Constitutive expression of a grapevine polygalacturonase-inhibiting protein affects gene expression and cell wall properties in uninfected tobacco

BMC Research Notes

Volumn 4, Issue , 2011, Pages

  Alexandersson, Erik ^a,d   Becker, John V W ^a,e   Jacobson, Dan ^a   Nguema Ona, Eric ^a   Steyn, Cobus ^a   Denby, Katherine J ^b,c   Vivier, Melané A ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^e UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

BOTRYTIS; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; SOLANUM TUBEROSUM; VITACEAE; VITIS; VITIS VINIFERA;

EID: 81055126989     PISSN: None     EISSN: 17560500     Source Type: Journal    
DOI: 10.1186/1756-0500-4-493     Document Type: Article

References (72)

1. The role of polygalacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi. De Lorenzo G, D'Ovidio R, Cervone F, Annu Rev Phytopathol 2001 39 313 335 10.1146/annurev.phyto.39.1.313 11701868 (Pubitemid 32965188)
2. Polygalacturonase is a virulence factor in Agrobacterium tumefaciens biovar 3. Rodriguez-Palenzuela P, Burr TJ, Collmer A, J Bacteriol 1991 173 20 6547 6552 1655716
3. Molecular genetic evidence for the involvement of a specific polygalacturonase, P2c, in the invasion and spread of Aspergillus flavus in cotton bolls. Shieh MT, Brown RL, Whitehead MP, Cary JW, Cotty PJ, Cleveland TE, Dean RA, Appl Environ Microbiol 1997 63 9 3548 3552 9293005 (Pubitemid 27383151)
4. The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. ten Have A, Mulder W, Visser J, van Kan JA, Mol Plant Microbe Interact 1998 11 10 1009 1016 10.1094/MPMI.1998.11.10.1009 9768518 (Pubitemid 28456203)
5. Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. Kars I, Krooshof GH, Wagemakers L, Joosten R, Benen JA, van Kan JA, Plant J 2005 43 2 213 225 10.1111/j.1365-313X.2005.02436.x 15998308 (Pubitemid 41009339)
6. The grapevine polygalacturonase-inhibiting protein (VvPGIP1) reduces Botrytis cinerea susceptibility in transgenic tobacco and differentially inhibits fungal polygalacturonases. Joubert DA, Slaughter AR, Kemp G, Becker JV, Krooshof GH, Bergmann C, Benen J, Pretorius IS, Vivier MA, Transgenic Res 2006 15 6 687 702 10.1007/s11248-006-9019-1 17072564 (Pubitemid 44833182)
7. Host-Pathogen Interactions: XXXIII. A Plant Protein Converts a Fungal Pathogenesis Factor into an Elicitor of Plant Defense Responses. Cervone F, Hahn MG, De Lorenzo G, Darvill A, Albersheim P, Plant Physiol 1989 90 2 542 548 10.1104/pp.90.2.542 16666805
8. Polygalacturonase inhibiting proteins: players in plant innate immunity? Federici L, Di Matteo A, Fernandez-Recio J, Tsernoglou D, Cervone F, Trends Plant Sci 2006 11 2 65 70 10.1016/j.tplants.2005.12.005 16406303 (Pubitemid 43238417)
9. A polygalacturonase-inhibiting protein from grapevine reduces the symptoms of the endopolygalacturonase BcPG2 from Botrytis cinerea in Nicotiana benthamiana leaves without any evidence for in vitro interaction. Joubert DA, Kars I, Wagemakers L, Bergmann C, Kemp G, Vivier MA, van Kan JA, Mol Plant Microbe Interact 2007 20 4 392 402 10.1094/MPMI-20-4-0392 17427809 (Pubitemid 46449397)
10. Polygalacturonase-inhibiting protein interacts with pectin through a binding site formed by four clustered residues of arginine and lysine. Spadoni S, Zabotina O, Di Matteo A, Mikkelsen JD, Cervone F, De Lorenzo G, Mattei B, Bellincampi D, Plant Physiol 2006 141 2 557 564 10.1104/pp.106.076950 16648220 (Pubitemid 43974550)
