title: Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria.
abstract: Cell wall-bound invertase (cw-Inv) plays an important role in carbohydrate partitioning and regulation of sink-source interaction. There is increasing evidence that pathogens interfere with sink-source interaction, and induction of cw-Inv activity has frequently been shown in response to pathogen infection. To investigate the role of cw-Inv, transgenic tomato (Solanum lycopersicum) plants silenced for the major leaf cw-Inv isoforms were generated and analyzed during normal growth and during the compatible interaction with Xanthomonas campestris pv vesicatoria. Under normal growth conditions, activities of sucrolytic enzymes as well as photosynthesis and respiration were unaltered in the transgenic plants compared with wild-type plants. However, starch levels of source leaves were strongly reduced, which was most likely caused by an enhanced sucrose exudation rate. Following X. campestris pv vesicatoria infection, cw-Inv-silenced plants showed an increased sucrose to hexose ratio in the apoplast of leaves. Symptom development, inhibition of photosynthesis, and expression of photosynthetic genes were clearly delayed in transgenic plants compared with wild-type plants. In addition, induction of senescence-associated and pathogenesis-related genes observed in infected wild-type plants was abolished in cw-Inv-silenced tomato lines. These changes were not associated with decreased bacterial growth. In conclusion, cw-Inv restricts carbon export from source leaves and regulates the sucrose to hexose ratio in the apoplast. Furthermore, an increased apoplastic hexose to sucrose ratio can be linked to inhibition of photosynthesis and induction of pathogenesis-related gene expression but does not significantly influence bacterial growth. Indirectly, bacteria may benefit from low invertase activity, since the longevity of host cells is raised and basal defense might be dampened.
authors.affiliation: Friedrich-Alexander Universität Erlangen-Nürnberg, Lehrstuhl für Biochemie, 91058 Erlangen, Germany.
authors.forename: Nurcan
authors.initials: N
authors.lastname: Kocal
authors.forename: Uwe
authors.initials: U
authors.lastname: Sonnewald
authors.forename: Sophia
authors.initials: S
authors.lastname: Sonnewald
mesh_terms: D002473:Cell Wall / Q000201:enzymology* / Q000378:metabolism; D018551:Solanum lycopersicum / Q000378:metabolism / Q000382:microbiology / Q000502:physiology*; D008969:Molecular Sequence Data; D010788:Photosynthesis; D030821:Plants, Genetically Modified; D013395:Sucrose / Q000378:metabolism*; D016959:Xanthomonas campestris / Q000254:growth & development / Q000502:physiology*; D043324:beta-Fructofuranosidase / Q000378:metabolism*
chemical_list: D013395:Sucrose; D043324:beta-Fructofuranosidase
references.citation: J Plant Physiol. 2008 Jan;165(1):19-28
references.pmid: 17689830
references.citation: Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:509-540
references.pmid: 15012299
references.citation: Cell. 2005 Jun 3;121(5):749-59
references.pmid: 15935761
references.citation: J Exp Bot. 2007;58(15-16):4019-26
references.pmid: 18182420
references.citation: Plant Physiol. 2008 Jul;147(3):1288-99
references.pmid: 18502974
references.citation: Mol Plant Pathol. 2000 Mar 1;1(2):99-113
references.pmid: 20572957
references.citation: J Mol Evol. 2005 May;60(5):615-34
references.pmid: 15983871
references.citation: Plant J. 1991 Jul;1(1):95-106
references.pmid: 1844880
references.citation: Plant J. 1995 Jan;7(1):97-107
references.pmid: 7894514
references.citation: Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8577-82
references.pmid: 12817082
references.citation: J Exp Bot. 2006;57(3):547-57
references.pmid: 16377736
references.citation: Plant Physiol. 1949 Jan;24(1):1-15
references.pmid: 16654194
references.citation: J Exp Bot. 2005 Jun;56(416):1469-79
