Aphanomyces euteiches Cell Wall Fractions Containing Novel Glucan-Chitosaccharides Induce Defense Genes and Nuclear Calcium Oscillations in the Plant Host Medicago truncatula

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Nars, Amaury ^a,b   Lafitte, Claude ^a,b   Chabaud, Mireille ^c   Drouillard, Sophie ^d   Mélida, Hugo ^e   Danoun, Saïda ^a,b   Le Costaouëc, Tinaig ^d   Rey, Thomas ^a,b   Benedetti, Julie ^a,b,c   Bulone, Vincent ^e   Barker, David George ^c   Bono, Jean Jacques ^c   Dumas, Bernard ^a,b   Jacquet, Christophe ^a,b   Heux, Laurent ^d   Fliegmann, Judith ^a,b,c   Bottin, Arnaud ^a,b  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b Centre National de la Recherche Scientifique   (France)

^c LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^d CENTRE DE RECHERCHES SUR LES MACROMOLÉCULES VÉGÉTALES CERMAV CNRS   (France)

^e ALBANOVA UNIVERSITY CENTER   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 1,6 GLUCAN; CHITIN SYNTHASE; GLUCAN; GLUCOSE; GLYCOSIDASE; N ACETYLGLUCOSAMINE;

APHANOMYCES; APHANOMYCES EUTEICHES; ARTICLE; BARREL MEDIC; CALCIUM SIGNALING; CELL WALL; LEGUME; MYCORRHIZA; NONHUMAN; OOMYCETES; OSCILLATION; PLANT IMMUNITY; RHIZOBIACEAE; RICE; SEEDLING;

ACETYLGLUCOSAMINE; APHANOMYCES; CALCIUM SIGNALING; CELL NUCLEUS; CELL WALL; CHITIN; CHROMATOGRAPHY, GEL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUCANS; HOST-PATHOGEN INTERACTIONS; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; MEDICAGO TRUNCATULA; MODELS, MOLECULAR; PLANT EPIDERMIS; PLANT ROOTS;

EID: 84884528341     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075039     Document Type: Article

References (74)

