Lipopolysaccharides elicit an oxidative burst as a component of the innate immune system in the seagrass Thalassia testudinum

Plant Physiology and Biochemistry

Volumn 70, Issue , 2013, Pages 295-303

  Loucks, Kyle ^a   Waddell, David ^a   Ross, Cliff ^a  

^a UNIVERSITY OF NORTH FLORIDA   (United States)

Author keywords

Elicitation; Hydrogen peroxide; Oxidative burst; Pathogen defense; Seagrass; Signaling pathways

Indexed keywords

ARABIDOPSIS PROTEIN; COMPLEMENTARY DNA; DIPHENYLIODONIUM SALT; GUANINE NUCLEOTIDE BINDING PROTEIN; HYDROGEN PEROXIDE; ION CHANNEL; LIPOPOLYSACCHARIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PHOSPHOLIPASE A2; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RESPIRATORY BURST OXIDASE HOMOLOG D, ARABIDOPSIS;

2′,7′-DICHLORODIHYDROFLUORESCEINDIACETATE; ADAPTATION; ARABIDOPSIS; ARTICLE; CHEMICALLY INDUCED DISORDER; DPI; DRUG EFFECT; ELICITATION; ENZYMOLOGY; GENETICS; H(2)DCF-DA; H(2)O(2); HYDROCHARITACEAE; METABOLISM; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PAMP; PATHOGEN DEFENSE; PATHOGEN-ASSOCIATED MOLECULAR PATTERN; PHYSIOLOGICAL STRESS; PLANT DISEASE; PLANT IMMUNITY; RBOH; RESPIRATORY BURST; RESPIRATORY BURST OXIDASE HOMOLOG; ROS; SAR; SEAGRASS; SEQUENCE HOMOLOGY; SERUM-SEAWATER AGAR; SIGNAL TRANSDUCTION; SIGNALING PATHWAYS; SSA; SYSTEMIC ACQUIRED RESISTANCE;

2′,7′-DICHLORODIHYDROFLUORESCEINDIACETATE; DIPHENYLENEIODONIUM; DPI; ELICITATION; H(2)DCF-DA; H(2)O(2); HYDROGEN PEROXIDE; LIPOPOLYSACCHARIDE; LPS; NADPH; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; OXIDATIVE BURST; PAMP; PATHOGEN DEFENSE; PATHOGEN-ASSOCIATED MOLECULAR PATTERN; RBOH; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST OXIDASE HOMOLOG; ROS; SAR; SEAGRASS; SERUM-SEAWATER AGAR; SIGNALING PATHWAYS; SSA; SYSTEMIC ACQUIRED RESISTANCE;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; GTP-BINDING PROTEINS; HYDROCHARITACEAE; ION CHANNELS; LIPOPOLYSACCHARIDES; NADPH OXIDASE; PHOSPHOLIPASES A2; PLANT DISEASES; PLANT IMMUNITY; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

ARABIDOPSIS THALIANA; THALASSIA TESTUDINUM; TRACHEOPHYTA;

EID: 84879557208     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2013.05.023     Document Type: Article

References (55)

