PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

doi: 10.15389/agrobiology.2022.5.852eng

UDC: 632.4.01/.08:579.64:577

Acknowledgements:
The work was done within the framework of topic 10.6. Plant protection and biotechnology (FGUU-2022-0014)

 

ERGOT Claviceps purpurea (Fries) Tulasne ALKALOID DIVERSITY AND VIRULENCE: EVOLUTION, GENETIC DIVERSIFICATION, AND METABOLIC ENGINEERING (review)

A.A. Volnin, P.S. Savin

All-Russian Research Institute of Medicinal and Aromatic Plants, 7, ul. Grina, Moscow, 117216 Russia, e-mail volnin@vilarnii.ru (✉ corresponding author), savin@vilarnii.ru

ORCID:
Volnin A.A. orcid.org/000000019222536X
Savin P.S. orcid.org/0000000254413471

Received June 7, 2022

Claviceps purpurea (Fries) Tulasne is a valuable source of many bioactive metabolites (alkaloids) for pharmaceutical industry and a unique plant—parasite model but also a serious adversary for plant growing, feed and livestock industries causing significant economic damage in different countries. Ergot appeared in South America in the Paleocene, the age of the genus Claviceps is 20.4 million years (K. Píchová et al., 2018). Intraspecific diversity and divergence of indole alkaloid production gene cluster occurred in accordance with the evolutionary “hourglass model” (M. Liu et al., 2021). Ergometrine, ergosine, ergotamine, a-ergocryptine, ergocornine, ergocristine and 8-S(-inine-) epimers are the major identified ergoalkaloids which account for approximately 50 % of the ergot alkaloid metabolome. Claviceps alkaloid gene clusters consist of varying numbers of genes, posses two or three copies of dmaW, easE, easF genes, and there are many facts of frequent gene loss and acquisition (M. Liu et al., 2021). Differences in metabolomic profiles of C. purpurea indole alkaloids correlate with the lpsA gene variability. Diversity of the ergot alkaloids is a result of sequence diversity in the easH/lpsA tandem-duplicated region (C. Hicks et al., 2021). The lpsA1 and lpsA2 genes derived from recombination events (S. Wyka et al., 2022), i.e., the lpsA genes are supposed to be due to reshuffling (C. Hicks et al., 2021). C. purpurea has a relatively large accessory genome (~ 38 %), high recombination rates (ρ = 0.044), and transposon-mediated gene duplication (S. Wyka et al., 2022). A transgenic yeast line is capable of producing enantiopure D-lysergic acid up to a level of 1.7 mg/l (G. Wong et al., 2022). Genetically engineered cultures of Metarhizium brunneum can produce 86.9 % lysergic acid and 72.8% dihydrolysirgic acid (K. Davis et al., 2020). Expression of the trpE and dmaW genes is quantitatively related to intensity of alkaloid synthesis in saprophytic Claviceps cultures (M. Králová et al., 2021). Pectin is the main target of CAZymes proteins responsible for cell wall degradation during C. purpurea and C. paspali infection (B. Oeser et al., 2017; H. Oberti et al., 2021). Polygalacturonase, MAP kinase, transcription factor CPTF1 (Cptf1 gene), GTPase (Cdc42 gene) make the main contribution to Claviceps virulence (B. Oeser et al., 2017; E. Tente et al., 2021). Ergot affects the auxin, ethylene, and cytokinin pathways in plants, with varying effects depending on tissue type and time after inoculation (E. Tente, 2020; Tente et al., 2021). Wheat resistance is due to mutations in DELLA proteins (E. Tente, 2020; A. Gordon et al., 2020) while rye resistance is due to pectinesterase activity, cell wall modification, and modulation of pollen tube growth (COBRA-like protein and pectinesterase inhibitor) (K. Mahmood et al., 2020).

Keywords: Claviceps purpurea, ergot, alkaloids, biosynthesis pathways, toxicity, virulence, genotype, gene clusters, Claviceps, C. purpurea.

 

