Mining Indole Alkaloid Synthesis Gene Clusters from Genomes of 53 Claviceps Strains Revealed Redundant Gene Copies and an Approximate Evolutionary Hourglass Model

. 2021 Nov 13 ; 13 (11) : . [epub] 20211113

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid34822583

Ergot fungi (Claviceps spp.) are infamous for producing sclerotia containing a wide spectrum of ergot alkaloids (EA) toxic to humans and animals, making them nefarious villains in the agricultural and food industries, but also treasures for pharmaceuticals. In addition to three classes of EAs, several species also produce paspaline-derived indole diterpenes (IDT) that cause ataxia and staggers in livestock. Furthermore, two other types of alkaloids, i.e., loline (LOL) and peramine (PER), found in Epichloë spp., close relatives of Claviceps, have shown beneficial effects on host plants without evidence of toxicity to mammals. The gene clusters associated with the production of these alkaloids are known. We examined genomes of 53 strains of 19 Claviceps spp. to screen for these genes, aiming to understand the evolutionary patterns of these genes across the genus through phylogenetic and DNA polymorphism analyses. Our results showed (1) varied numbers of eas genes in C. sect. Claviceps and sect. Pusillae, none in sect. Citrinae, six idt/ltm genes in sect. Claviceps (except four in C. cyperi), zero to one partial (idtG) in sect. Pusillae, and four in sect. Citrinae, (2) two to three copies of dmaW, easE, easF, idt/ltmB, itd/ltmQ in sect. Claviceps, (3) frequent gene gains and losses, and (4) an evolutionary hourglass pattern in the intra-specific eas gene diversity and divergence in C. purpurea.

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Tenberge K.B. Biology and life strategy of the ergot fungi. In: Kren V., Cvak L., editors. Ergot: The Genus Claviceps. Hardwood Academic Publishers (republished 2006 by Taylor and Francise e-Library); Amsterdam, The Netherlands: 1999. pp. 25–56.

Luttrell E.S. Host-parasite relationships and development of the ergot sclerotium in Claviceps purpurea. Can. J. Bot. 1980;58:942–958. doi: 10.1139/b80-118. DOI

Píchová K., Pažoutová S., Kostovčík M., Chudíčková M., Stodůlková E., Novák P., Flieger M., van der Linde E., Kolařík M. Evolutionary history of ergot with a new infrageneric classification (Hypocreales: Clavicipitaceae: Claviceps) Mol. Phylogenetics Evol. 2018;123:73–87. doi: 10.1016/j.ympev.2018.02.013. PubMed DOI

Liu M., Overy D.P., Cayouette J., Shoukouhi P., Hicks C., Bisson K., Sproule A., Wyka S.A., Broders K., Popovic Z., et al. Four phylogenetic species of ergot from Canada and their characteristics in morphology, alkaloid production, and pathogenicity. Mycologia. 2020;112:974–988. doi: 10.1080/00275514.2020.1797372. PubMed DOI

Campbell W.P., Freisen H.A. The control of ergot in cereal crops. Plant Dis. Rep. 1959;43:1266–1267.

European Food Safety Authority Scientific opinion on ergot allkaloids in food and feed. EFSA J. 2012;10:2798.

Tfelt-Hansen P., Saxena P.R., Dahlöf C., Pascual J., Láinez M., Henry P., Diener H.-C., Schoenen J., Ferrari M.D., Goadsby P.J. Ergotamine in the acute treatment of migraine: A review and European consensus. Brain. 2000;123:9–18. doi: 10.1093/brain/123.1.9. PubMed DOI

Schiff P.L., Jr. Ergot and its alkaloids. Am. J. Pharm. Educ. 2006;70:98. doi: 10.5688/aj700598. PubMed DOI PMC

Barger G. Ergot and Ergotism: A Monograph Based on the Dohme Lecture Delivered in Johns Hopkins University, Baltimore. Gurney and Jackson; London, UK: 1931.

