title: Role of beta-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato.
abstract: Jasmonic acid (JA) is a lipid-derived signal that regulates plant defense responses to biotic stress. Here, we report the characterization of a JA-deficient mutant of tomato (Lycopersicon esculentum) that lacks local and systemic expression of defensive proteinase inhibitors (PIs) in response to wounding. Map-based cloning studies demonstrated that this phenotype results from loss of function of an acyl-CoA oxidase (ACX1A) that catalyzes the first step in the peroxisomal beta-oxidation stage of JA biosynthesis. Recombinant ACX1A exhibited a preference for C12 and C14 straight-chain acyl-CoAs and also was active in the metabolism of C18 cyclopentanoid-CoA precursors of JA. The overall growth, development, and reproduction of acx1 plants were similar to wild-type plants. However, the mutant was compromised in its defense against tobacco hornworm (Manduca sexta) attack. Grafting experiments showed that loss of ACX1A function disrupts the production of the transmissible signal for wound-induced PI expression but does not affect the recognition of this signal in undamaged responding leaves. We conclude that ACX1A is essential for the beta-oxidation stage of JA biosynthesis and that JA or its derivatives is required both for antiherbivore resistance and the production of the systemic wound signal. These findings support a role for peroxisomes in the production of lipid-based signaling molecules that promote systemic defense responses.
authors.affiliation: Department of Energy-Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, USA.
authors.forename: Chuanyou
authors.initials: C
authors.lastname: Li
authors.forename: Anthony L
authors.initials: AL
authors.lastname: Schilmiller
authors.forename: Guanghui
authors.initials: G
authors.lastname: Liu
authors.forename: Gyu In
authors.initials: GI
authors.lastname: Lee
authors.forename: Sastry
authors.initials: S
authors.lastname: Jayanty
authors.forename: Carolyn
authors.initials: C
authors.lastname: Sageman
authors.forename: Julia
authors.initials: J
authors.lastname: Vrebalov
authors.forename: James J
authors.initials: JJ
authors.lastname: Giovannoni
authors.forename: Kaori
authors.initials: K
authors.lastname: Yagi
authors.forename: Yuichi
authors.initials: Y
authors.lastname: Kobayashi
authors.forename: Gregg A
authors.initials: GA
authors.lastname: Howe
mesh_terms: D042962:Acyl-CoA Oxidase / Q000235:genetics / Q000378:metabolism; D000818:Animals; D001483:Base Sequence; D002874:Chromosome Mapping; D003517:Cyclopentanes / Q000378:metabolism*; D018744:DNA, Plant / Q000235:genetics; D017343:Genes, Plant; D018551:Solanum lycopersicum / Q000235:genetics / Q000378:metabolism* / Q000469:parasitology; D018402:Manduca / Q000472:pathogenicity; D008969:Molecular Sequence Data; D009154:Mutation; D010084:Oxidation-Reduction; D054883:Oxylipins; D020675:Peroxisomes / Q000378:metabolism; D010641:Phenotype; D010935:Plant Diseases / Q000235:genetics / Q000469:parasitology; D011994:Recombinant Proteins / Q000235:genetics / Q000378:metabolism; D015398:Signal Transduction
chemical_list: D003517:Cyclopentanes; D018744:DNA, Plant; D054883:Oxylipins; D011994:Recombinant Proteins; C011006:jasmonic acid; D042962:Acyl-CoA Oxidase
references.citation: Prog Nucleic Acid Res Mol Biol. 2002;72:165-221
references.pmid: 12206452
references.citation: Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12837-42
references.pmid: 11592974
references.citation: Plant J. 2003 Feb;33(3):577-89
references.pmid: 12581315
references.citation: Plant J. 2002 Nov;32(3):299-315
references.pmid: 12410809
references.citation: Plant Cell. 1992 Feb;4(2):129-134
references.pmid: 12297644
references.citation: Am J Physiol Regul Integr Comp Physiol. 2001 Aug;281(2):R391-400
references.pmid: 11448840
references.citation: Anal Biochem. 1980 Sep 1;107(1):193-8
references.pmid: 6776842
references.citation: Nat Prod Rep. 1998 Dec;15(6):533-48
references.pmid: 10036771
references.citation: Plant Cell. 2002;14 Suppl:S153-64
references.pmid: 12045275
references.citation: Plant Cell. 1998 Feb;10(2):183-95
references.pmid: 9490742
references.citation: Plant J. 2003 Feb;33(3):567-76
references.pmid: 12581314
references.citation: Plant Physiol. 2001 Nov;127(3):1266-78
references.pmid: 11706205
references.citation: Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6416-21
references.pmid: 11959903
references.citation: Genetics. 1992 Dec;132(4):1141-60
references.pmid: 1360934
