Receptor-mediated exopolysaccharide perception controls bacterial infection

Nature

Volumn 523, Issue 7560, 2015, Pages 308-312

  Kawaharada, Y ^a   Kelly, S ^a,b   Nielsen, M Wibroe ^a   Hjuler, C T ^a,c   Gysel, K ^a   Muszynski A ^d   Carlson, R W ^d   Thygesen, M B ^a,c   Sandal, N ^a   Asmussen, M H ^a   Vinther, M ^a   Andersen, S U ^a   Krusell, L ^a   Thirup, S ^a   Jensen, K J ^a,c   Ronson, C W ^a,b   Blaise, M ^a,e   Radutoiu, S ^a   Stougaard, J ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF GEORGIA   (United States)

^e UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EPR3 PROTEIN; EXOPOLYSACCHARIDE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; CELL SURFACE RECEPTOR; LIPOPOLYSACCHARIDE; PLANT PROTEIN; PROTEIN KINASE;

BACTERIAL DISEASE; CELL ORGANELLE; DEVELOPMENTAL BIOLOGY; DISEASE CONTROL; ENZYME ACTIVITY; GENE EXPRESSION; LEGUME; MUTATION; PERCEPTION; POLYSACCHARIDE; RHIZOBACTERIUM; SYMBIOSIS; VIRULENCE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL STRAIN; CELLULAR DISTRIBUTION; INFECTION CONTROL; LOTUS JAPONICUS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NODULATION; NONHUMAN; PLANT EPIDERMIS CELL; PLANT GENE; PLANT ROOT; PRIORITY JOURNAL; PROCESS CONTROL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; AMINO ACID SEQUENCE; CARBOHYDRATE ANALYSIS; CHEMISTRY; GENE REPRESSION; GENETICS; LOTUS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; PHENOTYPE; PLANT EPIDERMIS; PROTEIN TERTIARY STRUCTURE; RHIZOBIUM; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; SYMBIOSIS;

BACTERIA (MICROORGANISMS); LOTUS CORNICULATUS VAR. JAPONICUS; RHIZOBIUM;

AMINO ACID SEQUENCE; CARBOHYDRATE SEQUENCE; LIPOPOLYSACCHARIDES; LOTUS; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PLANT EPIDERMIS; PLANT PROTEINS; PLANT ROOT NODULATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; RHIZOBIUM; ROOT NODULES, PLANT; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; SUPPRESSION, GENETIC; SYMBIOSIS;

EID: 84937418034     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14611     Document Type: Article

References (62)