REFERENCES

  1. Jamieson C.S., Misa J., Tang Y., Billingsley J.M. Biosynthesis and synthetic biology of psychoactive natural products. Chemical Society Reviews, 2021, 50(12): 6950-7008 CrossRef
  2. Rämä T., Quandt C.A. Improving fungal cultivability for natural products discovery. Frontires in Microbiology, 2021, 12: 706044 CrossRef
  3. Liu H., Jia Y. Ergot alkaloids: synthetic approaches to lysergic acid and clavine alkaloids. Natural Product Reports, 2017, 34(4): 411-432 CrossRef
  4. Gerhards N., Matuschek M., Wallwey C., Li S.M. Genome mining of ascomycetous fungi reveals their genetic potential for ergot alkaloid production. Archives Microbiology, 2015, 197(5): 701-713 CrossRef
  5. Chan J.D., Agbedanu P.N., Grab T., Zamanian M., Dosa P.I., Day T.A., Marchant J.S. Ergot Alkaloids (re)generate new leads as antiparasitics. PLoS Neglected Tropical Diseases, 2015, 9(9): e0004063 CrossRef
  6. Smakosz A., Kurzyna W., Rudko M., Dąsal M. The usage of ergot (Claviceps purpurea (Fr.) Tul.) in obstetrics and gynecology: a historical perspective. Toxins, 2021, 13(7): 492 CrossRef
  7. Králová M., Bergougnoux V., Frébort I., CRISPR/Cas9 genome editing in ergot fungus Claviceps purpurea. Journal of Biotechnology, 2021, 325: 341-354 CrossRef
  8. Králová M., Frébortová J., Pěnčík A., Frébort I. Overexpression of Trp-related genes in Claviceps purpurea leading to increased ergot alkaloid production. New Biotechnology, 2021, 61: 69-79 CrossRef
  9. Wong G., Lim L.R., Tan Y.Q., Go M.K., Bell D.J., Freemont P.S., Yew W.S. Reconstituting the complete biosynthesis of D-lysergic acid in yeast. Nature Communication, 2022, 13(1): 712 CrossRef
  10. Lieberman A., Kupersmith M., Estey E., Goldstein M. Treatment of Parkinson’s disease with bromocriptine. New England Journal of Medicine, 1976, 295(25): 1400-1404 CrossRef
  11. Winblad B., Fioravanti M., Dolezal T., Logina I., Milanov I.G., Popescu D.C., Solomon A. Therapeutic use of nicergoline. Clinical Drug Investigation, 2008, 28(9): 533-552 CrossRef
  12. Tandowsky R.M. Clinical evaluation of combined hydrogenated ergot alkaloids (hydergine) in arterial hypertension: with special reference to their action in central manifestations. Circulation, 1954, 9(1): 48-56 CrossRef
  13. Johnson J.W., Ellis M.J., Piquette Z.A., MacNair C., Carfrae L., Bhando T., Ritchie N.E., Saliba P., Brown E.D., Magolan J. Antibacterial activity of metergoline analogues: revisiting the ergot alkaloid scaffold for antibiotic discovery. ACS Medicinal Chemistry Letters, 2022, 13(2): 284-291 CrossRef
  14. Fitopreparaty VILAR: nauchno-spravochnoe izdanie /Pod redaktsiey T.A. Sokol’skoy [Herbal medicines VILAR: scientific reference edition. T.A. Sokol’skaya (ed.)]. Moscow, 2009 (in Russ.).
  15. Savina T.A., Savin P.S., Bobyleva R.I. Voprosy biologicheskoy, meditsinskoy i farmatsevticheskoy khimii, 2018, 21(12): 28-34 CrossRef (in Russ.).
  16. Bobyleva R.I., Savin P.S. Voprosy biologicheskoy, meditsinskoy i farmatsevticheskoy khimii, 2019, 22(10): 30-36 CrossRef (in Russ.).
  17. Bobyleva R.I., Savin P.S. Voprosy biologicheskoy, meditsinskoy i farmatsevticheskoy khimii, 2021, 24(12): 57-62 CrossRef (in Russ.).
  18. Franzmann C., Schröder J., Mϋnzing K., Wolf K., Lindhauer M.G., Humpf H. Distribution of ergot alkaloids and ricinoleic acid in different milling fractions. Mycotoxin Research, 2011, 27(1): 13-21 CrossRef
  19. Menzies J.G., Turkington T.K. An overview of the ergot (Claviceps purpurea) issue in western Canada: challenges and solutions. Canadian Journal of Plant Pathology, 2015, 37(1): 40-51 CrossRef
  20. Klotz J.L. Activities and effects of ergot alkaloids on livestock physiology and production. Toxins, 2015, 7(8): 2801-2821 CrossRef
  21. Klotz J.L., Nicol A.M. Ergovaline, an endophytic alkaloid. 1. Animal physiology and metabolism. Animal Production Science, 2016, 56: 1761-1774 CrossRef
  22. Reddy P., Hemsworth J., Guthridge K.M., Vinh A., Vassiliadis S., Ezernieks V., Spangenberg G.C., Rochfort S.J. Ergot alkaloid mycotoxins: physiological effects, metabolism and distribution of the residual toxin in mice. Scientific Reports, 2020, 10(1): 9714 CrossRef
  23. Bauermeister A., Aguiar F., Marques L., Malta J., Barros F., Callejon D., Lopes N. In vitro metabolism evaluation of the ergot alkaloid dihydroergotamine: application of microsomal and biomimetic oxidative model. Planta Medica, 2016, 82(15): 1368-1373 CrossRef
  24. Lünne F., Niehaus E.-M., Lipinski S., Kunigkeit J., Kalinina S. A., Humpf H.-U. Identification of the polyketide synthase PKS7 responsible for the production of lecanoric acid and ethyl lecanorate in Claviceps purpurea. Fungal Genetics and Biology, 2020, 145: 103481 CrossRef
  25. Flieger M., Stodůlková E., Wyka S.A., Černý J., Grobárová V., Píchová K., Novák P., Man P., Kuzma M., Cvak L., Broders K.D., Kolařík M. Ergochromes: heretofore neglected side of ergot toxicity. Toxins (Basel), 2019, 11(8): 439 CrossRef
  26. 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. Journal of Agricultural and Food Chemistry, 2009, 57(23): 11112-11119 CrossRef
  27. Kozák L., Szilágyi Z., Vágó B., Kakuk A., Tóth L., Molnár I., Pócsi I. Inactivation of the indole-diterpene biosynthetic gene cluster of Claviceps paspali by Agrobacterium-mediated gene replacement. Applied Microbiology and Biotechnology, 2018, 102(7): 3255-3266 CrossRef
  28. 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 Microbiologica, 2020, 65(3): 605-613 CrossRef
  29. Dopstadt J., Neubauer L., Tudzynski P., Humpf H.-U. The epipolythiodiketopiperazine gene cluster in Claviceps purpurea: dysfunctional cytochrome P450 enzyme prevents formation of the previously unknown clapurines. PLoS ONE, 2016, 11(7): e0158945 CrossRef
  30. Florea S., Panaccione D.G., Schardl C.L. Ergot alkaloids of the family Clavicipitaceae. Phytopathology, 2017, 107(5): 504-518 CrossRef
  31. Schwake-Anduschus C., Lorenz N., Lahrssen-Wiederholt M., Lauche A., Dänicke S. German monitoring 2012-2014: ergot of Claviceps purpurea and ergot alkaloids (EA) in feedingstuffs and their toxicological relevance for animal feeding.  Journal für Verbraucherschutz und Lebensmittelsicherheit, 2020, 15: 321-329 CrossRef
  32. Tente E. Investigations into the molecular interactions between Claviceps purpurea, the causal agent of ergot, and cereal hosts. Doctoral thesis, University of Cambridge, 2020 CrossRef
  33. Wallwey C., Li S. Ergot alkaloids: structure diversity, biosynthetic gene clusters and functional proof of biosynthetic genes. Natural Product Reports, 2011, 28(3): 496-510 CrossRef
  34. Robinson S.L., Panaccione D.G. Diversification of ergot alkaloids in natural and modified fungi. Toxins, 2015, 7: 201-218 CrossRef
  35. 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 (Basel), 2015, 7(4): 1273-1302 CrossRef
  36. Chen J., Han M., Gong T., Yang J., Zhu P. Recent progress in ergot alkaloid research. RSC Advances, 2017, 7(44): 27384-27396 CrossRef
  37. Tasker N.R., Wipf P. Biosynthesis, total synthesis, and biological profiles of ergot alkaloids. Alkaloids: Chemistry and Biology, 2021, 85: 1-112 CrossRef