Belser-Ehrlich S., Harper A., Hussey J., Hallock R. Human and cattle ergotism since 1900: Symptoms, outbreaks, and regulations. Toxicol. Ind. Health. 2013;29:307–316. doi: 10.1177/0748233711432570. PubMed DOI

Schardl C.L., Panaccione D.G., Tudzynski P., Geoffrey A.C. The Alkaloids: Chemistry and Biology. Volume 63. Academic Press; Cambridge, MA, USA: 2006. Ergot alkaloids—Biology and molecular biology; pp. 45–86. PubMed

Tudzynski P., Holter K., Correia T., Arntz C., Grammel N., Keller U. Evidence for an ergot alkaloid gene cluster in Claviceps purpurea. Mol. Gen. Genet. 1999;261:133–141. doi: 10.1007/s004380050950. PubMed DOI

Young C.A., Schardl C.L., Panaccione D.G., Florea S., Takach J.E., Charlton N.D., Moore N., Webb J.S., Jaromczyk J. Genetics, genomics and evolution of ergot alkaloid diversity. Toxins. 2015;7:1273–1302. doi: 10.3390/toxins7041273. PubMed DOI PMC

Schardl C.L., Young C.A., Hesse U., Amyotte S.G., Andreeva K., Calie P.J., Fleetwood D.J., Haws D.C., Moore N., Oeser B., et al. Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet. 2013;9:e1003323. doi: 10.1371/journal.pgen.1003323. PubMed DOI PMC

Robinson S.L., Panaccione D.G. Diversification of ergot alkaloids in natural and modified fungi. Toxins. 2015;7:201–218. doi: 10.3390/toxins7010201. PubMed DOI PMC

Knaus H.G., McManus O.B., Lee S.H., Schmalhofer W.A., Garcia-Calvo M., Helms L.M., Sanchez M., Giangiacomo K., Reuben J.P., Smith A.B., 3rd, et al. Tremorgenic indole alkaloids potently inhibit smooth muscle high-conductance calcium-activated potassium channels. Biochemistry. 1994;33:5819–5828. doi: 10.1021/bi00185a021. PubMed DOI

Smith M.M., Warren V.A., Thomas B.S., Brochu R.M., Ertel E.A., Rohrer S., Schaeffer J., Schmatz D., Petuch B.R., Tang Y.S., et al. Nodulisporic acid opens insect glutamate-gated chloride channels: Identification of a new high affinity modulator. Biochemistry. 2000;39:5543–5554. doi: 10.1021/bi992943i. PubMed DOI

Turland N.J., Wiersema J.H., Barrie F.R., Greuter W., Hawksworth D.L., Herendeen P.S., Knapp S., Kusber W.-H., Li D.-Z., Marhold K. International Code of Nomenclature for Algae, Fungi, and Plants (Shenzhen Code) Adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Regnum Vegetabile 159. Volume 159 Koeltz Botanical Books; Glashütten, Germany: 2018.

Botha C.J., Kellerman T.S., Fourie N. A tremorgenic mycotoxicosis in cattle caused by Paspalum distichum (L.) infected by Claviceps paspali. J. S. Afr. Vet. Assoc. 1996;67:36–37. PubMed

Prestidge R.A. Causes and control of perennial ryegrass staggers in New Zealand. Agric. Ecosyst. Environ. 1993;44:283–300. doi: 10.1016/0167-8809(93)90051-P. DOI

Uhlig S., Botha C.J., Vrålstad T., Rolén E., Miles C.O. Indole−diterpenes and ergot alkaloids in Cynodon dactylon (bermuda grass) infected with Claviceps cynodontis from an outbreak of tremors in cattle. J. Agric. Food Chem. 2009;57:11112–11119. doi: 10.1021/jf902208w. PubMed DOI

