title: Vegetative hyphal fusion and subsequent nuclear behavior in Epichloë grass endophytes.
abstract: Epichloë species (including the former genus Neotyphodium) are fungal symbionts of many agronomically important forage grasses, and provide their grass hosts with protection from a wide range of biotic and abiotic stresses. Epichloë species include many interspecific hybrids with allodiploid-like genomes, which may provide the potential for combined traits or recombination to generate new traits. Though circumstantial evidence suggests that such interspecific hybrids might have arisen from nuclear fusion events following vegetative hyphal fusion between different Epichloë strains, this hypothesis has not been addressed empirically. Here, we investigated vegetative hyphal fusion and subsequent nuclear behavior in Epichloë species. A majority of Epichloë strains, especially those having a sexual stage, underwent self vegetative hyphal fusion. Vegetative fusion also occurred between two hyphae from different Epichloë strains. Though Epichloë spp. are uninucleate fungi, hyphal fusion resulted in two nuclei stably sharing the same cytoplasm, which might ultimately lead to nuclear fusion. In addition, protoplast fusion experiments gave rise to uninucleate putative hybrids, which apparently had two markers, one from each parent within the same nucleus. These results are consistent with the notion that interspecific hybrids arise from vegetative hyphal fusion. However, we also discuss additional factors, such as post-hybridization selection, that may be important to explain the recognized prevalence of hybrids in Epichloë species.
authors.affiliation: The Samuel Roberts Noble Foundation, Plant Biology Division, 2510 Sam Noble Parkway, Ardmore, Oklahoma 73401, United States of America.
authors.forename: Jun-Ya
authors.initials: JY
authors.lastname: Shoji
authors.affiliation: The Samuel Roberts Noble Foundation, Forage Improvement Division, 2510 Sam Noble Parkway, Ardmore, Oklahoma 73401, United States of America.
authors.forename: Nikki D
authors.initials: ND
authors.lastname: Charlton
authors.affiliation: The Samuel Roberts Noble Foundation, Forage Improvement Division, 2510 Sam Noble Parkway, Ardmore, Oklahoma 73401, United States of America.
authors.forename: Mihwa
authors.initials: M
authors.lastname: Yi
authors.affiliation: The Samuel Roberts Noble Foundation, Forage Improvement Division, 2510 Sam Noble Parkway, Ardmore, Oklahoma 73401, United States of America.
authors.forename: Carolyn A
authors.initials: CA
authors.lastname: Young
authors.affiliation: The Samuel Roberts Noble Foundation, Plant Biology Division, 2510 Sam Noble Parkway, Ardmore, Oklahoma 73401, United States of America.
authors.forename: Kelly D
authors.initials: KD
authors.lastname: Craven
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D002467:Cell Nucleus / Q000235:genetics* / Q000378:metabolism / Q000648:ultrastructure; D060026:Endophytes; D055329:Epichloe / Q000145:classification / Q000235:genetics* / Q000378:metabolism / Q000648:ultrastructure; D005656:Fungal Proteins / Q000235:genetics* / Q000378:metabolism; D015966:Gene Expression Regulation, Fungal; D017930:Genes, Reporter; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D006824:Hybridization, Genetic; D025301:Hyphae / Q000235:genetics* / Q000378:metabolism / Q000648:ultrastructure; D008164:Luminescent Proteins / Q000235:genetics / Q000378:metabolism; D009681:Nuclear Fusion; D010802:Phylogeny; D010957:Plasmids / Q000737:chemistry / Q000378:metabolism; D006109:Poaceae / Q000382:microbiology / Q000502:physiology; D011523:Protoplasts / Q000378:metabolism / Q000648:ultrastructure; D013172:Spores, Fungal / Q000235:genetics / Q000378:metabolism / Q000648:ultrastructure; D013559:Symbiosis / Q000502:physiology
chemical_list: D001426:Bacterial Proteins; D005656:Fungal Proteins; D008164:Luminescent Proteins; C054562:yellow fluorescent protein, Bacteria; D049452:Green Fluorescent Proteins
references.citation: Mycologia. 2014 Mar-Apr;106(2):202-15
references.pmid: 24459125
references.citation: Proc Natl Acad Sci U S A. 2011 Feb 15;108(7):2861-6
references.pmid: 21282602
references.citation: Appl Environ Microbiol. 2001 Dec;67(12):5377-83
references.pmid: 11722882
references.citation: Fungal Genet Biol. 2002 Oct;37(1):109-19
references.pmid: 12223195
references.citation: Eukaryot Cell. 2010 Aug;9(8):1216-24
references.pmid: 20543061
references.citation: Appl Environ Microbiol. 2012 Aug;78(16):5501-10
references.pmid: 22660705
references.citation: New Phytol. 2009 Mar;181(4):924-37
references.pmid: 19140939
references.citation: FEMS Microbiol Lett. 2009 Apr;293(1):1-10
references.pmid: 19175410
references.citation: Eukaryot Cell. 2012 Dec;11(12):1463-71
references.pmid: 23042130
references.citation: New Phytol. 2012 Jul;195(1):231-6
references.pmid: 22489964
