Horizontal gene transfer of a bacterial insect toxin gene into the Epichloë fungal symbionts of grasses

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Ambrose, Karen V ^a   Koppenhöfer, Albrecht M ^a   Belanger, Faith C ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN;

ANIMAL; ENDOPHYTE; EPICHLOE; FUNGAL GENE; GENE EXPRESSION; GENETICS; HERBIVORY; HORIZONTAL GENE TRANSFER; LARVA; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOTH; PHOTORHABDUS; PHYLOGENY; PHYSIOLOGY; POACEAE;

ANIMALS; BACTERIAL TOXINS; ENDOPHYTES; EPICHLOE; EVOLUTION, MOLECULAR; GENE EXPRESSION; GENE TRANSFER, HORIZONTAL; GENES, FUNGAL; HERBIVORY; LARVA; MOLECULAR SEQUENCE DATA; MOTHS; PHOTORHABDUS; PHYLOGENY; POACEAE;

EID: 84903974186     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep05562     Document Type: Article

References (61)

1. Keeling, P. J. & Palmer, J. D. Horizontal gene transfer in eukaryotic evolution. Nature Rev. Genetics 9, 605-618 (2008).
2. Syvanen, M. Evolutionary implications of horizontal gene transfer. Annu. Rev. Genet. 46, 341-358 (2012).
3. Richards, T. A., Leonard, G., Soanes, M. & Talbot, N. J. Gene transfer into the fungi. Fungal Biol. Rev. 25, 98-110 (2011).
4. Marcet-Houben, M. & Gabaldon, T. Acquisition of prokaryotic genes by fungal genomes. Trends Genet. 26, 5-8 (2010).
5. Fitzpatrick, D. A. Horizontal gene transfer in fungi. FEMS Microbiol. Lett. 329, 1-8 (2012).
6. Strope, P. K., Nickerson, K. W., Harris, S. D. & Moriyama, E. N. Molecular evolution of urea amidolyase and urea carboxylase in fungi. BMC Evol. Biol. 11, 80 (2011).
7. Friesen, T. L. et al. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38, 953-956 (2006). (Pubitemid 44141666)
8. Daborn, P. J. et al. A single Photorhabdus gene makes caterpillars floppy (mcf) allows Escherichia coli to persist within and kill insects. Proc. Natl. Acad. Sci. USA 99, 10742-10747 (2002).
9. Waterfield, N. R. et al. The insecticidal toxin Makes caterpillars floppy 2 (Mcf2) shows similarity to HrmA, an avirulence protein from a plant pathogen. FEMS Microbiol. Lett. 229, 265-270 (2003). (Pubitemid 37532880)
10. Hinchliffe, S. J., Hares, M. C., Dowling, A. J.& ffrench-Constant, R. H. Insecticidal toxins from the Photorhabdus and Xenorhabdus bacteria. Open Toxinol. J. 3, 101-118 (2010).
11. Clay, K. & Schardl, C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am. Nat. 160, S99-S127 (2002).
12. Schardl, C. L., Scott, B., Florea, S. & Zhang, D. Epichloë endophytes: clavicipitaceous symbionts of grasses. Plant Relationships, 2nd Edition, The Mycota V [Deising, H. (ed.)] [275-306] (Springer-Verlag, Berlin Heidelberg, 2009).
13. Kuldau, G. & Bacon, C. Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol. Control 46, 57-71 (2008).
14. Schardl, C. L., Young, C. A., Faulkner, J. R., Florea, S. & Pan, J. Chemotypic diversity of epichloae, fungal symbionts of grasses. Fungal Ecol. 5, 331-344 (2012).
15. Schardl, C. L. et al. Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genetics 9, e1003323 (2013).
16. Ambrose, K. V. & Belanger, F. C. SOLiD-SAGE of endophyte-infected red fescue reveals numerous effects on host transcriptome and an abundance of highly expresed fungal secreted proteins. PLoS ONE 7, e53214 (2012).
17. Ruemmele, B. A., Wipff, J. K., Brilman, L. & Hignight, K.W. Fine-leaved Festuca species. Turfgrass Biology, Genetics, and Breeding [Cassler, M.D. & Duncan, R.R. (eds.)] [129-174] (John Wiley & Sons, Inc., Hoboken, 2003).
18. Scott, B., Becker, Y., Becker, M. & Cartwright, G. Morphogenesis, growth, and development of the grass symbiont Epichloë festucae. Morphogenesis and Pathogenicity in Fungi [Perez-Martin, J. & Di Pietro, A. (eds.)] [243-264] (Springer-Verlag, Berlin, 2012).
