Sulfated macroalgal polysaccharides λ-carrageenan and ι-carrageenan differentially alter Arabidopsis thaliana resistance to Sclerotinia sclerotiorum

Physiological and Molecular Plant Pathology

Volumn 75, Issue 1-2, 2010, Pages 38-45

  Sangha, Jatinder Singh ^a   Ravichandran, Sridhar ^a   Prithiviraj, Kalyani ^a   Critchley, Alan T ^b   Prithiviraj, Balakrishnan ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b Acadian Seaplants Limited   (Canada)

Author keywords

Arabidopsis; Carrageenans; Elicitor; Glucosinolate; Induced resistance; Jasmonic acid; Oxalic acid; Salicylic acid; Sclerotinia sclerotiorum; Virulence factor

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; SCLEROTINIA; SCLEROTINIA SCLEROTIORUM;

EID: 78649822313     PISSN: 08855765     EISSN: 10961178     Source Type: Journal    
DOI: 10.1016/j.pmpp.2010.08.003     Document Type: Article

References (73)

1. Nürnberger T., Lipka V. Non-host resistance in plants: new insights into an old phenomenon. Mol Plant Path 2005, 6:335-345.
2. Dixon R.A., Harrison M.J., Lamb C.J. Early events in the activation of plant defense responses. Ann Rev Plant Pathol 1994, 32:479-501.
3. Cluzet S., Torregrosa C., Jacquet C., Lafitte C., Fournier J., Mercier L., et al. Gene expression profiling and protection of Medicago truncatula against a fungal infection in response to an elicitor from green alga Ulva spp. Plant Cell Environ 2004, 27:917-928.
4. Mercier L., Lafitte C., Borderies G., Briand X., Esquerre-Tugaye M.T., Fournier J. The algal polysaccharide carrageenans can act as an elicitor of plant defence. New Phytol 2001, 149:43-51.
5. Scheel D. Resistance response physiology and signal transduction. Curr Opin Plant Biol 1998, 1:305-310.
6. Sticher L., Mauch-Mani B., Métraux J.P. Systemic acquired resistance. Annu Rev Phytopathol 1997, 35:235-270.
7. Reymond P., Farmer E.E. Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1998, 1:404-411.
8. Kombrink E., Somssich I.E. Defense responses of plants to pathogens. Adv Bot Res 1995, 21:1-34.
9. Pieterse C.M.J., Wees S.C.M., Van Pelt J.A., Knoester M., Laan R., Gerrits H., et al. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 1998, 10:1571-1580.
10. Lorenzo O., Solano R. Molecular players regulating the jasmonate signaling network. Curr Opin Plant Biol 2005, 8:532-540.
11. Rostas M., Bennett R., Hilker M. Comparative physiological responses in Chinese cabbage induced by herbivory and fungal infection. J Chem Ecol 2002, 28:2449-2463.
12. Boller T. Chemoperception of microbial signals in plant cells. Annu Rev Plant Physiol Plant Mol Biol 1995, 46:189-214.
13. Klarzynski O., Plesse B., Joubert J.M., Yvin J.C., Kopp M., Kloareg B., et al. Linear beta-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol 2000, 124:1027-1038.
14. Khan W., Rayirath U.P., Subramanian S., Jithesh M.N., Rayorath P., Hodges D.M., et al. Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul 2009, 28:386-399.
15. Kloareg B., Quatrano R.S. Structure of cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Annu Rev 1988, 26:259-315.
16. Jayaraj J., Wan A., Rahman M., Punja Z.K. Seaweed extract reduces foliar fungal diseases on carrot. Crop Prot 2008, 27:1360-1366.
17. Rayorath P., Khan W., Palanisamy R., MacKinnon S.L., Stefanova R., Hankins S.D., et al. Extracts of brown seaweed, Ascophyllum nodosum, induce gibberellic acid (GA3) independent amylase activity in barley. J Plant Growth Regul 2008, 27:270-279.
18. Rayorath P., Benkel B., Hodges D.M., Allan-Wojtas P., Mackinnon S., Critchley A.T., et al. Lipophilic components of the brown seaweed, Ascophyllum nodosum, enhance freezing tolerance in Arabidopsis thaliana. Planta 2009, 230:135-147.
19. Kobayashi A., Tai A., Kanzaki H., Kawazu K. Elicitor active oligosaccharides from algal laminaran stimulate the production of antifungal compounds in alfalfa. Zeitschrift für Naturforschung 1993, 48:575-579.
20. Bouarab K., Potin P., Correa J., Kloareg B. Sulfated oligosaccharides mediate the interaction between a marine red algae and its green algal pathogenic endophytes. Plant Cell 1999, 11:1635-1650.
21. Gordon-Mills E.M., McCandless E.L. Carrageenans in the cell walls of Chondrus crispus Stack. (Rhodophyceae, Gigartinales). I. Localization with fluorescent antibody. Phycologia 1975, 14:275-281.
