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.2013 Jun 6;5(6):1064-88.
doi: 10.3390/toxins5061064.

Currencies of mutualisms: sources of alkaloid genes in vertically transmitted epichloae

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Currencies of mutualisms: sources of alkaloid genes in vertically transmitted epichloae

Christopher L Schardl et al. Toxins (Basel)..

Abstract

The epichloae (Epichloë and Neotyphodium species), a monophyletic group of fungi in the family Clavicipitaceae, are systemic symbionts of cool-season grasses (Poaceae subfamily Poöideae). Most epichloae are vertically transmitted in seeds (endophytes), and most produce alkaloids that attack nervous systems of potential herbivores. These protective metabolites include ergot alkaloids and indole-diterpenes (tremorgens), which are active in vertebrate systems, and lolines and peramine, which are more specific against invertebrates. Several Epichloë species have been described which are sexual and capable of horizontal transmission, and most are vertically transmissible also. Asexual epichloae are mainly or exclusively vertically transmitted, and many are interspecific hybrids with genomic contributions from two or three ancestral Epichloë species. Here we employ genome-scale analyses to investigate the origins of biosynthesis gene clusters for ergot alkaloids (EAS), indole-diterpenes (IDT), and lolines (LOL) in 12 hybrid species. In each hybrid, the alkaloid-gene and housekeeping-gene relationships were congruent. Interestingly, hybrids frequently had alkaloid clusters that were rare in their sexual ancestors. Also, in those hybrids that had multiple EAS, IDT or LOL clusters, one cluster lacked some genes, usually for late pathway steps. Possible implications of these findings for the alkaloid profiles and endophyte ecology are discussed.

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Figures

Figure 1
Figure 1
Structures and pathways for alkaloids produced by epichloae (adapted from [6]). Summaries of pathways are shown for indole-diterpenes (A), ergot alkaloids (B) and lolines (C) with structures of major forms of the alkaloids found in grasses symbiotic with epichloae. Panel (D) shows the structure of a fourth protective alkaloid, peramine, also produced by many epichloae.
Figure 2
Figure 2
Structures of the alkaloid biosynthesis gene clusters inNeotyphodium coenophialum e4163. Maps are color coded according to ancestral clade of origin (see Figure 3). The indole-diterpene (IDT) gene cluster was from clade II (E. festucae). Each gene in theIDT cluster (accession number KC970578) is designated by its final letter, whereK =idtK,etc. Two ergot-alkaloid gene clusters were identified, one from clade V (EAS1, accession number KC989569), and the other from clade II (EAS2, accession number KC989570). Genes in theEAS clusters are abbreviated as follows:A = easA,B = cloA,C = easC,D = easD,E = easE,F = easF,G = easG,H = easH. OtherEAS cluster gene names are given in full. The loline alkaloid (LOL, accession numbers KC990458, KC990457 and KC990459) gene cluster was from clade Ib (E. poae). Each gene in theLOL cluster is designated by its final letter, whereF =lolF,etc.
Figure 3
Figure 3
Phylogeny oftubB genes from all known haploid (non-hybrid) and ten hybrid epichloae. Where hybrids have multiple gene copies from different ancestral species, the different copies are indicated by symbols of the same shape with different colors. Phylogenetic clades contributing to hybrids are color coded and numbered Ia, Ib, II, III, IV, V, and VI. Supplementary Table S1 contains thetubB accession numbers.
Figure 4
Figure 4
Phylogeny of twoIDT genes,idtM andidtP in epichloae. Inactive genes (pseudogenes) are labeled ψ. Clades and multiple gene copies are labeled as in Figure 3. Supplementary Table S2 contains theIDT accession numbers.
Figure 5
Figure 5
Phylogeny of twoEAS genes,dmaW andcloA. Clades and multiple gene copies are labeled as in Figure 3. Supplementary Table S2 contains theEAS accession numbers.
Figure 6
Figure 6
Phylogeny of threeLOL genes,lolC,lolN, andlolP. Pseudogenes oflolC andlolP are labeledlolCψ andlolPψ, respectively. Clades and multiple gene copies are labeled as in Figure 3. ThelolN gene of FaTG-3 was not sequenced. Supplementary Table S2 contains theLOL accession numbers.
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References

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