Functional analysis of endo-1,4-β-glucanases in response to Botrytis cinerea and Pseudomonas syringae reveals their involvement in plant-pathogen interactions

Plant Biology

Volumn 15, Issue 5, 2013, Pages 819-831

  Finiti, I ^a   Leyva, M O ^a   Lopez Cruz J ^a   Calderan Rodrigues, B ^a   Vicedo, B ^b   Angulo, C ^a   Bennett, A B ^c   Grant, M ^d   Garcia Agustin P ^b   Gonzalez Bosch C ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITAT JAUME I   (Spain)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Arabidopsis; Botrytis cinerea; Cell wall; Defence response; Endo glucanases; Pseudomonas syringae; Solanum lycopersicum; Tomato

Indexed keywords

ABSCISSION; BACTERIUM; DEFENSE MECHANISM; DICOTYLEDON; ENZYME ACTIVITY; FRUIT; FUNGUS; GENE EXPRESSION; HOST-PATHOGEN INTERACTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BOTRYOTINIA FUCKELIANA; LYCOPERSICON ESCULENTUM; PSEUDOMONAS SYRINGAE;

CALLOSE; CELLULASE; CYCLOPENTANE DERIVATIVE; GLUCAN; JASMONIC ACID; OXYLIPIN; PHYTOHORMONE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; BOTRYTIS; BOTRYTIS CINEREA; CELL WALL; DEFENCE RESPONSE; DISEASE RESISTANCE; ENDO-GLUCANASES; ENZYMOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PLANT DISEASE; PLANT GENE; PSEUDOMONAS SYRINGAE; SIGNAL TRANSDUCTION; TOMATO;

ARABIDOPSIS; BOTRYTIS CINEREA; CELL WALL; DEFENCE RESPONSE; ENDO-GLUCANASES; PSEUDOMONAS SYRINGAE; SOLANUM LYCOPERSICUM; TOMATO;

ARABIDOPSIS; BOTRYTIS; CELL WALL; CELLULASE; CYCLOPENTANES; DISEASE RESISTANCE; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUCANS; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; OXYLIPINS; PLANT DISEASES; PLANT GROWTH REGULATORS; PLANT PROTEINS; PSEUDOMONAS SYRINGAE; SIGNAL TRANSDUCTION;

EID: 84882284558     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/j.1438-8677.2012.00701.x     Document Type: Article

References (55)

