Deciphering the responses of root border-like cells of arabidopsis and flax to pathogen-derived elicitors

Plant Physiology

Volumn 163, Issue 4, 2013, Pages 1584-1597

  Plancot, Barbara ^a   Santaella, Catherine ^b   Jaber, Rim ^a   Kiefer Meyer, Marie Christine ^a   Follet Gueye, Marie Laure ^a   Leprince, Jérôme ^c   Gattin, Isabelle ^e   Souc, Céline ^d   Driouich, Azeddine ^a   Vicré Gibouin, Maïté ^a  

^a UNIVERSITÉ DE ROUEN   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c UNIVERSITÉ DE ROUEN   (France)

^d Coopérative Terre de Lin ^*  (France)

^e BioSol Laboratory   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CALLOSE; EPITOPE; EXTENSIN PROTEIN, PLANT; FLAGELLIN; GLUCAN; GLYCOPROTEIN; PATTERN RECOGNITION RECEPTOR; PEPTIDOGLYCAN; REACTIVE OXYGEN METABOLITE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CELL SURVIVAL; CELL WALL; CYTOLOGY; DRUG EFFECT; FLAX; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PLANT CELL; PLANT ROOT; TIME; ULTRASTRUCTURE;

ARABIDOPSIS; BIOLOGICAL MARKERS; CELL SURVIVAL; CELL WALL; EPITOPES; FLAGELLIN; FLAX; GENE EXPRESSION REGULATION, PLANT; GLUCANS; GLYCOPROTEINS; PEPTIDOGLYCAN; PLANT CELLS; PLANT PROTEINS; PLANT ROOTS; REACTIVE OXYGEN SPECIES; RECEPTORS, PATTERN RECOGNITION; TIME FACTORS;

EID: 84888866939     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.222356     Document Type: Article

References (83)