22. Zablackis E., Vreeland V., Doboszewski B., Laetsch W.M. Differential localization of carrageenan gelling sequences in Kappaphycus alvarezii var. tambalang (Rhodophyta) with FITC conjugated carrageenan oligosaccharides. J Phycol 1991, 27:241-248.
23. Boland G.J., Hall R. Index of plant hosts of Sclerotinia sclerotiorum. Can J Plant Pathol 1994, 16:93-100.
24. Purdy L.H. Sclerotinia sclerotiorum: history, diseases and symptomatology, host range, geographic distribution, and impact. Phytopathology 1979, 69:875-880.
25. Guo X., Stotz H.U. Defense against Sclerotinia sclerotiorum in Arabidopsis is dependent on jasmonic acid, salicylic acid, and ethylene signaling. Mol Plant Microbe Interact 2007, 20:1384-1395.
26. Godoy G., Steadman J.R., Dickman M.B., Dam R. Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiol Mol Plant Pathol 1990, 37:179-191.
27. Livingstone D.M., Jaime L.H., Patrick M.P., Elizabeth A.G. Enhancing resistance to Sclerotinia minor in peanut by expressing a barley oxalate oxidase gene. Plant Physiol 2005, 137:1354-1362.
28. Cessna S.G., Sears V.E., Dickman M.B., Low P.S. Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell 2000, 12:2191-2199.
29. Hegedus D.D., Rimmer S.R. Sclerotinia sclerotiorum: when " to be or not to be" a pathogen?. FEMS Microbiol Lett 2005, 251:177-184.
30. Kim H.S., Diers B.W. Inheritance of partial resistance to Sclerotinia stem rot in soybean. Crop Sci 2000, 40:55-61.
31. Dickman M.B., Mitra A. Arabidopsis thaliana as a model for studying Sclerotinia sclerotiorum pathogenesis. Physiol Mol Plant Pathol 1992, 41:255-263.
32. Xu X.-Q., Zhang Z.-Q. Kinetic spectrophotometric determination of oxalic acid based on the catalytic oxidation of bromophenol blue by dichromate. Mikrochim Acta 2000, 135:169-172.
33. Dong X., Ji R., Guo X., Foster S.J., Chen H., Dong C., et al. Expressing a gene encoding wheat oxalate oxidase enhances resistance to Sclerotinia sclerotiorum in oilseed rape (Brassica napus). Planta 2008, 228:331-340.
34. Sugiura M., Yamamura H., Harano K., Sasaki M., Morikawa M., Tsuboi M. Purification and properties of oxalate oxidase from barley seedlings. Chem Pharmaceut Bull (Tokyo) 1979, 27:2003-2007.
35. Sangha J.S., Gu K., Kaur J., Yin Z. An improved method for RNA isolation and cDNA library construction from immature seeds of Jatropha curcas L. BMC Res Notes 2010, 3:26. 10.1186/1756-0500-3-126.
36. Prithiviraj B., Bais H.P., Weir T., Suresh B., Schweizer H.P., Vivanco J.M. Down regulation of virulence factors of Pseudomonas aeruginosa by salicylic acid attenuates its virulence on Arabidopsis thaliana and Caenorhabditis elegans. Infect Immun 2005, 73:5319-5328.
37. Sugita-Konoshi Y., Yamashita S., Amano F., Shimizu M. Effects of carrageenans on the binding, phagocytotic, and killing abilities of macrophages to salmonella. Biosci Biotechnol Biochem 2003, 67:1425-1428.
38. Buck C.B., Thompson C.D., Roberts J.N., Muller M., Lowy D.R., Schiller J.T. Carrageenan is a potent inhibitor of papillomavirus infection. PLoS Pathogens 2006, 2:e69. 10.1371/journal.ppat.0020069.
39. Hu X., Bidney D.L., Yalpani N., Duvick J.P., Crasta O., Folkerts O., et al. Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiol 2003, 133:170-181.
40. Benhamou N. Elicitor-induced plant defense pathways. Trends Plant Sci 1996, 1:233-240.
41. Bradley D.J., Kjelvom P., Lamb C.J. Elicitor- and wound induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 1992, 70:2-30.
42. Reglinski T., Poole P.R., Whitaker G., Hoyte S.M. Induced resistance against Sclerotinia sclerotiorum in kiwifruit leaves. Plant Pathol 1997, 46:716-721.
43. Dann E., Diers B., Byrum J., Hammerschmidt R. Effect of treating soybean with 2,6-dichloroisonicotinic acid (INA) and benzothiadiazole (BTH) on seed yields and the level of disease caused by Sclerotinia sclerotiorum in field and greenhouse studies. Eur J Plant Pathol 1998, 104:271-278.
44. Carlucci M.J., Ciancia M., Matulewicz M.C., Cerezo A.S., Damonte E.B. Protective effect of a natural carrageenan on genital Herpes simplex virus infection in mice. Antiviral Res 2004, 64:137-141.
45. Nagorskaya V.P., Reunov A.V., Lapshina L.A., Yermak I.M., Barabanova A.O. Influence of k/b-carrageenan from red alga Tichocarpus crinitus on development of local infection induced by tobacco mosaic virus in xanthi-nc tobacco leaves. Biol Bull 2008, 35:310-314.
46. Yeh S., Chen J. Immunomodulation by carrageenans in the white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Aquaculture 2008, 276:22-28.