1. Latgé JP, (2010) Tasting the fungal cell wall. Cell Microbiol 12: 863-872.
2. Boller T, Felix G, (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406.
3. Tyler BM, (2007) Phytophthora sojae: root rot pathogen of soybean and model oomycete. Mol Plant Pathol 8: 1-8.
4. Phillips AJ, Anderson VL, Robertson EJ, Secombes CJ, van West P, (2008) New insights into animal pathogenic oomycetes. Trends Microbiol 16: 13-19.
5. Beakes GW, Glockling SL, Sekimoto S, (2012) The evolutionary phylogeny of the oomycete "fungi". Protoplasma 249: 3-19.
6. Frey R, (1950) Chitin und Zellulose in Pilzzellwänden. Ber Schweiz Bot Ges 60: 199-230.
7. Bartnicki-García S, (1968) Cell wall chemistry, morphogenesis and taxonomy of fungi. Annu Rev Microbiol 22: 87-108.
8. Blum M, Boehler M, Randall E, Young V, Csukai M, et al. (2010) Mandipropamid targets the cellulose synthase-like PiCesA3 to inhibit cell wall biosynthesis in the oomycete plant pathogen, Phytophthora infestans. Mol Plant Pathol 11: 227-243.
9. Blum M, Gamper HA, Waldner M, Sierotzki H, Gisi U, (2012) The cellulose synthase 3 (CesA3) gene of oomycetes: structure, phylogeny and influence on sensitivity to carboxylic acid amide (CAA) fungicides. Fungal Biol 116: 529-542.
10. Blum M, Gisi U, (2012) Insights into the molecular mechanism of tolerance to carboxylic acid amide (CAA) fungicides in Pythium aphanidermatum. Pest Manag Sci 68: 1171-1183.
11. Lin CC, Aronson JM, (1970) Chitin and cellulose in the cell walls of the oomycete, Apodachlya sp. Arch Mikrobiol 72: 111-114.
12. Bulone V, Chanzy H, Gay L, Girard V, Fèvre M, (1992) Characterization of chitin and chitin synthase from the cellulosic cell wall fungus Saprolegnia monoica. Exp Mycol 16: 8-21.
13. Campos-Takaki GM, Dietrich SMC, Mascarenhas Y, (1982) Isolation and characterization of chitin from the cell walls of Achlya radiosa. J Gen Microbiol 128: 207-209.
14. Badreddine I, Lafitte C, Heux L, Skandalis N, Spanou Z, et al. (2008) Cell wall chitosaccharides are essential components and exposed patterns of the phytopathogenic oomycete Aphanomyces euteiches. Eukaryot Cell 7: 1980-1993.
15. Werner S, Steiner U, Becher R, Kortekamp A, Zyprian E, et al. (2002) Chitin synthesis during in planta growth and asexual propagation of the cellulosic oomycete and obligate biotrophic grapevine pathogen Plasmopara viticola. FEMS Microbiol Lett 208: 169-173.
16. Guerriero G, Avino M, Zhou Q, Fugelstad J, Clergeot P-H, et al. (2010) Chitin synthases from Saprolegnia are involved in tip growth and represent a potential target for anti-oomycete drugs. PLoS Pathog 6: e1001070.
17. Grenville-Briggs L, Gachon CMM, Strittmatter M, Sterck L, Kupper FC, et al. (2011) A molecular insight into algal-oomycete warfare: cDNA analysis of Ectocarpus siliculosus infected with the basal oomycete Eurychasma dicksonii. Plos One 6: 14.
18. Gaulin E, Jacquet C, Bottin A, Dumas B, (2007) Root rot disease of legumes caused by Aphanomyces euteiches. Mol Plant Pathol 8: 539-548.
19. Mélida H, Sandoval-Sierra JV, Diéguez-Uribeondo J, Bulone V, (2013) Analyses of extracellular carbohydrates in oomycetes unveil the existence of three different cell wall types. Eukaryot Cell 12: 194-203.
20. Cabib E, Durán A, (2005) Synthase III-dependent chitin is bound to different acceptors depending on location on the cell wall of budding yeast. J Biol Chem 280: 9170-9179.
21. Fontaine T, Sinenel C, Dubreucq G, Adam O, Delepierre M, et al. (2000) Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J Biol Chem 275: 41528-41529.
22. Kollár R, Petrakova E, Ashwell G, Robbins PW, Cabib E, (1995) Architecture of the yeast cell wall. The linkage between chitin and beta(1→3)-glucan. J Biol Chem 270: 1170-1178.
23. Silipo A, Erbs G, Shinya T, Dow JM, Parrilli M, et al. (2010) Glyco-conjugates as elicitors or suppressors of plant innate immunity. Glycobiology 20: 406-419.
24. Shibuya N, Minami E, (2001) Oligosaccharide signalling for defence responses in plant. Physiol Mol Plant Pathol 59: 223-233.
25. Oldroyd GE, (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11: 252-263.
26. Kombrink A, Sánchez-Vallet A, Thomma BP, (2011) The role of chitin detection in plant-pathogen interactions. Microbes Infect 13: 1168-1176.