1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399
2. Attard A, Gourgues M, Callemeyn-Torre N, Keller H (2010) The immediate activation of defense responses in Arabidopsis roots is not sufficient to prevent Phytophthora parasitica infection. New Phytol 187: 449-460
3. Balestrini R, Hahn MG, Faccio A, Mendgen K, Bonfante P (1996) Differential localization of carbohydrate epitopes in plant cell walls in the presence and absence of arbuscular mycorrhizal fungi. Plant Physiol 111: 203-213
4. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbeassociated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406
5. Bookout AL, Mangelsdorf DJ (2003) Quantitative real-time PCR protocol for analysis of nuclear receptor signaling pathways. Nucl Recept Signal 1: e012
6. Bradley DJ, Kjellbom P, Lamb CJ (1992) Elicitor-and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70: 21-30
7. Brigham LA, Woo HH, Nicoll SM, Hawes MC (1995) Differential expression of proteins and mRNAs from border cells and root tips of pea. Plant Physiol 109: 457-463
8. Brisson LF, Tenhaken R, Lamb C (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6: 1703-1712
9. Cannesan MA, Durand C, Burel C, Gangneux C, Lerouge P, Ishii T, Laval K, Follet-Gueye ML, Driouich A, Vicré-Gibouin M (2012) Effect of arabinogalactan proteins from the root caps of pea and Brassica napus on Aphanomyces euteiches zoospore chemotaxis and germination. Plant Physiol 159: 1658-1670
10. Cannesan MA, Gangneux C, Lanoue A, Giron D, Laval K, Hawes M, Driouich A, Vicré-Gibouin M (2011) Association between border cell responses and localized root infection by pathogenic Aphanomyces euteiches. Ann Bot (Lond) 108: 459-469
11. Chevalier L, Bernard S, Ramdani Y, Lamour R, Bardor M, Lerouge P, Follet-Gueye ML, Driouich A (2010) Subcompartment localization of the side chain xyloglucan-synthesizing enzymes within Golgi stacks of tobacco suspension-cultured cells. Plant J 64: 977-989
12. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497-500
13. Choi O, Hu Z (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42: 4583-4588
14. Daudi A, Cheng Z, O'Brien JA, Mammarella N, Khan S, Ausubel FM, Bolwell GP (2012) The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24: 275-287
15. Deepak S, Shailasree S, Kini RK, Hause B, Shetty SH, Mithöfer A (2007) Role of hydroxyproline-rich glycoproteins in resistance of pearl millet against downy mildew pathogen Sclerospora graminicola. Planta 226: 323-333
16. Driouich A, Cannesan MA, Dardelle F, Durand C, Plancot B, Bernard S, Follet-Gueye ML, Vicré-Gibouin M (2012) Unity is strength: the power of border cells and border-like cells in relation with plant defense. In JM Vivanco, F Baluska, eds, Secretions and Exudates in Biological Systems, Signaling and Communication in Plants. Springer-Verlag, Berlin, Heidelberg, pp 91-107
17. Driouich A, Durand C, Cannesan MA, Percoco G, Vicré-Gibouin M (2010) Border cells versus border-like cells: are they alike? J Exp Bot 61: 3827-3831
18. Driouich A, Durand C, Vicré-Gibouin M (2007) Formation and separation of root border cells. Trends Plant Sci 12: 14-19
19. Durand C, Vicré-Gibouin M, Follet-Gueye ML, Duponchel L, Moreau M, Lerouge P, Driouich A (2009) The organization pattern of root borderlike cells of Arabidopsis is dependent on cell wall homogalacturonan. Plant Physiol 150: 1411-1421
20. Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265-276
21. Flors C, Fryer MJ, Waring J, Reeder B, Bechtold U, Mullineaux PM, Nonell S, Wilson MT, Baker NR (2006) Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet Oxygen Sensor Green. J Exp Bot 57: 1725-1734
22. Flors C, Nonell S (2006) Light and singlet oxygen in plant defense against pathogens: phototoxic phenalenone phytoalexins. Acc Chem Res 39: 293-300
23. Follet-Gueye ML, Mollet JC, Vicré-Gibouin M, Bernard S, Chevalier L, Plancot B, Dardelle F, Ramdani Y, Coimbra S, Driouich A (2012) Immuno-glyco-imaging in plant cells: localization of cell wall carbohydrate epitopes and their biosynthesizing enzymes. In H Dehghani, ed, Applications of Immunocytochemistry. In Tech, Rijeka, pp 297-320
24. Gaspar Y, Johnson KL, McKenna JA, Bacic A, Schultz CJ (2001) The complex structures of arabinogalactan-proteins and the journey towards understanding function. Plant Mol Biol 47: 161-176
25. Gómez-Gómez L, Bauer Z, Boller T (2001) Both the extracellular leucinerich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 13: 1155-1163
26. Gunawardena U, Hawes MC (2002) Tissue specific localization of root infection by fungal pathogens: role of root border cells. Mol Plant Microbe Interact 15: 1128-1136
27. Gunawardena U, Rodriguez M, Straney D, Romeo JT, VanEtten HD, Hawes MC (2005) Tissue-specific localization of pea root infection by Nectria haematococca: mechanisms and consequences. Plant Physiol 137: 1363-1374
