title: Pseudomonas syringae pv. syringae uses proteasome inhibitor syringolin A to colonize from wound infection sites.
abstract: Infection of plants by bacterial leaf pathogens at wound sites is common in nature. Plants defend wound sites to prevent pathogen invasion, but several pathogens can overcome spatial restriction and enter leaf tissues. The molecular mechanisms used by pathogens to suppress containment at wound infection sites are poorly understood. Here, we studied Pseudomonas syringae strains causing brown spot on bean and blossom blight on pear. These strains exist as epiphytes that can cause disease upon wounding caused by hail, sand storms and frost. We demonstrate that these strains overcome spatial restriction at wound sites by producing syringolin A (SylA), a small molecule proteasome inhibitor. Consequently, SylA-producing strains are able to escape from primary infection sites and colonize adjacent tissues along the vasculature. We found that SylA diffuses from the primary infection site and suppresses acquired resistance in adjacent tissues by blocking signaling by the stress hormone salicylic acid (SA). Thus, SylA diffusion creates a zone of SA-insensitive tissue that is prepared for subsequent colonization. In addition, SylA promotes bacterial motility and suppresses immune responses at the primary infection site. These local immune responses do not affect bacterial growth and were weak compared to effector-triggered immunity. Thus, SylA facilitates colonization from wounding sites by increasing bacterial motility and suppressing SA signaling in adjacent tissues.
authors.affiliation: Plant Chemetics Lab, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
authors.forename: Johana C
authors.initials: JC
authors.lastname: Misas-Villamil
authors.forename: Izabella
authors.initials: I
authors.lastname: Kolodziejek
authors.forename: Emerson
authors.initials: E
authors.lastname: Crabill
authors.forename: Farnusch
authors.initials: F
authors.lastname: Kaschani
authors.forename: Sherry
authors.initials: S
authors.lastname: Niessen
authors.forename: Takayuki
authors.initials: T
authors.lastname: Shindo
authors.forename: Markus
authors.initials: M
authors.lastname: Kaiser
authors.forename: James R
authors.initials: JR
authors.lastname: Alfano
authors.forename: Renier A L
authors.initials: RA
authors.lastname: van der Hoorn
mesh_terms: D000595:Amino Acid Sequence; D054884:Host-Pathogen Interactions; D008969:Molecular Sequence Data; D010456:Peptides, Cyclic / Q000378:metabolism*; D010935:Plant Diseases / Q000382:microbiology*; D010940:Plant Proteins; D046988:Proteasome Endopeptidase Complex / Q000235:genetics; D061988:Proteasome Inhibitors / Q000378:metabolism*; D044224:Pseudomonas syringae / Q000378:metabolism*; D015398:Signal Transduction; D014026:Nicotiana / Q000382:microbiology*; D014946:Wound Infection / Q000382:microbiology*
chemical_list: D010456:Peptides, Cyclic; D010940:Plant Proteins; D061988:Proteasome Inhibitors; C407267:syringolin A; D046988:Proteasome Endopeptidase Complex
references.citation: Nature. 2011 Oct 05;478(7369):395-8
references.pmid: 21976020
references.citation: Microbiol Mol Biol Rev. 2000 Sep;64(3):624-53
references.pmid: 10974129
references.citation: Cell Microbiol. 2004 Mar;6(3):201-11
references.pmid: 14764104
references.citation: Mol Plant Microbe Interact. 2007 Aug;20(8):955-65
references.pmid: 17722699
references.citation: Med Res Rev. 2008 Mar;28(2):309-27
references.pmid: 17880010
references.citation: Plant J. 2007 Apr;50(2):253-64
references.pmid: 17355437
references.citation: Plant J. 2003 Nov;36(3):342-52
references.pmid: 14617091