27. Gust AA, Willmann R, Desaki Y, Grabherr HM, Nürnberger T, (2012) Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci 17: 495-502.
28. Gough C, Cullimore J, (2011) Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol Plant Microbe Interact 24: 867-878.
29. Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, et al. (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63.
30. Genre A, Chabaud M, Balzergue C, Puech-Pagès V, Novero M, et al. (2013) Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol 198: 190-202.
31. Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, et al. (2006) The Medicago truncatula lysin motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142: 265-279.
32. Fliegmann J, Uhlenbroich S, Shinya T, Martinez Y, Lefèbvre B, et al. (2011) Biochemical and phylogenetic analysis of CEBiP-like LysM domain-containing extracellular proteins in higher plants. Plant Physiol Biochem 49: 709-720.
33. Nyamsuren O, Colditz F, Rosendahl S, Tamasloukht M, Bekel T, et al. (2003) Transcriptional profiling of Medicago truncatula roots after infection with Aphanomyces euteiches (Oomycota) identifies novel genes upregulated during this pathogenic interaction. Physiol Mol Plant Pathol 63: 17-26.
34. Djébali N, Jauneau A, Ameline-Torregrosa C, Chardon F, Jaulneau V, et al. (2009) Partial resistance of Medicago truncatula to Aphanomyces euteiches is associated with protection of the root stele and is controlled by a major QTL rich in proteasome-related genes. Mol Plant Microbe Interact 22: 1043-1055.
35. Rey T, Nars A, Bonhomme M, Bottin A, Huguet S, et al. (2013) NFP, a LysM protein controlling Nod factor perception, also intervenes in Medicago truncatula resistance to pathogens. New Phytol 198: 875-886.
36. van Loon LC, Rep M, Pieterse CMJ, (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44: 135-162.
37. Gaulin E, Madoui M-A, Bottin A, Jacquet C, Mathé C, et al. (2008) Transcriptome of Aphanomyces euteiches: new oomycete putative pathogenicity factors and metabolic pathways. Plos One 3: e1723.
38. Henrissat B, Davies G, (1997) Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol 7: 637-644.
39. Nars A, Rey T, Lafitte C, Vergnes S, Amatya S, et al. (2013) An experimental system to study responses of Medicago truncatula roots to chitin oligomers of high degree of polymerization and other microbial elicitors. Plant Cell Rep 32: 489-502.
40. 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.
41. Vadassery J, Ranf S, Drzewiecki C, Mithöfer A, Mazars C, et al. (2009) A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J 59: 193-206.
42. Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, et al. (2011) Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis. New Phytol 189: 347-355.
43. Burton RA, Fincher GB, (2009) (1,3;1,4)-β-D-glucans in cell walls of the Poaceae, lower plants, and fungi: a tale of two linkages. Mol Plant 2: 873-882.
44. Chérif M, Benhamou N, Bélanger RR, (1992) Occurrence of cellulose and chitin in the hyphal walls of Pythium ultimum: a comparative study with other plant pathogenic fungi. Can J Microbiol 39: 213-222.
45. Asiegbu FO, Lonneborg A, Johansson M, (1996) Chitin and glucans detected in the cell walls of Pythium dimorphum, an oomycetous fungus. Eur J Forest Pathol 26: 315-321.
46. Bertke CC, Aronson JM, (1992) Hyphal wall chemistry of Lagenidium callinectes and Lagenidium chthamalophilum. Botanica Marina 35: 147-152.
47. Bertke CC, Aronson JM, (1992) Hyphal wall composition of Lagenidium giganteum. Mycologia 84: 571-574.
48. Dietrich SM, (1975) Comparative study of hyphal wall components of Oomycetes: Saprolegniaceae and Pythiaceae. An Acad Brasil Ciênc 47: 155-162.
49. Yim NH, Il Hwang E, Yun BS, Park KD, Moon JS, et al. (2008) Sesquiterpene furan compound CJ-01, a novel chitin synthase 2 inhibitor from Chloranthus japonicus SIEB. Biol Pharm Bull 31: 1041-1044.
50. Ruiz-Herrera J, Gonzalez-Prieto JM, Ruiz-Medrano R, (2002) Evolution and phylogenetic relationships of chitin synthases from yeasts and fungi. FEMS Yeast Res 1: 247-256.
51. Blank CE, (2011) An expansion of age constraints for microbial clades that lack a conventional fossil record using phylogenomic dating. J Mol Evol 73: 188-208.
