Arabidopsis and Brachypodium distachyon transgenic plants expressing Aspergillus nidulans acetylesterases have decreased degree of polysaccharide acetylation and increased resistance to pathogens

Plant Physiology

Volumn 162, Issue 1, 2013, Pages 9-23

  Pogorelko, Gennady ^a,d   Lionetti, Vincenzo ^b   Fursova, Oksana ^a   Sundaram, Raman M ^a,c   Qi, Mingsheng ^a   Whitham, Steven A ^a   Bogdanove, Adam J ^a,c   Bellincampi, Daniela ^b   Zabotina, Olga A ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c Department of Obstetrics Gynecology   (United States)

^d VAVILOV INSTITUTE OF GENERAL GENETICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); BIPOLARIS SOROKINIANA; BOTRYOTINIA FUCKELIANA; BRACHYPODIUM; BRACHYPODIUM DISTACHYON; DICOTYLEDONEAE; EMERICELLA NIDULANS; PSEUDOMONAS SYRINGAE; XANTHOMONAS ORYZAE;

EID: 84877043826     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.214460     Document Type: Article

References (71)

1. Abramoff MD, Magalhães PJ (2004) Image processing with ImageJ. Biophotonics Int 11: 36-42.
2. Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2010) Plant Cell Walls. Garland Science, New York
3. Bauer S, Vasu P, Persson S, Mort AJ, Somerville CR (2006) Development and application of a suite of polysaccharide-degrading enzymes for analyzing plant cell walls. Proc Natl Acad Sci USA 10: 11417-11422.
4. Bily AC, Reid LM, Taylor JH, Johnston D, Malouin C, Burt AJ, Bakan B, Regnault-Roger C, Pauls KP, Arnason JT, et al (2003) Dehydrodimers of ferulic acid in maize grain pericarp and aleurone: resistance factors to Fusarium graminearum. Phytopathology 93: 712-719.
5. Buanafina MMdO (2009) Feruloylation in grasses: current and future perspectives. Mol Plant 2: 861-872.
6. Burton RA, Gidley MJ, Fincher GB (2010) Heterogeneity in the chemistry, structure and function of plant cell walls. Nat Chem Biol 6: 724-732.
7. Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344: 1879-1900.
8. Carter CJ, Thornburg RW (2004) Tobacco nectarin V is a flavin-containing berberine bridge enzyme-like protein with glucose oxidase activity. Plant Physiol 134: 460-469.
9. Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10: 281.
10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
11. Denby KJ, Kumar P, Kliebenstein DJ (2004) Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana. Plant J 38: 473-486.
12. Dong X, Mindrinos M, Davis KR, Ausubel FM (1991) Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 3: 61-72.
13. Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14: 1557-1566.
14. Ferrari S, Galletti R, Denoux C, De Lorenzo G, Ausubel FM, Dewdney J (2007) Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol 144: 367-379.
15. Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, Bellincampi D, Cervone F, De Lorenzo G (2008) Transgenic expression of a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol 146: 669-681.
16. Fry SC, York WS, Albersheim P, Darvill A, Hayashi T, Joseleau J-P, Lorences EP, Maclachlan GA, McNeil M, Mort AJ, et al (1993) An unambiguous nomenclature for xyloglucan-derived oligosaccharides. Physiol Plant 89: 1-3.
17. Fursova O, Pogorelko G, Zabotina OA (2012) An efficient method for transient gene expression in monocots applied to modify the Brachypodium distachyon cell wall. Ann Bot (Lond) 110: 47-56.
18. Galletti R, Denoux C, Gambetta S, Dewdney J, Ausubel FM, De Lorenzo G, Ferrari S (2008) The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiol 148: 1695-1706.
19. Gille S, Pauly M (2012) O-Acetylation of plant cell wall polysaccharides. Front Plant Sci 3: 12.
20. Gleave AP (1992) A versatile binary vector system with a T-DNA organizational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 6: 1203-1207.
21. Gou JY, Miller LM, Hou G, Yu XH, Chen XY, Liu CJ (2012) Acetylesterasemediated deacetylation of pectin impairs cell elongation, pollen germination, and plant reproduction. Plant Cell 24: 50-65.
22. Hamann T (2012) Plant cell wall integrity maintenance as an essential component of biotic stress response mechanisms. Front Plant Sci 3: 77.
23. Hamann T, Bennett M, Mansfield J, Somerville C (2009) Identification of cell-wall stress as a hexose-dependent and osmosensitive regulator of plant responses. Plant J 57: 1015-1026.
