β-glucan: Crucial component of the fungal cell wall and elusive MAMP in plants

Fungal Genetics and Biology

Volumn 90, Issue , 2016, Pages 53-60

  Fesel, Philipp H ^a   Zuccaro, Alga ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Chitin; Dectin 1; Fungal MAMPs; Pattern recognition receptor; Plant immune system; glucan

Indexed keywords

BETA 1,3 GLUCAN; BETA 1,6 GLUCAN; BETA GLUCAN; CHITIN; DECTIN 1; N ACETYLGLUCOSAMINE; FUNGAL POLYSACCHARIDE; PATTERN RECOGNITION RECEPTOR;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL STRUCTURE; FUNGAL CELL WALL; FUNGAL STRUCTURES; HOST PARASITE INTERACTION; MICROBE ASSOCIATED MOLECULAR PATTERN; NONHUMAN; PHAGOCYTOSIS; PLANT IMMUNITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; ANIMAL; CELL WALL; FUNGUS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; MICROBIOLOGY; PLANT;

ANIMALS; BETA-GLUCANS; CELL WALL; CHITIN; FUNGAL POLYSACCHARIDES; FUNGI; HOST-PATHOGEN INTERACTIONS; HUMANS; PLANTS; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION;

EID: 84950336203     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2015.12.004     Document Type: Article

References (90)