1. Waycott M., Duarte C.M., Carruthers T.J.B., Orth R.J., Dennison W.C., Olyarnik S., Calladine A., Fourqurean J.W., Heck K.L., Hughes A.R., Kendrick G.A., Kenworthy W.J., Short F.T., Williams S.L. Accelerating loss of seagrasses across the global threatens coastal ecosystems. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:12377-12381.
2. Muehlstein L. Perspectives on the wasting disease of eelgrass, Zostera marina. Dis. Aquat. Organ. 1989, 7:211-221.
3. Young E.L. Studies on Labyrinthula. The etiologic agent of the wasting disease of eelgrass. Am. J. Bot. 1943, 30:586-593.
4. Trevathan S.M., Kahn A., Ross C. Effects of short-term hypersalinity exposure on the susceptibility to wasting disease in the subtropical seagrass Thalassia testudinum. Plant Physiol. Biochem. 2011, 49:1051-1058.
5. Bockelmann A.C., Beining K., Reusch T.B.H. Widespread occurance of endophytic Labyrinthula spp. in northern European eelgrass Zostera marina beds. Mar. Ecol. Prog. Ser. 2012, 445:109-116.
6. Janssen T., Bremer B. The age of major monocot groups inferred from 800+ rbcL sequences. J.Linn. Soc. Bot. 2004, 146:385-398.
7. Jones J.D.G., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
8. Dow M., Newman M.A., von Roepenack E. The induction and modulation of plant defense responses by bacterial lipopolysaccharides. Annu. Rev. Phytopathol. 2000, 38:241-261.
9. Coventry H.S., Dubery I.A. Lipopolysaccharides from Burkholderia cepacia contribute to an enhanced defensive capacity and the induction of pathogenesis-related proteins in Nicotiana tabacum. Physiol. Mol. Plant 2001, 58:149-158.
10. Erbs G., Newman M. The role of lipopolysaccharide and peptidoglycan, two glycosylated bacterial microbe-associated molecular patterns (MAMPs), in plant innate immunity. Mol. Plant Pathol. 2012, 13:95-104.
11. Gerber I.B., Zeidler D., Durner J., Duber I.A. Early perception responses of Nicotiana tabacum cells in response to lipopolysaccharides from Burkholderia cepacia. Planta 2004, 218:647-657.
12. Desaki Y., Miya A., Venkatesh B., Tsuyumu B., Yamane H., Kaku H., Minami E., Shibuya N. Bacterial lipopolysaccharides induce defense responses associated with programmed cell death in rice cells. Plant Cell Physiol. 2006, 47:1530-1540.
13. Doke N. Generation of superoxide anion by potato tuber protoplasts during the hypersensitive response to hyphal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressors of hypersensitivity. Physiol. Plant Pathol. 1983, 23:359-367.
14. Wojtaszek P. Oxidative burst: an early plant response to pathogen infection. Biochem. J. 1997, 322:681-692.
15. 2-producing enzyme, accumulates in barley attacked by the powdery mildew fungus. Plant J. 1995, 8:139-145.
16. Allan A.C., Fluhr R. Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 1997, 9:1559-1572.
17. Bolwell G.P., Butt V.S., Davies D.R., Zimmerlin A. The origin of the oxidative burst in plants. Free Radic. Res. 1995, 23:517-532.
18. Bolwell G.P., Davies D.R., Gerrish C., Auh C.K., Murphy T.M. Comparative biochemistry of the oxidative burst produced by rose and french bean cells reveals two distinct mechanisms. Plant Physiol. 1998, 116:1379-1385.
19. Sagi M., Fluhr R. Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 2006, 141:336-340.
20. Küpper F.C., Kloareg B., Guern J., Potin P. Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. Plant Physiol. 2001, 125:278-291.
21. Küpper F.C., Müller D.G., Peters A.F., Kloareg B., Potin P. Oligoalginate recognition and oxidative burst play a key role in natural and induced resistance of sporophytes of Laminariales. J.Chem. Ecol. 2002, 28:2057-2081.
22. Zambounis A.G., Kalamaki M.S., Tani E.E., Paplomatas E.J., Tsaftaris A.S. Expression anlaysis of defense related genes in cotton (Gossypium hirsutum) after Fusarium oxysporum f. sp. vasinfectum infection and following chemical elicitation using salicylic acid analog and methyl jasmonate. Plant Mol. Biol. Rep. 2012, 30:225-234.
23. Weinberger F., Friedlander M., Hoppe H.G. Oligoagars elicit a physiological response in Gracilaria conferta (Rhodophyta). J.Phycol. 1999, 35:747-755.
24. Weinberger F., Leonardi P., Miravalles A., Correa J.A., Lion U., Kloareg B., Potin P. Dissection of two distinct defense-related response to agar oligosaccharides in Gracilaria chilensis (Rhodophyta) and Gracilaria conferta (Rhodophyta). J.Phycol. 2005, 41:863-873.
25. Üpper F.C.K., Gaquerel E., Boneberg E.M., Morath S., Salaün J.P., Potin P. Early events in the perception of lipopolysaccharides in the brown alga Laminaria digitata include an oxidative burst and activation of fatty acid oxidation cascades. J.Exp. Bot. 2006, 57:1991-1999.
26. Weinberger F. Pathogen-induced defense and innate immunity in macroalgae. Biol. Bull. 2007, 213:290-302.