24. Haswell ES, Peyronnet R, Barbier-Brygoo H, Meyerowitz EM, Frachisse JM (2008) Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr Biol 18: 730-734.
25. Jakab G, Ton J, Flors V, Zimmerli L, Métraux JP, Mauch-Mani B (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139: 267-274.
26. Jordan DB, Bowman MJ, Braker JD, Dien BS, Hector RE, Lee CC, Mertens JA, Wagschal K (2012) Plant cell walls to ethanol. Biochem J 442: 241-252.
27. Jung HJ, Samac DA, Sarath G (2012) Modifying crops to increase cell wall digestibility. Plant Sci 185-186: 65-77.
28. Koch JL, Nevins DJ (1989) Tomato fruit cell wall. I. Use of purified tomato polygalacturonase and pectinmethylesterase to identify developmental changes in pectins. Plant Physiol 91: 816-822.
29. Lee C, Teng Q, Zhong R, Ye ZH (2011) The four Arabidopsis reduced wall acetylation genes are expressed in secondary wall-containing cells and required for the acetylation of xylan. Plant Cell Physiol 52: 1289-1301.
30. Lerouxel O, Choo TS, Séveno M, Usadel B, Faye L, Lerouge P, Pauly M (2002) Rapid structural phenotyping of plant cell wall mutants by enzymatic oligosaccharide fingerprinting. Plant Physiol 130: 1754-1763.
31. Lever M (1972) A new reaction for colorimetric determination of carbohydrates. Anal Biochem 47: 273-279.
32. Limberg G, Körner R, Buchholt HC, Christensen TM, Roepstorff P, Mikkelsen JD (2000) Analysis of different de-esterification mechanisms for pectin by enzymatic fingerprinting using endopectin lyase and endopolygalacturonase II from A. niger. Carbohydr Res 327: 293-307.
33. Linthorst HJM (1991) Pathogenesis-related proteins of plants. Crit Rev Plant Sci 10: 123-150.
34. Lionetti V, Cervone F, Bellincampi D (2012) Methyl esterification of pectin plays a role during plant-pathogen interactions and affects plant resistance to diseases. J Plant Physiol 169: 1623-1630.
35. Lionetti V, Francocci F, Ferrari S, Volpi C, Bellincampi D, Galletti R, D'Ovidio R, De Lorenzo G, Cervone F (2010) Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion. Proc Natl Acad Sci USA 107: 616-621.
36. Lionetti V, Raiola A, Camardella L, Giovane A, Obel N, Pauly M, Favaron F, Cervone F, Bellincampi D (2007) Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiol 143: 1871-1880.
37. Magi B, Liberatori S (2005) Immunoblotting techniques. Methods Mol Biol 295: 227-254.
38. Manabe Y, Nafisi M, Verhertbruggen Y, Orfila C, Gille S, Rautengarten C, Cherk C, Marcus SE, Somerville S, Pauly M, et al (2011) Loss-offunction mutation of REDUCED WALL ACETYLATION2 in Arabidopsis leads to reduced cell wall acetylation and increased resistance to Botrytis cinerea. Plant Physiol 155: 1068-1078.
39. Mauch F, Mauch-Mani B, Boller T (1988) Antifungal hydrolases in pea tissue. II. Inhibition of fungal growth by combinations of chitinase and b-1,3-glucanase. Plant Physiol 88: 936-942.
40. McComb EA, McCready RM (1957) Determination of acetyl in pectin and in acetylated carbohydrate polymers. Anal Chem 29: 819-821.
41. Nühse TS (2012) Cell wall integrity signaling and innate immunity in plants. Front Plant Sci 3: 280.
42. Obel N, Erben V, Schwarz T, Kühnel S, Fodor A, Pauly M (2009) Microanalysis of plant cell wall polysaccharides. Mol Plant 2: 922-932.
43. Osorio S, Castillejo C, Quesada MA, Medina-Escobar N, Brownsey GJ, Suau R, Heredia A, Botella MA, Valpuesta V (2008) Partial demethylation of oligogalacturonides by pectin methyl esterase 1 is required for eliciting defence responses in wild strawberry (Fragaria vesca). Plant J 54: 43-55.
44. Pattathil S, Avci U, Baldwin D, Swennes AG, McGill JA, Popper Z, Bootten T, Albert A, Davis RH, Chennareddy C, et al (2010) A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol 153: 514-525.
45. Pauly M, Andersen LN, Kauppinen S, Kofod LV, York WS, Albersheim P, Darvill A (1999) A xyloglucan-specific endo-beta-1,4-glucanase from Aspergillus aculeatus: expression cloning in yeast, purification and characterization of the recombinant enzyme. Glycobiology 9: 93-100.
46. Pauly M, Qin Q, Greene H, Albersheim P, Darvill A, York WS (2001) Changes in the structure of xyloglucan during cell elongation. Planta 212: 842-850.
