Cloning and functional analysis of three genes encoding polygalacturonase-inhibiting proteins from Capsicum annuum and transgenic CaPGIP1 in tobacco in relation to increased resistance to two fungal pathogens

Plant Molecular Biology

Volumn 81, Issue 4-5, 2013, Pages 379-400

  Wang, Xiuju ^a   Zhu, Xiaoping ^a   Tooley, Paul ^b   Zhang, Xiuguo ^a  

^a SHANDONG AGRICULTURAL UNIVERSITY   (China)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Abiotic stress; Biotic stress; Capsicum annuum; Disease resistance; Endopolygalacturonases; Polygalacturonase inhibitingproteins; Transient expression

Indexed keywords

ALTERNARIA ALTERNATA; CAPSICUM ANNUUM; COLLETOTRICHUM; FUNGI; NICOTIANA TABACUM; PHYTOPHTHORA; PHYTOPHTHORA CAPSICI;

EID: 84874297625     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-013-0007-6     Document Type: Article

References (123)

1. Adie BAT, Pérez-Pérez J, Pérez-Pérez MM, Godoy M, Sánchez-Serrano JJ, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19: 1665-1681.
2. Afzal AJ, Lightfoot DA (2007) Soybean disease resistance protein RHG1-LRR domain expressed, purified and refolded from Escherichia coli inclusion bodies: preparation for a functional analysis. Pro Exp Pur 53: 346-355.
3. Agüero CB, Uratsu SL, Greve C, Powell AT, Labavitch JM, Meredith CP, Dandekar AM (2005) Evaluation of tolerance to Pierce's disease and Botrytis in transgenic plants of Vitis vinifera L. expressing the pear PGIP gene. Mol Plant Pathol 6: 43-51.
4. Albersheim P, Anderson AJ (1971) Proteins from plant cell walls inhibit polygalacturonases secreted by plant pathogens. Proc Natl Acad Sci USA 68: 1815-1819.
5. An SH, Sohn KH, Choi HW, Hwang IS, Lee SC, Hwang BK (2008) Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 228: 61-78.
6. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16: 3460-3479.
7. Asselbergh B, Achuo AE, Höfte M, van Gijsegem F (2008) Abscisic acid de ficiency leads to rapid activation of tomato defence responses upon infection with Erwinia chrysanthemi. Mol Plant Pathol 9: 11-24.
8. Audenaert K, De Meyer GB, Höfte MM (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol 128: 491-501.
9. Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69: 473-488.
10. Bergmann CW, Ito Y, Singer D, Albersheim P, Darvill AG, Benhamou N, Nuss L, Salvi G, Cervone F, De Lorenzo G (1994) Polygalacturonase-inhibiting protein accumulates in Phaseolus vulgaris L. in response to wounding, elicitors and fungal infection. Plant J 5: 625-634.
11. Bezier A, Lambert B, Baillieul F (2002) Cloning of a grapevine Botrytis-responsive gene that has homology to the tobacco hypersensitivity-related hsr203. J Exp Bot 53: 2279-2280.
12. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
13. Centis S, Guillas I, Séjalon N, Tugayé MTE, Dumas B (1997) Endopolygalacturonase genes from Colletotrichum lindemuthianum: cloning of CLPG2 and comparison of its expression to that of CLPG1 during saprophytic and parasitic growth of the fungus. Mol Plant Microb Interact 10(6): 769-775.
14. Cheng Q, Cao YZH, Pan HX, Wang MX, Huang MR (2008) Isolation and characterization of two genes encoding polygalacturonase-inhibiting protein from Populus deltoides. J Genet Genomics 35(10): 631-638.
15. Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129(2): 661-677.
16. Chinnusamy V, Gong ZZ, Zhu JK (2008) Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol 50: 1187-1195.
17. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124(4): 803-814.