28. Guzzardi P, Genot G, Jamet E (2004) The Nicotiana sylvestris extensin gene, Ext 1.2A, is expressed in the root transition zone and upon wounding. Biochim Biophys Acta 1680: 83-92
29. Hano C, Addi M, Bensaddek L, Crônier D, Baltora-Rosset S, Doussot J, Maury S, Mesnard F, Chabbert B, Hawkins S, et al (2006) Differential accumulation of monolignol-derived compounds in elicited flax (Linum usitatissimum) cell suspension cultures. Planta 223: 975-989
30. Hao P, Liu C, Wang Y, Chen R, Tang M, Du B, Zhu L, He G (2008) Herbivoreinduced callose deposition on the sieve plates of rice: an important mechanism for host resistance. Plant Physiol 146: 1810-1820
31. Hardham AR, Jones DA, Takemoto D (2007) Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol 10: 342-348
32. Hawes MC, Bengough G, Cassab G, Ponce G (2003) Root caps and rhizosphere. J Plant Growth Regul 21: 352-367
33. Hawes MC, Curlango-Rivera G, Wen F, White GJ, Vanetten HD, Xiong Z (2011) Extracellular DNA: the tip of root defenses? Plant Sci 180: 741-745
34. Hawes MC, Gunawardena U, Miyasaka S, Zhao X (2000) The role of root border cells in plant defense. Trends Plant Sci 5: 128-133
35. Hempel SL, Buettner GR, O'Malley YQ, Wessels DA, Flaherty DM (1999) Dihydrofluorescein diacetate is superior for detecting intracellular oxidants: comparison with 2',7'-dichlorodihydrofluorescein diacetate, 5 (and 6)-carboxy-2',7'-dichlorodihydrofluorescein diacetate, and dihydrorhodamine 123 Free Radic Biol Med 27: 146-159
36. Hirao T, Fukatsu E, Watanabe A (2012) Characterization of resistance to pine wood nematode infection in Pinus thunbergii using suppression subtractive hybridization. BMC Plant Biol 12: 13
37. Huang GT, Ma SL, Bai LP, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo ZF (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 39: 969-987
38. Hückelhoven R (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45: 101-127
39. Jensen JK, Sørensen SO, Harholt J, Geshi N, Sakuragi Y, Møller I, Zandleven J, Bernal AJ, Jensen NB, Sørensen C, et al (2008) Identification of a xylogalacturonan xylosyltransferase involved in pectin biosynthesis in Arabidopsis. Plant Cell 20: 1289-1302
40. Kieliszewski MJ, Lamport DT (1994) Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J 5: 157-172
41. 2DCFDA and confocal laser microscopy. Physiol Plant 136: 369-383
42. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, FelixG (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16: 3496-3507
43. Lakshmanan V, Kitto SL, Caplan JL, Hsueh YH, Kearns DB, Wu YS, Bais HP (2012) Microbe-associated molecular patterns-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis. Plant Physiol 160: 1642-1661
44. Laloi C, Stachowiak M, Pers-Kamczyc E, Warzych E, Murgia I, Apel K (2007) Cross-talk between singlet oxygen-and hydrogen peroxidedependent signaling of stress responses in Arabidopsis thaliana. Proc Natl Acad Sci USA 104: 672-677
45. Lorenc-Kukuła K, Zuk M, Kulma A, Czemplik M, Kostyn K, Skała J, Starzycki M, Szopa J (2009) Engineering flax with the GT family 1 Solanum sogarandinum glycosyltransferase SsGT1 confers increased resistance to Fusarium infection. J Agric Food Chem 57: 6698-6705
46. Marcus SE, Verhertbruggen Y, Hervé C, Ordaz-Ortiz JJ, Farkas V, Pedersen HL, Willats WG, Knox JP (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8: 60
47. McCann HC, Nahal H, Thakur S, Guttman DS (2012) Identification of innate immunity elicitors using molecular signatures of natural selection. Proc Natl Acad Sci USA 109: 4215-4220
48. Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D, Ausubel FM (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22: 973-990
49. Møller IM, Sweetlove LJ (2010) ROS signalling: specificity is required. Trends Plant Sci 15: 370-374
50. Mueller K, Bittel P, Chinchilla D, Jehle AK, Albert M, Boller T, Felix G (2012) Chimeric FLS2 receptors reveal the basis for differential flagellin perception in Arabidopsis and tomato. Plant Cell 24: 2213-2224
51. Nguema-Ona E, Coimbra S, Vicré-Gibouin M, Mollet JC, Driouich A (2012) Arabinogalactan proteins in root and pollen-tube cells: distribution and functional aspects. Ann Bot (Lond) 110: 383-404
52. Nguema-Ona E, Vicré-Gibouin M, Cannesan MA, Driouich A (2013) Arabinogalactan proteins in root-microbe interactions. Trends Plant Sci 18: 440-449
53. Pan JW, Ye D, Wang LL, Hua J, Zhao GF, Pan WH, Han N, Zhu MY (2004) Root border cell development is a temperature-insensitive and Al-sensitive process in barley. Plant Cell Physiol 45: 751-760
54. Pandey SP, Roccaro M, Schön M, Logemann E, Somssich IE (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J 64: 912-923
55. 2-induced reduction in primary cell wall hydration. BMC Plant Biol 11: 106