references.citation: Plant Mol Biol. 1998 Sep;38(1-2):163-89
references.pmid: 9738966
references.citation: J Exp Bot. 2001 Jan;52(354):11-23
references.pmid: 11181709
references.citation: Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8794-7
references.pmid: 1528894
references.citation: Plant Cell. 2004 Mar;16(3):616-28
references.pmid: 14973161
references.citation: Plant Cell. 1996 Mar;8(3):403-416
references.pmid: 12239389
references.citation: Plant J. 2002 Nov;32(4):585-601
references.pmid: 12445129
references.citation: Plant Physiol. 2004 Sep;136(1):2587-608
references.pmid: 15333753
references.citation: Plant Cell. 2004 Jan;16(1):126-43
references.pmid: 14688297
references.citation: Plant Cell. 2003 Jul;15(7):1646-61
references.pmid: 12837953
references.citation: Biochem Biophys Res Commun. 1979 Apr 27;87(4):1200-6
references.pmid: 465034
references.citation: Plant Physiol. 2003 Jun;132(2):1065-76
references.pmid: 12805634
references.citation: Plant Cell. 2004 Aug;16(8):2117-27
references.pmid: 15258265
references.citation: Science. 2002 May 31;296(5573):1649-50
references.pmid: 12040182
references.citation: Plant J. 2000 Oct;24(1):113-26
references.pmid: 11029709
references.citation: J Org Chem. 2003 Oct 3;68(20):7825-32
references.pmid: 14510562
references.citation: Plant J. 1999 Oct;20(1):1-13
references.pmid: 10571860
references.citation: Plant J. 2004 Sep;39(5):790-808
references.pmid: 15315639
references.citation: Proc Natl Acad Sci U S A. 2000 Sep 12;97(19):10625-30
references.pmid: 10973494
references.citation: Nucleic Acids Res. 1997 Dec 15;25(24):4876-82
references.pmid: 9396791
references.citation: Biochem Soc Trans. 2000 Dec;28(6):755-7
references.pmid: 11171196
references.citation: EMBO J. 2002 Jun 17;21(12):2912-22
references.pmid: 12065405
references.citation: Plant Physiol. 2002 Sep;130(1):494-503
references.pmid: 12226528
references.citation: J Mol Biol. 1990 Oct 5;215(3):403-10
references.pmid: 2231712
references.citation: Plant Physiol. 2004 May;135(1):85-94
references.pmid: 15141068
references.citation: Biochim Biophys Acta. 2000 Mar 7;1477(1-2):112-21
references.pmid: 10708853
references.citation: Plant J. 2003 Nov;36(4):485-99
references.pmid: 14617079
references.citation: Biol Chem. 2000 Aug;381(8):741-8
references.pmid: 11030431
references.citation: Biol Chem. 2003 Mar;384(3):437-46
references.pmid: 12715894
references.citation: Trends Plant Sci. 2001 Apr;6(4):145-50
references.pmid: 11286918
references.citation: Plant Physiol. 2000 Jun;123(2):733-42
references.pmid: 10859203
references.citation: Eur J Biochem. 2004 Feb;271(3):483-93
references.pmid: 14728675
references.citation: Plant Physiol. 1999 Sep;121(1):153-62
references.pmid: 10482670
references.citation: Trends Plant Sci. 2003 Jun;8(6):247-50
references.pmid: 12818656
references.citation: Plant Mol Biol. 2001 Nov;47(4):519-31
references.pmid: 11669577
references.citation: Proc Natl Acad Sci U S A. 2002 May 14;99(10):6519-20
references.pmid: 12011413
references.citation: FEBS Lett. 1994 May 23;345(1):9-13
references.pmid: 8194607
references.citation: Genome Res. 2000 Jan;10(1):129-36
references.pmid: 10645957
references.citation: Trends Plant Sci. 2002 May;7(5):217-24
references.pmid: 11992827
references.citation: Prog Lipid Res. 2002 Mar;41(2):156-81
references.pmid: 11755682
references.citation: EMBO J. 2000 Dec 15;19(24):6770-7
references.pmid: 11118212
references.citation: Plant Physiol. 1984 Jun;75(2):458-61
references.pmid: 16663643
references.citation: Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1786-91
references.pmid: 14745029
references.citation: Plant Cell. 2001 Jan;13(1):179-91
references.pmid: 11158538
references.citation: J Biochem. 2002 Mar;131(3):365-74
references.pmid: 11872165
references.citation: Genome Res. 1998 Mar;8(3):175-85
references.pmid: 9521921
references.citation: Mol Gen Genet. 1993 Dec;241(5-6):595-601
references.pmid: 8264534
references.citation: J Biol Chem. 2004 Feb 27;279(9):7487-94
references.pmid: 14660652
references.citation: Biol Chem. 2000 Aug;381(8):715-22
references.pmid: 11030429
references.citation: Plant Physiol. 2003 Jun;132(2):999-1010
references.pmid: 12805628
references.citation: J Biol Chem. 2000 Nov 3;275(44):34375-81
references.pmid: 10918060
references.citation: Plant Cell Physiol. 2002 Apr;43(4):384-92
references.pmid: 11978866
references.citation: Plant Physiol. 2004 May;135(1):161-72
references.pmid: 15133155
references.citation: Plant Cell Physiol. 2003 Jun;44(6):643-8
references.pmid: 12826630