  38. Hinsch J., Tudzynski P. Claviceps: the Ergot fungus. In: Molecular biology of food and water borne mycotoxigenic and mycotic fungi, 1st edn. R. Paterson, N.Lima (eds.). CRC Press, Boca Raton, 2015: 229-250.
  39. Miedaner T., Geiger H.H. Biology, genetics, and management of ergot (Claviceps spp.) in rye, sorghum, and pearl millet. Toxins (Basel), 2015, 7(3): 659-678 CrossRef
  40. Mantle P. Comparative ergot alkaloid elaboration by selected plectenchymatic mycelia of Claviceps purpurea through sequential cycles of axenic culture and plant parasitism. Biology (Basel), 2020, 9(3): 41 CrossRef
  41. 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.C., Martin P.A., Dadej K., De Beer Z.W., Findlay W., Havenga M., Kolařík M., Menzies J.G., Naidoo K., Pochopski O., Shoukouhi P., Santana Q.C., Seifert K.A., Soal N., Steenkamp E.T., Tatham C.T., van der Nest M.A., Wingfield M.J. 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(2): 401-418 CrossRef
  42. Wyka S., Mondo S., Liu M., Nalam V., Broders K. A large accessory genome and high recombination rates may influence global distribution and broad host range of the fungal plant pathogen Claviceps purpurea. PLoS ONE, 2022, 17(2): e0263496 CrossRef
  43. 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 Biology and Evolution, 2021, 13(2): evaa267 CrossRef
  44. Liu M., Findlay W., Dettman J., Wyka S.A., Broders K., Shoukouhi P., Dadej K., Kolařík M., Basnyat A., Menzies J.G. Mining indole alkaloid synthesis gene clusters from genomes of 53 Claviceps strains revealed redundant gene copies and an approximate evolutionary hourglass model. Toxins, 2021, 13(11): 799 CrossRef
  45. Hicks C., Witte T.E., Sproule A., Lee T., Shoukouhi P., Popovic Z., Menzies J.G., Boddy C.N., Liu M., Overy D.P. Evolution of the ergot alkaloid biosynthetic gene cluster results in divergent mycotoxin profiles in Claviceps purpurea Sclerotia. Toxins, 2021, 13(12): 861 CrossRef
  46. 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., Panaccione D.G., Schweri K.K., Voisey C.R., Farman M.L., Jaromczyk J.W., Roe B.A., O'Sullivan D.M., Scott B., Tudzynski P., An Z., Arnaoudova E.G., Bullock C.T., Charlton N.D., Chen L., Cox M., Dinkins R.D., Florea S., Glenn A.E., Gordon A., Güldener U., Harris D.R., Hollin W., Jaromczyk J., Johnson R.D., Khan A.K., 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 J.E., Tanaka E., Webb J.S., Wilson E.V., Wiseman J.L., Yoshida R., Zeng Z. Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the Slavicipitaceae reveals dynamics of alkaloid loci. PLoS Genetetics, 2013, 9(2): e1003323 CrossRef
  47. Oeser B., Kind S., Schurack S., Schmutzer T., Tudzynski P., Hinsch J. Cross-talk of the biotrophic pathogen Claviceps purpurea and its host Secale cereale. BMC Genomics, 2017, 18: 273 CrossRef
  48. Oberti H., Abreo E., Reyno R., Feijoo M., Murchio S., Dalla-Rizza M., Rokas A. New draft genome sequence of the ergot disease fungus Claviceps paspali. Microbiology Resource Announcements, 2020, 9(29): e00498-20 CrossRef
  49. Tente E., Ereful N., Rodriguez A.C., Grant P., O’Sullivan D.M., Boyd L.A., Gordon A. Reprogramming of the wheat transcriptome in response to infection with Claviceps purpurea, the causal agent of ergot. BMC Plant Biology, 2021, 21: 316 CrossRef
  50. 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). Molecular Phylogenetics and Evolution, 2018, 123: 73-87 CrossRef
  51. Bouchenak-Khelladi Y., Verboom G.A., Savolainen V., Hodkinson T.R. Biogeography of the grasses Poaceae: a phylogenetic approach toreveal evolutionary history in geographical space and geologicaltime. Botanical Journal of the Linnean Society, 2010, 162(4): 543-557 CrossRef
  52. Soreng R.J., Peterson P.M., Romaschenko K., Davidse G., Teisher J.K., Clark L.G., Barber P., Gillespie L.J., Zuloaga F.O. A worldwide phylogenetic classification of the Poaceae gramineae II: an update and a comparison of two 2015 classifications. Journal of Systematics and Evolution, 2017, 55(4): 259-290 CrossRef
  53. Pažoutová S., Pešicová K., Chudíčková M., Šrůtka P., Kolařík M. Delimitation of cryptic species inside Claviceps purpurea. Fungal Biology, 2015, 119(1): 7-26 CrossRef
  54. Liu M., Overy D.P., Cayouette J., Shoukouhi P., Hicks C., Bisson K., Sproule A., Wyka S.A., Broders K., Popovic Z., Menzies J.G. Four phylogenetic species of ergot from Canada and their characteristics in morphology, alkaloid production, and pathogenicity. Mycologia, 2020, 112(5): 974-988 CrossRef
  55. Oberti H., Dalla R.M., Reyno R., Murchio S., Altier N., Abreo E. Diversity of Claviceps paspali reveals unknown lineages and unique alkaloid genotypes. Mycologia, 2020, 112(2): 230-243 CrossRef
  56. Liu M., Tanaka E., Kolarik M. Neotypification of Claviceps humidiphila and recognition of C. bavariensis sp. nov. Mycotaxon, 2022, 137(1): 73-87 CrossRef
  57. Wyka S., Broders K. Population biology and comparative genomics of Claviceps purpurea and other defensive mutualists in the Hypocreales. In: Roster thesis of 2017 APS Annual Meeting, San Antonio, USA, 2017: 126 CrossRef
  58. 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. Ecology and Evolution, 2021, 11(1): 273-293 CrossRef
  59. Cheng Q., Frost K., Dung J.K.S. Population genetic structure of Claviceps purpurea in cool-season grass seed crops of Oregon. Phytopathology, 2020, 110(11): 1773-1778 CrossRef
  60. Dung J.K.S., Duringer J.M., Kaur N., Scott J.C., Frost K.E., Walenta D.L., Alderman S.C., Craig A.M., Hamm P.B. Molecular and alkaloid characterization of Claviceps purpurea sensu lato from grass seed production areas of the U.S. Pacific Northwest. Phytopathology, 2021, 111(5): 831-841 CrossRef
  61. Pažoutová S., Olšovská J., Linka M., Kolínská R., Flieger M. Chemoraces and habitat specialization of Claviceps purpurea populations. Applied and Environmental Microbiology, 2000, 66(12): 5419-5425 CrossRef
  62. Douhan G.W., Smith M.E., Huyrn K.L., Westbrook A., Beerli P., Fisher A.J. Multigene analysis suggests ecological speciation in the fungal pathogen Claviceps purpurea. Molecular Ecology, 2008, 17(9): 2276-2286 CrossRef
  63. Jungehülsing U., Tudzynski P. Analysis of genetic diversity in Claviceps purpurea by RAPD markers. Mycological Research, 1997, 101(1): 1-6 CrossRef
  64. Slack J.M.W., Holland P.W.H., Graham C.F. The zootype and the phylotypic stage. Nature,1993, 361(6412): 490-492 CrossRef
  65. 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 Supplement, 1994, 1994: 135-142 CrossRef
  66. Prud’homme B., Gompel N. Genomic hourglass. Nature, 2010, 468(7325): 768-769 CrossRef
  67. Galis F., van Dooren T.J., Metz J.A. Conservation of the segmented germband stage: Robustness or pleiotropy? Trends in Genetics, 2002, 18(10): 504-509 CrossRef
  68. Panaccione D.G. Origins and significance of ergot alkaloid diversity in fungi. FEMS Microbiology Letters, 2005, 251(1): 9-17 CrossRef
  69. Gilmore B.S., Alderman S.C., Knaus B.J., Bassil N.V., Martin R.C., Dombrowski J.E., Dung J.K.S. Simple sequence repeat markers that identify Claviceps species and strains. Fungal Biology and Biotechnology, 2016, 3(1): 1-13 CrossRef
  70. Shoukouhi P., Hicks C., Menzies J.G., Popovic Z., Chen W., Seifert K.A., Assabgui R., Liu M. Phylogeny of Canadian ergot fungi and a detection assay by real-time polymerase chain reaction. Mycologia, 2019, 111(3): 493-505 CrossRef
