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大学・研究所にある論文を検索できる 「The rhizobial autotransporter determines the symbiotic nitrogen fixation activity of Lotus japonicus in a host-specific manner」の論文概要。リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

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The rhizobial autotransporter determines the symbiotic nitrogen fixation activity of Lotus japonicus in a host-specific manner

Yoshikazu Shimoda Yuki Nishigaya Hiroko Yamaya-Ito Noritoshi Inagaki Yosuke Umehara Hideki Hirakawa Shusei Sato Toshimasa Yamazaki Makoto Hayashi 東北大学 DOI:10.1073/pnas.1913349117

2020.01.03

概要

Leguminous plants establish endosymbiotic associations with rhi- zobia and form root nodules in which the rhizobia fix atmospheric nitrogen. The host plant and intracellular rhizobia strictly control this symbiotic nitrogen fixation. We recently reported a Lotus japonicus Fix− mutant, apn1 (aspartic peptidase nodule-induced 1), that impairs symbiotic nitrogen fixation. APN1 encodes a nodule- specific aspartic peptidase involved in the Fix− phenotype in a rhi- zobial strain-specific manner. This host-strain specificity implies that some molecular interactions between host plant APN1 and rhizobial factors are required, although the biological function of APN1 in nodules and the mechanisms governing the interactions are un- known. To clarify how rhizobial factors are involved in strain- specific nitrogen fixation, we explored transposon mutants of Mes- orhizobium loti strain TONO, which normally form Fix− nodules on apn1 roots, and identified TONO mutants that formed Fix+ nodules on apn1. The identified causal gene encodes an autotransporter, part of a protein secretion system of Gram-negative bacteria. Ex-pression of the autotransporter gene in M. loti strain MAFF3030399, which normally forms Fix+ nodules on apn1 roots, resulted in Fix− nodules. The autotransporter of TONO functions to secrete a part of its own protein (a passenger domain) into extracellular spaces, and the recombinant APN1 protein cleaved the passenger protein in vitro. The M. loti autotransporter showed the activity to induce the genes involved in nodule senescence in a dose-dependent manner. There- fore, we conclude that the nodule-specific aspartic peptidase, APN1, suppresses negative effects of the rhizobial autotransporter in order to maintain effective symbiotic nitrogen fixation in root nodules.

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参考文献

1. H. Kouchi et al., How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol. 51, 1381–1397 (2010).

2. H. Kouchi, Symbiotic Nitrogen Fixation, Plant Metabolism and Biotechnology, H. Ashihara, A. Crozier, A. Komamine, Eds. (John Wiley & Sons, Ltd., Hoboken, NJ, 2011).

3. G. E. Oldroyd, Speak, friend, and enter: Signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252–263 (2013).

4. E. B. Madsen et al., A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637–640 (2003).

5. S. Radutoiu et al., Plant recognition of symbiotic bacteria requires two LysM receptor- like kinases. Nature 425, 585–592 (2003).

6. J. Lévy et al., A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361–1364 (2004).

7. L. Tirichine et al., Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441, 1153–1156 (2006).

8. E. Messinese et al., A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol. Plant Mi- crobe Interact. 20, 912–921 (2007).

9. K. Yano et al., CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl. Acad. Sci. U.S.A. 105, 20540–20545 (2008).

10. L. Schauser, A. Roussis, J. Stiller, J. Stougaard, A plant regulator controlling devel- opment of symbiotic root nodules. Nature 402, 191–195 (1999).

11. L. Krusell et al., The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. Plant Cell 17, 1625–1636 (2005).

12. T. Hakoyama et al., Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation. Nature 462, 514–517 (2009).

13. T. Hakoyama et al., The SNARE protein SYP71 expressed in vascular tissues is involved in symbiotic nitrogen fixation in Lotus japonicus nodules. Plant Physiol. 160, 897–905 (2012).

14. T. Hakoyama et al., The integral membrane protein SEN1 is required for symbiotic nitrogen fixation in Lotus japonicus nodules. Plant Cell Physiol. 53, 225–236 (2012).

15. H. Kumagai et al., A novel ankyrin-repeat membrane protein, IGN1, is required for persistence of nitrogen-fixing symbiosis in root nodules of Lotus japonicus. Plant Physiol. 143, 1293–1305 (2007).

16. D. Wang et al., A nodule-specific protein secretory pathway required for nitrogen- fixing symbiosis. Science 327, 1126–1129 (2010).

17. M. Bourcy et al., Medicago truncatula DNF2 is a PI-PLC-XD-containing protein re- quired for bacteroid persistence and prevention of nodule early senescence and defense-like reactions. New Phytol. 197, 1250–1261 (2013).

18. P. Mergaert et al., A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol. 132, 161–173 (2003).

19. B. Horváth et al., Loss of the nodule-specific cysteine rich peptide, NCR169, abolishes symbiotic nitrogen fixation in the Medicago truncatula dnf7 mutant. Proc. Natl. Acad. Sci. U.S.A. 112, 15232–15237 (2015).