1. Adie B.A., Perez-Perez J., Perez-Perez M.M., Godoy M., Sanchez-Serrano J.J., Schmelz E.A., 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. Asselbergh B., De Vleesschauwer D., Hofte M. (2008) Global switches and fine-tuning - ABA modulates plant pathogen defense. Molecular Plant-Microbe Interactions, 21, 709-719.
3. Bestwick C.S., Brown I.R., Mansfield J.W. (1998) Localized changes in peroxidase activity accompany hydrogen peroxide generation during the development of a nonhost hypersensitive reaction in lettuce. Plant Physiology, 118, 1067-1078.
4. Brummell D.A., Harpster M.H. (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Molecular Biology, 47, 311-340.
5. Brummell D.A., Catala C., Lashbrook C.C., Bennett A.B. (1997) A membrane-anchored E-type endo-1, 4-beta-glucanase is localized on Golgi and plasma membranes of higher plants. Proceedings of the National Academy of Sciences USA, 94, 4794-4799.
6. Brummell D.A., Hall B.D., Bennett A.B. (1999) Antisense suppression of tomato endo-1, 4-beta-glucanase Cel2 mRNA accumulation increases the force required to break fruit abscission zones but does not affect fruit softening. Plant Molecular Biology, 40, 615-622.
7. Cantu D., Vicente A.R., Greve L.C., Dewey F.M., Bennett A.B., Labavitch J.M., Powell A.L. (2008) The intersection between cell wall disassembly, ripening, and fruit susceptibility to Botrytis cinerea. Proceedings of the National Academy of Sciences USA, 105, 859-864.
8. Catala C., Rose J.K., Bennett A.B. (1997) Auxin regulation and spatial localization of an endo-1, 4-beta-D-glucanase and a xyloglucan endotransglycosylase in expanding tomato hypocotyls. Plant Journal, 12, 417-426.
9. Clay N.K., Adio A.M., Denoux C., Jander G., Ausubel F.M. (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science, 323, 95-101.
10. Del Campillo E., Bennett A.B. (1996) Pedicel breakstrength and cellulase gene expression during tomato flower abscission. Plant Physiology, 111, 813-820.
11. Flors V., Leyva M.L., Vicedo B., Finiti I., Real M.D., Garcia-Agustin P., Bennett A.B., Gonzalez-Bosch C. (2007) Absence of the endo-beta-1, 4-glucanases Cel1 and Cel2 reduces susceptibility to Botrytis cinerea in tomato. Plant Journal, 52, 1027-1040.
12. Forcat S., Bennett M., Grant M., Mansfield J.W. (2010) Rapid linkage of indole carboxylic acid to the plant cell wall identified as a component of basal defence in Arabidopsis against hrp mutant bacteria. Phytochemistry, 71, 870-876.
13. Ham J.H., Kim M.G., Lee S.Y., Mackey D. (2007) Layered basal defenses underlie non-host resistance of Arabidopsis to Pseudomonas syringae pv. phaseolicola. Plant Journal, 51, 604-616.
14. 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 Journal, 57, 1015-1026.
15. Hauck P., Thilmony R., He S.Y. (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proceedings of the National Academy of Sciences USA, 100, 8577-8582.
16. Henrissat B., Coutinho P.M., Davies G.J. (2001) A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Molecular Biology, 47, 55-72.
17. Hernandez-Blanco C., Feng D.X., Hu J., Sanchez-Vallet A., Deslandes L., Llorente F., Berrocal-Lobo M., Keller H., Barlet X., Sanchez-Rodriguez C., Anderson L.K., Somerville S., Marco Y., Molina A. (2007) Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell, 19, 890-903.
18. Huckelhoven R. (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annual Review of Phytopathology, 45, 101-127.
19. Kang J.S., Frank J., Kang C.H., Kajiura H., Vikram M., Ueda A., Kim S., Bahk J.D., Triplett B., Fujiyama K., Lee S.Y., von Schaewen A., Koiwa H. (2008) Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus. Proceedings of the National Academy of Sciences USA, 105, 5933-5938.
20. Katagiri F., Thilmony R., He S.Y. (2002). The Arabidopsis thaliana-Pseudomonas syringae interaction. The Arabidopsis Book. The American Society of Plant Biologists. 1: e0039.
21. Kravchuk Z., Vicedo B., Flors V., Camanes G., Gonzalez-Bosch C., Garcia-Agustin P. (2011) Priming for JA-dependent defenses using hexanoic acid is an effective mechanism to protect Arabidopsis against B. cinerea. Journal of Plant Physiology, 168, 359-366.
22. Kruger W.M., Carver T.L.W., Zeyen R.J. (2002) Effects of inhibiting phenolic biosynthesis on penetration resistance of barley isolines containing seven powdery mildew resistance genes or alleles. Physiological.and Molecular Plant Pathology, 61, 41-51.
23. Lashbrook C.C., Gonzalez-Bosch C., Bennett A.B. (1994) Two divergent endo-beta-1, 4-glucanase genes exhibit overlapping expression in ripening fruit and abscising flowers. Plant Cell, 6, 1485-1493.
24. Lashbrook C.C., Giovannoni J.J., Hall B.D., Fischer R.L., Bennett A.B. (1998) Transgenic analysis of tomato endo-beta-1, 4-glucanase gene function. Role of cel1 in floral abscission. Plant Journal, 13, 303-310.
25. Libertini E., Li Y., Queen-Mason S.J. (2004) Phylogenetic analysis of the plant endo-beta-1, 4-glucanase gene family. Journal of Molecular Evolution, 58, 506-515.
26. 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 Physiology, 143, 1871-1880.
27. Milligan S.B., Gasser C.S. (1995) Nature and regulation of pistil-expressed genes in tomato. Plant Molecular Biology, 28, 691-711.
28. Minic Z., Jouranin L. (2006) Plant glycoside hydrolases involved in cell wall polysaccaride degradation. Plant Physiology and Biochemistry, 44, 435-449.