references.citation: Mol Plant Microbe Interact. 2010 Aug;23(8):991-9
references.pmid: 20615110
references.citation: Curr Biol. 1998 Oct 8;8(20):1129-32
references.pmid: 9778530
references.citation: Genes Dev. 2009 Nov 1;23(21):2496-506
references.pmid: 19833761
references.citation: Gene. 1990 Apr 30;89(1):37-46
references.pmid: 2115488
references.citation: Nature. 2006 Nov 16;444(7117):323-9
references.pmid: 17108957
references.citation: Plant J. 1996 Mar;9(3):341-56
references.pmid: 8919911
references.citation: Plant J. 2010 May 1;62(4):628-40
references.pmid: 20163553
references.citation: Chembiochem. 2009 Nov 2;10(16):2638-43
references.pmid: 19746508
references.citation: Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15977-82
references.pmid: 14665692
references.citation: Appl Environ Microbiol. 1999 Apr;65(4):1435-43
references.pmid: 10103233
references.citation: Plant J. 2007 Feb;49(4):607-18
references.pmid: 17217460
references.citation: Mol Plant Microbe Interact. 2010 Oct;23(10):1287-93
references.pmid: 20831408
references.citation: Curr Opin Microbiol. 2009 Feb;12(1):53-60
references.pmid: 19168384
references.citation: Mol Plant Microbe Interact. 2004 Jan;17(1):90-7
references.pmid: 14714872
references.citation: Plant Cell. 2010 Apr;22(4):1388-403
references.pmid: 20435900
references.citation: Plant Physiol. 2011 Jan;155(1):477-89
references.pmid: 21045122
references.citation: Plant Physiol. 2002 Mar;128(3):1046-56
references.pmid: 11891259
references.citation: Mol Microbiol. 2006 Oct;62(1):26-44
references.pmid: 16942603
references.citation: Annu Rev Phytopathol. 2009;47:177-206
references.pmid: 19400653
references.citation: Mol Plant Microbe Interact. 2008 Aug;21(8):1015-26
references.pmid: 18616398
references.citation: Proc Natl Acad Sci U S A. 2009 Apr 21;106(16):6507-12
references.pmid: 19359491
references.citation: Plant J. 2003 Feb;33(4):733-42
references.pmid: 12609045
references.citation: Cell Host Microbe. 2012 Jun 14;11(6):587-96
references.pmid: 22704619
references.citation: Plant J. 2010 Apr 1;62(1):160-70
references.pmid: 20042019
references.citation: Plant Cell. 2012 Jan;24(1):336-52
references.pmid: 22286136
references.citation: EMBO J. 2003 Nov 3;22(21):5690-9
references.pmid: 14592968
references.citation: Genetics. 2006 Oct;174(2):1041-56
references.pmid: 16951068
references.citation: Plant J. 2011 Sep;67(5):774-82
references.pmid: 21554458
references.citation: Science. 2006 Jul 14;313(5784):220-3
references.pmid: 16840699
references.citation: Cell. 2006 Sep 8;126(5):969-80
references.pmid: 16959575
references.citation: Mol Plant Pathol. 2010 Sep;11(5):597-611
references.pmid: 20695999
references.citation: Proc Natl Acad Sci U S A. 2005 Feb 1;102(5):1791-6
references.pmid: 15657122
references.citation: Appl Environ Microbiol. 2006 Jan;72(1):702-12
references.pmid: 16391110
references.citation: BMC Biochem. 2009 Oct 28;10:26
references.pmid: 19863801
references.citation: PLoS Pathog. 2009 Apr;5(4):e1000388
references.pmid: 19381254
references.citation: Plant J. 2007 Jul;51(1):32-46
references.pmid: 17559511
references.citation: Plant J. 2004 Dec;40(6):942-56
references.pmid: 15584959
references.citation: Plant Physiol. 2012 Apr;158(4):1803-18
references.pmid: 22319072
references.citation: Nature. 2007 Jul 19;448(7151):370-4
references.pmid: 17637671
references.citation: Appl Environ Microbiol. 1996 Jul;62(7):2560-6
references.pmid: 16535362
references.citation: Cell. 1993 Jul 2;73(7):1255-66
references.pmid: 8324821
references.citation: Cell. 2009 May 29;137(5):860-72
references.pmid: 19490895
references.citation: Nature. 2008 Apr 10;452(7188):755-8
references.pmid: 18401409