references.citation: Annu Rev Plant Biol. 2004;55:315-40
references.pmid: 15377223
references.citation: Bioessays. 2008 Nov;30(11-12):1193-203
references.pmid: 18937373
references.citation: Mol Ecol. 2003 Nov;12(11):2861-73
references.pmid: 14629368
references.citation: New Phytol. 2007;173(3):452-8
references.pmid: 17244040
references.citation: FEMS Microbiol Ecol. 2014 Oct;90(1):276-89
references.pmid: 25065688
references.citation: Evolution. 2012 Jun;66(6):1917-30
references.pmid: 22671556
references.citation: Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2542-6
references.pmid: 8172623
references.citation: New Phytol. 2012 Dec;196(4):1015-23
references.pmid: 22998436
references.citation: FEMS Microbiol Lett. 2005 Aug 15;249(2):191-8
references.pmid: 16040203
references.citation: Annu Rev Genet. 2012;46:341-58
references.pmid: 22934638
references.citation: Curr Genet. 1992 Nov;22(5):399-406
references.pmid: 1423727
references.citation: Curr Genet. 1998 May;33(5):368-77
references.pmid: 9618588
references.citation: New Phytol. 2008;177(3):583-5
references.pmid: 18086225
references.citation: Nat Rev Genet. 2008 Aug;9(8):605-18
references.pmid: 18591983
references.citation: Nature. 2010 Mar 18;464(7287):367-73
references.pmid: 20237561
references.citation: PLoS Genet. 2014 Mar 06;10(3):e1004180
references.pmid: 24603805
references.citation: Mol Ecol. 2004 Jun;13(6):1455-67
references.pmid: 15140090
references.citation: Eukaryot Cell. 2012 Nov;11(11):1345-52
references.pmid: 22962278
references.citation: FEMS Microbiol Rev. 2011 May;35(3):542-54
references.pmid: 21223323
references.citation: Mycologia. 2012 Sep-Oct;104(5):1187-99
references.pmid: 22675049
references.citation: Mycol Res. 2007 Apr;111(Pt 4):466-72
references.pmid: 17512714
references.citation: Fungal Genet Biol. 2003 Nov;40(2):138-45
references.pmid: 14516766
references.citation: Evolution. 2003 Dec;57(12):2703-20
references.pmid: 14761051
references.citation: Nat Genet. 2006 Aug;38(8):953-6
references.pmid: 16832356
references.citation: Oecologia. 1985 Apr;66(1):1-5
references.pmid: 28310805
references.citation: Mol Microbiol. 2013 Nov;90(3):551-68
references.pmid: 23998652
references.citation: Eukaryot Cell. 2010 Dec;9(12):1856-66
references.pmid: 20952581
references.citation: Plant J. 1999 May;18(4):349-58
references.pmid: 10406120
references.citation: FEMS Yeast Res. 2008 Nov;8(7):996-1007
references.pmid: 18355270
references.citation: Curr Genet. 2007 Nov;52(5-6):259-66
references.pmid: 17929020
references.citation: PLoS Genet. 2013;9(2):e1003323
references.pmid: 23468653
references.citation: Cell Motil Cytoskeleton. 1999;42(2):114-24
references.pmid: 10215421
references.citation: Mol Plant Microbe Interact. 2015 Jan;28(1):69-85
references.pmid: 25303335
references.citation: Biosci Biotechnol Biochem. 2006 Aug;70(8):1882-9
references.pmid: 16880596
references.citation: PLoS One. 2012;7(8):e42565
references.pmid: 22900028
references.citation: Proc Natl Acad Sci U S A. 2013 Aug 6;110(32):12875-80
references.pmid: 23861490
references.citation: PLoS One. 2010 Dec 20;5(12):e15650
references.pmid: 21187926
references.citation: Mol Plant Microbe Interact. 2001 Apr;14(4):580-4
references.pmid: 11310747
references.citation: Fungal Genet Biol. 2009 Aug;46(8):585-94
references.pmid: 19389478
references.citation: Cytometry. 1989 Jan;10(1):103-7
references.pmid: 2492919
references.citation: Eukaryot Cell. 2006 Feb;5(2):411-21
references.pmid: 16467481
references.citation: Fungal Genet Biol. 2002 Jul;36(2):91-7
references.pmid: 12081462
references.citation: Microbes Infect. 2002 Nov;4(13):1353-9
references.pmid: 12443900
references.citation: PLoS One. 2012;7(2):e31175
references.pmid: 22319613
references.citation: J Gen Microbiol. 1984 Sep;130(9):2229-36
references.pmid: 6389760
references.citation: Toxins (Basel). 2013 Jun 06;5(6):1064-88
references.pmid: 23744053
references.citation: Fungal Genet Biol. 2013 Jul;56:87-97
references.pmid: 23684536
references.citation: Eukaryot Cell. 2010 Aug;9(8):1171-83
references.pmid: 20207852
references.citation: Fungal Genet Biol. 2012 Nov;49(11):896-902
references.pmid: 22939838
references.citation: Curr Opin Microbiol. 2009 Dec;12(6):608-15
references.pmid: 19864177
references.citation: FEMS Microbiol Lett. 2012 Apr;329(1):1-8
references.pmid: 22112233
references.citation: Annu Rev Genet. 2000;34:165-186
references.pmid: 11092825
references.citation: Appl Environ Microbiol. 1987 Jan;53(1):70-3
references.pmid: 3827250
references.citation: J Gen Microbiol. 1983 Dec;129(12):3643-9
references.pmid: 6366117
references.citation: Mol Phylogenet Evol. 2005 Apr;35(1):196-208
references.pmid: 15737591
references.citation: Can J Microbiol. 1998 Oct;44(10):959-64
references.pmid: 9933914
references.citation: FEMS Yeast Res. 2002 Jan;1(4):323-31
references.pmid: 12702336