title: Horizontal transfer of a subtilisin gene from plants into an ancestor of the plant pathogenic fungal genus Colletotrichum.
abstract: The genus Colletotrichum contains a large number of phytopathogenic fungi that produce enormous economic losses around the world. The effect of horizontal gene transfer (HGT) has not been studied yet in these organisms. Inter-Kingdom HGT into fungal genomes has been reported in the past but knowledge about the HGT between plants and fungi is particularly limited. We describe a gene in the genome of several species of the genus Colletotrichum with a strong resemblance to subtilisins typically found in plant genomes. Subtilisins are an important group of serine proteases, widely distributed in all of the kingdoms of life. Our hypothesis is that the gene was acquired by Colletotrichum spp. through (HGT) from plants to a Colletotrichum ancestor. We provide evidence to support this hypothesis in the form of phylogenetic analyses as well as a characterization of the similarity of the subtilisin at the primary, secondary and tertiary structural levels. The remarkable level of structural conservation of Colletotrichum plant-like subtilisin (CPLS) with plant subtilisins and the differences with the rest of Colletotrichum subtilisins suggests the possibility of molecular mimicry. Our phylogenetic analysis indicates that the HGT event would have occurred approximately 150-155 million years ago, after the divergence of the Colletotrichum lineage from other fungi. Gene expression analysis shows that the gene is modulated during the infection of maize by C. graminicola suggesting that it has a role in plant disease. Furthermore, the upregulation of the CPLS coincides with the downregulation of several plant genes encoding subtilisins. Based on the known roles of subtilisins in plant pathogenic fungi and the gene expression pattern that we observed, we postulate that the CPLSs have an important role in plant infection.
authors.affiliation: Centro Hispano-Luso de Investigaciones Agrarias, Departamento de Microbiología y Genética, Universidad de Salamanca, Villamayor, Spain.
authors.forename: Vinicio Danilo
authors.initials: VD
authors.lastname: Armijos Jaramillo
authors.forename: Walter Alberto
authors.initials: WA
authors.lastname: Vargas
authors.forename: Serenella Ana
authors.initials: SA
authors.lastname: Sukno
authors.forename: Michael R
authors.initials: MR
authors.lastname: Thon
mesh_terms: D000595:Amino Acid Sequence; D020231:Colletotrichum / Q000235:genetics*; D015870:Gene Expression; D022761:Gene Transfer, Horizontal; D054884:Host-Pathogen Interactions; D008958:Models, Molecular; D008969:Molecular Sequence Data; D010802:Phylogeny; D010935:Plant Diseases / Q000235:genetics / Q000382:microbiology; D010944:Plants / Q000235:genetics* / Q000382:microbiology*; D011487:Protein Conformation; D054730:Protein Interaction Domains and Motifs; D016415:Sequence Alignment; D020860:Subtilisin / Q000737:chemistry / Q000235:genetics*
chemical_list: D020860:Subtilisin
references.citation: J Mol Evol. 2010 Jan;70(1):85-97
references.pmid: 20033398
references.citation: Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2851-6
references.pmid: 16477026
references.citation: J Biol Chem. 2009 May 22;284(21):14068-78
references.pmid: 19332543
references.citation: Gene. 1999 Jul 22;235(1-2):121-9
references.pmid: 10415340
references.citation: Syst Biol. 2007 Aug;56(4):564-77
references.pmid: 17654362
references.citation: Bioinformatics. 2001 Dec;17(12):1246-7
references.pmid: 11751242
references.citation: Nucleic Acids Res. 2010 Jul;38(Web Server issue):W545-9
references.pmid: 20457744
references.citation: Nature. 2011 Oct 05;478(7369):395-8
references.pmid: 21976020
references.citation: Proc Natl Acad Sci U S A. 2012 Mar 27;109(13):5110-5
references.pmid: 22416119
references.citation: Nat Protoc. 2009;4(3):363-71
references.pmid: 19247286
references.citation: FEMS Microbiol Lett. 2012 Apr;329(1):1-8
references.pmid: 22112233
references.citation: Proc Natl Acad Sci U S A. 2010 Jun 1;107(22):10136-41
references.pmid: 20479238
references.citation: Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14921-5
references.pmid: 20679205
references.citation: Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
references.pmid: 12136088
references.citation: Curr Biol. 2003 Jan 21;13(2):R53-4
references.pmid: 12546803
references.citation: Plant J. 2008 Oct;56(2):181-195
references.pmid: 18564380
references.citation: J Biol Chem. 1988 Sep 15;263(26):12959-63
references.pmid: 3047114
references.citation: BMC Evol Biol. 2004 Mar 24;4:10
references.pmid: 15038836
references.citation: Biochem J. 2003 Feb 15;370(Pt 1):57-67
references.pmid: 12413398
references.citation: Biochemistry. 1995 Aug 15;34(32):10310-8
references.pmid: 7640287
references.citation: BMC Evol Biol. 2006 Mar 24;6:29
references.pmid: 16563161
references.citation: Biochem Biophys Res Commun. 2000 Dec 20;279(2):313-9
references.pmid: 11118284
references.citation: Nucleic Acids Res. 2011 Jan;39(Database issue):D32-7
references.pmid: 21071399
references.citation: Plant Physiol. 2012 Mar;158(3):1342-58
references.pmid: 22247271
references.citation: Plant Cell. 2009 Jul;21(7):1897-911
