Expressed sequence tags and genes associated with loline alkaloid expression by the fungal endophyte Neotyphodium uncinatum

Spiering, Martin J.; Wilkinson, Heather H.; Blankenship, Jimmy D.; Schardl, Christopher L.

doi:10.1016/s1087-1845(02)00023-3

Cited by 51 publications

(42 citation statements)

References 50 publications

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“…One possibility is that relative amino acid levels available to the endophyte are crucial signals affecting transcriptional responses. In support of this possibility, differences in LA production and LOL gene expression by N. uncinatum have been demonstrated in different culture conditions, including minimal media with different N sources (Blankenship et al, 2001;Spiering et al, 2002). However, failure to obtain lolines in cultures of N. siegelii, N. coenophialum, and other endophytes suggests that more specific plant signals may also be involved in regulating LOL gene expression.…”

Section: Discussionmentioning

confidence: 98%

Regulation of a Chemical Defense against Herbivory Produced by Symbiotic Fungi in Grass Plants

2009

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Neotyphodium uncinatum and Neotyphodium siegelii are fungal symbionts (endophytes) of meadow fescue (MF; Lolium pratense), which they protect from insects by producing loline alkaloids. High levels of lolines are produced following insect damage or mock herbivory (clipping). Although loline alkaloid levels were greatly elevated in regrowth after clipping, loline-alkaloid biosynthesis (LOL) gene expression in regrowth and basal tissues was similar to unclipped controls. The dramatic increase of lolines in regrowth reflected the much higher concentrations in young (center) versus older (outer) leaf blades, so LOL gene expression was compared in these tissues. In MF-N. siegelii, LOL gene expression was similar in younger and older leaf blades, whereas expression of N. uncinatum LOL genes and some associated biosynthesis genes was higher in younger than older leaf blades. Because lolines are derived from amino acids that are mobilized to new growth, we tested the amino acid levels in center and outer leaf blades. Younger leaf blades of aposymbiotic plants (no endophyte present) had significantly higher levels of asparagine and sometimes glutamine compared to older leaf blades. The amino acid levels were much lower in MF-N. siegelii and MF-N. uncinatum compared to aposymbiotic plants and MF with Epichloë festucae (a closely related symbiont), which lacked lolines. We conclude that loline alkaloid production in young tissue depleted these amino acid pools and was apparently regulated by availability of the amino acid substrates. As a result, lolines maximally protect young host tissues in a fashion similar to endogenous plant metabolites that conform to optimal defense theory.

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Section: Discussionmentioning

confidence: 98%

Regulation of a Chemical Defense against Herbivory Produced by Symbiotic Fungi in Grass Plants

2009

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“…Protection of the symbiotum from insect and small animal herbivory through endophyte synthesis of bioprotective secondary metabolites (alkaloids) is the best-studied benefit of this association (Bush et al, 1997;Lane et al, 2000). Genes for the biosynthesis of the four main classes of bioprotective alkaloids have now been cloned, including genes for the biosynthesis of ergot alkaloids (Panaccione et al, 2001;Wang et al, 2004), lolines (Spiering et al, 2002(Spiering et al, , 2005, peramine (Tanaka et al, 2005), and indole-diterpenes (Young et al, 2005). Expression studies have shown that the genes for all four pathways are preferentially and highly expressed in planta (Spiering et al, 2002;Tanaka et al, 2005;Young et al, 2005), suggesting that host-specific signaling is required for the induction of these pathways.…”

Section: Introductionmentioning

confidence: 99%

Reactive Oxygen Species Play a Role in Regulating a Fungus–Perennial Ryegrass Mutualistic Interaction

et al. 2006

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Although much is known about the signals and mechanisms that lead to pathogenic interactions between plants and fungi, comparatively little is known about fungus-plant mutualistic symbioses. We describe a novel role for reactive oxygen species (ROS) in regulating the mutualistic interaction between a clavicipitaceous fungal endophyte, Epichloe¨festucae, and its grass host, Lolium perenne. In wild-type associations, E. festucae grows systemically in intercellular spaces of leaves as infrequently branched hyphae parallel to the leaf axis. A screen to identify symbiotic genes isolated a fungal mutant that altered the interaction from mutualistic to antagonistic. This mutant has a single-copy plasmid insertion in the coding region of a NADPH oxidase gene, noxA. Plants infected with the noxA mutant lose apical dominance, become severely stunted, show precocious senescence, and eventually die. The fungal biomass in these associations is increased dramatically, with hyphae showing increased vacuolation. Deletion of a second NADPH oxidase gene, noxB, had no effect on the E. festucaeperennial ryegrass symbiosis. ROS accumulation was detected cytochemically in the endophyte extracellular matrix and at the interface between the extracellular matrix and host cell walls of meristematic tissue in wild-type but not in noxA mutant associations. These results demonstrate that fungal ROS production is critical in maintaining a mutualistic fungus-plant interaction.

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“…Furthermore, PhyloCon-based (Wang and Stormo 2003) comparison of the putative lol gene promoter regions yielded the identification of four motifs conserved across the genes in all five clusters, with each motif having significant similarity to known fungal transcription factor binding sites in the TRANSFAC database (Wingender et al 1996). Conservation of these motifs further supported the hypothesis of the lol genes being co-regulated (Spiering et al 2002(Spiering et al , 2005.…”

Section: Loline Alkaloids (La)mentioning

confidence: 66%

“…The recent development of novel highly effective methods for identifying differentially expressed transcripts, enabled the application of suppression subtractive hybridization technique (Diatchenko et al 1996(Diatchenko et al , 1999 and provided for a successful identification of two genes, lolA and lolC, associated with endophytic loline synthesis (Spiering et al 2002).…”

Section: Loline Alkaloids (La)mentioning

confidence: 99%

Endophytes: exploiting biodiversity for the improvement of natural product-based drug discovery

Staniek

Woerdenbag

Kayser

2008

Journal of Plant Interactions

130

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Endophytes, microorganisms that colonize internal tissues of all plant species, create a huge biodiversity with yet unknown novel natural products, presumed to push forward the frontiers of drug discovery. Next to the clinically acknowledged antineoplastic agent, paclitaxel, endophyte research has yielded potential drug lead compounds with antibacterial, antiviral, antioxidant, insulin mimetic, anti-neurodegenerative and immunosuppressant properties. Furthermore, while being implicated in livestock neurotoxicosis, some endophyte-produced alkaloids have been shown to display insecticidal activity. The endophyte-host relationship is postulated to be a 'balanced antagonism'. Moreover, the plausibility of horizontal gene transfer (HGT) hypothesis is taken into account. Knowledge of the genetic background of endophytic natural product biosynthesis is discussed on the basis of loline alkaloids, ergopeptines, lolitrems and maytansinoids. The current dynamic progress in genomics will contribute to a better understanding of endophytic microbes and to further exploiting them as a source of pharmaceutically relevant compounds.

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Expressed sequence tags and genes associated with loline alkaloid expression by the fungal endophyte Neotyphodium uncinatum

Cited by 51 publications

References 50 publications

Regulation of a Chemical Defense against Herbivory Produced by Symbiotic Fungi in Grass Plants

Regulation of a Chemical Defense against Herbivory Produced by Symbiotic Fungi in Grass Plants

Reactive Oxygen Species Play a Role in Regulating a Fungus–Perennial Ryegrass Mutualistic Interaction

Endophytes: exploiting biodiversity for the improvement of natural product-based drug discovery

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