  71. 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. Journal of Agricultural and Food Chemistry, 2021, 69(25): 7137-7148 CrossRef
  72. Hulvová H., Galuszka P., Frébortová J., Frébort I. Parasitic fungus Claviceps as a source for biotechnological production of ergot alkaloids. Biotechnology Advances, 2013, 31(1): 79-89 CrossRef
  73. Yao Y., Wang W., Shi W., Yan R., Zhang J., Wei G., Liu L., Che Y., An C., Gao S., Overproduction of medicinal ergot alkaloids based on a fungal platform. Metabolic Engineering, 2022, 69: 198-208 CrossRef
  74. Hendrickson J.B., Wang J. A new synthesis of lysergic acid. Organic Letters, 2004, 6(1): 3-5 CrossRef
  75. Umezaki S., Yokoshima S., Fukuyama T. Total synthesis of lysergic acid. Organic Letters, 2013, 15(16): 4230-4233 CrossRef
  76. Majeská Čudejková M., Vojta P., Valík J., Galuszka P. Quantitative and qualitative transcriptome analysis of four industrial strains of Claviceps purpurea with respect to ergot alkaloid production. New Biotechnology, 2016, 33(5 Pt B): 743-754 CrossRef
  77. Fonin V.S., Sidyakina T.M., Shain S.S., Ozerskaya S.M., Pavlova E.F. Prikladnaya biokhimiya i mikrobiologiya, 1996, 32(4): 406-410 (in Russ.).
  78. Tonolo A., Scotti T., Vero-Barcellona L. Morphological observations on different species of Claviceps Tul. grown in submerged culture. Scientific Reports of the Istituto Superiore di Sanita, 1961, 1: 404-422.
  79. Mantle P.G., Tonolo A. Relationship between the morphology of Claviceps purpurea and the production of alkaloids. Transactions of the British Mycological Society, 1968, 51(3-4): 499-505 CrossRef
  80. Mantle P.G. Development of alkaloid production in vitro by a strain of Claviceps purpurea from Spartina townsendii. Transactions of the British Mycological Society, 1969, 52(3): 381-392 CrossRef
  81. Strnadová K. UV-Mutanten bei Claviceps purpurea. Planta Medica, 1964, 12(4): 521-527 CrossRef
  82. Křen V., Pažoutová S., Sedmera P., Rylko V., Řeháček Z. High-production mutant Claviceps purpurea 59 accumulating secoclavines. FEMS Microbiology Letters, 1986, 37(1): 31-34 CrossRef
  83. Smit R., Tudzynski P. Efficient transformation of Claviceps purpurea using pyrimidine auxotrophic mutants: cloning of the OMP decarboxylase gene. Molecular Genetics and Genomics, 1992, 234(2): 297-305 CrossRef
  84. Strnadová K. A method of preparation and application of nitrous acid as a mutagen in Claviceps purpurea. Folia Microbiologica, 1976, 21(6): 455-458 CrossRef
  85. Brauer K.L., Robbers J.E. Induced parasexual processes in Claviceps sp. strain SD58. Applied and Environmental Microbiology, 1987, 53(1): 70-73 CrossRef
  86. Davis K.A., Sampson J.K., Panaccione D.G. Genetic reprogramming of the ergot alkaloid pathway of Metarhizium brunneum. Applied and Environmental Microbiology, 2020, 86(19): e01251-20 CrossRef
  87. Yu L., Xiao M., Zhu Z., Wang Y., Zhou Z., Wang P., Zou G. Efficient genome editing in Claviceps purpurea using a CRISPR/Cas9 ribonucleoprotein method. Synthetic and Systems Biotechnology, 2022, 7(2): 664-670 CrossRef
  88. van Engelenburg F., Smit R., Goosen T, van den Broek H., Tudzynski P. Transformation of Claviceps purpurea using a bleomycin resistance gene. Applied Microbiology and Biotechnology,1989, 30: 364-370 CrossRef
  89. Winston F., Dollard C., Ricupero-Hovasse S.L. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast, 1995, 11(1): 53-55 CrossRef
  90. Colot H.V., Park G., Turner G.E., Ringelberg C., Crew C.M., Litvinkova L., Weiss R.L., Borkovich K.A., Dunlap J.C. A hight hroughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(27): 10352-10357 CrossRef
  91. Kouprina N., Larionov V. Transformation-associated recombination (TAR) cloning for genomics studies and synthetic biology. Chromosoma, 2016, 125(4): 621-632 CrossRef
  92. Crews C. Analysis of ergot alkaloids. Toxins (Basel), 2015, 7(6): 2024-2050 CrossRef
  93. Schummer C., Brune L., Moris G. Development of a UHPLC-FLD method for the analysis of ergot alkaloids and application to different types of cereals from Luxembourg. Mycotoxin Research, 2018, 34(4): 279-287 CrossRef
  94. Kuner M., Kühn S., Haase H., Meyer K., Koch M. Cleaving ergot alkaloids by hydrazinolysis — a promising approach for a sum parameter screening method. Toxins (Basel), 2021, 13(5): 342 CrossRef
  95. Kodisch A., Oberforster M., Raditschnig A., Rodemann B., Tratwal A., Danielewicz J., Korbas M., Schmiedchen B., Eifler J., Gordillo A., Siekmann D., Fromme F.J., Wuppermann F.N., Wieser F., Zechner E., Niewińska M., Miedaner T. Covariation of ergot severity and alkaloid content measured by HPLC and one ELISA Method in inoculated winter rye across three isolates and three European countries. Toxins, 2020, 12(11): 676 CrossRef
  96. Franzmann C., Wächter J., Dittmer N., Humpf H.-U. Ricinoleic acid as a marker for ergot impurities in rye and rye products. Journal of Agricultural and Food Chemistry, 2010, 58(7): 4223-4229 CrossRef
  97. Appelt M., Ellner F.M. Investigations into the occurrence of alkaloids in ergot and single sclerotia from the 2007 and 2008 harvests. Mycotoxin Research, 2009, 25(2): 95-101 CrossRef
  98. Miedaner T., Dänicke S., Schmiedchen B., Wilde P., Wortmann H., Dhillon B., Geiger H., Mirdita V. Genetic variation for ergot (Claviceps purpurea) resistance and alkaloid concentrations in cytoplasmic-male sterile winter rye under pollen isolation. Euphytica,2010, 173: 299-306 CrossRef
  99. Aboling S., Drotleff A., Cappai M., Kamphues J. Contamination with ergot bodies (Claviceps purpurea sensu lato) of two horse pastures in Northern Germany. Mycotoxin Research 2016, 32(4): 207-219 CrossRef
  100. Uhlig S., Vikøren T., Ivanova L., Handeland K. Ergot alkaloids in Norwegian wild grasses: A mass spectrometric approach. Rapid Communications in Mass Spectrometry, 2007, 21(10): 1651-1660 CrossRef
  101. Dopstadt J., Vens-Cappell S., Neubauer L., Tudzynski P., Cramer B., Dreisewerd K., Humpf H.-U. Localization of ergot alkaloids in sclerotia of Claviceps purpurea by matrix-assisted laser desorption/ionization mass spectrometry imaging. Analytical and Bioanalytical Chemistry, 2017, 409(5): 1221-1230 CrossRef
  102. Tudzynski P., Correia T., Keller U. Biotechnology and genetics of ergot alkaloids. Applied Microbiology and Biotechnology, 2001, 57(5-6): 593-605 CrossRef
  103. Haarmann T., Machado C., Lübbe Y., Correia T., Schardl C.L., Panaccione D.G., Tudzynski P. The ergot alkaloid gene cluster in Claviceps purpurea: extension of the cluster sequence and intra species evolution. Phytochemistry, 2005, 66(11): 1312-1320 CrossRef
  104. Ryan K.L., Akhmedov N.G., Panaccione D.G. Identification and structural elucidation of ergotryptamine, a new ergot alkaloid produced by genetically modified Aspergillus nidulans and natural isolates of Epichloe species. Journal of Agricultural and Food Chemistry, 2015, 63(1): 61-67 CrossRef
  105. Steen C.R., Sampson J.K., Panaccione D.G. A Baeyer-Villiger monooxygenase gene involved in the synthesis of lysergic acid amides affects the interaction of the fungus Metarhizium brunneum with insects. Applied and Environmental Microbiology, 2021, 87(17): e0074821 CrossRef