references.pmid: 19584142
references.citation: Microbiology (Reading). 2008 Apr;154(Pt 4):1204-1217
references.pmid: 18375813
references.citation: Int J Parasitol. 2012 May 15;42(6):597-612
references.pmid: 22543039
references.citation: Proc Natl Acad Sci U S A. 2009 Oct 6;106(40):17223-8
references.pmid: 19805099
references.citation: Mol Plant Pathol. 2001 Jul 1;2(4):187-98
references.pmid: 20573006
references.citation: Nat Methods. 2011 Sep 29;8(10):785-6
references.pmid: 21959131
references.citation: Mol Microbiol. 1990 Feb;4(2):295-304
references.pmid: 2110997
references.citation: Nucleic Acids Res. 2011 Jul;39(Web Server issue):W29-37
references.pmid: 21593126
references.citation: Nat Rev Genet. 2003 Feb;4(2):121-32
references.pmid: 12560809
references.citation: Nucleic Acids Res. 2010 Jan;38(Database issue):D204-10
references.pmid: 20015972
references.citation: J Biol Chem. 1999 Jan 22;274(4):2360-5
references.pmid: 9891003
references.citation: Front Microbiol. 2012 Apr 17;3:132
references.pmid: 22529840
references.citation: J Biol Chem. 1997 May 30;272(22):14412-9
references.pmid: 9162080
references.citation: Bioinformatics. 2002 Mar;18(3):502-4
references.pmid: 11934758
references.citation: Nucleic Acids Res. 2012 Jan;40(Database issue):D343-50
references.pmid: 22086950
references.citation: Proc Natl Acad Sci U S A. 2010 Mar 30;107(13):5897-902
references.pmid: 20304790
references.citation: Mol Biol Evol. 2005 Oct;22(10):1948-63
references.pmid: 15944438
references.citation: Plant Physiol. 1996 Aug;111(4):1209-18
references.pmid: 8756501
references.citation: Plant Mol Biol. 1999 Mar;39(4):749-60
references.pmid: 10350089
references.citation: Nat Genet. 2006 Aug;38(8):953-6
references.pmid: 16832356
references.citation: Protein Eng. 1991 Oct;4(7):719-37
references.pmid: 1798697
references.citation: Syst Biol. 2003 Oct;52(5):696-704
references.pmid: 14530136
references.citation: Plant J. 2009 Jun;58(5):766-77
references.pmid: 19220794
references.citation: Curr Microbiol. 2008 Mar;56(3):256-60
references.pmid: 18071791
references.citation: Biochemistry (Mosc). 2007 Mar;72(3):345-50
references.pmid: 17447890
references.citation: Annu Rev Phytopathol. 2000 Sep;38:325-363
references.pmid: 11701846
references.citation: PLoS One. 2009 Aug 05;4(8):e6515
references.pmid: 19654869
references.citation: EMBO J. 2010 Mar 17;29(6):1149-61
references.pmid: 20111004
references.citation: Mol Plant Pathol. 2001 Mar 1;2(2):101-8
references.pmid: 20572997
references.citation: Trends Genet. 2010 Jan;26(1):5-8
references.pmid: 19969385
references.citation: Bioinformatics. 2003 Aug 12;19(12):1572-4
references.pmid: 12912839
references.citation: Nat Rev Genet. 2008 Aug;9(8):605-18
references.pmid: 18591983
references.citation: Plant Signal Behav. 2010 Feb;5(2):180-3
references.pmid: 20173418
references.citation: Mol Biol Evol. 2011 Dec;28(12):3395-404
references.pmid: 21727238
references.citation: Bioinformatics. 2009 Aug 1;25(15):1972-3
references.pmid: 19505945
references.citation: Nucleic Acids Res. 2012 Jan;40(Database issue):D290-301
references.pmid: 22127870
references.citation: Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
references.pmid: 9254694
references.citation: BMC Evol Biol. 2009 Jul 19;9:168
references.pmid: 19615101
references.citation: Plant Cell. 2004 Apr;16(4):857-73
references.pmid: 15020745
references.citation: Bioinformatics. 2006 Nov 1;22(21):2688-90
references.pmid: 16928733
references.citation: BMC Genomics. 2006 Aug 09;7:200
references.pmid: 16895613
references.citation: J Biosci. 2002 Feb;27(1 Suppl 1):27-33
references.pmid: 11927775
references.citation: Proc Natl Acad Sci U S A. 1989 Aug;86(16):6201-5
references.pmid: 2762323
references.citation: Curr Biol. 2006 Sep 19;16(18):1857-64
references.pmid: 16979565
references.citation: Nucleic Acids Res. 2007 Jul;35(Web Server issue):W585-7
references.pmid: 17517783
references.citation: Curr Opin Struct Biol. 2009 Jun;19(3):341-8
references.pmid: 19481444
references.citation: Protein Sci. 1997 Mar;6(3):501-23
references.pmid: 9070434
references.citation: J Mol Evol. 2004 Apr;58(4):424-41
references.pmid: 15114421
references.citation: EMBO J. 2003 Jan 2;22(1):60-9
references.pmid: 12505984
references.citation: Biotechnol Lett. 2005 Aug;27(15):1123-8
references.pmid: 16132863
references.citation: J Microbiol Biotechnol. 2012 Apr;22(4):563-6
references.pmid: 22534306
references.citation: Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4489-94
references.pmid: 17360551
references.citation: Nat Rev Microbiol. 2009 Nov;7(11):787-97
references.pmid: 19806153
references.citation: Evolution. 2005 Jun;59(6):1245-58
references.pmid: 16050101
references.citation: Syst Biol. 2006 Aug;55(4):539-52
references.pmid: 16785212
references.citation: J Biol Chem. 2010 Sep 24;285(39):29797-807
references.pmid: 20639575
references.citation: Environ Biosafety Res. 2007 Jan-Jun;6(1-2):3-13
references.pmid: 17961477
references.citation: Nature. 2000 May 18;405(6784):299-304
references.pmid: 10830951
references.citation: Nat Genet. 2012 Sep;44(9):1060-5
references.pmid: 22885923
references.citation: Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6332-7
references.pmid: 8692815