27. Lawrie A.M., Noble E.M., Tunnah P., Brown N.R., Endicott J.A. Protein kinase inhibition by staurosporine revealed in details the molecular interaction with CDK2. Nat. Struct. Mol. Biol. 1997, 4:796-800.
28. Chandra S., Heinstein P.F., Low P.S. Activation of phospholipase A by plant defense elicitors. Plant Physiol. 1996, 110:979-986.
29. Fujisawa Y., Kato H., Iwasaki Y. Structure and function of heterotrimeric G proteins in plants. Plant Cell Physiol. 2001, 42:789-794.
30. Zeidler D., Zähringer U., Gerber I., Dubrey I., Hartung T., Bors W., Hutzler P., Durner J. Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:15811-15816.
31. Seydel U., Labischinki K., Kastowsky M., Brandenburg K. Phase behavior, supramolecular structure, and molecular conformation of lipopolysaccharide. Immunobiology 1993, 187:191-211.
32. Bahnweg G., Jäckle I. Anew approach to taxonomy of the thraustochytriales and labyrinthulales. The Biology of Marine Fungi 1986, 131-140. Cambridge Publishing, New York. S.T. Moss (Ed.).
33. Raghukumar S. Ecology of the marine protists, the labyrinthulomycetes (thraustochytrids and labyrinthulids). Eur. J. Protistol. 2002, 38:127-145.
34. Preston T.M., King C.A. Actin-based motility in the net slime mould Labyrinthula: evidence for the role of myosin in gliding movement. J.Eukaryot. Microbiol. 2005, 52:461-475.
35. Ndimba B.K., Chivasa S., Hamilton J.M., Simon W.J., Slabas A.R. Proteomic analysis of changes in the extracellular matrix of Arabidopsis cell suspension cultures induced by fungal elicitors. Proteomics 2003, 3:1047-1059.
36. Baker J.C., Orlandi E.W., Deahl K.L. Oxidative metabolism in plant/bacteria interactions: characterization of a unique oxygen uptake response of potato suspension cells. Physiol. Mol. Plant 2001, 59:25-32.
37. Boller T. Chemoperception of microbial signals in plant cells. Annu. Rev. Plant Phys. 1995, 46:189-214.
38. Zhao J., Davis L.C., Verpoote R. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol. Adv. 2005, 23:283-333.
39. Davies D.R., Bindschedler L.V., Strickland T.S., Bolwell P.G. Production of reactive oxygen species in Arabidopsis thaliana cell suspension cultures in response to an elicitor from Fusarium oxysporum: implications for basal resistance. J.Exp. Bot. 2006, 57:1817-1827.
40. Liu P., Zhang L., Wang Q.L., Niehaus K., Baluška F., Šamaj J., Lin J.X. Lipid microdomain polarization is required for NADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. Plant J. 2009, 60:303-313.
41. Daudi A., Cheng Z., O'Brien J.A., Mammarella N., Khan S., Ausubel F.M., Bolwell G.P. The apoplastic oxidative burst peroxidase in Arabidopsis isamajor component of pattern-triggered immunity. Plant Cell 2012, 24:275-287.
42. Viard M.P., Martin F., Pugin A., Ricci P., Blein J.P. Protein phosphorylation is induced in tobacco cells by the elicitor cryptogein. Plant Physiol. 1994, 104:1245-1249.
43. 2+ and protein-kinase activity. Planta 1992, 187:136-141.
44. Castro R., Zarra I., Lamas J. Water soluble seaweed extracts modulate the respiratory burst activity of turbot phagocytes. Aquaculture 2004, 229:67-78.
45. Ross C., Küpper F.C., Jacobs R.S. Involvement of reactive oxygen species and reactive nitrogen species in the wound response of Dasycladus vermicularis. Chem. Biol. 2006, 13:353-364.
46. Whiteley B., Cassel D., Zhuang Y.X., Glaser L. Tumor promoter phorbol 12-myristate 13-acetate inhibits mitogen-stimulated Na+/H+ exchange in human epidermoid carcinoma A431 cells. J.Cell Biol. 1984, 99:1162-1166.
47. Afrasiabi E., Ahlgren J., Bergelin N., Törnquist K. Phorbol 12-myristate 13-acetate inhibits FRO anaplastic human thyroid cancer cell proliferation by inducing cell cycle arrest in G1/S phase: evidence for an effect mediated by PKCδ. Mol. Cell. Endocrinol. 2008, 292:26-35.
48. L. Legendre, Y.G. Yueh, R. Crain, N. Haddock, P.F. Heinstein, P.S. Low, Phospholipase C activation during elication of the oxidative burst in cultured plant cells, J. Biol. Chem. 268, 24559-24563.
49. 2+ fluxes during elicitation of the oxidative burst in aequorin-transformed tobacco cells. J.Biol. Chem. 1997, 272:28274-28280.
50. Moya C.E., Jacobs R.S. Pseudopterosin A inhibits phagocytosis and alters intracellular calcium turnover in a pertussis toxin sensitive site in Tetrahymena thermophile. Comp. Biochem. Physiol. C. 2006, 143:436-443.
51. Bolwell G.P., Rodgers M.W., Murphy D.L., Jones D. Modulation of the elicitation response in cultured French bean cells its implication for the mechanism of signal transduction. Phytochemistry 1991, 30:397-405.
52. Mahady G.B., Liu C., Beecher C.W.W. Involvement of protein kinase and G proteins in the signal transduction of benzophenanthridine alkaloid biosynthesis. Phytochemistry 1998, 48:93-102.
53. Dennison K.L., Spalding E.P. Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiol. 2000, 124:1511-1514.
54. 2+ and phosphorylation. J.Biol. Chem. 2008, 283:8885-8892.
55. 2+. New Phytol. 2001, 151:185-194.