Kozák L., Szilágyi Z., Tóth L., Pócsi I., Molnár I. Functional characterization of the idtF and idtP genes in the Claviceps paspali indole diterpene biosynthetic gene cluster. Folia Microbiol. 2020;65:605–613. doi: 10.1007/s12223-020-00777-6. PubMed DOI PMC

Saikia S., Takemoto D., Tapper B.A., Lane G.A., Fraser K., Scott B. Functional analysis of an indole-diterpene gene cluster for lolitrem B biosynthesis in the grass endosymbiont Epichloë festucae. FEBS Lett. 2012;586:2563–2569. doi: 10.1016/j.febslet.2012.06.035. PubMed DOI

Young C.A., Bryant M.K., Christensen M.J., Tapper B.A., Bryan G.T., Scott B. Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass. Mol. Genet. Genom. MGG. 2005;274:13–29. doi: 10.1007/s00438-005-1130-0. PubMed DOI

Young C.A., Felitti S., Shields K., Spangenberg G., Johnson R.D., Bryan G.T., Saikia S., Scott B. A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Neotyphodium lolii. Fungal Genet. Biol. 2006;43:679–693. doi: 10.1016/j.fgb.2006.04.004. PubMed DOI

Young C.A., Tapper B.A., May K., Moon C.D., Schardl C.L., Scott B. Indole-diterpene biosynthetic capability of Epichloë endophytes as predicted by ltm gene analysis. Appl. Environ. Microbiol. 2009;75:2200–2211. doi: 10.1128/AEM.00953-08. PubMed DOI PMC

Jiang Y., Ozaki T., Harada M., Miyasaka T., Sato H., Miyamoto K., Kanazawa J., Liu C., Maruyama J.-I., Adachi M., et al. Biosynthesis of indole diterpene lolitrems: Radical-induced cyclization of an epoxyalcohol affording a characteristic lolitremane skeleton. Angew. Chem. Int. Ed. 2020;59:17996–18002. doi: 10.1002/anie.202007280. PubMed DOI

Uhlig S., Egge-Jacobsen W., Vrålstad T., Miles C.O. Indole-diterpenoid profiles of Claviceps paspali and Claviceps purpurea from high-resolution Fourier transform Orbitrap mass spectrometry. Rapid Commun. Mass Spectrom. RCM. 2014;28:1621–1634. doi: 10.1002/rcm.6938. PubMed DOI

Negård M., Uhlig S., Kauserud H., Andersen T., Høiland K., Vrålstad T. Links between genetic groups, indole alkaloid profiles and ecology within the grass-parasitic Claviceps purpurea species complex. Toxins. 2015;7:1431–1456. doi: 10.3390/toxins7051431. PubMed DOI PMC

Uhlig S., Rangel-Huerta O.D., Divon H.H., Rolén E., Pauchon K., Sumarah M.W., Vrålstad T., Renaud J.B. Unraveling the ergot alkaloid and indole diterpenoid metabolome in the Claviceps purpurea species complex using lc–hrms/ms diagnostic fragmentation filtering. J. Agric. Food Chem. 2021;69:7137–7148. doi: 10.1021/acs.jafc.1c01973. PubMed DOI

Schardl C.L., Grossman R.B., Nagabhyru P., Faulkner J.R., Mallik U.P. Loline alkaloids: Currencies of mutualism. Phytochemistry. 2007;68:980–996. doi: 10.1016/j.phytochem.2007.01.010. PubMed DOI

Tanaka A., Tapper B.A., Popay A., Parker E.J., Scott B. A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol. Microbiol. 2005;57:1036–1050. doi: 10.1111/j.1365-2958.2005.04747.x. PubMed DOI

Duboule D. Temporal colinearity and the phylotypic progression: A basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Development. 1994;1994:135–142. doi: 10.1242/dev.1994.Supplement.135. PubMed DOI

Slack J.M.W., Holland P.W.H., Graham C.F. The zootype and the phylotypic stage. Nature. 1993;361:490–492. doi: 10.1038/361490a0. PubMed DOI

Von Baer K.E. Über Entwickelungsgeschichte der Thiere: Beobachtung und Reflexion. Volume 1 Bei den gebrüdern Bornträger; Königsberg, Russia: 1828.