47. Barbeyron T., Flament D., Gurvan M., Potin P., Kloareg B. The sulphated-galactan hydrolases, agarases and carrageenases: structural biology and molecular evolution. Proceedings of the international workshop " Current approaches in basic and applied phycology" 2001, vol. 42:169-183. Cahiers de Biologie Marine.
48. Lumsden R.D. Histology and physiology of pathogenesis in plant diseases caused by Sclerotinia species. Phytopathology 1979, 69:890-896.
49. Zhou T., Boland G.J. Mycelial growth and production of oxalic acid by virulent and hypovirulent isolates of Sclerotinia sclerotiorum. Can J Plant Pathol 1999, 21:93-99.
50. Lane B.G., Dunwell J.M., Ray J.A., Schmitt M.R., Cuming A.C. Germin, a protein marker of early plant development, is an oxalate oxidase. J Biol Chem 1993, 268:12239-12242.
51. Wojtaszek P. Oxidative burst: an early plant response to pathogen infection. Biochem J 1997, 322:681-692.
52. Zhou F., Zhang Z., Gregersen P.L., Mikkelsen J.D., De Neergaard E., Collinge D.B., et al. Molecular characterization of the oxalate oxidase involved in the response of barley to the powdery mildew fungus. Plant Physiol 1998, 117:33-41.
53. Dong X. SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1998, 1:316-323.
54. Feys B.J., Parker J.E. Interplay of signaling pathways in plant disease resistance. Trends Genet 2000, 16:449-455.
55. McDowell J.M., Dangl J.L. Signal transduction in the plant immune response. Trends Biochem Sci 2000, 25:79-82.
56. Martinez C., Blanc F., Le Claire E., Besnard O., Nicole M., Baccou J.C. Salicylic acid and ethylene pathways are differentially activated in melon cotyledons by active or heat-denatured cellulase from Trichoderma longibrachiatum. Plant Physiol 2001, 127:334-344.
57. Thomma B., Eggermont K., Penninckx I., Mauch-Mani B., Vogelsang R., Cammue B., et al. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 1998, 95:15107-15111.
58. Kachroo A., Kachroo P. Salicylic acid-, jasmonic acid- and ethylene-mediated regulation of plant defense signaling. Genetic regulation of plant defense mechanisms 2007, 55-83. Springer, New York. J. Setlow (Ed.).
59. Zhao J., Wang J., An L., Doerge R.W., Chen Z.J., Grau C.R., et al. Analysis of gene expression profiles in response to Sclerotinia sclerotiorum in Brassica napus. Planta 2007, 227:13-24.
60. Laudert D., Weiler E.W. Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J 1998, 15:675-684.
61. Schaller F. Enzymes of the biosynthesis of octadecanoid-derived signaling molecules. J Exp Bot 2001, 52:11-23.
62. Broekaert W.F., Terras F.R.G., Cammue B.P.A., Osborn R. Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol 1995, 108:1353-1358.
63. Penninckx I.A.M.A., Eggermont K., Terras F.R.G., Thomma B.P.H.J., De Samblanx G.W., Buchala A., et al. Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid independent pathway. Plant Cell 1996, 8:2309-2323.
64. Terras F.R.G., Eggermont K., Kovaleva V., Raikhel N.V., Osborn R.W., Kester A., et al. Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell 1995, 7:573-588.
65. Van Loon L.C., Van Strien E.A. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 1999, 55:85-97.
66. Mauch F., Mauch-Mani B., Boller T. Antifungal hydrolases in pea tissue. II. Inhibition of fungal growth by combinations of chitinase and β-1,3-glucanase. Plant Physiol 1988, 88:936-942.
67. Ji C., Kuc J. Antifungal activity of cucumber B-1,3-glucanase and chitinase. Physiol Mol Plant Pathol 1996, 49:257-265.
68. Côté F., Hahn M.G. Oligosaccharins: structures and signal transduction. Plant Mol Biol 1994, 26:1379-1411.
69. McConn M., Creelman R.A., Bell F., Mullet J.E., Browse J. Jasmonic is essential for insect defense in Arabidopsis. Proc Natl Acad Sci USA 1997, 94:5473-5477.
70. Thomma B., Eggermont K., Tierens K., Broekaert W. Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol 1999, 121:1093-1102.
71. Wildermuth M.C., Dewdney J., Wu G., Ausubel F.M. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 2001, 414:562-565.
72. Staswick P.E., Tiryaki I., Rowe M. The jasmonate response locus JAR1 and several related arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 2002, 14:1405-1415.
73. Ton J., Van Pelt J.A., Van Loon L.C., Pieterse C.M. Differential effectiveness of salicylate-dependent and jasmonate/ethylendependent induced resistance in Arabidopsis. Mol Plant Microbe Interact 2002, 15:27-34.