11. Transgenic expression of pear PGIP in tomato limits fungal colonization. Powell AL, van Kan J, ten Have A, Visser J, Greve LC, Bennett AB, Labavitch JM, Mol Plant Microbe Interact 2000 13 9 942 950 10.1094/MPMI.2000.13.9.942 10975651 (Pubitemid 30648042)
12. Evaluation of tolerance to Pierce's disease and Botrytis in transgenic plants of Vitis vinifera L. expressing the pear PGIP gene. Aguero CB, Uratsu SL, Greve C, Powell AL, Labavitch JM, Meredith CP, Dandekar AM, Mol Plant Pathol 2005 6 1 43 51 10.1111/j.1364-3703.2004.00262.x 20565637 (Pubitemid 40256955)
13. Tandemly duplicated Arabidopsis genes that encode polygalacturonase- inhibiting proteins are regulated coordinately by different signal transduction pathways in response to fungal infection. Ferrari S, Vairo D, Ausubel FM, Cervone F, De Lorenzo G, Plant Cell 2003 15 1 93 106 10.1105/tpc.005165 12509524 (Pubitemid 36137664)
14. Polygalacturonase-inhibiting protein 2 of Phaseolus vulgaris inhibits BcPG1, a polygalacturonase of Botrytis cinerea important for pathogenicity, and protects transgenic plants from infection. Manfredini C, Sicilia F, Ferrari S, Pontiggia D, Salvi G, Caprari C, Lorito M, De Lorenzo G, Physiol Mol Plant Pathol 2005 67 108 115 10.1016/j.pmpp.2005.10.002 (Pubitemid 43176467)
15. Antisense expression of the Arabidopsis thaliana AtPGIP1 gene reduces polygalacturonase-inhibiting protein accumulation and enhances susceptibility to Botrytis cinerea. Ferrari S, Galletti R, Vairo D, Cervone F, De Lorenzo G, Mol Plant Microbe Interact 2006 19 8 931 936 10.1094/MPMI-19-0931 16903359 (Pubitemid 44098625)
16. A polygalacturonase-inhibiting protein with a role in pea defence against the cyst nematode Heterodera goettingiana. Veronico P, Melillo MT, Saponaro C, Leonetti P, Picardi E, Jones JT, Mol Plant Pathol 2011 12 3 275 287 10.1111/j.1364-3703.2010.00671.x 21355999
17. A peroxisomal ABC transporter promotes seed germination by inducing pectin degradation under the control of ABI5. Kanai M, Nishimura M, Hayashi M, Plant J 2010 62 6 936 947 20345608
18. Isolation and identification of two genes encoding leucine-rich repeat (LRR) proteins differentially responsive to pathogen attack and salt stress in tobacco. Xu ZS, Xiong TF, Ni ZY, Chen XP, Chen M, Li LC, Gao DY, Yu XD, Liu P, Ma YZ, Plant Sci 2009 176 38 45 10.1016/j.plantsci.2008.09.004
19. A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Murashige T, Skoog F, Physiol Plant 1962 15 3 473 497 10.1111/j.1399-3054.1962.tb08052.x
20. Limma: linear models for microarray data. Smyth GK, In: Bioinformatics and Computational Biology Solutions using R and Bioconductor, R. Gentleman, V. Carey, S. Dudoit, R. Irizarry, W. Huber (eds.) Springer, New York, 2005 397 420
21. A comparison of background correction methods for two-colour microarrays. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A, Smyth GK, Bioinformatics (Oxford, England) 2007 23 20 2700 2707 10.1093/bioinformatics/ btm412 (Pubitemid 350048334)
22. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Ramakers C, Ruijter JM, Deprez RH, Moorman AF, Neurosci Lett 2003 339 1 62 66 10.1016/S0304-3940(02)01423-4 12618301 (Pubitemid 36263221)
23. A new mathematical model for relative quantification in real-time RT-PCR. Pfaffl MW, Nucleic Acids Res 2001 29 9 45 10.1093/nar/29.9.e45 11328886
24. Novel 'dot-blot' assays for glycosyltransferases and glycosyl hydrolases: optimisation for xyloglucan endotransglycosylase (XET) activity. Fry SC, Plant J 1997 11 1141 1150 10.1046/j.1365-313X.1997.11051141.x (Pubitemid 27236439)
25. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Bradford MM, Anal Biochem 1976 72 248 254 10.1016/0003-2697(76)90527-3 942051
26. The reb1-1 mutation of Arabidopsis. Effect on the structure and localization of galactose-containing cell wall polysaccharides. Nguema-Ona E, Andeme-Onzighi C, Aboughe-Angone S, Bardor M, Ishii T, Lerouge P, Driouich A, Plant Physiol 2006 140 4 1406 1417 10.1104/pp.105.074997 16500990 (Pubitemid 43956225)
27. Lignin distribution in wood cell walls determined by TEM and backscattered SEM techniques. Fromm J, Rockel B, Lautner S, Windeisen E, Wanner G, J Struct Biol 2003 143 1 77 84 10.1016/S1047-8477(03)00119-9 12892728 (Pubitemid 36918494)
28. Ruzin SE, Plant Microtechnique and Microscopy New York: Oxford University Press 1999
29. Soluble and wall-bound phenolics and phenolic polymers in Musa acuminata roots exposed to elicitors from Fusarium oxysporum f.sp. cubense. de Ascensao AR, Dubery IA, Phytochemistry 2003 63 6 679 686 10.1016/S0031-9422(03)00286-3 12842140 (Pubitemid 36818550)
30. The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. Schmelz EA, Engelberth J, Tumlinson JH, Block A, Alborn HT, Plant J 2004 39 5 790 808 10.1111/j.1365-313X.2004.02168.x 15315639 (Pubitemid 39218785)
31. PlantGDB: a resource for comparative plant genomics. Duvick J, Fu A, Muppirala U, Sabharwal M, Wilkerson MD, Lawrence CJ, Lushbough C, Brendel V, Nucleic Acid Res 2008 36 Database issue 959 965 18063570
32. prot4EST: translating expressed sequence tags from neglected genomes. Wasmuth JD, Blaxter ML, BMC Bioinformatics 2004 5 187 10.1186/1471-2105-5-187 15571632 (Pubitemid 40195322)
33. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ, Nucleic Acid Res 1997 25 17 3389 3402 10.1093/nar/25.17.3389 9254694 (Pubitemid 27359211)
34. Modeling sequencing errors by combining Hidden Markov models. Lottaz C, Iseli C, Jongeneel CV, Bucher P, Bioinformatics (Oxford, England) 2003 19 Suppl 2 i103 112 10.1093/bioinformatics/btg1067 (Pubitemid 41296646)
35. Amino acid translation program for full-length cDNA sequences with frameshift errors. Fukunishi Y, Hayashizaki Y, Physiol Genomics 2001 5 2 81 87 11242592 (Pubitemid 33675205)
36. PLAZA: a comparative genomics resource to study gene and genome evolution in plants. Proost S, Van Bel M, Sterck L, Billiau K, Van Parys T, Van de Peer Y, Vandepoele K, Plant Cell 2009 21 12 3718 3731 10.1105/tpc.109.071506 20040540
37. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Li L, Stoeckert CJ Jr, Roos DS, Genome Res 2003 13 9 2178 2189 10.1101/gr.1224503 12952885 (Pubitemid 37161775)
38. Integration of biological networks and gene expression data using Cytoscape. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, Christmas R, Avila-Campilo I, Creech M, Gross B, et al. Nat Protoc 2007 2 10 2366 2382 10.1038/nprot.2007.324 17947979
39. GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Zheng Q, Wang XJ, Nucleic Acid Res 2008 36 Web Server issue 358 363 18487275
40. CressExpress: a tool for large-scale mining of expression data from Arabidopsis. Srinivasasainagendra V, Page GP, Mehta T, Coulibaly I, Loraine AE, Plant Physiol 2008 147 3 1004 1016 10.1104/pp.107.115535 18467456 (Pubitemid 352844257)
41. Adaptation of the MapMan ontology to biotic stress responses: application in solanaceous species. Rotter A, Usadel B, Baebler S, Stitt M, Gruden K, Plant Methods 2007 3 10 10.1186/1746-4811-3-10 17784939 (Pubitemid 47583477)