18. Chung E, Seong E, Kim YC, Chung EJ, Oh SK, Lee S, Park JM, Joung YH, Choi D (2004) A method of high frequency virus-induced gene silencing in chili pepper (Capsicum annuum L. cv. Bukang). Mol Cell 17(2): 377-380.
19. Cook BJ, Clay RP, Bergmann CW, Albersheim P, Darvil AG (1999) Fungal polygalacturonase exhibit different substrate degradation patterns and differ in their susceptibilities to polygalacturonase-inhibiting proteins. Mol Plant Microb Interact 12(8): 703-711.
20. Darvill A, Bergmann C, Cervone F, De Lorenzo G, Ham KS, Spiro MD, York WS, Albersheim P (1994) Oligosaccharins involved in plant growth and host-pathogen interactions. Biochem Soc Symp 60: 89-94.
21. D'Ovidio R, Anderson OD (1994) Purification and molecular characterization of a soybean polygalacturonase-inhibiting protein. Theor App Genet 88: 759-763.
22. D'Ovidio R, Raiola A, Capodicasa C, Devoto A, Pontiggia D, Roberti S, Galletti R, Conti E, O'Sullivan D, De Lorenzo G (2004) Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects. Plant Physiol 135(4): 2424-2435.
23. D'Ovidio R, Roberti S, Di Giovanni M, Capodicasa C, Melaragni M, Sella L, Tosi P, Favaron F (2006) The characterization of the soybean polygalacturonase-inhibiting proteins (PGIP) gene family reveals that a single member is responsible for the activity detected in soybean tissues. Planta 224(3): 633-645.
24. de Bruxelles GL, Roberts MR (2001) Signals regulating multiple responses to wounding and herbivores. Crit Rev Plant Sci 20: 487-521.
25. De Lorenzo G, Ferrari S (2002) Polygalacturonase-inhibiting proteins in defense against phytopathogenic fungi. Curr Opin Plant Biol 5(4): 295-299.
26. De Lorenzo G, Castoria R, Bellincampi D, Cervone F (1997) Fungal invasion enzymes and their inhibition. In: Carroll G, Tudzynski P (eds) The mycota. Springer, Berlin, pp 61-83.
27. De Lorenzo G, Cervone F, Bellincampi D, Caprari C, Clark AJ, Desiderio A, Devoto A, Forrest R, Leckie F, Nuss L, Salvi G (1994) Polygalacturonase, PGIP and oligogalacturonides in cell-cell communication. Biochem Soc Trans 22: 396-399.
28. De Lorenzo G, D'Ovidio R, Cervone F (2001) The role of polygalacturonase-inhibiting proteins (PGIPS) in defense against pathogenic fungi. Ann Rev Phytopathol 39: 313-335.
29. Dempsey DA, Shah J, Klessig D (1999) Salicylic acid and disease resistance in plants. Crit Rev Plant Sci 18: 547-575.
30. Desiderio A, Aracri B, Leckie F, Mattei B, Salvi G, Tigelaar H, van Roekel JS, Baulcombe DC, Melchers LS, De Lorenzo G, Cervone F (1997) Polygalacturonase-inhibiting proteins (PGIPs) with different specificities are expressed in Phaseolus vulgaris. Mol Plant Microb Interact 10(7): 852-860.
31. Devoto A, Clark AJ, Nuss L, Cervone F, De Lorenzo G (1997) Developmental and pathogen-induced accumulation of transcripts of polygalacturonase-inhibiting protein in Phaseolus vulgaris L. Planta 202(3): 284-292.
32. Di Matteo A, Federici L, Mattei B, Salvi G, Johnson KA, Savino C, De Lorenzo G, Tsernoglou D, Cervone F (2003) The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense. Proc Natl Acad Sci USA 100(17): 10124-10128.
33. Di Matteo A, Bonivento D, Tsernoglou D, Federici L, Cervone F (2006) Polygalacturonase-inhibiting protein (PGIP) in plant defence: a structural view. Phytochemistry 67(6): 528-533.