1. Adachi Y., Ishii T., Ikeda Y., Hoshino A., Tamura H., Aketagawa J., Tanaka S., Ohno N. Characterization of β-glucan recognition site on C-type lectin, dectin 1. Infect. Immun. 2004, 72(7):4159-4171.
2. Albersheim P., Valent B.S. Host-pathogen interactions in plants. Plants, when exposed to oligosaccharides of fungal origin, defend themselves by accumulating antibiotics. J. Cell Biol. (United States) 1978, 78.
3. Anderson A.J. The isolation from three species of Colletotrichum of glucan containing polysaccharides that elicit a defense response in bean (Phaseolus vulgaris). Phytopathology 1978, 68:189-194.
4. Anderson A.J. Studies on the structure and elicitor activity of fungal glucans. Can. J. Bot. 1980, 58(22):2343-2348.
5. Ariizumi K., Shen G.L., Shikano S., Xu S., Ritter R., Kumamoto T., Edelbaum D., Morita A., Bergstrasser P.R., Takashima A. Identification of a novel, dendritic cell-associated molecule, dectin-1, by subtractive cDNA cloning. J. Biol. Chem. 2000, 275(26):20157-20167.
6. Ayers A.R., Ebel J., Valent B., Albersheim P. Host-pathogen interactions X. Fractionation and biological activity of an elicitor isolated from the mycelial walls of Phytophthora megasperma var. sojae. Plant Physiol. 1976, 57(5):760-765.
7. Aziz A., Poinssot B., Daire X., Adrian M., Bézier A., Lambert B., Joubert J.-M., Pugin A. Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Mol. Plant Microbe Interact. 2003, 16(12):1118-1128.
8. Bartnicki-Garcia S. Cell wall chemistry, morphogenesis, and taxonomy of fungi. Ann. Rev. Microbiol. 1968, 22(1):87-108.
9. Beffa R.S., Hofer R.M., Thomas M., Meins F. Decreased susceptibility to viral disease of [beta]-1, 3-glucanase-deficient plants generated by antisense transformation. Plant Cell 1996, 8(6):1001-1011.
10. Boller T., Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 2009, 60:379-406.
11. Bowman S.M., Free S.J. The structure and synthesis of the fungal cell wall. BioEssays 2006, 28(8):799-808.
12. Brown G.D. Dectin-1: a signalling non-TLR pattern-recognition receptor. Nat. Rev. Immunol. 2006, 6(1):33-43.
13. Brown G.D., Gordon S. Immune recognition: a new receptor for β-glucans. Nature 2001, 413(6851):36-37.
14. Brown G.D., Gordon S. Fungal β-glucans and mammalian immunity. Immunity 2003, 19(3):311-315.
15. Brown G.D., Gordon S. Immune recognition of fungal β-glucans. Cell. Microbiol. 2005, 7(4):471-479.
16. Brown G.D., Herre J., Williams D.L., Willment J.A., Marshall A.S., Gordon S. Dectin-1 mediates the biological effects of β-glucans. J. Exp. Med. 2003, 197(9):1119-1124.
17. Brown J., O'Callaghan C.A., Marshall A.S., Gilbert R.J., Siebold C., Gordon S., Brown G.D., Jones E.Y. Structure of the fungal β-glucan-binding immune receptor dectin-1: implications for function. Protein Sci. 2007, 16(6):1042-1052.
18. Cao Y., Liang Y., Tanaka K., Nguyen C.T., Jedrzejczak R.P., Joachimiak A., Stacey G. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife 2014, 3:e03766.
19. Cheong J.J., Birberg W., Fügedi P., Pilotti A., Garegg P.J., Hong N., Ogawa T., Hahn M.G. Structure-activity relationships of oligo-beta-glucoside elicitors of phytoalexin accumulation in soybean. Plant Cell 1991, 3(2):127-136.
20. Cheong J.J., Hahn M.G. A specific, high-affinity binding site for the hepta-beta-glucoside elicitor exists in soybean membranes. Plant Cell 1991, 3(2):137-147.
21. Cline K., Wade M., Albersheim P. Host-pathogen interactions XV. Fungal glucans which elicit phytoalexin accumulation in soybean also elicit the accumulation of phytoalexins in other plants. Plant Physiol. 1978, 62(6):918-921.
22. Cosio E.G., Feger M., Miller C.J., Antelo L., Ebel J. High-affinity binding of fungal β-glucan elicitors to cell membranes of species of the plant family Fabaceae. Planta 1996, 200(1):92-99.
23. Cosio E.G., Frey T., Ebel J. Identification of a high-affinity binding protein for a hepta-β-glucoside phytoalexin elicitor in soybean. Eur. J. Biochem. 1992, 204(3):1115-1123.
24. Cosio E.G., Frey T., Verduyn R., van Boom J., Ebel J. High-affinity binding of a synthetic heptaglucoside and fungal glucan phytoalexin elicitors to soybean membranes. FEBS Lett. 1990, 271(1):223-226.