references.pmid: 15863446
references.citation: Plant Biotechnol J. 2006 Mar;4(2):231-42
references.pmid: 17177799
references.citation: Annu Rev Phytopathol. 2004;42:385-414
references.pmid: 15283671
references.citation: Plant Physiol. 2003 Feb;131(2):603-9
references.pmid: 12586884
references.citation: J Exp Bot. 2003 Jan;54(382):525-31
references.pmid: 12508063
references.citation: Trends Plant Sci. 2004 Dec;9(12):606-13
references.pmid: 15564128
references.citation: J Exp Bot. 2000 Feb;51 Spec No:439-45
references.pmid: 10938852
references.citation: Anal Biochem. 1976 May 7;72:248-54
references.pmid: 942051
references.citation: Plant Cell. 1992 Feb;4(2):129-134
references.pmid: 12297644
references.citation: Physiol Plant. 2001 Apr;111(4):457-465
references.pmid: 11299010
references.citation: J Exp Bot. 2003 Jan;54(382):513-24
references.pmid: 12508062
references.citation: Plant Cell. 2003 Feb;15(2):317-30
references.pmid: 12566575
references.citation: Plant Cell Environ. 2008 Jan;31(1):165-76
references.pmid: 17999659
references.citation: Biometrika. 1947;34(1-2):28-35
references.pmid: 20287819
references.citation: FEBS Lett. 2007 May 29;581(13):2401-10
references.pmid: 17485088
references.citation: Annu Rev Plant Physiol Plant Mol Biol. 2000 Jun;51:49-81
references.pmid: 15012186
references.citation: Science. 2004 Sep 17;305(5691):1786-9
references.pmid: 15375271
references.citation: Plant Cell. 1992 Mar;4(3):297-305
references.pmid: 12297647
references.citation: Mol Plant Microbe Interact. 2008 Feb;21(2):269-82
references.pmid: 18184070
references.citation: Plant Mol Biol. 1992 Nov;20(3):513-27
references.pmid: 1421154
references.citation: Plant Cell Rep. 1998 Aug;17(11):843-847
references.pmid: 30736554
references.citation: Proc Natl Acad Sci U S A. 2001 May 22;98(11):6522-7
references.pmid: 11371651
references.citation: Mol Plant Pathol. 2000 Jan 1;1(1):51-9
references.pmid: 20572950
references.citation: Plant Cell. 2007 May;19(5):1649-64
references.pmid: 17513504
references.citation: Annu Rev Plant Biol. 2006;57:675-709
references.pmid: 16669778
references.citation: Plant Cell. 2008 Jul;20(7):1915-29
references.pmid: 18664616
references.citation: Plant J. 2006 Apr;46(1):14-33
references.pmid: 16553893
references.citation: Plant Cell. 1996 May;8(5):793-803
references.pmid: 12239401
references.citation: J Allergy Clin Immunol. 2006 Nov;118(5):1176-83
references.pmid: 17088146
references.citation: Plant Mol Biol. 1990 Apr;14(4):527-36
references.pmid: 2102832
references.citation: Plant Cell Environ. 2006 Jun;29(6):1061-76
references.pmid: 17080933
references.citation: EMBO J. 1990 Oct;9(10):3033-44
references.pmid: 2209536
references.citation: Mol Plant Microbe Interact. 2006 Jun;19(6):625-34
references.pmid: 16776296
references.citation: J Bacteriol. 2005 Sep;187(17):6231-7
references.pmid: 16109965
references.citation: Trends Plant Sci. 2002 May;7(5):193-5
references.pmid: 11992820
references.citation: FEBS Lett. 1996 Nov 18;397(2-3):239-44
references.pmid: 8955355
references.citation: Anal Biochem. 1987 May 15;163(1):16-20
references.pmid: 2441623
references.citation: J Plant Physiol. 2006 Feb;163(3):307-18
references.pmid: 16368160
references.citation: Plant Physiol. 2002 Apr;128(4):1480-9
references.pmid: 11950996
references.citation: Plant Physiol Biochem. 2004 May;42(5):437-44
references.pmid: 15191748
references.citation: Plant Physiol. 2007 Nov;145(3):905-18
references.pmid: 17827265
references.citation: Planta. 2006 Dec;225(1):1-12
references.pmid: 16807755
references.citation: Funct Plant Biol. 2007 Jun;34(6):499-507
references.pmid: 32689379
references.citation: Trends Plant Sci. 2006 Dec;11(12):581-6
references.pmid: 17092762
references.citation: Nat Biotechnol. 1997 Aug;15(8):794-7
references.pmid: 9255797
references.citation: Plant Physiol. 1997 Sep;115(1):273-82
references.pmid: 9306701