29. Molhoj M., Johansen B., Ulvskov P., Borkhardt B. (2001) Expression of a membrane-anchored endo-1, 4-beta-glucanase from Brassica napus, orthologous to KOR from Arabidopsis thaliana, is inversely correlated to elongation in light-grown plants. Plant Molecular Biology, 45, 93-105.
30. Molhoj M., Pagant S., Hofte H. (2002) Towards understanding the role of membrane-bound endo-beta-1, 4-glucanases in cellulose biosynthesis. Plant Cell Physiology, 43, 1399-1406.
31. Nickle T.C., Meinke D.W. (1998) A cytokinesis-defective mutant of Arabidopsis (cyt1) characterized by embryonic lethality, incomplete cell walls, and excessive callose accumulation. Plant Journal, 15, 321-332.
32. Nicol F., His I., Jauneau A., Vernhettes S., Canut H., Hofte H. (1998) A plasma membrane-bound putative endo-1, 4-beta-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO Journal, 17, 5563-5576.
33. Nishimura M.T., Stein M., Hou B.H., Vogel J.P., Edwards H., Somerville S.C. (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science, 301, 969-972.
34. Ohmiya Y., Samejima M., Shiroishi M., Amano Y., Kanda T., Sakai F., Hayashi T. (2000) Evidence that endo-1, 4-beta-glucanases act on cellulose in suspension-cultured poplar cells. Plant Journal, 24, 147-158.
35. Pfaffl M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, e45.
36. Real M.D., Company P., Garcia-Agustin P., Bennett A.B., Gonzalez-Bosch C. (2004) Characterization of tomato endo-beta-1, 4-glucanase Cel1 protein in fruit during ripening and after fungal infection. Planta, 220, 80-86.
37. Robert S., Bichet A., Grandjean O., Kierzkowski D., Satiat-Jeunemaitre B., Pelletier S., Hauser M.T., Hofte H., Vernhettes S. (2005) An Arabidopsis endo-1, 4-beta-D-glucanase involved in cellulose synthesis undergoes regulated intracellular cycling. Plant Cell, 17, 3378-3389.
38. Robert-Seilaniantz A., Grant M., Jones J.D. (2011) Hormone crosstalk in plant disease and defense: more than just Jasmonate-Salicylate Antagonism. Annual Review of Phytopathology, 49, 317-343.
39. Shen M., Cao Q., Li Y. (2008) Characterization of an endo-1, 4-glucanase from Lilium longiflorum that functioned in pollen germination and pollen tube growth. Chinese Science Bulletin, 53, 739-745.
40. Singh A., Prasad R. (2009) Salt stress effects growth and cell wall bound enzymes in Arachis hypogaea L. seedlings. International Journal of Integrative Biology, 7, 117-123.
41. Soylu S., Brown I., Mansfield J.W. (2005) Cellular reactions in Arabidopsis following challenge by strains of Pseudomonas syringae: from basal resistance to compatibility. Physiological and Molecular Plant Pathology, 66, 232-243.
42. Takahashi J., Rudsander U.J., Hedenstrom M., Banasiak A., Hartholdt J., Amelot N., Immerzeel P., Ryden P., Endo S., Ibatullin F.M., Brumer H., De Campillo E., Master E.R., Scheller H.V., Sunderberg B., Teeri T.T., Mellerowicz E.J. (2009) KORRIGAN1 and its aspen homolog PttCel9A1 decrease cellulose crystallinity in Arabidopsis stems. Plant and Cell Physiology, 50, 1099-1115.
43. 2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal, 11, 1187-1194.
44. Ton J., Mauch-Mani B. (2004) β-Amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant Journal, 38, 119-130.
45. de Torres-Zabala M., Sanchez P., Fernandez-Delmond I., Grant M. (2003) Expression profiling of the host response to bacterial infection: the transition from basal to induced defence responses in RPM1-mediated resistance. Plant Journal, 33, 665-676.
46. de Torres-Zabala M., Mansfield J.W., Grabov N., Brown I.R., Ammouneh H., Tsiamis G., Forsyth A., Robatzek S., Grant M., Boch J. (2006) Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis. Plant Journal, 47, 368-382.
47. de Torres-Zabala M., Truman W., Bennett M.H., Lafforgue G., Mansfield J.W., Rodriguez E.P., Bogre L., Grant M. (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO Journal, 26, 1434-1443.
48. de Torres-Zabala M., Bennett M.H., Truman W.H., Grant M.R. (2009) Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses. Plant Journal, 59, 375-386.
49. Urbanowicz B.R., Bennett A.B., Del C.E., Catala C., Hayashi T., Henrissat B., Hofte H., Queen-Mason S.J., Patterson S.E., Shoseyov O., Teeri T.T., Rose J.K. (2007a) Structural organization and a standardized nomenclature for plant endo-1, 4-beta-glucanases (cellulases) of glycosyl hydrolase family 9. Plant Physiology, 144, 1693-1696.
50. Urbanowicz B.R., Catala C., Irwin D., Wilson D.B., Ripoll D.R., Rose J.K. (2007b) A tomato endo-beta-1, 4-glucanase, SlCel9C1, represents a distinct subclass with a new family of carbohydrate binding modules (CBM49). Journal of Biological Chemistry, 282, 12066-12074.
51. Vicedo B., Flors V., de la O Leyva M., Finiti I., Kravchuk Z., Real M.D., Garcia-Agustin P., Gonzalez-Bosch C. (2009) Hexanoic acid-induced resistance against Botrytis cinerea in tomato plants. Molecular Plant-Microbe Interactions, 22, 1455-1465.
52. Vogel J.P., Raab T.K., Schiff C., Somerville S.C. (2002) PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell, 14, 2095-2106.
53. Wildermuth M.C., Dewdney J., Wu G., Ausubel F.M. (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414, 562-565.
54. Zhao Y., Thilmony R., Bender C.L., Schaller A., He S.Y., Howe G.A. (2003) Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant Journal, 36, 485-499.
55. Zimmermann P., Hirsch-Hoffmann M., Hennig L., Gruissem W. (2004) .GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiology, 136, 2621-2632.