doi: 10.15389/agrobiology.2017.5.869eng

UDC 633.31/.37:631.461.52:577.21

Acknowlegdgements:
Supported by Russian Science Foundation (grant № 14-24-00135);
V.A. Zhukov is supported by grant № 14-04-01442-а form Russian Foundation
for Basic Research

 

NCR PEPTIDES — PLANT EFFECTORS GOVERNING TERMINAL
DIFFERENTIATION OF NODULE BACTERIA INTO
THE SYMBIOTIC FORM (review)

M.S. Kliukova1, V.A. Zhukov1, I.A. Tikhonovich1, 2

1All-Russian Research Institute for Agricultural Microbiology, Federal Agency of Scientific Organizations, 3, sh. Podbel’skogo, St. Petersburg, 196608 Russia,
e-mail: zhukoff01@yahoo.com, Zhukov@ARRIAM.ru (corresponding author);
2Saint-Petersburg State University, 7/9, Universitetskaya nab., St. Petersburg, 199034 Russia

ORCID:
Kliukova M.S. orcid.org/0000-0003-1119-5512
Zhukov V.A. orcid.org/0000-0002-2411-9191
Tikhonovich I.A. orcid.org/0000-0001-8968-854X

Received December 12, 2016

Uptake of mineral nutrients from the soil is the challenge of plant survival. In particular, the availability of such macro-elements as nitrogen and phosphorus is the limiting factor for plant growth and development. Some plant genera overcome this limitation by establishing symbiotic relationships with microorganisms. A remarkable example of such symbiosis is one between legumes and rhizobia — a group of nitrogen fixing soil bacteria. Rhizobial penetration into roots of a specific host plant causes initiation of a specialized organ, symbiotic nodule. Within cells of symbiotic nodule free-living bacteria differentiate into a symbiotic form called «bacteroids». Such organelle-like structures provide plants with fixed nitrogen in exchange for nutrients (B.J. Ferguson et al., 2010). A number of legumes form nodules, in which bacteria terminally (irreversibly) differentiate into bacteroids, thus losing the opportunity to return to the free-living state. Terminal differentiation of bacteroids begins soon after release of the rhizobia into plant cells and leads to morphological, physiological and genetic changes in bacterial cells. It has been shown that a large family of antimicrobial peptides of plants called Nodule-specific Cysteine-Rich peptides (NCR peptides) plays a key regulatory role in this process (P. Mergaert et al., 2003). Its representatives are similar in structure and mode of action to defensins — plant innate immunity factors; however, NCR genes are expressed only in nodules, which fact is reflected in their name. At the moment, about 700 genes encoding NCR peptides that are highly variable in their amino acid sequence but possess a distinct conservative cysteine motif required for the adoption of correct conformation were identified in the genome of the model legume Medicago truncatula Gaertn. NCR peptides are delivered to their intracellular target symbiosome (сell compartments containing bacteroides) triggering the process of differentiation by interacting with the components of membranes and various intracellular targets of bacteria (D. Wang et al., 2010). The most studied member of this family in M. truncatula is MtNCR247 a cationic peptide with four cysteines forming two disulfide bonds in oxidized form. MtNCR247 affects transcription, translation and cell division processes in M. truncatula microsymbiont Sinorhizobium meliloti at low concentrations, and also exhibits antimicrobial activity at higher concentrations (A. Farkas et al., 2014). To date, NCR peptides are identified only in plants belonging to IRLC (Inverted Repeat-lacking Clade) legumes which are characterized by terminal differentiation of bacteria into bacteroids. Probably, evolutionary acquisition of the variable gene family encoding NCR peptides has been the selective advantage of this group of plants.

Keywords: rhizobium-legume symbiosis, nitrogen-fixing nodules, differentiation of bacteroides, NCR-peptides, regulation of symbiosis development.

 

Full article (Rus)

Full text (Eng)

 

