Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 48, 2016, Pages 13875-13880

  Ling, Jun ^a   Wang, Hui ^a   Wu, Ping ^a   Li, Tao ^a   Tang, Yu ^a   Naseer, Nawar ^b   Zheng, Huiming ^a   Masson Boivin, Catherine ^c   Zhong, Zengtao ^a,c   Zhu, Jun ^a,b  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c CEMAGREF   (France)

Author keywords

Horizontal gene transfer; Host range; Integrative and conjugative element; Naringenin; Nodulation

Indexed keywords

CIRCULAR DNA; FLAVONOID; REGULATOR PROTEIN;

ARTICLE; AZORHIZOBIUM CAULINODANS; GENE EXPRESSION; HORIZONTAL GENE TRANSFER; HOST RANGE; NODULATION; NONHUMAN; PRIORITY JOURNAL; RHIZOBIACEAE; RHIZOSPHERE; SESBANIA; SYMBIOSIS; FABACEAE; GENETICS; GENOMIC ISLAND; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION;

AZORHIZOBIUM CAULINODANS; FABACEAE; GENE TRANSFER, HORIZONTAL; GENOMIC ISLANDS; NITROGEN FIXATION; PLANT ROOT NODULATION; SYMBIOSIS;

EID: 84999143638     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1615121113     Document Type: Article

References (44)

