOL genes are greatly and coordinately upregulated during loline alkaloid production, [24] and experimental genetic tests involving manipulation of selected LOL genes by RNA interference and gene knockout have directly confirmed the involvement of two of the LOL genes in loline biosynthesis. [27] [28] These tests and similarities in the peptide sequences of the proteins encoded by these genes to known enzymes indicate that one gene, termed lolC, is likely required for the first step in loline biosynthesis (condensation of L-proline and L-homoserine for NACPP formation), [27] and another gene, LolP —likely encoding a cytochrome P450 monooxygenase—, for oxygenation of one methyl group on the C-1 amine of N-methylloline, which gives the most abundant loline in many grass–endophyte symbionts, N-formylloline. [28]

Related Research Articles

<span class="mw-page-title-main">Ergot</span> Group of fungi of the genus Claviceps

Ergot or ergot fungi refers to a group of fungi of the genus Claviceps.

<span class="mw-page-title-main">Ergoline</span> Chemical compound

Ergoline is a chemical compound whose structural skeleton is contained in a variety of alkaloids, referred to as ergoline derivatives or ergoline alkaloids. Ergoline alkaloids, one being ergine, were initially characterized in ergot. Some of these are implicated in the condition ergotism, which can take a convulsive form or a gangrenous form. Even so, many ergoline alkaloids have been found to be clinically useful. Annual world production of ergot alkaloids has been estimated at 5,000–8,000 kg of all ergopeptines and 10,000–15,000 kg of lysergic acid, used primarily in the manufacture of semi-synthetic derivatives.

<span class="mw-page-title-main">Endophyte</span> Endosymbiotic bacterium or fungus

An endophyte is an endosymbiont, often a bacterium or fungus, that lives within a plant for at least part of its life cycle without causing apparent disease. Endophytes are ubiquitous and have been found in all species of plants studied to date; however, most of the endophyte/plant relationships are not well understood. Some endophytes may enhance host growth and nutrient acquisition and improve the plant's ability to tolerate abiotic stresses, such as drought, and decrease biotic stresses by enhancing plant resistance to insects, pathogens and herbivores. Although endophytic bacteria and fungi are frequently studied, endophytic archaea are increasingly being considered for their role in plant growth promotion as part of the core microbiome of a plant.

<i>Lolium</i> Genus of plants (tufted grasses)

Lolium is a genus of tufted grasses in the bluegrass subfamily (Pooideae). It is often called ryegrass, but this term is sometimes used to refer to grasses in other genera.

<i>Festuca</i> Genus in the grass family Poaceae

Festuca (fescue) is a genus of flowering plants belonging to the grass family Poaceae. They are evergreen or herbaceous perennial tufted grasses with a height range of 10–200 cm (4–79 in) and a cosmopolitan distribution, occurring on every continent except Antarctica. The genus is closely related to ryegrass (Lolium), and recent evidence from phylogenetic studies using DNA sequencing of plant mitochondrial DNA shows that the genus lacks monophyly. As a result, plant taxonomists have moved several species, including the forage grasses tall fescue and meadow fescue, from the genus Festuca into the genus Lolium, or alternatively into the segregate genus Schedonorus.

<i>Claviceps purpurea</i> Species of fungus

Claviceps purpurea is an ergot fungus that grows on the ears of rye and related cereal and forage plants. Consumption of grains or seeds contaminated with the survival structure of this fungus, the ergot sclerotium, can cause ergotism in humans and other mammals. C. purpurea most commonly affects outcrossing species such as rye, as well as triticale, wheat and barley. It affects oats only rarely.

<i>Lolium temulentum</i> Species of plant

Lolium temulentum, typically known as darnel, poison darnel, darnel ryegrass or cockle, is an annual plant of the genus Lolium within the family Poaceae. The plant stem can grow up to one meter tall, with inflorescence in the ears and purple grain. It has a cosmopolitan distribution.

<i>Epichloë</i> Genus of fungi

Epichloë is a genus of ascomycete fungi forming an endophytic symbiosis with grasses. Grass choke disease is a symptom in grasses induced by some Epichloë species, which form spore-bearing mats (stromata) on tillers and suppress the development of their host plant's inflorescence. For most of their life cycle however, Epichloë grow in the intercellular space of stems, leaves, inflorescences, and seeds of the grass plant without incurring symptoms of disease. In fact, they provide several benefits to their host, including the production of different herbivore-deterring alkaloids, increased stress resistance, and growth promotion.

Epichloë aotearoae is a systemic and seed-transmissible symbiont of Echinopogon ovatus, a grass endemic to Australia and New Zealand. It was originally described as a Neotyphodium species in 2002 but moved to Epichloë in 2014.

Epichloë melicicola is a systemic and seed-transmissible endophyte of Melica dendroides and Melica racemosa, grasses endemic to southern Africa. It was described as a Neotyphodium species in 2002 but transferred to the genus Epichloë in 2014.

<i>Epichloë coenophiala</i> Species of fungus

Epichloë coenophiala is a systemic and seed-transmissible endophyte of tall fescue, a grass endemic to Eurasia and North Africa, but widely naturalized in North America, Australia and New Zealand. The endophyte has been identified as the cause of the "fescue toxicosis" syndrome sometimes suffered by livestock that graze the infected grass. Possible symptoms include poor weight gain, elevated body temperature, reduced conception rates, agalactia, rough hair coat, fat necrosis, loss of switch and ear tips, and lameness or dry gangrene of the feet. Because of the resemblance to symptoms of ergotism in humans, the most likely agents responsible for fescue toxicosis are thought to be the ergot alkaloids, principally ergovaline produced by E. coenophiala.