20. M. Kim et al., An antimicrobial peptide essential for bacterial survival in the nitrogen- fixing symbiosis. Proc. Natl. Acad. Sci. U.S.A. 112, 15238–15243 (2015).

21. M. K. Udvardi, D. A. Day, Metabolite transport across symbiotic membranes of le- gume nodules. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 493–523 (1997).

22. B. N. Kaiser et al., Characterization of an ammonium transport protein from the peribacteroid membrane of soybean nodules. Science 281, 1202–1206 (1998).

23. K. Takanashi et al., LjMATE1: A citrate transporter responsible for iron supply to the nodule infection zone of Lotus japonicus. Plant Cell Physiol. 54, 585–594 (2013).

24. I. S. Kryvoruchko et al., An iron-activated citrate transporter, MtMATE67, is required for symbiotic nitrogen fixation. Plant Physiol. 176, 2315–2329 (2018).

25. P. Mergaert et al., Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc. Natl. Acad. Sci. U.S.A. 103, 5230–5235 (2006).

26. W. Van de Velde et al., Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327, 1122–1126 (2010).

27. P. Czernic et al., Convergent evolution of endosymbiont differentiation in dalbergioid and inverted repeat-lacking clade legumes mediated by nodule-specific cysteine-rich peptides. Plant Physiol. 169, 1254–1265 (2015).

28. F. Lamouche, N. Bonadé-Bottino, P. Mergaert, B. Alunni, Symbiotic efficiency of spherical and elongated bacteroids in the Aeschynomene-Bradyrhizobium symbiosis. Front. Plant Sci. 10, 377 (2019).

29. Q. Wang et al., Host-secreted antimicrobial peptide enforces symbiotic selectivity in Medicago truncatula. Proc. Natl. Acad. Sci. U.S.A. 114, 6854–6859 (2017).

30. Q. Wang et al., Nodule-specific cysteine-rich peptides negatively regulate nitrogen- fixing symbiosis in a strain-specific manner in Medicago truncatula. Mol. Plant Mi- crobe Interact. 31, 240–248 (2018).

31. S. Yang et al., Microsymbiont discrimination mediated by a host-secreted peptide in Medicago truncatula. Proc. Natl. Acad. Sci. U.S.A. 114, 6848–6853 (2017).

32. H. Yamaya-Ito et al., Loss-of-function of ASPARTIC PEPTIDASE NODULE-INDUCED 1 (APN1) in Lotus japonicus restricts efficient nitrogen-fixing symbiosis with specific Mesorhizobium loti strains. Plant J. 93, 5–16 (2018).

33. M. Kawaguchi et al., Root, root hair, and symbiotic mutants of the model legume Lotus japonicus. Mol. Plant Microbe Interact. 15, 17–26 (2002).

34. Y. Shimoda, H. Hirakawa, S. Sato, K. Saeki, M. Hayashi, Whole genome sequence of the nitrogen-fixing symbiotic rhizobia Mesorhizobium loti strain TONO. Genome Announc. 4, e01016-16 (2016).

35. T. Kaneko et al., Complete genome structure of the nitrogen-fixing symbiotic bac- terium Mesorhizobium loti. DNA Res. 7, 331–338 (2000).

36. F. Berrabah et al., A nonRD receptor-like kinase prevents nodule early senescence and defense-like reactions during symbiosis. New Phytol. 203, 1305–1314 (2014).

37. Y. Shimoda et al., Construction of signature-tagged mutant library in Mesorhizobium loti as a powerful tool for functional genomics. DNA Res. 15, 297–308 (2008).

38. M. Junker et al., Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc. Natl. Acad. Sci. U.S.A. 103, 4918–4923 (2006).

39. X. Yuan et al., Molecular basis for the folding of β-helical autotransporter passenger domains. Nat. Commun. 9, 1395 (2018).

40. S. Kelly et al., Genome sequence of the Lotus spp. microsymbiont Mesorhizobium loti strain R7A. Stand. Genomic Sci. 9, 6 (2014).

41. B. van den Berg, Crystal structure of a full-length autotransporter. J. Mol. Biol. 396, 627–633 (2010).

42. Y. Zhang, I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9, 40 (2008).

43. I. R. Henderson, F. Navarro-Garcia, M. Desvaux, R. C. Fernandez, D. Ala’Aldeen, Type V protein secretion pathway: The autotransporter story. Microbiol. Mol. Biol. Rev. 68, 692–744 (2004).

44. N. R. Movva, K. Nakamura, M. Inouye, Amino acid sequence of the signal peptide of ompA protein, a major outer membrane protein of Escherichia coli. J. Biol. Chem. 255, 27–29 (1980).

45. D. J. Gage, Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. J. Bacteriol. 184, 7042–7046 (2002).

46. Y. Xia et al., An extracellular aspartic protease functions in Arabidopsis disease re- sistance signaling. EMBO J. 23, 980–988 (2004).

47. J. E. Olivares et al., Nodulin 41, a novel late nodulin of common bean with peptidase activity. BMC Plant Biol. 11, 134 (2011).

48. M. Ramalho-Santos et al., Identification and proteolytic processing of procardosin A. Eur. J. Biochem. 255, 133–138 (1998).