25. Côté F., Roberts K.A., Hahn M.G. Identification of high-affinity binding sites for the hepta-β-glucoside elicitor in membranes of the model legumes Medicago truncatula and Lotus japonicus. Planta 2000, 211(4):596-605.
26. Czop J.K. The role of β-glucan receptors on blood and tissue leukocytes in phagocytosis and metabolic activation. Pathol. Immunopathol. Res. 1986, 5(3-5):286-296.
27. de Jonge R., van Esse H.P., Kombrink A., Shinya T., Desaki Y., Bours R., van der Krol S., Shibuya N., Joosten M.H.A.J., Thomma B.P. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 2010, 329(5994):953-955.
28. Douglas C.M. Fungal β (1, 3)-D-glucan synthesis. Med. Mycol. 2001, 39(1):55-66.
29. Ebel J., Ayers A.R., Albersheim P. Host-pathogen interactions XII. Response of suspension-cultured soybean cells to the elicitor isolated from Phytophthora megasperma var. sojae, a fungal pathogen of soybeans. Plant Physiol. 1976, 57(5):775-779.
30. El Gueddari N.E., Rauchhaus U., Moerschbacher B.M., Deising H.B. Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytol. 2002, 156(1):103-112.
31. Erbs G., Newman M.A. The role of lipopolysaccharides in induction of plant defence responses. Mol. Plant Pathol. 2003, 4(5):421-425.
32. Faulkner C., Petutschnig E., Benitez-Alfonso Y., Beck M., Robatzek S., Lipka V., Maule A.J. LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc. Natl. Acad. Sci. 2013, 110(22):9166-9170.
33. Feinberg H., Rowntree T.J., Tan S.L., Drickamer K., Weis W.I., Taylor M.E. Common polymorphisms in human langerin change specificity for glycan ligands. J. Biol. Chem. 2013, 288(52):36762-36771.
34. Felix G., Duran J.D., Volko S., Boller T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 1999, 18(3):265-276.
35. Fliegmann J., Mithöfer A., Wanner G., Ebel J. An ancient enzyme domain hidden in the putative β-glucan elicitor receptor of soybean may play an active part in the perception of pathogen-associated molecular patterns during broad host resistance. J. Biol. Chem. 2004, 279(2):1132-1140.
36. Fujikawa T., Sakaguchi A., Nishizawa Y., Kouzai Y., Minami E., Yano S., Koga H., Meshi T., Nishimura M. Surface α-1, 3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants. PLoS Pathog 2012, 8(8):e1002882.
37. Gauthier A., Trouvelot S., Kelloniemi J., Frettinger P., Wendehenne D., Daire X., Joubert J.-M., Ferrarini A., Delledonne M., Flors V., Poinssot B. The sulfated laminarin triggers a stress transcriptome before priming the SA-and ROS-dependent defenses during grapevine's induced resistance against Plasmopara viticola. PLoS ONE 2014, 9(2).
38. 2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol. 2013, 198(1):190-202.
39. Greeff C., Roux M., Mundy J., Petersen M. Receptor-like kinase complexes in plant innate immunity. Front. Plant Sci. 2012, 3.
40. Gust A.A., Biswas R., Lenz H.D., Rauhut T., Ranf S., Kemmerling B., Götz F., Glawischnig E., Lee J., Felix G., Nürnberger T. Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J. Biol. Chem. 2007, 282(44):32338-32348.
41. Ham K.S., Kauffmann S., Albersheim P., Darvill A.G. Host pathogen Interactions XXXIX. A soybean pathogenesis-related protein with b-1, 3-glucanase activity releases phytoalexin elicitor-active heat stable fragments from fungal walls. Mol. Plant-Microbe Interact 1991, 4:545-552.
42. Ham K.S., Wu S.C., Darvill A.G., Albersheim P. Fungal pathogens secrete an inhibitor protein that distinguishes isoforms of plant pathogenesis-related endo-β-1, 3-glucanases. Plant J. 1997, 11(2):169-179.
43. Henriquez M.A., Wolski E.A., Molina O.I., Adam L.R., Andreu A.B., Daayf F. Effects of glucans and eicosapentaenoic acid on differential regulation of phenylpropanoid and mevalonic pathways during potato response to Phytophthora infestans. Plant Physiol. Biochem. 2012, 60:119-128.
44. Inui H., Yamaguchi Y., Hirano S. Elicitor actions of N-acetylchitooligosaccharides and laminarioligosaccharides for chitinase and L-phenylalanine ammonia-lyase induction in rice suspension culture. Biosci. Biotechnol. Biochem. 1997, 61(6):975-978.
45. Kaku H., Nishizawa Y., Ishii-Minami N., Akimoto-Tomiyama C., Dohmae N., Takio K., Minami E., Shibuya N. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. 2006, 103(29):11086-11091.