52. Aziz A, Gauthier A, Bézier A, Poinssot B, Joubert JM, et al. (2007) Elicitor and resistance-inducing activities of beta-1,4 cellodextrins in grapevine, comparison with beta-1,3 glucans and alpha-1,4 oligogalacturonides. J Exp Bot 58: 1463-1472.
53. Zhang B, Ramonell K, Somerville S, Stacey G, (2002) Characterization of early, chitin-induced gene expression in Arabidopsis. Mol Plant Microbe Interact 15: 963-970.
54. Mithöfer A, Fliegmann J, Daxberger A, Ebel C, Neuhaus-Url G, et al. (2001) Induction of H2O2 synthesis by beta-glucan elicitors in soybean is independent of cytosolic calcium transients. Febs Lett 508: 191-195.
55. Okinaka Y, Mimori K, Takeo K, Kitamura S, Takeuchi Y, et al. (1995) A structural model for the mechanisms of elicitor release from fungal cell walls by plant beta-1,3-endoglucanase. Plant Physiol 109: 839-845.
56. Cheong JJ, Birberg W, Fugedi P, Pilotti A, Garegg PJ, et al. (1991) Structure-activity relationships of oligo-beta-glucoside elicitors of phytoalexin accumulation in soybean. Plant Cell 3: 127-136.
57. Fliegmann J, Mithöfer A, Wanner G, Ebel J, (2004) An ancient enzyme domain hidden in the putative beta-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 279: 1132-1140.
58. Waldmüller T, Cosio EG, Grisebach H, Ebel J, (1992) Release of highly elicitor-active glucans by germinating zoospores of Phytophthora megasperma f. sp. glycinea. Planta 188: 498-505.
59. Sieberer BJ, Chabaud M, Timmers AC, Monin A, Fournier J, et al. (2009) A nuclear-targeted cameleon demonstrates intranuclear Ca2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol 151: 1197-1206.
60. Zhu XH, Caplan J, Mamillapalli P, Czymmek K, Dinesh-Kumar SP, (2010) Function of endoplasmic reticulum calcium ATPase in innate immunity-mediated programmed cell death. EMBO J 29: 1007-1018.
61. Lecourieux D, Ranjeva R, Pugin A, (2006) Calcium in plant defence-signalling pathways. New Phytol 171: 249-269.
62. Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D, (2011) Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J 68: 100-113.
63. Navazio L, Baldan B, Moscatiello R, Zuppini A, Woo SL, et al. (2007) Calcium-mediated perception and defense responses activated in plant cells by metabolite mixtures secreted by the biocontrol fungus Trichoderma atroviride. BMC Plant Biol 7: 41.
64. Francia D, Chiltz A, Lo Schiavo F, Pugin A, Bonfante P, et al. (2011) AM fungal exudates activate MAP kinases in plant cells in dependence from cytosolic Ca2+ increase. Plant Physiol Biochem 49: 963-969.
65. Leclercq J, Fliegmann J, Tellström V, Niebel A, Cullimore JV, et al. (2008) Identification of a multigene family encoding putative β-glucan-binding proteins in Medicago truncatula. J Plant Physiol 165: 766-776.
66. Ben Amor B, Shaw SL, Oldroyd GED, Maillet F, Penmetsa RV, et al. (2003) The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J 34: 495-506.
67. Pauly N, Knight MR, Thuleau P, Graziana A, Muto S, et al. (2001) The nucleus together with the cytosol generates patterns of specific cellular calcium signatures in tobacco suspension culture cells. Cell Calcium 30: 413-421.
68. Rupley JA, (1964) The hydrolysis of chitin by concentrated hydrochloric acid, and the preparation of low-molecular-weight substrates for lysozyme. Biochim Biophys Acta 83: 245-255.
69. Somogyi M, (1952) Notes on sugar determination. J Biol Chem 195: 19-23.
70. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ, (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
71. Selvendran RR, Stevens BJH, O'Neil MA, (1985) Developments in the isolation and analysis of cell walls from edible plants. In: Seminar series Brett CT, Hillman JR, editors. Biochemistry of plant cell walls. Society for Experimental Biology. 28: 39-78.
72. Ciucanu I, Kerek F, (1984) A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res 131: 209-217.
73. Heux L, Brugnerotto J, Desbrières J, Versali MF, Rinaudo M, (2000) Solid state NMR for determination of degree of acetylation of chitin and chitosan. Biomacromolecules 1: 746-751.
74. Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, et al. (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388: 882-887.