  106. Lorenz N., Wilson E.V., Machado C., Schardl C.L., Tudzynski P. Comparison of ergot alkaloid biosynthesis gene clusters in Claviceps Species indicates loss of late pathway steps in evolution of C. fusiformis. Applied and Environmental Microbiology, 2007, 73(22): 7185-7191 CrossRef
  107. Coyle C.M., Panaccione D.G. An ergot alkaloid biosynthesis gene and clustered hypothetical genes from Aspergillus fumigatus. Applied and Environmental Microbiology, 2005, 71(6): 3112-3118 CrossRef
  108. Coyle C.M., Cheng J.Z., O’Connor S.E., Panaccione D.G. An old yellow enzyme gene controls the branch point between Aspergillus fumigatus and Claviceps purpurea ergot alkaloid pathways. Applied and Environmental Microbiology, 2010, 76(12): 3898-3903 CrossRef
  109. Liu M., Panaccione D.G., Schardl C.L. Phylogenetic analyses reveal monophyletic origin of the ergot alkaloid gene dmaW in fungi. Evolutionary Bioinformatics, 2009, 5: 15-30 CrossRef
  110. Goetz K.E., Coyle C.M., Cheng J.Z., O”Connor S.E., Panaccione D.G. Ergot cluster-encoded catalase is required for synthesis of chanoclavine-I in Aspergillus fumigatus. Current Genetics, 2011, 57(3): 201-211 CrossRef
  111. Jones A.M., Steen C.R., Panaccione D.G. Independent evolution of a lysergic acid amide in Aspergillus species. Applied and Environmental Microbiology, 2021, 87(24): e01801-21 CrossRef
  112. Nielsen C.A., Folly C., Hatsch A., Molt A., Schröder H., O'Connor S.E., Naesby M. The important ergot alkaloid intermediate chanoclavine-I produced in the yeast Saccharomyces cerevisiae by the combined action of EasC and EasE from Aspergillus japonicus. Microbial Cell Factories, 2014, 13(1): 95 CrossRef
  113. An C., Zhu F., Yao Y., Zhang K., Wang W., Zhang J., Wei G., Xia Y., Gao Q., Gao S. Beyond the cyclopropyl ring formation: fungal Aj_EasH catalyzes asymmetric hydroxylation of ergot alkaloids. Applied Microbiology and Biotechnology, 2022, 106(8): 2981-2991 CrossRef
  114. Jakubczyk D., Cheng J.Z., O’Connor S.E. Biosynthesis of the ergot alkaloids. Natural Product Reports, 2014, 31(10): 1328-1338 CrossRef
  115. Wallwey C., Heddergott C., Xie X., Brakhage A.A., Li S. Genome mining reveals the presence of a conserved gene cluster for the biosynthesis of ergot alkaloid precursors in the fungal family Arthrodermataceae. Microbiology (Reading), 2012, 158(Pt 6): 1634-1644 CrossRef
  116. Fabian S.J., Maust M.D., Panaccione D.G. Ergot alkaloid synthetic capacity of Penicillium camemberti. Applied and Environmental Microbiology, 2018, 84(191): e01583-18 CrossRef
  117. Pertz H., Eich E. Ergot alkaloids and their derivatives as ligands for serotoninergic, dopaminergic, and adrenergic receptors.In: Ergot: the genus Claviceps. V. Kren, L. Cvak (eds.). Amsterdam, Harwood Academic Publishers, 1999: 411-440.
  118. Mantegani S., Brambilla E., Varasi M. Ergoline derivatives: receptor affinity and selectivity. Farmaco, 1999, 54(5): 288-296 CrossRef
  119. 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(5): 1431-1456 CrossRef
  120. Uhlig S., Petersen D. Lactam ergot alkaloids (ergopeptams) as predominant alkaloids in sclerotia of Claviceps purpurea from Norwegian wild grasses. Toxicon, 2008, 52(1): 175-185 CrossRef
  121. Cheng J.Z., Coyle C.M., Panaccione D.G., O’Connor S.E. Controlling a structural branch point in ergot alkaloid biosynthesis. Journal of the American Chemical Society, 2010, 132(37): 12835-12837 CrossRef
  122. Wei X., Wang W.G., Matsuda Y. Branching and converging pathways in fungal natural product biosynthesis. Fungal Biology and Biotechnology, 2022, 9: 6 CrossRef
  123. Jakubczyk D., Caputi L., Hatsch A., Nielsen C.A.F., Diefenbacher M., Klein J., Molt A., Schröder H., Cheng J.Z., Naesby M., O’Connor S.E. Discovery and reconstitution of the cycloclavine biosynthetic pathway-enzymatic formation of a cyclopropyl group. Angewandte Chemie International Edition, 2015, 54(17): 5117-5121 CrossRef
  124. Hütter R., DeMoss J.A. Organization of the tryptophan pathway: a phylogenetic study of the fungi. Journal of Bacteriology, 1967, 94(6): 1896-1907 CrossRef
  125. Hütter R., Niederberger P., DeMoss J.A. Tryptophan biosynthetic genes in eukaryotic microorganisms. Annual Review of Microbiology, 1986, 40: 55-77 CrossRef
  126. Crawford I.P., Eberly L. Structure and regulation of the anthranilate synthase genes in Pseudomonas aeruginosa: I. Sequence of trpG encoding the glutamine amidotransferase subunit. Molecular Biology and Evolution, 1986, 3(5): 436-448 CrossRef
  127. Metzger U., Schall C., Zocher G., Unsöld I., Stec E., Li S.M., Heide L., Stehle T. The structure of dimethylallyl tryptophan synthase reveals a common architecture of aromatic prenyltransferases in fungi and bacteria. Proceedings of the National Academy of Sciences, 2009, 106(34): 14309-14314 CrossRef
  128. Ruijter G.J., Visser J. Carbon repression in Aspergilli. FEMS Microbiology Letters, 1997, 151(2): 103-114 CrossRef
  129. Arst H.N., Cove D.J. Nitrogen metabolite repression in Aspergillus nidulans. Molecular Genetics and Genomics, 1973, 126: 111-141 CrossRef
  130. Bignell E., Negrete-Urtasun S., Calcagno A.M., Haynes K., Arst Jr H.N., Rogers T. The Aspergillus pH-responsive transcription factor PacC regulates virulence. Molecular Microbiology, 2005, 55(4): 1072-1084 CrossRef
  131. Kang S., Metzenberg R.L. Molecular analysis of nuc-1+, a gene controlling phosphorus acquisition in Neurospora crassa. Molecular and Cellular Biology, 1990, 10(11): 5839-5848 CrossRef
  132. Otsuka H., Quigley F.R., Gröger J., Anderson A., Floss H.G. In vivo and in vitro evidence for N-methylation as the pathway specific step in ergoline biosynthesis. Planta Medica, 1980, 40(10): 109-119 CrossRef
  133. Yao Y., An C., Evans D., Liu W., Wang W., Wei G., Ding N., Houk K.N., Gao S. Catalase involved in oxidative cyclization of the tetracyclic ergoline of fungal ergot alkaloids. Journal of the American Chemical Society, 2019, 141(44): 17517-17521 CrossRef
  134. Wallwey C., Matuschek M., Li S. Ergot alkaloid biosynthesis in Aspergillus fumigatus: conversion of chanoclavine-I to chanoclavine-I aldehyde catalyzed by a short-chain alcohol dehydrogenase FgaDH. Archives of Microbiology, 2010, 192(2): 127-134 CrossRef
  135. Arnold S.L., Panaccione D.G. Biosynthesis of the pharmaceutically important fungal ergot alkaloid dihydrolysergic acid requires a specialized allele of cloA. Applied and Environmental Microbiology, 2017, 83(14): e00805-17 CrossRef
  136. Robinson S.L., Panaccione D.G. Heterologous expression of lysergic acid and novel ergot alkaloids in Aspergillus fumigatus. Applied and Environmental Microbiology, 2014, 80(20): 6465-6472 CrossRef
  137. Haarmann T., Ortel I., Tudzynski P., Keller U. Identification of the cytochrome P450 monooxygenase that bridges the clavine and ergoline alkaloid pathways. ChemBiochem, 2006, 7(4): 645-652 CrossRef
  138. Riederer B., Han M., Keller U. D-Lysergyl peptide synthetase from the ergot fungus Claviceps purpurea. Journal of Biological Chemistry, 1996, 271(44): 27524-27530 CrossRef