19. Loper, J. E. et al. Comparative genomics of plant-associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet 8, e1002784 (2012).
20. ffrench-Constant, R. H., Dowling, A. &Waterfield, N. R. Insecticidal toxins from Photorhabdus bacteria and their potential use in agriculture. Toxicon 49, 436-451 (2007). (Pubitemid 46341394)
21. Ramette, A. et al. Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2, 4-diacetylphloroglucinol and pyoluteorin. Syst. Appl. Microbiol. 34, 180-188 (2011).
22. Pechy-Tarr, M. et al.Molecular analysis of a novel gene cluster encoding an insect toxin in plant-associated strains of Pseudomonas fluorescens. Environ. Microbiol. 10, 2368-2386 (2008).
23. Genisyuerek, S. et al Structural determinants for membrane insertion, pore formation and translocation of Clostridium difficile toxin B. Mol. Microbiol. 79, 1643-1654 (2011).
24. Dowling, A. J. et al. The insecticidal toxin Makes caterpillars floppy (Mcf) promotes apoptosis in mammalian cells. Cellular Microbiol. 6, 345-353 (2004). (Pubitemid 38379817)
25. Ruffner, B. et al. Oral insecticidal activity of plant-associated pseudomonads. Environ. Microbiol. 15, 751-763 (2013).
26. Tadych, M., Ambrose, K. V., Bergen, M. S., Belanger, F. C. & White, J. F. Jr. Taxonomic placement of Epichloë poae sp. nov. and horizontal dissemination to seedlings via conidia. Fungal Divers. 54, 117-131 (2012).
27. Leuchtmann, A., Bacon, C. W., Schardl, C. L., White, J. F. Jr & Tadych, M. (2014) Nomenclatural realignment of Neotyphodium species with genus Epichloë. Mycologia 106, 202-215 (2014).
28. Da Lage, J.-L., Binder, M., Hua-Van, A., Janecek, S. & Casane, D. Gene make-up: rapid and massive intron gains after horizontal transfer of a bacterial a-amylase gene to Basidiomycetes. BMC Evol. Biol. 13, 40 (2013).
29. Aguileta, G. et al. Assessing the performance of single-copy genes for recovering robust phylogenies. Syst. Biol. 57, 613-627 (2008).
30. Alabert, C. & Groth, A. Chromatin replication and epigenome maintenance. Nat. Rev. Mol. Cell. Bio. 13, 153-167 (2012).
31. Gelperin, D., Horton, L., Beckman, J., Hensold, J. &Lemmon, S. K.Bms1p, a novel GTP-binding protein, and the related Tsr1p are required for distinct steps of 40S ribosome biogenesis in yeast. RNA 7, 1268-1283 (2001). (Pubitemid 32831355)
32. Schmitt, I. et al. New primers for promising single-copy genes in fungal phylogenetics and systematics. Persoonia 23, 35-40 (2009).
33. Raja, H. A., Schoch, C. L., Hustad, V. P., Shearer, C. A. &Miller, A. N. Testing the phylogenetic utility of MCM7 in the Ascomycota. MycoKeys 1, 63-94 (2011).
34. Tretter, E. D., Johnson, E. M., Wang, Y., Kandel, P. & White, M. M. Examining new phylogenetic markers to uncover the evolutionary history of early-diverging fungi: comparing MCM7, TSR1, and rRNA genes for single-and multi-gene analyses of Kickxellomycotina. Persoonia 30, 106-125 (2013).
35. Sung, G.-H., Poinar, G. O. Jr&Spatafora, J. W. The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal-arthropod symbioses. Mol. Phylogenet. Evol. 49, 495-502 (2008).
36. Li, W.-H. Molecular Evolution [Sinauer Associates, Sunderland, 1997].
37. Senchina, D. S. et al. Rate variation among nuclear genes and the age of polyploidy in Gossypium. Mol. Biol. Evol. 20, 633-643 (2003). (Pubitemid 36437913)
38. Brunner, S., Fengler, K., Morgante, M., Tingey, S. & Rfalski, A. Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17, 343-360 (2005). (Pubitemid 41672960)
