Limits...
Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the clavicipitaceae reveals dynamics of alkaloid loci.

Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, Panaccione DG, Schweri KK, Voisey CR, Farman ML, Jaromczyk JW, Roe BA, O'Sullivan DM, Scott B, Tudzynski P, An Z, Arnaoudova EG, Bullock CT, Charlton ND, Chen L, Cox M, Dinkins RD, Florea S, Glenn AE, Gordon A, Güldener U, Harris DR, Hollin W, Jaromczyk J, Johnson RD, Khan AK, Leistner E, Leuchtmann A, Li C, Liu J, Liu J, Liu M, Mace W, Machado C, Nagabhyru P, Pan J, Schmid J, Sugawara K, Steiner U, Takach JE, Tanaka E, Webb JS, Wilson EV, Wiseman JL, Yoshida R, Zeng Z - PLoS Genet. (2013)

Bottom Line: Epichloae produce alkaloids of four distinct classes, all of which deter insects, and some-including the infamous ergot alkaloids-have potent effects on mammals.We profiled the alkaloids and sequenced the genomes of 10 epichloae, three ergot fungi (Claviceps species), a morning-glory symbiont (Periglandula ipomoeae), and a bamboo pathogen (Aciculosporium take), and compared the gene clusters for four classes of alkaloids.We suggest that such selection is related to the variable life histories of the epichloae, their protective roles as symbionts, and their associations with the highly speciose and ecologically diverse cool-season grasses.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology, University of Kentucky, Lexington, Kentucky, USA. Schardl@uky.edu

ABSTRACT
The fungal family Clavicipitaceae includes plant symbionts and parasites that produce several psychoactive and bioprotective alkaloids. The family includes grass symbionts in the epichloae clade (Epichloë and Neotyphodium species), which are extraordinarily diverse both in their host interactions and in their alkaloid profiles. Epichloae produce alkaloids of four distinct classes, all of which deter insects, and some-including the infamous ergot alkaloids-have potent effects on mammals. The exceptional chemotypic diversity of the epichloae may relate to their broad range of host interactions, whereby some are pathogenic and contagious, others are mutualistic and vertically transmitted (seed-borne), and still others vary in pathogenic or mutualistic behavior. We profiled the alkaloids and sequenced the genomes of 10 epichloae, three ergot fungi (Claviceps species), a morning-glory symbiont (Periglandula ipomoeae), and a bamboo pathogen (Aciculosporium take), and compared the gene clusters for four classes of alkaloids. Results indicated a strong tendency for alkaloid loci to have conserved cores that specify the skeleton structures and peripheral genes that determine chemical variations that are known to affect their pharmacological specificities. Generally, gene locations in cluster peripheries positioned them near to transposon-derived, AT-rich repeat blocks, which were probably involved in gene losses, duplications, and neofunctionalizations. The alkaloid loci in the epichloae had unusual structures riddled with large, complex, and dynamic repeat blocks. This feature was not reflective of overall differences in repeat contents in the genomes, nor was it characteristic of most other specialized metabolism loci. The organization and dynamics of alkaloid loci and abundant repeat blocks in the epichloae suggested that these fungi are under selection for alkaloid diversification. We suggest that such selection is related to the variable life histories of the epichloae, their protective roles as symbionts, and their associations with the highly speciose and ecologically diverse cool-season grasses.

Show MeSH

Related in: MedlinePlus

Summary of indole-diterpene biosynthesis pathway.Arrows indicate one or more steps catalyzed by products of the genes indicated, where each idt/ltm gene is designated by its final letter (G = idtG/ltmG, etc.). Arrows and genes in blue indicate steps in synthesis of the first fully cyclized intermediate (paspaline). Arrows and genes in red indicate steps in decoration of paspaline to give the variety of indole-diterpenes in the Clavicipitaceae. Structures shown in gray are not yet verified.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3585121&req=5

pgen-1003323-g003: Summary of indole-diterpene biosynthesis pathway.Arrows indicate one or more steps catalyzed by products of the genes indicated, where each idt/ltm gene is designated by its final letter (G = idtG/ltmG, etc.). Arrows and genes in blue indicate steps in synthesis of the first fully cyclized intermediate (paspaline). Arrows and genes in red indicate steps in decoration of paspaline to give the variety of indole-diterpenes in the Clavicipitaceae. Structures shown in gray are not yet verified.

Mentions: Other alkaloids produced by Clavicipitaceae variously present hazards or benefits to agriculture. The indole-diterpenes (Figure 3) represent a broad diversity of bioactive compounds that exhibit mammalian and insect toxicity through activation of various ion channels [36], [37]. Livestock afflicted with indole-diterpene toxicity display symptoms of ataxia and sustained tremors [20]. For example, Paspalum staggers is caused by paspalitrems produced by Claviceps paspali and Claviceps cynodontis on seed-heads of dallisgrass (Paspalum dilatatum) and Bermuda grass (Cynodon dactylon), respectively [3], and common strains of Neotyphodium lolii symbiotic with perennial ryegrass (Lolium perenne) produce lolitrems, which cause ryegrass staggers [20]. In contrast, lolines (Figure 4) and peramine produced by many endophytic epichloae in forage grasses have not been linked to any toxic symptoms in grazing mammals, but instead provide potent protection from herbivorous insects [15], [16].


Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the clavicipitaceae reveals dynamics of alkaloid loci.

Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, Panaccione DG, Schweri KK, Voisey CR, Farman ML, Jaromczyk JW, Roe BA, O'Sullivan DM, Scott B, Tudzynski P, An Z, Arnaoudova EG, Bullock CT, Charlton ND, Chen L, Cox M, Dinkins RD, Florea S, Glenn AE, Gordon A, Güldener U, Harris DR, Hollin W, Jaromczyk J, Johnson RD, Khan AK, Leistner E, Leuchtmann A, Li C, Liu J, Liu J, Liu M, Mace W, Machado C, Nagabhyru P, Pan J, Schmid J, Sugawara K, Steiner U, Takach JE, Tanaka E, Webb JS, Wilson EV, Wiseman JL, Yoshida R, Zeng Z - PLoS Genet. (2013)

Summary of indole-diterpene biosynthesis pathway.Arrows indicate one or more steps catalyzed by products of the genes indicated, where each idt/ltm gene is designated by its final letter (G = idtG/ltmG, etc.). Arrows and genes in blue indicate steps in synthesis of the first fully cyclized intermediate (paspaline). Arrows and genes in red indicate steps in decoration of paspaline to give the variety of indole-diterpenes in the Clavicipitaceae. Structures shown in gray are not yet verified.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3585121&req=5

pgen-1003323-g003: Summary of indole-diterpene biosynthesis pathway.Arrows indicate one or more steps catalyzed by products of the genes indicated, where each idt/ltm gene is designated by its final letter (G = idtG/ltmG, etc.). Arrows and genes in blue indicate steps in synthesis of the first fully cyclized intermediate (paspaline). Arrows and genes in red indicate steps in decoration of paspaline to give the variety of indole-diterpenes in the Clavicipitaceae. Structures shown in gray are not yet verified.
Mentions: Other alkaloids produced by Clavicipitaceae variously present hazards or benefits to agriculture. The indole-diterpenes (Figure 3) represent a broad diversity of bioactive compounds that exhibit mammalian and insect toxicity through activation of various ion channels [36], [37]. Livestock afflicted with indole-diterpene toxicity display symptoms of ataxia and sustained tremors [20]. For example, Paspalum staggers is caused by paspalitrems produced by Claviceps paspali and Claviceps cynodontis on seed-heads of dallisgrass (Paspalum dilatatum) and Bermuda grass (Cynodon dactylon), respectively [3], and common strains of Neotyphodium lolii symbiotic with perennial ryegrass (Lolium perenne) produce lolitrems, which cause ryegrass staggers [20]. In contrast, lolines (Figure 4) and peramine produced by many endophytic epichloae in forage grasses have not been linked to any toxic symptoms in grazing mammals, but instead provide potent protection from herbivorous insects [15], [16].

Bottom Line: Epichloae produce alkaloids of four distinct classes, all of which deter insects, and some-including the infamous ergot alkaloids-have potent effects on mammals.We profiled the alkaloids and sequenced the genomes of 10 epichloae, three ergot fungi (Claviceps species), a morning-glory symbiont (Periglandula ipomoeae), and a bamboo pathogen (Aciculosporium take), and compared the gene clusters for four classes of alkaloids.We suggest that such selection is related to the variable life histories of the epichloae, their protective roles as symbionts, and their associations with the highly speciose and ecologically diverse cool-season grasses.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology, University of Kentucky, Lexington, Kentucky, USA. Schardl@uky.edu

ABSTRACT
The fungal family Clavicipitaceae includes plant symbionts and parasites that produce several psychoactive and bioprotective alkaloids. The family includes grass symbionts in the epichloae clade (Epichloë and Neotyphodium species), which are extraordinarily diverse both in their host interactions and in their alkaloid profiles. Epichloae produce alkaloids of four distinct classes, all of which deter insects, and some-including the infamous ergot alkaloids-have potent effects on mammals. The exceptional chemotypic diversity of the epichloae may relate to their broad range of host interactions, whereby some are pathogenic and contagious, others are mutualistic and vertically transmitted (seed-borne), and still others vary in pathogenic or mutualistic behavior. We profiled the alkaloids and sequenced the genomes of 10 epichloae, three ergot fungi (Claviceps species), a morning-glory symbiont (Periglandula ipomoeae), and a bamboo pathogen (Aciculosporium take), and compared the gene clusters for four classes of alkaloids. Results indicated a strong tendency for alkaloid loci to have conserved cores that specify the skeleton structures and peripheral genes that determine chemical variations that are known to affect their pharmacological specificities. Generally, gene locations in cluster peripheries positioned them near to transposon-derived, AT-rich repeat blocks, which were probably involved in gene losses, duplications, and neofunctionalizations. The alkaloid loci in the epichloae had unusual structures riddled with large, complex, and dynamic repeat blocks. This feature was not reflective of overall differences in repeat contents in the genomes, nor was it characteristic of most other specialized metabolism loci. The organization and dynamics of alkaloid loci and abundant repeat blocks in the epichloae suggested that these fungi are under selection for alkaloid diversification. We suggest that such selection is related to the variable life histories of the epichloae, their protective roles as symbionts, and their associations with the highly speciose and ecologically diverse cool-season grasses.

Show MeSH
Related in: MedlinePlus