  139. Walzel B., Riederer B., Keller U. Mechanism of alkaloid cyclopeptide synthesis in the ergot fungus Claviceps purpurea. Chemistry & Biology, 1997, 4(3): 223-230 CrossRef
  140. Haarmann T., Lorenz N., Tudzynski P. Use of a nonhomologous end joining deficient strain (Δku70) of the ergot fungus Claviceps purpurea for identification of a nonribosomal peptide synthetase gene involved in ergotamine biosynthesis. Fungal Genetics and Biology, 2008, 45(1): 35-44 CrossRef
  141. Ortel I., Keller U. Combinatorial assembly of simple and complex D-lysergic acid alkaloid peptide classes in the ergot fungus Claviceps purpurea. Journal of Biological Chemistry, 2009, 284(11): 6650-6660 CrossRef
  142. Havemann J., Vogel D., Loll B., Keller U. Cyclolization of D-lysergic acid alkaloid peptides. Chemistry & Biology, 2014, 21(1): 146-155 CrossRef
  143. Berry D., Mace W., Grage K., Wesche F., Gore S., Schardl C.L., Young C.A., Dijkwel P.P., Leuchtmann A., Bode H.B., Barry S. Efficient nonenzymatic cyclization and domain shuffling drive pyrrolopyrazine diversity from truncated variants of a fungal NRPS. Proceedings of the National Academy of Sciences, 2019, 116(51): 25614-25623 CrossRef
  144. Baunach M., Chowdhurry S., Stallforth P., Dittmann E. The landscape of recombination events that create nonribosomal peptide diversity. Molecular Biology and Evolution, 2021, 38(5): 2116-2130 CrossRef
  145. Wang P., Choera T., Wiemann P., Pisithkul T., Amador-Noguez D., Keller N.P. TrpE feedback mutants reveal roadblocks and conduits toward increasing secondary metabolism in Aspergillus fumigatus. Fungal Genetics and Biology, 2016, 89: 102-113 CrossRef
  146. Ryan K.L., Moore C.T., Panaccione D.G. Partial reconstruction of the ergot alkaloid pathway by heterologous gene expression in Aspergillus nidulans. Toxins (Basel), 2013, 5(2): 445-455 CrossRef
  147. Tudzynski P., Scheffer J. Claviceps purpurea: molecular aspects of a unique pathogenic lifestyle. Molecular Plant Pathology, 2004, 5(5): 377-388 CrossRef
  148. Kodisch A., Wilde P., Schmiedchen B., Fromme F.-J., Rodemann B., Tratwal A., Oberforster M., Schiemann A., Jørgensen L., Miedaner T. Ergot infection in winter rye hybrids shows differential contribution of male and female genotypes and environment. Euphytica, 2020, 216(4): 65 CrossRef 
  149. Pageau D., Wauthy J., Collin J. Evaluation of barley cultivars for resistance to ergot fungus, Claviceps purpurea (Fr.) Tul. Canadian Journal of Plant Science, 1994, 74(3): 663-665 CrossRef
  150. Mette M.F., Gils M., Longin C.F.H., Reif J.C. Hybrid breeding in wheat. In: Advances in wheat genetics: from genome to field. Y. Ogihara, S. Takumi, H. Handa (eds.). Springer, Tokyo, 2015: 225-232 CrossRef
  151. Platford R.G., Bernier C.C. Resistance to Claviceps purpurea in spring and durum wheat. Nature, 1970, 226(5247): 770 CrossRef
  152. Gordon A., McCartney C., Knox R.E., Ereful N., Hiebert C.W., Konkin D.J., Hsueh Ya.-C., Bhadauria V., Sgroi M., O’Sullivan D.M., Hadley C., Boyd L.A., Menzies J.G. Genetic and transcriptional dissection of resistance to Claviceps purpurea in the durum wheat cultivar Greenshank. Theoretical and Applied Genetics, 2020, 133: 1873-1886 CrossRef
  153. Thakur R.P., Rai K.N. Pearl millet ergot research: advances and implications. In: Sorghum and millets diseases. J.F. Leslie (ed.). Iowa State Press, Ames, IA, USA, 2003: 57-64 CrossRef
  154. Pažoutová S., Frederickson D.E. Genetic diversity of Claviceps africana on sorghum and Hyparrhenia. Plant Pathology, 2005, 54: 749-763 CrossRef
  155. Haarmann T., Rolke Y., Giesbert S., Tudzynski P. Ergot: from witchcraft to biotechnology. Molecular Plant Pathology, 2009, 10(4): 563-577 CrossRef
  156. Wäli P.P., Wäli P.R., Saikkonen K., Tuomi J. Is the pathogenic ergot fungus a conditional defensive mutualist for its host grass? PLoS ONE, 2013, 8(7): e69249 CrossRef
  157. Menzies J.G., Klein-Gebbinck H.W., Gordon A., O’Sullivan D.M. Evaluation of Claviceps purpurea isolates on wheat reveals complex virulence and host susceptibility relationships. Canadian Journal of Plant Pathology, 2017, 39(3): 307-317 CrossRef
  158. Platford R.G., Bernier C.C. Reaction of cultivated cereals to Claviceps purpurea. Canadian Journal of Plant Science, 1976, 56: 51-58 CrossRef
  159. Cooke R.C., Mitchell D.T. Sclerotium size and germination in Claviceps purpurea. Transactions of the British Mycological Society, 1966, 49(1): 95-100 CrossRef
  160. Likar M., Grandi M., Strajn B.J., Kos K., Celar F.A. Links between genetic groups, host specificity, and ergot-alkaloid profiles within Claviceps purpurea (Fr.) Tul. on Slovenian grasses. Plant Disease, 2018, 102(7): 1334-1340 CrossRef
  161. Pažoutová S., Cagaš B., Kolínská R., Honzátko A. Host specialization of different 424 populations of ergot fungus (Claviceps purpurea). Czech Journal of Genetics and Plant Breeding, 2002, 38(2): 75-81.
  162. Pažoutová S. The evolutionary strategy of Claviceps. In: Clavicipitalean fungi: evolutionary biology, chemistry, biocontrol and cultural impacts. F. White, C.W. Bacon, N.L. Hywel-Jones (eds.). Marcel Dekker, New York, 2002: 329-354.
  163. Dung J.K.S., Alderman S.C., Walenta D.L., Hamm P.B. Spatial patterns of ergot and quantification of sclerotia in perennial ryegrass seed fields in eastern Oregon. Plant Disease, 2016, 100(6): 1110-1117 CrossRef
  164. Dung J.K., Scott J., Cheng Q., Alderman S.C., Kaur N., Walenta D.L., Frost K.E., Hamm P.B. Detection and quantification of airborne Claviceps purpurea sensu lato ascospores from hirst-type spore traps using real-time quantitative PCR. Plant Disease, 2018, 102(12): 2487-2493 CrossRef
  165. Butler M.D., Alderman S.C., Hammond P.C., Berry R.E. Association of insects and ergot (Claviceps purpurea) in Kentucky bluegrass seed production fields. Journal of Economic Entomology, 2001, 94(6): 1471-1476 CrossRef
  166. Kaur N., Cating R.A., Rondon S.I., Scott J.C., Alderman S.C., Walenta D.L., Frost K.E., Hamm P.B., Dung J.K.S. Dispersal potential of ergot spores by insects foraging in perennial ryegrass fields in the Columbia Basin of Oregon and Washington. Crop, Forage & Turfgrass Management, 2019, 5(1): 1-5 CrossRef
  167. Alderman S.C., Halse R.R., White J.F. A reevaluation of the host range and geographical distribution of Claviceps species in the United States. Plant Disease, 2004, 88(1): 63-81 CrossRef
  168. Shain S.S. Prikladnaya biokhimiya i mikrobiologiya, 1996, 32(3): 275-279 (in Russ.).
  169. Hanosová H., Koprna R., Valík J., Knoppová L., Frébort I., Dzurová L., Galuszka P. Improving field production of ergot alkaloids by application of gametocide on rye host plants. New Biotechnology, 2015, 32(6): 739-746 CrossRef
  170. Menzies J.G. The reactions of Canadian spring wheat genotypes to inoculation with Claviceps purpurea, the causal agent of ergot. Canadian Journal of Plant Science, 2004, 84(4): 625-629 CrossRef
  171. Gordon A., Basler R., Bansept-Basler P., Fanstone V., Harinarayan L., Grant P.K., Birchmore R., Bayles R.A., Boyd L.A., O’Sullivan D.M. The identification of QTL controlling ergot sclerotia size in hexaploid wheat implicates a role for the Rht dwarfing alleles. Theoretical and Applied Genetics, 2015, 128: 2447-2460 CrossRef