1. Chu, H. & Mazmanian, S. K. Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nature Immunol. 14, 668-675 (2013).
2. Flemming, H. C. & Wingender, J. The biofilm matrix. Nature Rev. Microbiol. 8, 623-633 (2010).
3. Silipo, A. et al. Glyco-conjugates as elicitors or suppressors of plant innate immunity. Glycobiology 20, 406-419 (2010).
4. Becker, A., Fraysse, N. & Sharypova, L. Recent advances in studies on structure and symbiosis-related function of rhizobial K-antigens and lipopolysaccharides. Mol. Plant Microbe Interact. 18, 899-905 (2005).
5. Fraysse, N., Couderc, F. & Poinsot, V. Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. Eur. J. Biochem. 270, 1365-1380 (2003).
6. Jones, K. M., Kobayashi, H., Davies, B.W., Taga, M. E. & Walker, G. C. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nature Rev. Microbiol. 5, 619-633 (2007).
7. Desbrosses, G. J. & Stougaard, J. Root nodulation: a paradigm for how plantmicrobe symbiosis influences host developmental pathways. Cell Host Microbe10, 348-358 (2011).
8. Oldroyd, G. E. D., Murray, J. D., Poole, P. S. & Downie, J. A. The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet. 45, 119-144 (2011).
9. Fournier, J. et al. Mechanism of IT elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization. Plant Physiol. 148, 1985-1995 (2008).
10. Xie, F. et al. Legume pectate lyase required for root infection by rhizobia. Proc. Natl Acad. Sci. USA 109, 633-638 (2012).
11. Breedveld, M.W. et al. Polysaccharide synthesis in relation to nodulation behavior of Rhizobium leguminosarum. J. Bacteriol. 175, 750-757 (1993).
12. Cheng, H. P. & Walker, G. C. Succinoglycan is required for initiation and elongation of ITs during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 180, 5183-5191 (1998).
13. Wang, L. X., Wang, Y., Pellock, B. & Walker, G. C. Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti. J. Bacteriol. 181, 6788-6796 (1999).
14. Skorupska, A., Janczarek, M., Marczak, M., Mazur, A. & Krol, J. Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb. Cell Fact. 5, 7. (2006).
15. Åman, P., Franzen, L. E., Darvill, J. E. & Albersheim, P. Structural eludication, using HPLC-MSandGLC-MSof the acidic polysaccharide secreted by Rhizobiummeliloti strain 1021. Carbohydr. Res. 95, 263-282 (1981).
16. Reinhold, B. B. et al. Detailed structural characterization of succinoglycan, the major exopolysaccharide of Rhizobium meliloti Rm1021. J. Bacteriol. 176, 1997-2002 (1994).
17. Her, G.R., Glazebrook, J., Walker, G.C. & Reinhold, V. N. Structural studies of a novel exopolysaccharide produced by a mutant of Rhizobium meliloti strain Rm1021. Carbohydr. Res. 198, 305-312 (1990).
18. Robertsen, B.K., Aman, P., Darvill, A. G., McNeil, M. & Albersheim, P. Host-Symbiont Interactions. The structure of acidic extracellular polysaccharides secreted by Rhizobium leguminosarum and Rhizobium trifolii. Plant Physiol. 67, 389-400 (1981).
19. Battisti, L., Lara, J. C. & Leigh, J. A. Specific oligosaccharide form of the Rhizobium meliloti exopolysaccharide promotes nodule invasion in alfalfa. Proc. Natl Acad. Sci. USA 89, 5625-5629 (1992).
20. Urzainqui, A. & Walker, G. C. Exogenous suppression of the symbiotic deficiencies of Rhizobium meliloti exo mutants. J. Bacteriol. 174, 3403-3406 (1992).
21. Laus, M. C., van Brussel, A. A. & Kijne, J. W. Role of cellulose fibrils and exopolysaccharides of Rhizobium leguminosarum in attachment to and infection of Vicia sativa root hairs. Mol. Plant Microbe Interact. 18, 533-538 (2005).
22. Aslam, S.N. et al. Bacterial polysaccharides suppress induced innate immunity by calcium chelation. Curr. Biol. 18, 1078-1083 (2008).
23. Lehman, A. P. & Long, S. R. Exopolysaccharides from Sinorhizobium meliloti can protect against H2O2-dependent damage. J. Bacteriol. 195, 5362-5369 (2013).
24. Kelly, S. J. et al. Conditional requirement for exopolysaccharide in the Mesorhizobium-Lotus symbiosis. Mol. Plant Microbe Interact. 26, 319-329 (2013).
25. Lohmann, G. V. et al. Evolution and regulation of the Lotus japonicus LysM receptor gene family. Mol. Plant Microbe Interact. 23, 510-521 (2010).
26. Perry, J. A. et al. A TILLING reverse genetics tool and a web-accessible collection of mutants of the legume Lotus japonicus. Plant Physiol. 131, 866-871 (2003).
27. Fukai, E. et al. Establishment of a Lotus japonicus gene tagging population using the exon-targeting endogenous retrotransposon LORE1. Plant J. 69, 720-730 (2012).
28. Urbański, D. F., Malolepszy, A., Stougaard, J. & Andersen, S. U. Genome-wide LORE1 retrotransposon mutagenesis and high-throughput insertion detection in Lotus japonicus. Plant J. 69, 731-741 (2012).
29. Tanaka, K. et al. Role of LysM receptors in chitin-triggered plant innate immunity. Plant Signal. Behav. 8, e22598 (2013).