1. Polz MF, Alm EJ, Hanage WP (2013) Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet 29(3):170-175.
2. Ochman H, Moran NA (2001) Genes lost and genes found: Evolution of bacterial pathogenesis and symbiosis. Science 292(5519):1096-1099.
3. Wozniak RA, Waldor MK (2010) Integrative and conjugative elements: Mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 8(8):552-563.
4. Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: How many rhizobium recipes? Trends Microbiol 17(10):458-466.
5. Boivin TNI, et al. (1997) Stem nodulation in legumes: Diversity, mechanisms, and unusual characteristics. Crit Rev Plant Sci 16(1):1-30.
6. Fisher RF, Long SR (1992) Rhizobium-plant signal exchange. Nature 357(6380):655-660.
7. Wang D, Yang S, Tang F, Zhu H (2012) Symbiosis specificity in the legume: Rhizobial mutualism. Cell Microbiol 14(3):334-342.
8. Remigi P, Zhu J, Young JP, Masson-Boivin C (2016) Symbiosis within symbiosis: Evolving nitrogen-fixing legume symbionts. Trends Microbiol 24(1):63-75.
9. Servín-Garcidueñas LE, et al. (2016) Complete genome sequence of Bradyrhizobium sp. strain CCGE-LA001, isolated from field nodules of the enigmatic wild bean Phaseolus microcarpus. Genome Announc 4(2):e00126-16.
10. Lee KB, et al. (2008) The genome of the versatile nitrogen fixer Azorhizobium caulinodans ORS571. BMC Genomics 9:271.
11. Wang S, et al. (2014) Whole-genome sequencing of Mesorhizobium huakuii 7653R provides molecular insights into host specificity and symbiosis island dynamics. BMC Genomics 15:440.
12. Sullivan JT, Patrick HN, Lowther WL, Scott DB, Ronson CW (1995) Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci USA 92(19):8985-8989.
13. Sullivan JT, Ronson CW (1998) Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci USA 95(9):5145-5149.
14. Ramsay JP, et al. (2013) A widely conserved molecular switch controls quorum sensing and symbiosis island transfer in Mesorhizobium loti through expression of a novel antiactivator. Mol Microbiol 87(1):1-13.
15. Ramsay JP, et al. (2009) A LuxRI-family regulatory system controls excision and transfer of the Mesorhizobium loti strain R7A symbiosis island by activating expression of two conserved hypothetical genes. Mol Microbiol 73(6):1141-1155.
16. Ramsay JP, et al. (2015) Ribosomal frameshifting and dual-target antiactivation restrict quorum-sensing-activated transfer of a mobile genetic element. Proc Natl Acad Sci USA 112(13):4104-4109.
17. Goethals K, Van den Eeede G, Van Montagu M, Holsters M (1990) Identification and characterization of a functional nodD gene in Azorhizobium caulinodans ORS571. J Bacteriol 172(5):2658-2666.
18. Mergaert P, et al. (1996) Fucosylation and arabinosylation of Nod factors in Azorhizobium caulinodans: Involvement of nolK, nodZ as well as noeC and/or downstream genes. Mol Microbiol 21(2):409-419.
19. John M, Röhrig H, Schmidt J, Wieneke U, Schell J (1993) Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc Natl Acad Sci USA 90(2):625-629.
20. D'Haeze W, Mergaert P, Promé JC, Holsters M (2000) Nod factor requirements for efficient stem and root nodulation of the tropical legume Sesbania rostrata. J Biol Chem 275(21):15676-15684.
21. Maddocks SE, Oyston PC (2008) Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154(Pt 12):3609-3623.
22. Johnson CM, Grossman AD (2015) Identification of host genes that affect acquisition of an integrative and conjugative element in Bacillus subtilis. Mol Microbiol 98(6):1222.
23. Johnson CM, Grossman AD (2015) Integrative and conjugative elements (ICEs): What they do and how they work. Annu Rev Genet 49:577-601.
24. Lewis JA, Hatfull GF (2001) Control of directionality in integrase-mediated recombination: Examination of recombination directionality factors (RDFs) including Xis and Cox proteins. Nucleic Acids Res 29(11):2205-2216.
25. Ramsay JP, Sullivan JT, Stuart GS, Lamont IL, Ronson CW (2006) Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS. Mol Microbiol 62(3):723-734.
26. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: The microbial ecology of the rhizosphere. Nat Rev Microbiol 11(11):789-799.
27. Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64(1):180-201.
28. Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329(1-2):1-25.
29. Webster G, et al. (1998) The flavonoid naringenin stimulates the intercellular colonization of wheat roots by Azorhizobium caulinodans. Plant Cell Environ 21(4):373-383.
30. Gough C, et al. (1997) Specific flavonoids promote intercellular root colonization of Arabidopsis thaliana by Azorhizobium caulinodans ORS571. Mol Plant Microbe Interact 10(5):560-570.
31. Zhu J, et al. (2000) The bases of crown gall tumorigenesis. J Bacteriol 182(14):3885-3895.
32. Mølbak L, Molin S, Kroer N (2007) Root growth and exudate production define the frequency of horizontal plasmid transfer in the Rhizosphere. FEMS Microbiol Ecol 59(1):167-176.
33. Kroer N, Barkay T, Sørensen S, Weber D (1998) Effect of root exudates and bacterial metabolic activity on conjugal gene transfer in the rhizosphere of a marsh plant. FEMS Microbiol Ecol 25(4):375-384.
34. Waldor MK, Mekalanos JJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272(5270):1910-1914.
35. Peterson G, Kumar A, Gart E, Narayanan S (2011) Catecholamines increase conjugative gene transfer between enteric bacteria. Microb Pathog 51(1-2):1-8.
36. Popa O, Dagan T (2011) Trends and barriers to lateral gene transfer in prokaryotes. Curr Opin Microbiol 14(5):615-623.
37. Haukka K, Lindström K, Young JP (1998) Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolates from leguminous trees growing in Africa and Latin America. Appl Environ Microbiol 64(2):419-426.
38. Normand P, et al. (2007) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17(1):7-15.
39. Smillie CS, et al. (2011) Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480(7376):241-244.
40. Adebayo A, Watanabe I, Ladha JK (1989) Epiphytic occurrence of Azorhizobium caulinodans and other rhizobia on host and nonhost legumes. Appl Environ Microbiol 55(9):2407-2409.
41. Bulgarelli D, et al. (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488(7409):91-95.
42. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405(6784):299-304.
43. Remigi P, et al. (2014) Transient hypermutagenesis accelerates the evolution of legume endosymbionts following horizontal gene transfer. PLoS Biol 12(9):e1001942.
44. Cai T, et al. (2009) Host legume-exuded antimetabolites optimize the symbiotic rhizosphere. Mol Microbiol 73(3):507-517.