Richardson M.K. Vertebrate evolution: The developmental origins of adult variation. Bioessays. 1999;21:604–613. doi: 10.1002/(SICI)1521-1878(199907)21:7<604::AID-BIES9>3.0.CO;2-U. PubMed DOI

Poe S., Wake M.H. Quantitative tests of general models for the evolution of development. Am. Nat. 2004;164:415–422. doi: 10.1086/422658. PubMed DOI

Cheng X., Hui J.H., Lee Y.Y., Wan Law P.T., Kwan H.S. A “developmental hourglass in fungi”. Mol. Biol. Evol. 2015;32:1556–1566. doi: 10.1093/molbev/msv047. PubMed DOI

Prud‘homme B., Gompel N. Genomic hourglass. Nature. 2010;468:768–769. doi: 10.1038/468768a. PubMed DOI

Quint M., Drost H.-G., Gabel A., Ullrich K.K., Bönn M., Grosse I. A transcriptomic hourglass in plant embryogenesis. Nature. 2012;490:98–101. doi: 10.1038/nature11394. PubMed DOI

Haeckel E. Generelle Morphologie der Organismen. Allgemeine Grundzüge der Organischen Formen-Wissenschaft, Mechanisch Begründet Durch Die von Charles Darwin Reformirte Descendenztheorie. Volume 1 G. Reimer; Berlin, Germany: 1866.

Gould S.J. Ontogeny and Phylogeny. Harvard University Press; Cambridge, MA, USA: 1985.

Cruickshank T., Wade M.J. Microevolutionary support for a developmental hourglass: Gene expression patterns shape sequence variation and divergence in Drosophila. Evol. Dev. 2008;10:583–590. doi: 10.1111/j.1525-142X.2008.00273.x. PubMed DOI

Wyka S.A., Mondo S.J., Liu M., Dettman J., Nalam V., Broders K.D. Whole-genome comparisons of ergot fungi reveals the divergence and evolution of species within the genus Claviceps are the result of varying mechanisms driving genome evolution and host range expansion. Genome Biol. Evol. 2021;13:evaa267. doi: 10.1093/gbe/evaa267. PubMed DOI PMC

Wingfield B.D., Liu M., Nguyen H.D.T., Lane F.A., Morgan S.W., De Vos L., Wilken P.M., Duong T.A., Aylward J., Coetzee M.P.A., et al. Nine draft genome sequences of Claviceps purpurea s.lat., including C. arundinis, C. humidiphila, and C. cf. spartinae, pseudomolecules for the pitch canker pathogen Fusarium circinatum, draft genome of Davidsoniella eucalypti, Grosmannia galeiformis, Quambalaria eucalypti, and Teratosphaeria destructans. IMA Fungus. 2018;9:401–418. doi: 10.5598/imafungus.2018.09.02.10. PubMed DOI PMC

Flieger M., Wurst M., Shelby R. Ergot alkaloids--sources, structures and analytical methods. Folia Microbiol. 1997;42:3–29. doi: 10.1007/BF02898641. PubMed DOI

Tanda S. Mycological studies on ergot in Japan (Part 9). Distinct variety of Claviceps purpurea Tul. on Phalaris arundinacea L. and P. arundinacea var. picta L. J. Agric. Sci. Tokyo Nogyo Daigaku. 1979;24:67–95.

Pažoutová S., Parbery D.P. The taxonomy and phylogeny of Claviceps. In: Kren V., Cvak L., editors. Ergot: The Genus Claviceps. Hardwood Academic Publishers (republished 2006 by Taylor and Francise e-Library); Amsterdam, The Netherlands: 1999. pp. 57–77.