30. Liu, T. et al. Chitin-induced dimerization activates a plant immune receptor. Science 336, 1160-1164 (2012).
31. Madsen, L. H. et al. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Naure Commun. 1, 10 (2010).
32. Tirichine, L. et al. spontaneous root-nodule formation in the model legume Lotus japonicus: a novel class ofmutants nodulates in the absence of rhizobia. Mol. Plant Microbe Interact. 19, 373-382 (2006).
33. Rodpothong, P. et al. Nodulation gene mutants of Mesorhizobium loti R7A-nodZ and nolL mutants have host-specific phenotypes on Lotus spp. Mol. Plant Microbe Interact. 22, 1546-1554 (2009).
34. Thygesen, M. B. et al. Nucleophilic catalysis of carbohydrate oxime formation by anilines. J. Org. Chem. 75, 1752-1755 (2010).
35. Radutoiu, S. et al. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585-592 (2003).
36. Broghammer, A. et al. Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc. Natl Acad. Sci. USA 109, 13859-13864 (2012).
37. Høgslund, N. et al. Dissection of symbiosis and organ development by integrated transcriptome analysis of Lotus japonicus mutant and wild-type plants. PLoS ONE 4, e6556 (2009).
38. Jones, K. M. et al. Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proc. Natl Acad. Sci. USA 105, 704-709 (2008).
39. Laroche, F. J. et al. Theembryonic expressionpatterns of zebrafish genes encoding LysM-domains. Gene Expr. Patterns 13, 212-224 (2013).
40. Wong, J. E. M. M. et al. An intermolecular binding mechanism involving multiple LysM domains mediates carbohydrate recognition by an endopeptidase. Acta Crystallogr. D 71, 592-605 (2015).
41. Handberg, K. & Stougaard, J. Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Plant J. 2, 487-496 (1992).
42. Broughton, W. J. & Dilworth, M. J. Control of leghaemoglobin synthesis in snake beans. Biochem. J. 125, 1075-1080 (1971).
43. Sullivan, J. T. et al. Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J. Bacteriol. 184, 3086-3095 (2002).
44. Kelly, S. et al. Genome sequence of the Lotus spp. microsymbiont Mesorhizobium loti strain R7A. Stand. Genomic Sci. 9, 6 (2014).
45. Leong, S. A., Williams, P. H. & Ditta, G. S. Analysis of the 59 regulatory region of the gene for delta-aminolevulinic acid synthetase of Rhizobium meliloti. Nucleic Acids Res. 13, 5965-5976 (1985).
46. Kawaharada, Y., Eda, S., Minamisawa, K. & Mitsui, H. A Mesorhizobium loti mutant with reduced glucan content shows defective invasion of its host plant Lotus japonicus. Microbiology 153, 3983-3993 (2007).
47. Hansen, J., Jørgensen, J.-E., Stougaard, J. & Marcker, K. Hairy roots-a short cut to transgenic root nodules. Plant Cell Rep. 8, 12-15 (1989).
48. Stougaard, J., Abildsten, D. & Marcker, K. The Agrobacterium rhizogenes pRi TLDNA segment as a gene vector system for transformation of plants. Mol. Gen. Genet. 207, 251-255 (1987).
49. Petit, A. et al. Transformation and regeneration of the legume Lotus corniculatus: A systemfor molecular studies of symbiotic nitrogen fixation. Mol. Gen. Genet. 207, 245-250 (1987).
50. Thygesen, M. B., Sauer, J. & Jensen, K. J. Chemoselective capture of glycans for analysis on gold nanoparticles: carbohydrate oxime tautomers provide functional recognition by proteins. Chemistry 15, 1649-1660 (2009).
51. Xiong, X. et al. Receptor binding by an H7N9 influenza virus fromhumans. Nature 499, 496-499 (2013).
52. Heckmann, A. B. et al. Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol. Plant Microbe Interact. 24, 1385-1395 (2011).
53. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K. & Scheible, W. R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5-17 (2005).
54. Vandesompele, J. et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, 7 (2002).
55. Earley, K. W. et al. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629 (2006).
56. Voinnet, O., Rivas, S., Mestre, P. & Baulcombe, D. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956 (2003).
57. Hayashi, M. et al. Construction of a genetic linkage map of the model legume Lotus japonicus using an intraspecific F2 population. DNA Res. 8, 301-310 (2001).
58. Sandal, N. et al. A genetic linkage map of the model legume Lotus japonicus and strategies for fast mapping of new loci. Genetics 161, 1673-1683 (2002).
59. Krusell, L. et al. Shoot control of root development and nodulation ismediated by a receptor-like kinase. Nature 420, 422-426 (2002).
60. Nishimura, R. et al. HAR1 mediates systemic regulation of symbiotic organ development. Nature 420, 426-429 (2002).
61. Tirichine, L. et al. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441, 1153-1156 (2006).
62. Tirichine, L. et al. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315, 104-107 (2007).