46. Keen N.T., Yoshikawa M. β-1, 3-Endoglucanase from soybean releases elicitor-active carbohydrates from fungus cell walls. Plant Physiol. 1983, 71(3):460-465.
47. Klarzynski O., Plesse B., Joubert J.M., Yvin J.C., Kopp M., Kloareg B., Fritig B. Linear β-1, 3 glucans are elicitors of defense responses in tobacco. Plant Physiol. 2000, 124(3):1027-1038.
48. Latgé J.P. The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 2007, 66(2):279-290.
49. Latgé J.P. Tasting the fungal cell wall. Cell. Microbiol. 2010, 12(7):863-872.
50. Levitz S.M. Innate recognition of fungal cell walls. PLoS Pathog 2010, 6(4):e1000758.
51. Liang Y., Cao Y., Tanaka K., Thibivilliers S., Wan J., Choi J., Kang C., Qiu J., Stacey G. Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 2013, 341(6152):1384-1387.
52. Liang Y., Tóth K., Cao Y., Tanaka K., Espinoza C., Stacey G. Lipochitooligosaccharide recognition: an ancient story. New Phytol. 2014, 204(2):289-296.
53. Liu T., Liu Z., Song C., Hu Y., Han Z., She J., Fan F., Wang J., Jin C., Chang J., Zhou J.-M., Chai J. Chitin-induced dimerization activates a plant immune receptor. Science 2012, 336(6085):1160-1164.
54. Marshall R., Kombrink A., Motteram J., Loza-Reyes E., Lucas J., Hammond-Kosack K.E., Thomma B.P., Rudd J.J. Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol. 2011, 156(2):756-769.
55. Ménard R., Alban S., de Ruffray P., Jamois F., Franz G., Fritig B., Yvin J.-C., Kauffmann S. β-1, 3 glucan sulfate, but not β-1, 3 glucan, induces the salicylic acid signaling pathway in tobacco and Arabidopsis. Plant Cell 2004, 16(11):3020-3032.
56. Ménard R., de Ruffray P., Fritig B., Yvin J.C., Kauffmann S. Defense and resistance-inducing activities in tobacco of the sulfated β-1, 3 glucan PS3 and its synergistic activities with the unsulfated molecule. Plant Cell Physiol. 2005, 46(12):1964-1972.
57. Mentlak T.A., Kombrink A., Shinya T., Ryder L.S., Otomo I., Saitoh H., Terauchi R., Nishizawa Y., Shibuya N., Thomma B., Talbot N.J. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 2012, 24(1):322-335.
58. Miller K.J., Hadley J.A., Gustine D.L. Cyclic [beta]-1, 6-1, 3-glucans of Bradyrhizobium japonicum USDA 110 elicit isoflavonoid production in the soybean (Glycine max) host. Plant Physiol. 1994, 104(3):917-923.
59. Mithöfer A., Bhagwat A.A., Feger M., Ebel J. Suppression of fungal β-glucan-induced plant defence in soybean (Glycine max L.) by cyclic 1, 3-1, 6-β-glucans from the symbiont Bradyrhizobium japonicum. Planta 1996, 199(2):270-275.
60. Miya A., Albert P., Shinya T., Desaki Y., Ichimura K., Shirasu K., Narusaka Y., Kawakami N., Kaku H., Shibuya N. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. 2007, 104(49):19613-19618.
61. Narusaka Y., Shinya T., Narusaka M., Motoyama N., Shimada H., Murakami K., Shibuya N. Presence of LYM2 dependent but CERK1 independent disease resistance in Arabidopsis. Plant Signal. Behavior 2013, 8(9):e25345.
62. Ning J., Zhang W., Yi Y., Yang G., Wu Z., Yi J., Kong F. Synthesis of β-(1 → 6)-branched β-(1 → 3) glucohexaose and its analogues containing an α-(1 → 3) linked bond with antitumor activity. Bioorg. Med. Chem. 2003, 11(10):2193-2203.
63. Oliveira-Garcia E., Deising H.B. Infection structure-specific expression of β-1, 3-glucan synthase is essential for pathogenicity of Colletotrichum graminicola and evasion of β-glucan-triggered immunity in maize. Plant Cell 2013, 25(6):2356-2378.
64. Palma A.S., Feizi T., Zhang Y., Stoll M.S., Lawson A.M., Díaz-Rodríguez E., Campanero-Rhodes M.A., Costa J., Gordon S., Brown G.D., Chai W. Ligands for the β-glucan receptor, Dectin-1, assigned using "designer" microarrays of oligosaccharide probes (neoglycolipids) generated from glucan polysaccharides. J. Biol. Chem. 2006, 281(9):5771-5779.
65. Robinson S.M., Bostock R.M. β-glucans and eicosapolyenoic acids as MAMPs in plant-oomycete interactions: past and present. Front. Plant Sci. 2014, 5.
66. Ruel K., Joseleau J.P. Involvement of an extracellular glucan sheath during degradation of Populus wood by Phanerochaete chrysosporium. Appl. Environ. Microbiol. 1991, 57(2):374-384.
67. Ruiz-Herrera J. Fungal Cell Wall: Structure, Synthesis, and Assembly 1991, CRC Press.