56. Pogány M, von Rad U, Grün S, Dongó A, Pintye A, Simoneau P, Bahnweg G, Kiss L, Barna B, Durner J (2009) Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem. Plant Physiol 151: 1459-1475
57. Puhlmann J, Bucheli E, Swain MJ, Dunning N, Albersheim P, Darvill AC, Hahn MC (1994) Generation of monoclonal antibodies against plant cellwall polysaccharides. I. Characterization of a monoclonal antibody to a terminal alpha-(1→2)-linked fucosyl-containing epitope. Plant Physiol 104: 699-710
58. Rastogi A, Pospísil P (2010) Effect of exogenous hydrogen peroxide on biophoton emission from radish root cells. Plant Physiol Biochem 48: 117-123
59. Ribeiro JM, Pereira CS, Soares NC, Vieira AM, Feijó JA, Jackson PA (2006) The contribution of extensin network formation to rapid, hydrogen peroxide-mediated increases in grapevine callus wall resistance to fungal lytic enzymes. J Exp Bot 57: 2025-2035
60. Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, Malinovsky FG, Tör M, de Vries S, Zipfel C (2011) The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23: 2440-2455
61. Saga H, Ogawa T, Kai K, Suzuki H, Ogata Y, Sakurai N, Shibata D, Ohta D (2012) Identification and characterization of ANAC042, a transcription factor family gene involved in the regulation of camalexin biosynthesis in Arabidopsis. Mol Plant Microbe Interact 25: 684-696
62. Salin ML, Bridges SM (1981) Chemiluminescence in wounded root tissue: evidence for peroxidase involvement. Plant Physiol 67: 43-46
63. Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58: 137-161
64. Siegel S, Castellan NJ (1988) Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York
65. Smallwood M, Martin H, Knox JP (1995) An epitope of rice threonine-and hydroxyproline-rich glycoprotein is common to cell wall and hydrophobic plasma-membrane glycoproteins. Planta 196: 510-522
66. Torres MA (2010) ROS in biotic interactions. Physiol Plant 138: 414-429
67. Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99: 517-522
68. Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14: 219-228
69. Underwood W (2012) The plant cell wall: a dynamic barrier against pathogen invasion. Front Plant Sci 3: 85
70. van Hengel AJ, Roberts K (2002) Fucosylated arabinogalactan-proteins are required for full root cell elongation in Arabidopsis. Plant J 32: 105-113
71. Velasquez M, Salter JS, Dorosz JG, Petersen BL, Estevez JM (2012) Recent advances on the posttranslational modifications of EXTs and their roles in plant cell walls. Front Plant Sci 3: 93
72. Velasquez SM, Ricardi MM, Dorosz JG, Fernandez PV, Nadra AD, Pol-Fachin L, Egelund J, Gille S, Harholt J, Ciancia M, et al (2011) O-Glycosylated cell wall proteins are essential in root hair growth. Science 332: 1401-1403
73. Vellosillo T, Vicente J, Kulasekaran S, Hamberg M, Castresana C (2010) Emerging complexity in reactive oxygen species production and signaling during the response of plants to pathogens. Plant Physiol 154: 444-448
74. Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res 344: 1858-1862
75. Vicré M, Santaella C, Blanchet S, Gateau A, Driouich A (2005) Root border-like cells of Arabidopsis: microscopical characterization and role in the interaction with rhizobacteria. Plant Physiol 138: 998-1008
76. Wang E, Schornack S, Marsh JF, Gobbato E, Schwessinger B, Eastmond P, Schultze M, Kamoun S, Oldroyd GE (2012) A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr Biol 22: 2242-2246
77. Wen F, VanEtten HD, Tsaprailis G, Hawes MC (2007) Extracellular proteins in pea root tip and border cell exudates. Plant Physiol 143: 773-783
78. Wen F, White GJ, VanEtten HD, Xiong Z, Hawes MC (2009) Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 151: 820-829
79. Willats WG, McCartney L, Knox JP (2001) In-situ analysis of pectic polysaccharides in seed mucilage and at the root surface of Arabidopsis thaliana. Planta 213: 37-44
80. Willats WG, McCartney L, Steele-King CG, Marcus SE, Mort A, Huisman M, van Alebeek GJ, Schols HA, Voragen AG, Le Goff A, et al (2004) A xylogalacturonan epitope is specifically associated with plant cell detachment. Planta 218: 673-681
81. Wojtaszek P, Trethowan J, Bolwell GP (1995) Specificity in the immobilisation of cell wall proteins in response to different elicitor molecules in suspension-cultured cells of French bean (Phaseolus vulgaris L.). Plant Mol Biol 28: 1075-1087
82. Xie D, Ma L, Samaj J, Xu C (2011) Immunohistochemical analysis of cell wall hydroxyproline-rich glycoproteins in the roots of resistant and susceptible wax gourd cultivars in response to Fusarium oxysporum f. sp. benincasae infection and fusaric acid treatment. Plant Cell Rep 30: 1555-1569
83. Xu X, Hu X, Neill SJ, Fang J, Cai W (2005) Fungal elicitor induces singlet oxygen generation, ethylene release and saponin synthesis in cultured cells of Panax ginseng C. A. Meyer. Plant Cell Physiol 46: 947-954