49. K. N. Lohman, S. S. Gan, M. C. John, R. M. Amasino, Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol. Plant. 92, 322–328 (1994).

50. J. C. Pérez Guerra et al., Comparison of developmental and stress-induced nodule senescence in Medicago truncatula. Plant Physiol. 152, 1574–1584 (2010).

51. S. G. van Wyk, M. Du Plessis, C. A. Cullis, K. J. Kunert, B. J. Vorster, Cysteine protease and cystatin expression and activity during soybean nodule development and se- nescence. BMC Plant Biol. 14, 294 (2014).

52. S. Sinharoy et al., The C2H2 transcription factor regulator of symbiosome differentiation represses transcription of the secretory pathway gene VAMP721a and promotes sym- biosome development in Medicago truncatula. Plant Cell 25, 3584–3601 (2013).

53. C. Wang et al., NODULES WITH ACTIVATED DEFENSE 1 is required for maintenance of rhizobial endosymbiosis in Medicago truncatula. New Phytol. 212, 176–191 (2016).

54. B. E. Caldwell, Inheritance of a strain specific-ineffective nodulation in soybeans. Crop Sci. 6, 427–428 (1966).

55. T. A. Lie, Gene centers, a source for genetic variants in symbiotic nitrogen fixation: Host induced ineffectivity in Pisum sativum ecotype fulvum. Plant Soil 61, 125–134 (1981).

56. G. Duc, J. Picard, Note on the presence of the Sym-1 gene in Vicia faba hampering the symbiosis with Rhizobium leguminosarum. Euphytica 35, 61–64 (1986).

57. N. Dautin, H. D. Bernstein, Protein secretion in gram-negative bacteria via the au- totransporter pathway. Annu. Rev. Microbiol. 61, 89–112 (2007).

58. J. C. Leo, I. Grin, D. Linke, Type V secretion: Mechanism(s) of autotransport through the bacterial outer membrane. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1088–1101 (2012).

59. T. Suzuki et al., An outer membrane autotransporter, AoaA, of Azorhizobium cauli- nodans is required for sustaining high N2-fixing activity of stem nodules. FEMS Mi- crobiol. Lett. 285, 16–24 (2008).

60. C. I. Pislariu et al., The nodule-specific PLAT domain protein NPD1 is required for nitrogen-fixing symbiosis. Plant Physiol. 180, 1480–1497 (2019).

61. F. Berrabah, P. Ratet, B. Gourion, Multiple steps control immunity during the in- tracellular accommodation of rhizobia. J. Exp. Bot. 66, 1977–1985 (2015).

62. I. Hara-Nishimura, N. Hatsugai, S. Nakaune, M. Kuroyanagi, M. Nishimura, Vacuolar pro- cessing enzyme: An executor of plant cell death. Curr. Opin. Plant Biol. 8, 404–408 (2005).

63. O. Pierre et al., Involvement of papain and legumain proteinase in the senescence process of Medicago truncatula nodules. New Phytol. 202, 849–863 (2014).

64. N. Suganuma et al., cDNA macroarray analysis of gene expression in ineffective nodules induced on the Lotus japonicus sen1 mutant. Mol. Plant Microbe Interact. 17, 1223–1233 (2004).

65. C. I. Pislariu et al., A Medicago truncatula tobacco retrotransposon insertion mutant collection with defects in nodule development and symbiotic nitrogen fixation. Plant Physiol. 159, 1686–1699 (2012).

66. V. C. Clarke et al., Proteomic analysis of the soybean symbiosome identifies new symbiotic proteins. Mol. Cell. Proteomics 14, 1301–1322 (2015).

67. O. Pierre et al., Peribacteroid space acidification: A marker of mature bacteroid functioning in Medicago truncatula nodules. Plant Cell Environ. 36, 2059–2070 (2013).

68. M. S. Nelson, M. J. Sadowsky, Secretion systems and signal exchange between nitrogen-fixing rhizobia and legumes. Front. Plant Sci. 6, 491 (2015).

69. S. Okazaki, S. Zehner, J. Hempel, K. Lang, M. Göttfert, Genetic organization and functional analysis of the type III secretion system of Bradyrhizobium elkanii. FEMS Microbiol. Lett. 295, 88–95 (2009).

70. S. Yang, F. Tang, M. Gao, H. B. Krishnan, H. Zhu, R gene-controlled host specificity in the legume-rhizobia symbiosis. Proc. Natl. Acad. Sci. U.S.A. 107, 18735–18740 (2010).

71. P. A. Price et al., Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility. Proc. Natl. Acad. Sci. U.S.A. 112, 15244–15249 (2015).

72. J. L. Sachs, K. W. Quides, C. E. Wendlandt, Legumes versus rhizobia: A model for ongoing conflict in symbiosis. New Phytol. 219, 1199–1206 (2018).

73. T. L. Bailey, C. Elkan, Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28–36 (1994).

74. L. J. McGuffin, K. Bryson, D. T. Jones, The PSIPRED protein structure prediction server. Bioinformatics 16, 404–405 (2000).

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