68. Ruiz-Herrera J. Fungal Cell Wall: Structure, Synthesis, and Assembly 2012, CRC Press, pp. 73-95, (Chapter 6). second ed.
69. Sánchez-Vallet A., Saleem-Batcha R., Kombrink A., Hansen G., Valkenburg D.J., Thomma B.P., Mesters J.R. Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. Elife 2013, 2:e00790.
70. Schmidt W.E., Ebel J. Specific binding of a fungal glucan phytoalexin elicitor to membrane fractions from soybean Glycine max. Proc. Natl. Acad. Sci. 1987, 84(12):4117-4121.
71. Shahinian S., Bussey H. β-1, 6-Glucan synthesis in Saccharomyces cerevisiae. Mol. Microbiol. 2000, 35(3):477-489.
72. Sharp J.K., McNeil M., Albersheim P. The primary structures of one elicitor-active and seven elicitor-inactive hexa (beta-D-glucopyranosyl)-D-glucitols isolated from the mycelial walls of Phytophthora megasperma f. sp. glycinea. J. Biol. Chem. 1984, 259(18):11321-11336.
73. Sharp J.K., Valent B., Albersheim P. Purification and partial characterization of a beta-glucan fragment that elicits phytoalexin accumulation in soybean. J. Biol. Chem. 1984, 259(18):11312-11320.
74. Shibuya N., Minami E. Oligosaccharide signalling for defence responses in plant. Physiol. Mol. Plant Pathol. 2001, 59(5):223-233.
75. Shinya T., Osada T., Desaki Y., Hatamoto M., Yamanaka Y., Hirano H., Takai H., Che F.-S., Kaku H., Shibuya N. Characterization of receptor proteins using affinity cross-linking with biotinylated ligands. Plant Cell Physiol. 2010, 51(2):262-270.
76. Sietsma J.H., Eveleigh D.E., Haskins R.H. Cell wall composition and protoplast formation of some oomycete species. Biochim. Biophys. Acta (BBA) - General Subjects 1969, 184(2):306-317.
77. Singh P., Zimmerli L. Lectin receptor kinases in plant innate immunity. Front. Plant Sci. 2013, 4.
78. Sobanov Y., Bernreiter A., Derdak S., Mechtcheriakova D., Schweighofer B., Düchler M., Kalthoff F., Hofer E. A novel cluster of lectin-like receptor genes expressed in monocytic, dendritic and endothelial cells maps close to the NK receptor genes in the human NK gene complex. Eur. J. Immunol. 2001, 31(12):3493-3503.
79. Sukhithasri V., Nisha N., Biswas L., Kumar V.A., Biswas R. Innate immune recognition of microbial cell wall components and microbial strategies to evade such recognitions. Microbiol. Res. 2013, 168(7):396-406.
80. Tai A., Ohsaw E., Kawazu K., Kobayashi A. A minimum essential structure of LN-3 elicitor activity in bean cotyledons. Z. Naturforsch. C 1996, 51(1-2):15-19.
81. Taylor M.E., Drickamer K. Convergent and divergent mechanisms of sugar recognition across kingdoms. Curr. Opin. Struct. Biol. 2014, 28:14-22.
82. Umemoto N., Kakitani M., Iwamatsu A., Yoshikawa M., Yamaoka N., Ishida I. The structure and function of a soybean β-glucan-elicitor-binding protein. Proc. Natl. Acad. Sci. 1997, 94(3):1029-1034.
83. van den Burg H.A., Harrison S.J., Joosten M.H., Vervoort J., de Wit P.J. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol. Plant Microbe Interact. 2006, 19(12):1420-1430.
84. Waldmüller T., Cosio E.G., Grisebach H., Ebel J. Release of highly elicitor-active glucans by germinating zoospores of Phytophthora megasperma f. sp. glycinea. Planta 1992, 188(4):498-505.
85. Wan J., Tanaka K., Zhang X.C., Son G.H., Brechenmacher L., Nguyen T.H.N., Stacey G. LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol. 2012, 160(1):396-406.
86. Weigel D., Mott R. The 1001 genomes project for Arabidopsis thaliana. Genome Biol. 2009, 10(5):107.
87. Williams D.L. Overview of (1 → 3)-β-D-glucan immunobiology. Mediators Inflamm. 1997, 6(4):247-250.
88. Willment J.A., Gordon S., Brown G.D. Characterization of the human β-glucan receptor and its alternatively spliced isoforms. J. Biol. Chem. 2001, 276(47):43818-43823.
89. Yamaguchi T., Yamada A., Hong N., Ogawa T., Ishii T., Shibuya N. Differences in the recognition of glucan elicitor signals between rice and soybean: β-glucan fragments from the rice blast disease fungus Pyricularia oryzae that elicit phytoalexin biosynthesis in suspension-cultured rice cells. Plant Cell 2000, 12(5):817-826.
90. Yoshikawa M., Keen N.T., Wang M.C. A receptor on soybean membranes for a fungal elicitor of phytoalexin accumulation. Plant Physiol. 1983, 73(2):497-506.