  172. Platford R.G., Bernier C.C., Evans L.E. Chromosome location of genes conditioning resistance to Claviceps purpurea in spring and durum wheat. Canadian Journal of Genetics and Cytology, 1977, 19: 679-682 CrossRef
  173. Komolong B., Chakraborty S., Ryley M., Yates D. Ovary colonization by Claviceps africana is related to ergot resistance in male-sterile sorghum lines. Plant Pathology, 2003, 52(5): 620-627 CrossRef
  174. Parh D.K., Jordan D.R., Aitken E.A., Mace E.S., Jun-ai P., McIntyre C.L., Godwin I.D. QTL analysis of ergot resistance in sorghum. Theoretical and Applied Genetics, 2008, 117(3): 369-382 CrossRef
  175. Tente E., Carrera E., Gordon A., Boyd L.A. The role of the wheat reduced height (Rht)-DELLA mutants and associated hormones in infection by Claviceps purpurea, the causal agent of ergot. Phytopathology, 2022, 112(4): 842-851 CrossRef
  176. Kind S., Schurack S., Hinsch J., Tudzynski P. Brachypodium distachyon as alternative model host system for the ergot fungus Claviceps purpurea. Molecular Plant Pathology, 2017, 19(4): 1005-1011 CrossRef
  177. Kind S., Hinsch J., Vrabka J., Hradilová M., Majeská-Čudejková M., Tudzynski P., Galuszka P. Manipulation of cytokinin level in the ergot fungus Claviceps purpurea emphasizes its contribution to virulence. Current Genetics, 2018, 64(6): 1303-1319 CrossRef
  178. Mirdita V., Dhillon B., Geiger H., Miedaner T. Genetic variation for resistance to ergot (Claviceps purpurea [Fr.] Tul.) among full-sib families of five populations of winter rye (Secale cereale L.). Theoretical and Applied Genetics, 2008, 118(1): 85-90 CrossRef
  179. Mirdita V., Miedaner T. Resistance to ergot in self-incompatible germplasm resources of winter rye. Journal of Phytopathology, 2009, 157(6): 350-355 CrossRef
  180. Mahmood K., Orabi J., Kristensen P.S., Sarup P., Jørgensen L.N., Jahoor A. De novo transcriptome assembly, functional annotation, and expression profiling of rye (Secale cereale L.) hybrids inoculated with ergot (Claviceps purpurea). Scientific Reports, 2020, 10(1): 13475 CrossRef
  181. Oeser B., Heidrich P.M., Müller U., Tudzynski P., Tenberge K.B. Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/rye interaction. Fungal Genetics and Biology, 2002, 36(3): 176-186 CrossRef
  182. Wang Z., Wan L., Zhang X., Xin Q., Song Y., Hong D., Sun Y., Yang G. Interaction between Brassica napus polygalacturonase inhibition proteins and Sclerotinia sclerotiorum polygalacturonase: implications for rapeseed resistance to fungal infection. Planta, 2021, 253(2): 34 CrossRef
  183. Volpi C., Raiola A., Janni M., Gordon A., O'Sullivan D.M., Favaron F., D’Ovidio R. Claviceps purpurea expressing polygalacturonases escaping PGIP inhibition fully infects PvPGIP2 wheat transgenic plants but its infection is delayed in wheat transgenic plants with increased level of pectin methyl esterification. Plant Physiology and Biochemistry, 2013, 73: 294-301 CrossRef
  184. Lionetti V., Cervone F., Bellincampi D. Methyl esterification of pectin plays a role during plant—pathogen interactions and affects plant resistance to diseases. Journal of Plant Physiology, 2012, 169(16): 1623-1630 CrossRef
  185. Malinovsky F.G., Fangel J.U., Willats W.G. The role of the cell wall in plant immunity. Frontiers in Plant Science, 2014, 6(5): 178 CrossRef
  186. Li S., Ge F.R., Xu M., Zhao X.Y., Huang G.Q., Zhou L.Z., Wang J.G., Kombrink A., McCormick S., Zhang X.S., Zhang Y. Arabidopsis COBRA-LIKE 10, a GPI-anchored protein, mediates directional growth of pollen tubes. The Plant Journal, 2013, 74(3): 486-497 CrossRef
  187. Darlington L.C., Mathre D.E., Johnston R.H. Variation in pathogenicity between isolates of Slaviceps purpurea. Canadian Journal of Plant Science, 1977, 57(3): 729-733 CrossRef
  188. Irzykowska L., Weber Z., Bocianowski J. Comparison of Claviceps purpurea populations originated from experimental plots or fields of rye. Central European Journal of Biology, 2012, 7: 839-849 CrossRef
  189. Fisher R., Zekert N., Takeshita N. Polarized growth in fungi — interplay between the cytoskeleton, positional markers and membrane domains. Molecular Microbiology, 2008, 68(4): 813-826 CrossRef
  190. Bormann J., Tudzynski P. Deletion of Mid1, a putative stretch-activated calcium channel in Claviceps purpurea, affects vegetative growth, cell wall synthesis and virulence. Microbiology, 2009, 155(Pt 12): 3922-3933 CrossRef
  191. Tsukiboshi T., Shimanuki T., Uematsu T. Claviceps sorghicola sp. nov., a destructive ergot pathogen of sorghum in Japan. Mycological Research, 1999, 103(11): 1403-1408 CrossRef
  192. Muthusubramanian V., Bandyopadhyay R., Rajaram-Reddy D., Tooley P.W. Cultural characteristics, morphology, and variation vithin Claviceps africana and C. sorghi from India. Mycological Research, 2006, 110(Pt 4): 452-464 CrossRef
  193. Oeser B., Beaussart F., Haarmann T., Lorenz N., Nathues E., Rolke Y., Scheffer J., Weiner J., Tudzynski P. Expressed sequence tags from the flower pathogen Claviceps purpurea. Molecular Plant Pathology, 2009, 10(5): 665-684 CrossRef
  194. Zhao Z., Liu H., Wang C., Xu J. Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics, 2013, 14: 274 CrossRef
  195. Oberti H., Spangenberg G., Cogan N., Reyno R., Feijoo M., Murchio S., Dalla-Rizza M. Genome-wide analysis of Claviceps paspali: insights into the secretome of the main species causing ergot disease in Paspalum spp. BMC Genomics, 2021, 22: 766 CrossRef
  196. Mey G., Held K., Scheffer J., Tenberge K.B., Tudzynski P. CPMK2, an SLT2-homologous mitogen-activated protein (MAP) kinase, is essential for pathogenesis of Claviceps purpurea on rye: evidence for a second conserved pathogenesis-related MAP kinase cascade in phytopathogenic fungi. Molecular Microbiology, 2002, 46(2): 305-318 CrossRef
  197. Mey G., Oeser B., Lebrun M.H., Tudzynski P. The biotrophic, non-appressorium-forming grass pathogen Claviceps purpurea needs a Fus3/Pmk1 homologous mitogen-activated protein kinase for colonization of rye ovarian tissue. Molecular Plant-Microbe Interactions, 2002, 15(4): 303-312 CrossRef
  198. Schürmann J., Buttermann D., Herrmann A., Giesbert S., Tudzynski P. Molecular characterization of the NADPH oxidase complex in the ergot fungus Claviceps purpurea: CpNox2 and CpPls1 are important for a balanced host-pathogen interaction. Molecular Plant-Microbe Interactions, 2013, 26(10): 1151-1164 CrossRef
  199. Hinsch J., Vrabka J., Oeser B., Novák O., Galuszka P., Tudzynski P. De novo biosynthesis of cytokinins in the biotrophic fungus Claviceps purpurea. Environmental Microbiology, 2015, 17(8): 2935-2951 CrossRef
  200. Hinsch J., Galuszka P., Tudzynski P. Functional characterization of the first filamentous fungal tRNA-isopentenyltransferase and its role in the virulence of Claviceps purpurea. New Phytologist, 2016, 211(3): 980-992 CrossRef
  201. Moore S., De Vries O.M., Tudzynski P. The major Cu, Zn SOD of the phytopathogen Claviceps purpurea is not essential for pathogenicity. Molecular Plant Pathology, 2002, 3(1): 9-22 CrossRef