<i>Lolium arundinaceum</i> Species of flowering plant

Lolium arundinaceum, tall fescue is a cool-season perennial C3 species of grass that is native to Europe and California. It occurs on woodland margins, in grassland and in coastal marshes. It is also an important forage grass with many cultivars that used in agriculture and is used as an ornamental grass in gardens, and sometimes as a phytoremediation plant.

<span class="mw-page-title-main">Ergocryptine</span> Chemical compound

Ergocryptine is an ergopeptine and one of the ergoline alkaloids. It is isolated from ergot or fermentation broth and it serves as starting material for the production of bromocriptine. Two isomers of ergocryptine exist, α-ergocryptine and β-ergocryptine. The beta differs from the alpha form only in the position of a single methyl group, which is a consequence of the biosynthesis in which the proteinogenic amino acid leucine is replaced by isoleucine. β-Ergocryptine was first identified in 1967 by Albert Hofmann. Ergot from different sources have different ratios of the two isomers.

<span class="mw-page-title-main">Ergovaline</span> Chemical compound

Ergovaline is an ergopeptine and one of the ergot alkaloids. It is usually found in endophyte-infected species of grass like Tall fescue or Perennial Ryegrass. It is toxic to cattle feeding on infected grass, probably because it acts as a vasoconstrictor.

<span class="mw-page-title-main">Plant use of endophytic fungi in defense</span>

Plant use of endophytic fungi in defense occurs when endophytic fungi, which live symbiotically with the majority of plants by entering their cells, are utilized as an indirect defense against herbivores. In exchange for carbohydrate energy resources, the fungus provides benefits to the plant which can include increased water or nutrient uptake and protection from phytophagous insects, birds or mammals. Once associated, the fungi alter nutrient content of the plant and enhance or begin production of secondary metabolites. The change in chemical composition acts to deter herbivory by insects, grazing by ungulates and/or oviposition by adult insects. Endophyte-mediated defense can also be effective against pathogens and non-herbivory damage.

<span class="mw-page-title-main">Lolitrem B</span> Chemical compound

Lolitrem B is one of many toxins produced by a fungus called Epichloë festucae var. lolii), which grows in Lolium perenne. The fungus is symbiotic with the ryegrass; it doesn't harm the plant, and the toxins it produces kill insects that feed on ryegrass. Lolitrem B is one of these toxins, but it is also harmful to mammals. The shoots and flowers of infected ryegrass have especially high concentrations of lolitrem B, and when livestock eat too much of them, they get perennial ryegrass staggers. At low doses the animals have tremors, and at higher doses they stagger, and at higher yet doses the animals become paralyzed and die. The blood pressure of the animals also goes up. The effect of the lolitrem B comes on slowly and fades out slowly, as it is stored in fat after the ryegrass is eaten. The condition is especially common in New Zealand and Australia, and plant breeders there have been trying to develop strains of fungus that produce toxins only harmful to pests, and not to mammals.

<i>Epichloë festucae</i> Species of fungus

Epichloë festucae is a systemic and seed-transmissible endophytic fungus of cool season grasses.

<i>Epichloë hybrida</i> Species of fungus

Epichloë hybrida is a systemic, asexual and seed-transmissible endophyte of perennial ryegrass within the genus Epichloë. An interspecies allopolyploid of two haploid parent species Epichloë typhina and Epichloë festucae var. lolii, E. hybrida was first identified in 1989, recognized as an interspecific hybrid in 1994, but only formally named in 2017. Previously this species was often informally called Epichloë typhina x Epichloë festucae var. lolii, or referenced by the identifier of its most well-studied strain, Lp1. Epichloë hybrida is a symbiont of perennial ryegrass where its presence is almost entirely asymptomatic. The species has been commercialized for the benefits of its anti-insect compounds in a pasture setting, although it is now more commonly used as an experimental model system for studying interspecific hybridization in fungi.

Epichloë brachyelytri is a haploid sexual species in the fungal genus Epichloë.

<span class="mw-page-title-main">Thomas Hartmann (biologist)</span> German pharmaceutical biologist (1937–2017)

Thomas Hartmann,, was a German pharmaceutical biologist and ecologist who was professor in the Department of Pharmaceutical Biology at the Technische Universität Braunschweig. His research focused on the biosynthesis, intracellular transport, and action of quinolizidine and pyrrolizidine alkaloids in fungi and plants and the sequestration of these secondary natural products by insects.

References

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  27. 1 2 Spiering MJ, Moon CD, Wilkinson HH, Schardl CL (2005). "Gene clusters for insecticidal loline alkaloids in the grass-endophytic fungus Neotyphodium uncinatum". Genetics . 169 (3): 1403–1414. doi:10.1534/genetics.104.035972. PMC   1449547 . PMID   15654104.
  28. 1 2 Spiering MJ, Faulkner JR, Zhang DX, Machado C, Grossman RB, Schardl CL (2008). "Role of the LolP cytochrome P450 monooxygenase in loline alkaloid biosynthesis". Fungal Genetics and Biology. 45 (9): 1307–1314. doi:10.1016/j.fgb.2008.07.001. PMID   18655839.
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