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Phylogenetic analyses reveal monophyletic origin of the ergot alkaloid gene dmaW in fungi.

ABSTRACT: Ergot alkaloids are indole-derived mycotoxins that are important in agriculture and medicine. Ergot alkaloids are produced by a few representatives of two distantly related fungal lineages, the Clavicipitaceae and the Trichocomaceae. Comparison of the ergot alkaloid gene clusters from these two lineages revealed differences in the relative positions and orientations of several genes. The question arose: is ergot alkaloid biosynthetic capability from a common origin? We used a molecular phylogenetic approach to gain insights into the evolution of ergot alkaloid biosynthesis. The 4-gamma,gamma-dimethylallyltryptophan synthase gene, dmaW, encodes the first step in the pathway. Amino acid sequences deduced from dmaW and homologs were submitted to phylogenetic analysis, and the results indicated that dmaW of Aspergillus fumigatus (mitosporic Trichocomaceae) has the same origin as corresponding genes from clavicipitaceous fungi. Relationships of authentic dmaW genes suggest that they originated from multiple gene duplications with subsequent losses of original or duplicate versions in some lineages.

SUBMITTER: Liu M

PROVIDER: S-EPMC2747131 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Phylogenetic analyses reveal monophyletic origin of the ergot alkaloid gene dmaW in fungi.

Liu Miao M Panaccione Daniel G DG Schardl Christopher L CL

Evolutionary bioinformatics online 20090604

Ergot alkaloids are indole-derived mycotoxins that are important in agriculture and medicine. Ergot alkaloids are produced by a few representatives of two distantly related fungal lineages, the Clavicipitaceae and the Trichocomaceae. Comparison of the ergot alkaloid gene clusters from these two lineages revealed differences in the relative positions and orientations of several genes. The question arose: is ergot alkaloid biosynthetic capability from a common origin? We used a molecular phylogene ...[more]

PMID: 19812724

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Project description:Pregnant Suffolk ewes (n = 19; 81.2kg ± 7.7) estimated to be carrying twins were assigned to endophyte-infected tall fescue seed (E+; 4.14 µg ergovaline + ergovalinine/g seed) or a control diet (CON; 0 µg ergovaline + ergovalinine) and evaluated at different stages of gestation (gd85 [pre-treatment, n = 3], gd110 [n = 4/treatment] or gd133 [n = 4/treatment). Ewes were individually fed a basal diet with (E+) or without (CON) endophyte-infected tall fescue seed from gd86 to gd110 or gd133. A terminal necropsy was performed, and uterine components were evaluated for size, weight, and type. Data were analyzed using a priori contrasts to test effects of stage of gestation (gd85 vs. gd110 or gd110 vs. gd133) and adaptive responses to feeding E+ fescue seed versus CON at gd110 and gd133. Serum prolactin concentrations were greater (P < 0.05) at gd110 than gd85, and then remained constant to gd133. Feeding E+ tall fescue seed reduced (P < 0.05) serum prolactin concentrations compared to CON at both gd110 and gd133. From gd85 to gd110, placentome type and number changed from type A to type B (P < 0.05) but did not change (P > 0.05) after gd110. Total fetal weight per ewe increased 2977 g from gd85 to gd110 (P = 0.011) and then 3151 g from gd110 to 133 (P = 0.012). Brain weight as a percentage of fetal body weight was higher (P = 0.029) for E+ fetuses on gd110 compared to CON, which demonstrates asymmetrical growth and intrauterine growth restriction (IUGR). In total, 15,961 genes were identified in the cotyledon through mapping to the ovine genome across all samples. There were 136 genes differentially expressed (FDR < 0.05; log2foldchange < -1 and > 1) from gd85 to gd110 with ovarian steroidogenesis and steroid biosynthesis pathways enriched and 469 genes differentially expressed from gd110 to gd133 with ribosome and oxidative phosphorylation pathways enriched. Exposure to E+ fescue resulted in differential expression of 22 genes at gd110 but only one gene at gd133 compared to CON. These results show that there are major changes in fetal growth and placental remodeling during the late gestation period that are influenced by exposure to ergot alkaloids from endophyte-infected tall fescue seed; however, major changes in the transcriptome of the cotyledon tissue in response to E+ fescue were not observed and other factors must be involved in the reduction of placental efficiency and fetal growth observed with E+ fescue exposure.

Project description:Ergot alkaloids are specialized fungal metabolites with potent biological activities. They are encoded by well-characterized gene clusters in the genomes of producing fungi. Penicillium camemberti plays a major role in the ripening of Brie and Camembert cheeses. The P. camemberti genome contains a cluster of five genes shown in other fungi to be required for synthesis of the important ergot alkaloid intermediate chanoclavine-I aldehyde and two additional genes (easH and easQ) that may control modification of chanoclavine-I aldehyde into other ergot alkaloids. We analyzed samples of Brie and Camembert cheeses, as well as cultures of P. camemberti, and did not detect chanoclavine-I aldehyde or its derivatives. To create a functioning facsimile of the P. camembertieas cluster, we expressed P. camemberti easH and easQ in a chanoclavine-I aldehyde-accumulating easA knockout mutant of Neosartorya fumigata The easH-easQ-engineered N. fumigata strain accumulated a pair of compounds of m/z 269.1288 in positive-mode liquid chromatography-mass spectrometry (LC-MS). The analytes fragmented in a manner typical of the stereoisomeric ergot alkaloids rugulovasine A and B, and the related rugulovasine producer Penicillium biforme accumulated the same isomeric pair of analytes. The P. camemberti eas genes were transcribed in culture, but comparison of the P. camemberti eas cluster with the functional cluster from P. biforme indicated 11 polymorphisms. Whereas other P. camembertieas genes functioned when expressed in N. fumigata, P. camembertieasC did not restore ergot alkaloids when expressed in an easC mutant. The data indicate that P. camemberti formerly had the capacity to produce the ergot alkaloids rugulovasine A and B.IMPORTANCE The presence of ergot alkaloid synthesis genes in the genome of Penicillium camemberti is significant, because the fungus is widely consumed in Brie and Camembert cheeses. Our results show that, although the fungus has several functional genes from the ergot alkaloid pathway, it produces only an early pathway intermediate in culture and does not produce ergot alkaloids in cheese. Penicillium biforme, a close relative of P. camemberti, contains a similar but fully functional set of ergot alkaloid synthesis genes and produces ergot alkaloids chanoclavine-I, chanoclavine-I aldehyde, and rugulovasine A and B. Our reconstruction of the P. camemberti pathway in the model fungus Neosartorya fumigata indicated that P. camemberti formerly had the capacity to produce these same ergot alkaloids. Neither P. camemberti nor P. biforme produced ergot alkaloids in cheese, indicating that nutritionally driven gene regulation prevents these fungi from producing ergot alkaloids in a dairy environment.

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Phylogenetic analyses reveal monophyletic origin of the ergot alkaloid gene dmaW in fungi.

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Phylogenetic analyses reveal monophyletic origin of the ergot alkaloid gene dmaW in fungi.

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