34. Di C, Zhang M, Xu S, Cheng T, An L (2006) Role of polygalacturonase inhibiting protein in plant defense. Crit Rev Microbiol 32(2): 91-100.
35. Di C, Li M, Long F, Bai M, Liu YJ, Zheng XL, Xu SJ, Xiang Y, Sun Z, An LZH (2009) Molecular cloning, functional analysis and localization of a novel gene encoding polygalacturonase-inhibiting protein in Chorispora bungeana. Planta 231(1): 169-178.
36. Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1: 316-323.
37. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12: 13-15.
38. Fang BH, Zhang GM, Chi CF, Liu P (2004) The dynamic effects of Colletotrichum capsici f. nicotianae toxin on MDA content and some protective enzymes in tobacco. Aata Phytopathologica Sinica 34(4): 27-31.
39. Favaron F, D'Ovidio R, Porceddu E, Alghisi P (1994) Purification and molecular characterization of a soybean polygalacturonase-inhibiting protein. Planta 195(1): 80-87.
40. Favaron F, Castiglioni C, D'Ovidio R, Alghisi P (1997) Polygalacturonase inhibiting proteins from Allium porrum L. and their role in plant tissue against fungal endo-polygalacturonases. Physiol Mol. Plant Pathol 50(6): 403-417.
41. Federici L, Di Matteo A, Fernandez-Recio J, Tsernoglou D, Cervone F (2006) Polygalacturonase inhibiting proteins: players in plant innate immunity. Trends Plant Sci 11(2): 65-70.
42. Feng JL, Wang K, Liu X, Chen SN, Chen JS (2009) The quantification of tomato microRNAs response to viral infection by stem-loop real-time RT-PCR. Gene 437(1-2): 14-21.
43. Ferrari S, Vairo D, Ausubel FM, Cervone F, de Lorenzo G (2003) Tandemly duplicated Arabidopsis genes that encode polygalacturonase-inhibiting proteins are regulated coordinately by different signal transduction pathways in response to fungal infection. Plant Cell 15: 93-106.
44. Ferrari S, Galletti R, Vairo D, de Cervone F, Lorenzo G (2006) Antisense expression of the Arabidopsis thaliana AtPGIP1 gene reduces polygalacturonase-inhibiting protein accumulation and enhances susceptibility to Botrytis cinerea. Mol Plant Microb Interact 19(8): 931-936.
45. Flors V, Ton J, Jakab G, Mauch-Mani B (2005) Abscisic acid and callose: team players in defence against pathogens? J Phytopathol 153: 377-383.
46. Frediani M, Cremonini R, Salvi G, Caprari C, Desiderio A (1993) Cytological localization of the PGIP genes in the embryo suspensor cells of Phaseolus vulgaris L. Theor Appl Genet 87(3): 369-373.
47. Gomathi V, Gayathri S, Anupama B, Silva JAT, Gnanamanickam SS (2006) Molecular aspects of polygalacturonase-inhibiting proteins (PGIPs) in plant defense. In: Silva JAT (ed) Floriculture, ornamental and plant biotechnology, vol 3. Global Science Books, London, pp 373-379.
48. Grüner R, Strompen G, Pfitzner AJP, Pfitzner UM (2003) Salicylic acid and the hypersensitive response initiate distinct signal transduction pathways in tobacco that converge on the as-1-like element of the PR-1a promoter. Euro J Biochem 270(24): 4876-4886.
49. Hegedus DD, Li R, Buchwaldt L, Parkin I, Whitwill S, Coutu C, Bekkaoui D, Rimmer SR (2008) Brassica napus possesses an expanded set of polygalacturonase inhibitor protein genes that are differentially regulated in response to Sclerotinia sclerotiorum infection, wounding and defense hormone treatment. Planta 228(2): 241-253.
50. Hu CG, Honda C, Kita M, Zhang Z, Tsuda T, Moriguchi TA (2002) Simple protocol for RNA isolation from fruit trees containing high levels of polysaccharides and polyphenol compounds. Plant Mol Bio Report 20(1): 69.