Pažoutová S., Olsovská J., Linka M., Kolínská R., Flieger M. Chemoraces and habitat specialization of Claviceps purpurea populations. Appl. Envron. Microbiol. 2000;66:5419–5425. doi: 10.1128/AEM.66.12.5419-5425.2000. PubMed DOI PMC

Tudzynski P., Correia T., Keller U. Biotechnology and genetics of ergot alkaloids. Appl. Microbiol. Biotechnol. 2001;57:593–605. doi: 10.1007/s002530100801. PubMed DOI

Liu M., Panaccione D.G., Schardl C.L. Phylogenetic analyses reveal monophyletic origin of the ergot alkaloid gene dmaW in fungi. Evol. Bioinform. 2009;5:EBO–S2633. doi: 10.4137/EBO.S2633. PubMed DOI PMC

Rokas A., Wisecaver J.H., Lind A.L. The birth, evolution and death of metabolic gene clusters in fungi. Nat. Rev. Microbiol. 2018;16:731–744. doi: 10.1038/s41579-018-0075-3. PubMed DOI

Lorenz N., Haarmann T., Pazoutová S., Jung M., Tudzynski P. The ergot alkaloid gene cluster: Functional analyses and evolutionary aspects. Phytochemistry. 2009;70:1822–1832. doi: 10.1016/j.phytochem.2009.05.023. PubMed DOI

Raff R.A. The Shape of Life: Genes, Development, and the Evolution of Animal Form. University of Chicago Press; Chicago, IL, USA: 2012.

Galis F., van Dooren T.J., Metz J.A. Conservation of the segmented germband stage: Robustness or pleiotropy? Trends Genet. TIG. 2002;18:504–509. doi: 10.1016/S0168-9525(02)02739-7. PubMed DOI

Schlosser G., Wagner G.P. Modularity in Development and Evolution. University of Chicago Press; Chicago, IL, USA: 2004.

Panaccione D.G. Origins and significance of ergot alkaloid diversity in fungi. FEMS Microbiol. Lett. 2005;251:9–17. doi: 10.1016/j.femsle.2005.07.039. PubMed DOI

Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–595. doi: 10.1093/genetics/123.3.585. PubMed DOI PMC

Liu M., Shoukouhi P., Bisson K.R., Wyka S.A., Broders K.D., Menzies J.G. Sympatric divergence of the ergot fungus, Claviceps purpurea, populations infecting agricultural and nonagricultural grasses in North America. Ecol. Evol. 2021;11:273–293. doi: 10.1002/ece3.7028. PubMed DOI PMC

Bankevich A., Nurk S., Antipov D., Gurevich A.A., Dvorkin M., Kulikov A.S., Lesin V.M., Nikolenko S.I., Pham S., Prjibelski A.D., et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 2012;19:455–477. doi: 10.1089/cmb.2012.0021. PubMed DOI PMC

Gurevich A., Saveliev V., Vyahhi N., Tesler G. QUAST: Quality assessment tool for genome assemblies. Bioinformatics. 2013;29:1072–1075. doi: 10.1093/bioinformatics/btt086. PubMed DOI PMC

Simão F.A., Waterhouse R.M., Ioannidis P., Kriventseva E.V., Zdobnov E.M. BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–3212. doi: 10.1093/bioinformatics/btv351. PubMed DOI

Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI

Rozas J., Ferrer-Mata A., Sanchez-DelBarrio J.C., Guirao-Rico S., Librado P., Ramos-Onsins S.E., Sanchez-Gracia A. DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. Mol. Biol. Evol. 2017;34:3299–3302. doi: 10.1093/molbev/msx248. PubMed DOI

Deng W., Maust B.S., Nickle D.C., Learn G.H., Liu Y., Heath L., Kosakovsky Pond S.L., Mullins J.I. DIVEIN: A web server to analyze phylogenies, sequence divergence, diversity, and informative sites. Biotechniques. 2010;48:405–408. doi: 10.2144/000113370. PubMed DOI PMC

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