47. Peraldi A, Beccari G, Steed A, Nicholson P (2011) Brachypodium distachyon: a new pathosystem to study Fusarium head blight and other Fusarium diseases of wheat. BMC Plant Biol 11: 100.
48. Perrone P, Hewage CM, Thomson AR, Bailey K, Sadler IH, Fry SC (2002) Patterns of methyl and O-acetyl esterification in spinach pectins: new complexity. Phytochemistry 60: 67-77.
49. Pogorelko G, Fursova O, Lin M, Pyle E, Jass J, Zabotina OA (2011) Postsynthetic modification of plant cell walls by expression of microbial hydrolases in the apoplast. Plant Mol Biol 77: 433-445.
50. Pogorelko GV, Fursova OV, Ogarkova OA, Tarasov VA (2008) A new technique for activation tagging in Arabidopsis. Gene 414: 67-75.
51. Po-Wen C, Singh P, Zimmerli L (2013) Priming of the Arabidopsis patterntriggered immunity response upon infection by necrotrophic Pectobacterium carotovorum bacteria. Mol Plant Pathol 14: 58-70.
52. Raiola A, Lionetti V, Elmaghraby I, Immerzeel P, Mellerowicz EJ, Salvi G, Cervone F, Bellincampi D (2011) Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol Plant Microbe Interact 24: 432-440.
53. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61: 263-289.
54. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
55. Schuhegger R, Nafisi M, Mansourova M, Petersen BL, Olsen CE, Svatos A, Halkier BA, Glawischnig E (2006) CYP71B15 (PAD3) catalyzes the final step in camalexin biosynthesis. Plant Physiol 141: 1248-1254.
56. Seo PJ, Lee AK, Xiang F, Park CM (2008) Molecular and functional profiling of Arabidopsis pathogenesis-related genes: insights into their roles in salt response of seed germination. Plant Cell Physiol 49: 334-344.
57. Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, et al (2004) Toward a systems approach to understanding plant cell walls. Science 306: 2206-2211.
58. Song L, Siguier B, Dumon C, Bozonnet S, O'Donohue MJ (2012) Engineering better biomass-degrading ability into a GH11 xylanase using a directed evolution strategy. Biotechnol Biofuels 5: 3.
59. Underwood W (2012) The plant cell wall: a dynamic barrier against pathogen invasion. Front Plant Sci 3: 85.
60. Vogel J, Hill T (2008) High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3. Plant Cell Rep 27: 471-478.
61. Vogel JP, Raab TK, Schiff C, Somerville SC (2002) PMR6, a pectate lyaselike gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 14: 2095-2106.
62. Vogel JP, Raab TK, Somerville CR, Somerville SC (2004) Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant J 40: 968-978.
63. Volpi C, Janni M, Lionetti V, Bellincampi D, Favaron F, D'Ovidio R (2011) The ectopic expression of a pectin methyl esterase inhibitor increases pectin methyl esterification and limits fungal diseases in wheat. Mol Plant Microbe Interact 24: 1012-1019.
64. Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9: 203-209.
65. Wang Y, Kausch AP, Chandlee JM, Luo H, Ruemmele BA, Browning M, Jackson N, Goldsmith MR (2003) Co-transfer and expression of chitinase, glucanase, and bar genes in creeping bentgrass for conferring fungal disease resistance. Plant Sci 165: 497-506.
66. Weng X, Huang Y, Hou C, Jiang D (2012) Effects of an exogenous xylanase gene expression on the growth of transgenic rice and the expression level of endogenous xylanase inhibitor gene RIXI. J Sci Food Agric 93: 173-179.
67. Willats WG, Orfila C, Limberg G, Buchholt HC, van Alebeek GJ, Voragen AG, Marcus SE, Christensen TM, Mikkelsen JD, Murray BS, et al (2001) Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion. J Biol Chem 276: 19404-19413.
68. Wolf S, Hématy K, Höfte H (2012a) Growth control and cell wall signaling in plants. Annu Rev Plant Biol 63: 381-407.
69. Wolf S, Mouille G, Pelloux J (2009) Homogalacturonan methyl-esterification and plant development. Mol Plant 2: 851-860.
70. Wolf S, Mravec J, Greiner S, Mouille G, Höfte H (2012b) Plant cell wall homeostasis is mediated by brassinosteroid feedback signaling. Curr Biol 22: 1732-1737.
71. Zabotina O, Malm E, Drakakaki G, Bulone V, Raikhel N (2008) Identification and preliminary characterization of a new chemical affecting glucosyltransferase activities involved in plant cell wall biosynthesis. Mol Plant 1: 977-989