51. Hwang BH, Bae H, Lim HS, Kim KB, Kim SJ, Im MH, Park BS, Kim DS, Kim J (2010) Overexpression of polygalacturonase-inhibiting protein 2 (PGIP2) of Chinese cabbage (Brassica rapa ssp. pekinensis) increased resistance to the bacterial pathogen Pectobacterium carotovorum ssp. Carotovorum. Plant Cell Tiss Organ Cult 103(3): 293-305.
52. Isshiki A, Akimitsu K, Yamamoto M, Yamamoto H (2001) Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but Not Brown Spot Caused by Alternaria alternata. Mol Plant Microb Interact 14(6): 749-757.
53. Janni M, Di Giovanni M, Roberti S, Capodicasa C, D'Ovidio R (2006) Characterization of expressed PGIP genes in rice and wheat reveals similar extent of sequence variation to dicto PGIPs and identifies an active PGIP lacking an entire LRR repeat. Theor Appl Genet 113(7): 1233-1245.
54. Janni M, Sella L, Favaron F, Blechl AE, Lorenzo GD, D'Ovido R (2008) The Expression of a bean PGIP in transgenic wheat confers increased resistance to the fungal pathogen Bipolaris sorokiniana. Mol Plant Microb Interact 21(2): 171-177.
55. Johnson C, Boden E, Arias J (2003) Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis. Plant Cell 15: 1846-1858.
56. Johnston DJ, Ramanathan V, Williamson B (1993) A protein from immature raspberry fruits which inhibits endopolygalacturonases from Botrytis cinerea and other micro-organisms. J Exp Bot 44(5): 971-976.
57. Jones JDG (2001) Putting knowledge of plant disease resistance genes towork. Curr Opin Plant Biol 4: 281-287.
58. Jones DA, Jones JDG (1997) The roles of leucine-rich repeat proteins in plant defences. Adv Bot Res 24: 89-167.
59. Jones AL, Hamilton AJ, Voinnet O, Thomas CL, Maule AJ, Baulcombe DC (1999) RNA-DNA interactions and DNA methylation in post-transcriptional gene silencing. Plant Cell 11(12): 2291-2302.
60. Joubert DA, Slaughter AR, Kemp G, Becker VWJ, Krooshof GH, Bergmann C, Benen J, Pretorius IS, Vivier MA (2006) The grapevine polygalacturonase-inhibiting protein (VvPGIP1) reduces Botrytis cinerea susceptibility in transgenic tobacco and differentially inhibits fungal polygalacturonases. Transgenic Res 15(6): 687-702.
61. Joubert DA, Kars I, Wagemakers L, Bergmann C, Kemp G, Vivier MA, van Kan JA (2007) 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. Mol Plant Microb Interact 20(4): 392-402.
62. Karr AL, Albersheim P (1970) Polysaccharide-degrading enzymes are unable to attack plant cell walls without prior action by a "all-modifying enzyme". Plant Physiol 46: 69-80.
63. Kars I, Krooshof GH, Wagemakers L, Joosten R, Benen JA, van Kan JA (2005) Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. Plant J 43(2): 213-225.
64. Kemp G, Stanton L, Bergmann CW, Clay RP, Albersheim P, Darvill A (2004) Polygalacturonase-inhibiting proteins can function as activators of polygalacturonase. Mol Plant Microb Interact 17: 888-894.
65. Kim ES, Hwang BK (1992) Virulence to Korean pepper cultivars of isolates of Phytophthora capsici from different geographic areas. Plant Dis 76: 486-489.
66. Kobe B, Deisenhofer JZ (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19(10): 415-421.
67. Komatsu K, Hashimoto M, Ozeki J, Yamaji Y, Maejima K, Senshu H, Himeno M, Kagiwada S, Okano Y, Namba S (2010) Viral-induced systemic necrosis in plants involves both programmed cell death and the inhibition of viral multiplication, which are regulated by independent pathways. Mol Plant Microb Interact 23(3): 283-293.