42. Comparative analyses of six solanaceous transcriptomes reveal a high degree of sequence conservation and species-specific transcripts. Rensink WA, Lee Y, Liu J, Iobst S, Ouyang S, Buell CR, BMC Genomics 2005 6 124 10.1186/1471-2164-6-124 16162286 (Pubitemid 41372416)
43. Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray. Renn SC, Aubin-Horth N, Hofmann HA, BMC Genomics 2004 5 1 42 10.1186/1471-2164-5-42 15238158 (Pubitemid 39565312)
44. Development and application of a salmonid EST database and cDNA microarray: data mining and interspecific hybridization characteristics. Rise ML, von Schalburg KR, Brown GD, Mawer MA, Devlin RH, Kuipers N, Busby M, Beetz-Sargent M, Alberto R, Gibbs AR, et al. Genome Res 2004 14 3 478 490 10.1101/gr.1687304 14962987 (Pubitemid 38380403)
45. MIPS Arabidopsis thaliana Database (MAtDB): an integrated biological knowledge resource for plant genomics. Schoof H, Ernst R, Nazarov V, Pfeifer L, Mewes HW, Mayer KF, Nucleic Acid Res 2004 32 Database issue 373 376 14681437
46. Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Stintzi A, Weber H, Reymond P, Browse J, Farmer EE, Proc Natl Acad Sci USA 2001 98 22 12837 12842 10.1073/pnas.211311098 11592974 (Pubitemid 33020031)
47. Regulation of disease resistance pathways by AP2/ERF transcription factors. Gutterson N, Reuber TL, Curr Opin Plant Biol 2004 7 4 465 471 10.1016/j.pbi.2004.04.007 15231271 (Pubitemid 38871622)
48. Role of plant hormones in plant defence responses. Bari R, Jones JD, Plant Mol Biol 2009 69 4 473 488 10.1007/s11103-008-9435-0 19083153
49. Structure and function of the primary cell walls of plants. McNeil M, Darvill AG, Fry SC, Albersheim P, Ann Rev Biochem 1984 53 625 663 10.1146/annurev.bi.53.070184.003205 6383202
50. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Carpita NC, Gibeaut DM, Plant J 1993 3 1 1 30 10.1111/j.1365-313X.1993.tb00007.x 8401598
51. Characterization of a new xyloglucan endotransglucosylase/hydrolase (XTH) from ripening tomato fruit and implications for the diverse modes of enzymic action. Saladie M, Rose JK, Cosgrove DJ, Catala C, Plant J 2006 47 2 282 295 10.1111/j.1365-313X.2006.02784.x 16774648 (Pubitemid 43974634)
52. The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Rose JK, Braam J, Fry SC, Nishitani K, Plant Cell Physiol 2002 43 12 1421 1435 10.1093/pcp/pcf171 12514239 (Pubitemid 36100979)
53. Functional characterisation of Nicotiana tabacum xyloglucan endotransglycosylase (NtXET-1): generation of transgenic tobacco plants and changes in cell wall xyloglucan. Herbers K, Lorences EP, Barrachina C, Sonnewald U, Planta 2001 212 2 279 287 10.1007/s004250000393 11216849 (Pubitemid 32139885)
54. Expression patterns of cell wall-modifying enzymes during grape berry development. Nunan KJ, Davies C, Robinson SP, Fincher GB, Planta 2001 214 2 257 264 10.1007/s004250100609 11800390 (Pubitemid 36059277)
55. Isolation and characterization of a polygalacturonase-inhibiting protein (PGIP) and its encoding gene from Vitis vinifera L. De Ascensao ARFDC, PhD thesis, Stellenbosch University. 2001
56. Purification and characterization of enzymes exhibiting beta-D-xylosidase activities in stem tissues of Arabidopsis. Minic Z, Rihouey C, Do CT, Lerouge P, Jouanin L, Plant Physiol 2004 135 2 867 878 10.1104/pp.104.041269 15181203 (Pubitemid 38819031)
57. Phenolic compounds and their role in disease resistance. Nicholson RL, Hammerschmidt R, Annu Rev Phytopathol 1992 30 369 389 10.1146/annurev.py.30. 090192.002101 (Pubitemid 24411041)