39. Xu, J.-H. & Messing, J. Diverged copies of the seed regulatory Opaque-2 gene by a segmental duplication in the progenitor genome of rice, sorghum, andmaize. Mol. Plant 1, 760-769 (2008).
40. Ginns, J. Balansia hypoxylon (Ascomycota: Clavicipitaceae) in Canada: a mycosymbiont with Danthonia spicata (Poaceae). North American Fungi 6, 1-6 (2011).
41. Kuldau, G. A., Liu, J.-S., White, J. F. Jr, Siegel, M. R. & Schardl, C. L. Molecular systematics of Clavicipitaceae supporting monophyly of genus Epichloë and form genus Ephelis. Mycologia 89, 431-441 (1997). (Pubitemid 27256199)
42. Kasuga, T., White, T. J. & Taylor, J. W. Estimation of nucleotide substitution rates in Eurotiomycete fungi. Mol. Biol. Evol. 19, 2318-2324 (2002). (Pubitemid 35440466)
43. Acuna, R. et al. Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc. Natl. Acad. Sci. USA 109, 4197-4202 (2012).
44. Pauchet, Y. & Heckel, D. G. The genome of the mustard leaf beetle encodes two active xylanases originally acquired from bacteria through horizontal gene transfer. Proc. R. Soc. B 280, 20131021 (2013).
45. Schardl, C. L. et al. Currencies of mutualisms: sources of alkaloid genes in vertically transmitted epichloae. Toxins 5, 1064-1088 (2013b).
46. Yue, Q., Johnson-Cicalese, J., Gianfagna, T. J.&Meyer, W. A. Alkaloid production and chinch bug resistance in endophyte-inoculated Chewings and strong creeping red fescues. J. Chem. Ecol. 26, 279-292 (2000). (Pubitemid 30091836)
47. Moran, Y., Fredman, D., Szczesny, P., Grynberg, M. & Technau, U. Recurrent horizontal transfer of bacterial toxin genes to eukaryotes. Mol. Biol. Evol. 29, 2223-2230 (2012).
48. Schardl, C. L. et al. A novel test for host-symbiont codivergence indicates ancient origin of fungal endophytes in grasses. Systematic Biol. 57, 483-498 (2008). (Pubitemid 351882208)
49. Kellogg, E. A. Evolutionary history of the grasses. Plant Physiol. 125, 1198-1205 (2001). (Pubitemid 32224610)
50. Bouchenak-Khelladi, Y. et al. Large multi-gene phylogenetic trees of the grasses (Poaceae): progress towards complete tribal and generic level sampling. Mol. Phylogenet. Evol. 47, 488-505 (2008).
51. Jackson, A. P. A reconciliation analysis of host switching in plant-fungal symbioses. Evolution 58, 1909-1923 (2004). (Pubitemid 39348496)
52. Lemaire, B., Vandamme, P., Merckx, V., Smets, E. & Dessesin, S. Bacterial leaf symbiosis in angiosperms: host specificity without co-speciation. PLoS ONE 6, e24430 (2011).
53. Moy, M., Li, H., Sullivan, R., White, J. F. Jr & Belanger, F. C. Endophytic fungal b-1, 6-glucanase expression in the infected host grass. Plant Physiol. 130, 1298-1308 (2002). (Pubitemid 35352957)
54. Korpimaki, T., Kurittu, J. & Karp, M. Surprisingly fast disappearance of b-lactam selection pressure in cultivation as detected with novel biosensing approaches. J. Microbiol. Methods 53, 37-42 (2003). (Pubitemid 36255524)
55. Collins, T. et al. Batch production of silk-elastin-like protein in E. coli BL21(DE3): key parameters for optimisation. Micro. Cell Fact. 12, 21 (2013).
56. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685 (1970).
57. Guo, A. Y., Zhu, Q. H., Chen, X.&Luo, J. C. GSDS:Agene structure display server. Yi Chuan 29, 1023-1026 (2007).
58. Fawal, N., Savelli, B., Dunand, C. & Mathé, C. GECA: a fast tool for Gene Evolution and Conservation Analysis in eukaryotic protein families. Bioinformatics 28, 1398-1399 (2012).
59. Marthey, S. et al. Funybase: a fungal phylogenomic database. BMC Bioinformatics 9, 456 (2008).
60. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nuc. Acids Res. 25, 4876-4882 (1997). (Pubitemid 28022245)
61. Tamura, K. et al. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739 (2011).