68. Kothari H, Kumar P, Singh N (2006) Prokaryotic expression, purification, and polyclonal antibody production against a novel drug resistance gene of Leishmania donovani clinical isolate. Protein Expr Purif 45: 15-21.
69. Kusaba M, Tsuge T (1994) Nuclear ribosomal DNA variation and pathogenic specialization in Alternaria fungi known to produce host-specific toxins. Appl Environ Microbiol 60(9): 3055-3062.
70. Leckie F, Mattei B, Capodicasa C, Hemmings A, Nuss L, Aracri B, De Lorenzo G, Cervone F (1999) The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent-exposed β-strand/β-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. Eur Mol Biol Organ 18(9): 2352-2363.
71. Li R, Rimmer R, Yu M, Sharpe AG, Seguin-Swartz G, Lydiate D, Hegedus DD (2003) Two Brassica napus polygalacturonase inhibitory protein genes are expressed at different levels in response to biotic and abiotic stresses. Planta 217(2): 299-308.
72. Liang FS, Zhang KCH, Zhou ChJ, Kong FN, Li J, Wang B (2005) Cloning, characterization and expression of the gene encoding polygalacturonase-inhibiting proteins (PGIPs) of peach (Prunus persica L.). Plant Sci 168: 481-486.
73. Liu YG, Whittier RF (1995) Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25(3): 674-681.
74. Liu Y, Schi VM, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31(6): 777-786.
75. Machinandiarena MF, Olivieri FP, Daleo GR, Oliva CR (2001) Isolation and characterization of a polygalacturonase-inhibiting protein from potato leaves: accumulation in response to salicylic acid, wounding and infection. Plant Physiol Biochem 39: 129-136.
76. Manfredini C, Sicilia F, Ferrari S, Pontiggia D, Salvi G, Caprai C, Lorito M, De Lorenzo G (2006) Polygalacturonase-inhibiting protein 2 of Phaseolus vulgaris inhibits BcPG1, a polygalacturonase of Botrytis cinerea important for pathogenicity, and protects transgenic plants from infection. Physiol Mol Plant Pathol 67: 108-115.
77. Mariotti L, Casasoli M, Migheli Q, Balmas V, Caprari C, De Lorenzo G (2008) Reclassification of Fusarium verticillioides (syn. F. moniliforme) strain FC-10 as F. phyllophilum. Mycol Res 112(9): 1010-1011.
78. Mattei B, Bernalda MS, Federici L, Roepstorff P, Cervone F, Boffi A (2001) Secondary structure and post-translational modifications of the leucine-rich repeat protein PGIP (polygalacturonase-inhibiting protein) from Phaseolus vulgaris. Biochemistry 40(2): 569-576.
79. Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol 8: 409-414.
80. Mehli L, Kjellsen TD, Dewey FM, Hietala AM (2005) A case study from the interaction of strawberry and Botrytis cinerea highlights the beneWts of comonitoring both partners at genomic and mRNA level. New Phytol 168(2): 465-474.
81. Morris PC, Kumar A, Bowles DJ, Cuming AC (1990) Osmotic stress and abscisic acid regulate the expression of the Em gene of wheat. Eur J Biochem 190: 625-630.
82. Nishimura S, Kohmoto K (1983) Host-specific toxins and chemical structures from Alternaria species. Annu Rev Phytopathol 21(1): 87-116.
83. Nothnagel EA, McNeil M, Albersheim P, Dell A (1983) Hostpathogen interactions. XXII. A galacturonic acid oligosaccharide from plant cell walls elicits phytoalexins. Plant Physiol 71(4): 916-926.
84. Nuss L, Mah A, Clark AJ, Grisvard J, Dron M (1996) Differential accumulation of polygalacturonase-inhibiting protein (PGIP) mRNA in two near-isogenic lines of Phaseolus vulgaris L. upon infection with Colletotrichum lindemuthianum. Physiol Mol Plant Patho 48(2): 83-89.
