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.
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.
Kocal
Nurcan
N
Friedrich-Alexander Universität Erlangen-Nürnberg, Lehrstuhl für Biochemie, 91058 Erlangen, Germany.
Sonnewald
Uwe
U
Sonnewald
Sophia
S
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*
D013395:Sucrose; D043324:beta-Fructofuranosidase
J Plant Physiol. 2008 Jan;165(1):19-28
17689830
Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:509-540
15012299
Cell. 2005 Jun 3;121(5):749-59
15935761
J Exp Bot. 2007;58(15-16):4019-26
18182420
Plant Physiol. 2008 Jul;147(3):1288-99
18502974
Mol Plant Pathol. 2000 Mar 1;1(2):99-113
20572957
J Mol Evol. 2005 May;60(5):615-34
15983871
Plant J. 1991 Jul;1(1):95-106
1844880
Plant J. 1995 Jan;7(1):97-107
7894514
Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8577-82
12817082
J Exp Bot. 2006;57(3):547-57
16377736
Plant Physiol. 1949 Jan;24(1):1-15
16654194
J Exp Bot. 2005 Jun;56(416):1469-79
15863446
Plant Biotechnol J. 2006 Mar;4(2):231-42
17177799
Annu Rev Phytopathol. 2004;42:385-414
15283671
Plant Physiol. 2003 Feb;131(2):603-9
12586884
J Exp Bot. 2003 Jan;54(382):525-31
12508063
Trends Plant Sci. 2004 Dec;9(12):606-13
15564128
J Exp Bot. 2000 Feb;51 Spec No:439-45
10938852
Anal Biochem. 1976 May 7;72:248-54
942051
Plant Cell. 1992 Feb;4(2):129-134
12297644
Physiol Plant. 2001 Apr;111(4):457-465
11299010
J Exp Bot. 2003 Jan;54(382):513-24
12508062
Plant Cell. 2003 Feb;15(2):317-30
12566575
Plant Cell Environ. 2008 Jan;31(1):165-76
17999659
Biometrika. 1947;34(1-2):28-35
20287819
FEBS Lett. 2007 May 29;581(13):2401-10
17485088
Annu Rev Plant Physiol Plant Mol Biol. 2000 Jun;51:49-81
15012186
Science. 2004 Sep 17;305(5691):1786-9
15375271
Plant Cell. 1992 Mar;4(3):297-305
12297647
Mol Plant Microbe Interact. 2008 Feb;21(2):269-82
18184070
Plant Mol Biol. 1992 Nov;20(3):513-27
1421154
Plant Cell Rep. 1998 Aug;17(11):843-847
30736554
Proc Natl Acad Sci U S A. 2001 May 22;98(11):6522-7
11371651
Mol Plant Pathol. 2000 Jan 1;1(1):51-9
20572950
Plant Cell. 2007 May;19(5):1649-64
17513504
Annu Rev Plant Biol. 2006;57:675-709
16669778
Plant Cell. 2008 Jul;20(7):1915-29
18664616
Plant J. 2006 Apr;46(1):14-33
16553893
Plant Cell. 1996 May;8(5):793-803
12239401
J Allergy Clin Immunol. 2006 Nov;118(5):1176-83
17088146
Plant Mol Biol. 1990 Apr;14(4):527-36
2102832
Plant Cell Environ. 2006 Jun;29(6):1061-76
17080933
EMBO J. 1990 Oct;9(10):3033-44
2209536
Mol Plant Microbe Interact. 2006 Jun;19(6):625-34
16776296
J Bacteriol. 2005 Sep;187(17):6231-7
16109965
Trends Plant Sci. 2002 May;7(5):193-5
11992820
FEBS Lett. 1996 Nov 18;397(2-3):239-44
8955355
Anal Biochem. 1987 May 15;163(1):16-20
2441623
J Plant Physiol. 2006 Feb;163(3):307-18
16368160
Plant Physiol. 2002 Apr;128(4):1480-9
11950996
Plant Physiol Biochem. 2004 May;42(5):437-44
15191748
Plant Physiol. 2007 Nov;145(3):905-18
17827265
Planta. 2006 Dec;225(1):1-12
16807755
Funct Plant Biol. 2007 Jun;34(6):499-507
32689379
Trends Plant Sci. 2006 Dec;11(12):581-6
17092762
Nat Biotechnol. 1997 Aug;15(8):794-7
9255797
Plant Physiol. 1997 Sep;115(1):273-82
9306701