58. Cell walls and other structural barriers in defense. Ride JP, In: Biochemical Plant Pathology, J.A. Callow (Ed) John Wiley and Sons, New York 1983 215 236
59. Tracking monolignols during wood development in lodgepole pine. Kaneda M, Rensing KH, Wong JC, Banno B, Mansfield SD, Samuels AL, Plant Physiol 2008 147 4 1750 1760 10.1104/pp.108.121533 18550683 (Pubitemid 352844218)
60. Gene expression profiling and silencing reveal that monolignol biosynthesis plays a critical role in penetration defence in wheat against powdery mildew invasion. Bhuiyan NH, Selvaraj G, Wei Y, King J, J Exp Bot 2009 60 2 509 521 10.1093/jxb/ern290 19039100
61. Down-regulation of Cinnamoyl-CoA Reductase induces significant changes of lignin profiles in transgenic tobacco plants. Piquemal J, Lapierre C, Myton K, O'Connell A, Schuch W, Grima-Pettenati J, Boudet AM, Plant J 1998 13 71 83 (Pubitemid 28065691)
62. Phytohormones and the cell wall in Arabidopsis during seedling growth. Sanchez-Rodriguez C, Rubio-Somoza I, Sibout R, Persson S, Trends in Plant Science 2010 15 5 291 301 10.1016/j.tplants.2010.03.002 20346727
63. Transgenic Tobacco Plants Coexpressing the Agrobacterium tumefaciens iaaM and iaaH Genes Display Altered Growth and Indoleacetic Acid Metabolism. Sitbon F, Hennion S, Sundberg B, Little CH, Olsson O, Sandberg G, Plant Physiol 1992 99 3 1062 1069 10.1104/pp.99.3.1062 16668972
64. Enhanced ethylene production and peroxidase activity in IAA-overproducing tobacco plants with increased lignin content and altered lignin deposition. Sitbon F, Hennion S, Anthony Little CH, Sundberg B, Plant Sci 1999 141 165 173 10.1016/S0168-9452(98)00236-2 (Pubitemid 29157076)
65. Characterization of a tomato xyloglucan endotransglycosylase gene that is down-regulated by auxin in etiolated hypocotyls. Catala C, Rose JK, York WS, Albersheim P, Darvill AG, Bennett AB, Plant Physiol 2001 127 3 1180 1192 10.1104/pp.010481 11706197 (Pubitemid 33112176)
66. Molecular analysis of a family of Arabidopsis genes related to galacturonosyltransferases. Kong Y, Zhou G, Yin Y, Xu Y, Pattathil S, Hahn MG, Plant Physiol 2011 155 4 1791 1805 10.1104/pp.110.163220 21300919
67. New insights into pectin methylesterase structure and function. Pelloux J, Rusterucci C, Mellerowicz EJ, Trends Plant Sci 2007 12 6 267 277 10.1016/j.tplants.2007.04.001 17499007 (Pubitemid 46880464)
68. The reb1-1 mutation of Arabidopsis alters the morphology of trichoblasts, the expression of arabinogalactan-proteins and the organization of cortical microtubules. Andeme-Onzighi C, Sivaguru M, Judy-March J, Baskin TI, Driouich A, Planta 2002 215 6 949 958 10.1007/s00425-002-0836-z 12355155 (Pubitemid 36080253)
69. UDP-glucose 4-epimerase isoforms UGE2 and UGE4 cooperate in providing UDP-galactose for cell wall biosynthesis and growth of Arabidopsis thaliana. Rosti J, Barton CJ, Albrecht S, Dupree P, Pauly M, Findlay K, Roberts K, Seifert GJ, Plant Cell 2007 19 5 1565 1579 10.1105/tpc.106.049619 17496119 (Pubitemid 47025377)
70. Asparagine in plants. Lea PJ, Sodek L, Parry MAJ, Shewry PR, Halford NG, Ann Appl Biol 2007 150 1 26 10.1111/j.1744-7348.2006.00104.x (Pubitemid 46197519)
71. Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses. Wingler A, Roitsch T, Plant Biol (Stuttgart, Germany) 2008 10 Suppl 1 50 62 (Pubitemid 352020108)
72. The OsFOR1 gene encodes a polygalacturonase-inhibiting protein (PGIP) that regulates floral organ number in rice. Jang S, Lee B, Kim C, Kim SJ, Yim J, Han JJ, Lee S, Kim SR, An G, Plant Mol Biol 2003 53 3 357 369 14750524 (Pubitemid 38097966)