  202. Nathues E., Joshi S., Tenberge K.B., von den Driesch M., Oeser B., Bäumer N., Mihlan M., Tudzynski P. CPTF1, a CREB-like transcription factor, is involved in the oxidative stress response in the phytopathogen Claviceps purpurea and modulates ROS level in its host Secale cereale. Molecular Plant-Microbe Interactions, 2004, 17(4): 383-393 CrossRef
  203. Scheffer J., Chen C., Heidrich P., Dickman M.B., Tudzynski P. A CDC42 homologue in Claviceps purpurea is involved in vegetative differentiation and is essential for pathogenicity. Eukaryot Cell, 2005, 4(7): 1228-1238 CrossRef
  204. Laihonen M., Saikkonen K., Helander M., Vázquez de Aldana B.R., Zabalgogeazcoa I., Fuchs B. Epichloe endophyte-promoted seed pathogen increases host grass resistance against insect herbivory. Frontiers in Microbiology, 2022, 12: 786619 CrossRef
  205. Jonkers W., Gundel P.E., Verma S.K., White J.F. Seed microbiome research. Frontiers in Microbiology, 2022, 13: 943329 CrossRef
  206. Pérez L.I., Gundel P.E., Ghersa C.M., Omacini M. Family issues: fungal endophyte protects host grass from the closely related pathogen Claviceps purpurea. Fungal Ecology, 2013, 6(5): 379-386 CrossRef
  207. Pérez L.I., Gundel P.E., Marrero H.J., Arzac A.G., Omacini M. Symbiosis with systemic fungal endophytes promotes host escape from vector-borne disease. Oecologia, 2017, 184(1): 237-245 CrossRef
  208. Zhang H., Li X., White J.F., Wei X., He Y., Li C. Epichloe endophyte improves ergot disease resistance of host (Achnatherum inebrians) by regulating leaf senescence and photosynthetic capacity. Journal of Plant Growth Regulation, 2022, 41: 808-817 CrossRef
  209. Saikkonen K., Young C.A., Helander M., Schardl C.L. Endophytic Epichloe species and their grass hosts: from evolution to applications. Plant Molecular Biology, 2016, 90(6): 665-675 CrossRef
  210. Malinowski D.P., Belesky D.P. Epichloe (formerly Neotyphodium) fungal endophytes increase adaptation of cool-season perennial grasses to environmental stresses. Acta Agrobotanica, 2019, 72(2): 1767 CrossRef
  211. Ordza T., Węgrzyn E., Dominiak-Świgoń M., Lembicz M. Mycobiota of rye seeds infected with ergot fungi. Current Research in Environmental & Applied Mycology (Journal of Fungal Biology), 2022, 12(1): 95-101 CrossRef
  212. Walkowiak S., Taylor D., Fu B.X., Drul D., Pleskach K., Tittlemier S.A. Ergot in Canadian cereals — relevance, occurrence, and current status. Canadian Journal of Plant Pathology, 2022, 0(0): 1-13 CrossRef
  213. Miedaner T., Kodisch A., Raditschnig A., Eifler J. Ergot alkaloid contents in hybrid rye are reduced by breeding. Agriculture, 2021, 11(6): 526 CrossRef
  214. Sheshegova T.K., Shchekleina L.M., Antipova T.V., Zhelifonova V.P., Kozlovskiy A.G. Search for rye and wheat genotypes which are resistant to Claviceps purpurea (Fr.) Tul. and hamper accumulation of ergoalkaloids in sclerotia Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2021, 56(3): 549-558 CrossRef
  215. Miedaner T., Korzun V., Wilde P. Effective pollen-fertility restoration is the basis of hybrid rye production and ergot mitigation. Plants, 2022, 11(9): 1115 CrossRef
  216. Kodisch A., Schmiedchen B., Eifler J. Gordillo A., Siekmann D., Fromme F.J., Oberforster M., Miedaner T. Maternal differences for the reaction to ergot in unfertilized hybrid rye (Secale cereale). European Journal of Plant Pathology, 2022, 163: 181-191 CrossRef
  217. Wilde P., Miedaner T. Hybrid rye breeding. In: The rye genome. Compendium of Plant Genomes. M.T.Rabanus-Wallace, N. Stein (eds.). Springer, Cham, Switzerland, 2021: 13-41
  218. Doi Y., Wakana D., Takeda H., Tanaka E., Hosoe T. Production of ergot alkaloids by the Japanese isolate Claviceps purpurea var. agropyri on rice medium. Advances in Microbiology, 2022, 12(4): 254-269 CrossRef
  219. Flieger M., Wurst M., Shelby R. Ergot alkaloids — sources, structures and analytical methods. Folia Microbiologica, 1997, 42(1): 3-29 CrossRef
  220. Kishimoto S., Sato M., Tsunematsu Y., Watanabe K. Evaluation of biosynthetic pathway and engineered biosynthesis of alkaloids. Molecules, 2016, 21(8): 1078 CrossRef
  221. Schardl C., Young C., Moore N., Krom N., Dupont P., Pan J., Florea S., Webb J., Jaromczyk J., Jaromczyk J., Cox M., Farman M. Genomes of plant-associated Clavicipitaceae. Advances in Botanical Research, 2014, 70: 291-327 CrossRef
  222. Lünne F., Köhler J., Stroh C., Müller L., Daniliuc C., Mück-Lichtenfeld C., Würthwein E., Esselen M., Humpf H., Kalinina S. Insights into ergochromes of the plant pathogen Claviceps purpurea. Journal of Natural Products, 2021, 84(10): 2630-2643 CrossRef
  223. Bauer J.I., Gross M., Cramer B., Wegner S., Hausmann H., Hamscher G., Uslebe E. Detection of the tremorgenic mycotoxin paxilline and its desoxy analog in ergot of rye and barley: a new class of mycotoxins added to an old problem. Analytical and Bioanalytical Chemistry,2017, 409(21): 5101-5112 CrossRef
  224. Qiao Y.-M., Wen Y.-H., Gong T., Chen J.-J., Chen T.-J., Yang J.-L., Zhu P. Improving ergometrine production by easO and easP knockout in Claviceps paspali. Fermentation, 2022, 8(6): 263 CrossRef
  225. Halliwell B., Cheah I., Ergothioneine, where are we now? FEBS Letters, 2022, 596(10): 1227-1230 CrossRef
  226. Xiong L., Xie Z., Ke J., Wang L., Gao B., Tao X., Zhao M., Shen Y., Wei D., Wang F., Engineering Mycolicibacterium neoaurum for the production of antioxidant ergothioneine. Food Bioengineering, 2022, 1(1): 26-36 CrossRef
  227. van der Hoek S. A., Rusnák M., Wang G., Dimitrov Stanchev L., Alves L.F., Jessop-Fabre M.M., Paramasivan K., Hjorth Jacobsen I., Sonnenschein N., Martínez J.L., Darbani B., Kell D.B., Borodina I. Engineering precursor supply for the high-level production of ergothioneine in Saccharomyces cerevisiae. Metabolic Engineering, 2022, 70: 129-142 CrossRef
  228. van der Hoek S.A., Rusnák M., Jacobsen I.H., Martínez J.L., Kell D.B., Borodina I. Engineering ergothioneine production in Yarrowia lipolytica. FEBS Letters, 2022, 596(10): 1356-1364 CrossRef
  229. Cherewyk J.E., Grusie-Ogilvie T.J., Parker S.E., Blakley B.R., Al-Dissi A.N. Ammonization of the R- and S-epimers of ergot alkaloids to assess detoxification potential. Journal of Agricultural and Food Chemistry, 2022, 70(29): 8931-8941 CrossRef
  230. Rahimabadi P.D., Yourdkhani S., Rajabi M., Sedaghat R., Golchin D., Rad H.A. Ergotism in feedlot cattle: clinical, hematological, and pathological findings. Comparative Clinical Pathology, 2022, 31(2): 281-291 CrossRef
  231. Klotz J.L. Global impact of ergot alkaloids. Toxins (Basel), 2022, 14(3): 186 CrossRef
  232. Pleadin J., Kudumija N., Škrivanko M., Cvetnić L., Petrović D., Vasilj V., Zadravec M. Ergot sclerotia and ergot alkaloids occurrence in wheat and rye grains produced in Croatia. Veterinarska Stanica,2022, 53(5): 503-511 CrossRef
  233. Eady C. The impact of alkaloid-producing Epichloe endophyte on forage ryegrass breeding: a New Zealand perspective. Toxins, 2021, 13(2): 158 CrossRef
  234. Liu M., Kolařík M., Tanaka E. The 168-year taxonomy of Claviceps in the light of variations: From three morphological species to four sections based on multigene phylogenies. Canadian Journal of Plant Pathology, 2022, 0(0): 1-10 CrossRef

 

back

 


CONTENTS

 

 

Full article PDF (Rus)