85. Oeser B, Heidrich PM, Muller U, Tudzynski P, Tenberge KB (2002) Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/rye interaction. Fungal Genet Biol 36(3): 176-186.
86. Oke OA (1989) Extracellular enzymes of Colltotrichum nicotianae causing tobacco leaf anthracnose in Nigeria. J Phytopath 127(4): 296-304.
87. Pietro AD, Roncero MIG (1998) Cloning, expression, and role in pathogenicity og pg1 encoding the major extracellular endopolygalacturonase of the vascular wilt pathogen Fusarium oxysporum. Mol Plant Microb Interact 11(1): 91-98.
88. Powell AL, van Kan J, Ten Have A, Visser J, Greve LC, Bennett AB, Labavitch JM (2000) Transgenic expression of pear PGIP in tomato limits fungal colonization. Mol Plant Microb Interact 13: 942-950.
89. Ramanathan V, Simpsom C, Thow G, Iannetta P, McNicol R, Williamson B (1997) cDNA cloning and expression of polygalacturonaseinhibiting proteins (PGIPs) from red raspberry (Rubus idaeus). J Exp Bot 48: 1185-1193.
90. Ramonel KM, Somerville S (2002) The genomics parade of defense responses: to infinity and beyond. Curr Opin Plant Biol 5(4): 291-294.
91. Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12(5): 707-720.
92. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
93. Sathiyaraj G, Srinivasan S, Subramanium S, Kim YJ, Kim YJ, Kwon WS, Yang DC (2010) Polygalacturonase inhibiting protein: isolation, developmental regulation and pathogen related expression in Panax ginseng. Mol Biol Rep 37(7): 3445-3454.
94. Schaart JG, Mehli L, Schouten HJ (2005) Quantification of allele-specific expression of a gene encoding strawberry polygalacturonase-inhibiting protein (PGIP) using pyrosequencing. Plant J 41(3): 493-500.
95. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97(21): 11655-11660.
96. Sella L, Castiglioni C, Roberti S, D'Ovidio R, Favaron F (2004) An endo-polygalacturonase (PG) of Fusarium moniliforme escaping inhibition by plant polygalacturonase-inhibiting proteins (PGIPs) provides new insights into the PG-PGIP interaction. FEMS Microbiol Lett 240: 117-124.
97. Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, Dietrich B, Ho P, Bacwaden J, Ko C, Clarke JD, Cotton D, Bullis D, Snell J, Miguel T, Hutchison D, Kimmerly B, Mitzel T, Katagiri F, Glazebrook J, Law M, Goffl SA (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14(12): 2985-2994.
98. Sharrock KR, Labavitch JM (1994) Polygalacturonase inhibitors of Bartlett pear fruits: differential effects on Botrytis cinerea polygalacturonase isozymes, and influence on products of fungal hydrolysis of pear cell walls and an ethylene induction in cell culture. Physiol Mol Plant Pathol 45(4): 305-319.
99. Shieh MT, Brown RL, Whitehead MP, Cary JW, Cotty PJ, Cleveland TE, Dean RA (1997) Molecular genetic evidence for the involvement of a specific polygalacturonase, P2c, in the invasion and spread of Aspergillus flavus in cotton bolls. Appl Environ Microbiol 63(9): 3548-3552.
100. Shirano Y, Kachroo P, Shah J, Klessig DF (2002) A gain-of-function mutation in an Arabidopsis toll interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell 14: 3149-3162.
101. Slavov S, Mayama S, Atanassov A (2004) Some aspects of epidemiology of Alternaria alternata tobacco pathotype. Biotechnol Biotechnol Equip 18(2): 28-33.
102. Song WW, Ma XR, Tan H, Zhou JY (2011) Abscisic acid enhances resistance to Alternaria solani in tomato seedlings. Plant Physiol Biochem 49: 693-700.
103. Spadoni S, Zabotina O, Di Matteo A, Mikkelsen JD, Cervone F, De Lorenzo G, Mattei B, Bellincampi D (2006) Polygalacturonase inhibiting protein interacts with pectin through a binding site formed by four clustered residues of arginine and lysine. Plant Physiol 141(2): 557-564.
104. Stotz HU, Contos JJA, Powell ALT, Bennett AB, La-bavitch JM (1994) Structure and expression of an inhibitor of fungal polygalacturonases from tomato. Plant Mol Biol 25: 607-617.
105. Stotz HU, Powell ALT, Damon SE, Greve LC, Bennett AB, Labavitch JM (1993) Molecular characterization of a polygalacturonase inhibitor from Pyrus communis L. cv. Bartlett. Plant Physiol 102(1): 133-138.
106. Stotz HU, Bishop JG, Bergmann CW, Koch M, Albersheim P, Darvill AG, Labavitch JM (2000) Identification of target amino acids that affect interactions of fungal polygalacturonases and their plant inhibitors. Physiol Mol Plant Pathol 56: 117-139.
107. Sun WX, Jia YJ, Feng BZ, O'Neill NR, Zhu XP, Xie BY, Zhang XG (2009) Functional analysis of Pcipg2 from the straminopilous plant pathogen Phytophthora capsici. Genesis 47(8): 535-544.
108. Taipalensuu J, Andreasson E, Eriksson S, Rask L (1997) Regulation of the wound-induced myrosinase-associated protein transcript in Brassica napus plants. Eur J Biochem 247(3): 963-971.
109. Taylor RJ, Secor GA (1988) An improved diffusion assay for quantifying the polygalacturonase content of Erwinia culture filtrates. Phytopathology 78(8): 1101-1103.
110. ten Have A, Mulder W, Visser J, van Kam JA (1998) The Endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol Plant Microb Interact 11(10): 1009-1016.
111. Thaler JS, Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology 85: 48-58.
112. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24): 4876-4882.
113. Ton J, Mauch-Mani B (2004) β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 38: 119-130.
114. Torto TA, Rauser L, Kamoun S (2002) The Pipg1 gene of the oomycete Phytophthora infestans encodes a fungal-like endopolygalacturonase. Curr Genet 40(6): 385-390.
115. Toubart P, Desiderio A, Salvi G, Cervone F, Daroda L, De Lorenzo G (1992) Cloning and characterization of the gene encoding the endopolygalacturonase-inhibiting protein (PGIP) of Phaseolus vulgaris L. Plant J 2(3): 367-373.
116. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793): 1596-1604.
117. Weurman C (1953) Pectinase inhibitors in pears. Acta Bot Neerl 2: 107-121.
118. Wiese J, Kranz T, Schubert S (2004) Induction of pathogen resistance in barley by abiotic stress. Plant Biol 6: 529-536.
119. Wu CH, Yan HZ, Liu LF, Liou RF (2008) Functional characterization of a gene family encoding polygalacturonases in Phytophthora parasitica. Mol Plant Microb Interact 21(4): 480-489.
120. Yang B, Yajima W, Das D, Suresh MR, Kav NNV (2009) Isolation, expression and characterization of two single-chain variable fragment antibodies against an endo-polygalacturonase secreted by Sclerotinia sclerotiorum. Pro Exp Pur 64: 237-243.
121. Yao C, Conway WS, Ren R, Smith D, Ross GS, Sams CE (1999) Gene encoding polygalacturonase inhibitor in apple fruit is developmentally regulated and activated by wounding and fungal infection. Plant Mol Biol 39: 1231-1241.
122. Zhang GM, Wang ZF, Chen RT, Liu YR (1994) On the pathogenicity of the tobacco black death disease. Aata Phytopathol Sinica 24(3): 367-371.
123. Zhang R, Yang D, Zhou CH, Cheng K, Liu ZH, Chen L, Fang L, Xie P (2012) β-Actin as a loading control for plasma-based Western blot analysis of major depressive disorder patients. Anal Biochem 427: 116-120.