REFERENCES

  1. Ferguson B.J., Indrasumunar A., Hayashi S., Lin M.H, Lin Y.H., Reid D.E., Gresshoff P.M. Molecular analysis of legume nodule development and autoregulation. Journal of Integrative Plant Biol., 2010, 52(1): 61-76 CrossRef
  2. Chen W.-M., Moulin L., Bontemps C., Vandamme P., Bena G., Boivin-Masson C. Legume symbiotic nitrogen fixation by β-proteobacteria is widespread in nature. J. Bacteriol., 2003, 185(24): 7266-7272 CrossRef
  3. MacLean A.M., Finan T.M., Sadowsky M.J. Genomes of the symbiotic nitrogen-fixing bacteria of legumes. J. Plant Physiol., 2007, 144(2): 615-622 CrossRef
  4. Oldroyd G.E., Downie J.A. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol., 2008, 59: 519-546 CrossRef
  5. Oldroyd G.E. Speak, friend, and enter: signaling systems that promote beneficial symbiotic associations in plant. Nat. Rev. Microbiol., 2013, 11(4): 252-263 CrossRef
  6. Mylona P., Pawlowski K., Bisseling T. Symbiotic nitrogen fixation. The Plant Cell, 1995, 7: 869-885.
  7. Mus F., Crook M.B., Garcia K., Garcia Costas A., Geddes B.A., Ko-
    uri E.D., Paramasivan P., Ryu M.-H., Oldroyd G.E.D., Poole P.S., Udvardi M.K., Voigt C.A., Ané J.-M., Peters J.W. Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl. Environ. Microbiol., 2016, 82(13): 3698-710 CrossRef
  8. Rolfe B.G., Gresshoff P.M. Genetic analysis of legume nodule initiation. Annu. Rev. Plant Physiol. Plant Mol. Biol., 1988, 39: 297-319 CrossRef
  9. Rhizobiaceae: Molekulyarnaya biologiya bakterii, vzaimodeistvuyushchikh s rasteniyami /Pod pedaktsiei G. Spaink; russkii perevod pod redaktsiei I.A. Tikhonovicha, N.A. Provorova [The Rhizobiaceae: molecular biology of model plant-associated bacteria. H.P. Spaink, A. Kondorosi, P. Hooykaas (eds.). Russian translation edited by I.A. Tikhonovich, N.A. Provorov]. St. Petersburg, 2002 (in Russ.).
  10. Mergaert P., Uchiumi T., Alunni B., Evanno G., Cheron A., Catrice O., Mausset A.E., Barloy-Hubler F., Galibert F., Kondorosi A., Kondorosi E. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium—legume symbiosis. PNAS USA, 2006, 103(13): 5230-5235 CrossRef
  11. Van de Velde W., Zehirov G., Szatmari A., Debreczeny M., Ishihara H., Kevei Z., Farkas A., Mikulass K., Nagy A., Tiricz H., Satiat-Jeunemaître B., Alunni B., Bourge M., Kucho K., Abe M., Kereszt A., Maroti G., Uchiumi T., Kondorosi E., Mergaert P. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science, 2010, 327(5969): 1122-1126 CrossRef
  12. Sen D., Weaver R.W. A basis for different rates of N2-fixation by the same strains of Rhizobium in peanut and cowpea root nodules. Plant Sci., 1984, 34(3): 239-246 CrossRef
  13. Bonaldi K., Gargani D., Prin Y., Fardoux J., Gully D., Nouwen N., Goormachtig S., Giraud E. Nodulation of Aeschynomene afraspera and A. indica by photosynthetic Bradyrhizobium sp. strain ORS285: the nod-dependent versus the nod-independent symbiotic interaction. Mol. Plant-Microbe Interact., 2011, 24(11): 1359-1371 CrossRef
  14. Mergaert P., Nikovics K., Kelemen Z., Munoury N., Vaubert D., Kondorosi A., Kondorosi E. 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., 2003, 132(1): 161-173 CrossRef
  15. Nallu S., Silverstein, K.A., Zhou P., Young N.D., VandenBosch K.A. Patterns of divergence of a large family of nodule cysteine-rich peptides in accessions of Medicago truncatula. The Plant Journal, 2014, 78(4): 697-705 CrossRef
  16. Maroti G., Downie J.A., Kondorosi E. Plant cysteine-rich peptides that inhibit pathogen growth and control rhizobial differentiation in legume nodules. Curr. Opin. Plant Biol., 2015, 26: 57-63 CrossRef
  17. Shabab M., Arnold M.F., Penterman J., Wommack A.J., Bocker H.T., Price P.A., Griffitts J.S., Nolan E.M., Walker G.C. Disulfide cross-linking influences symbiotic activities of nodule peptide NCR247. PNAS USA, 2016, 113(36): 10157-10162 CrossRef
  18. Fruhling M., Albus, U., Hohnjec N.,  Geise G., Pühler A.,  Perlick A.M. A small famiy of broad bean codes for late nodulins containing conserved cysteine clusters. Plant Sci., 2000, 152(1): 67-77 CrossRef
  19. Crockard A., Bjourson J., Dazzo B., Cooper J.E. A white clover nodulin gene, dd23b, encoding a cysteine cluster protein, is expressed in roots during the very early stages of interaction with Rhizobium leguminosarum biovar trifolii and after treatment with chitolipooligosaccharide Nod factors. J. Plant Res., 2002, 115(6): 439-447 CrossRef
  20. Kaijalainen S., Schroda M., Lindstrom K. Cloning of nodule-specific cDNAs of Galega orientalis. Plant Physiol., 2002, 114(4): 588-593 CrossRef
  21. Scheres B., van Engelen F., van der Knaap E., van de Wiel C., van Kammen A., Bisseling T. Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell, 1990, 2(8): 687-700 CrossRef
  22. Kardailsky I., Yang W-C., Zalensky A., van Kammen A., Bisseling T. The pea late nodulin gene PsNOD6 is homologous to the early nodulin genes PsENOD3/14 and is expressed after the leghaemoglobin genes. Plant Mol. Biol., 1993, 23(5): 1029-1037 CrossRef
  23. Kato T., Kawashima K., Miwa M., Mimura Y., Tamaoki M., Kouchi H., Suganuma N. Expression of genes encoding late nodulins characterized by a putative signal peptide and conserved cysteine residues is reduced in ineffective pea nodules. Mol. Plant-Microbe Interact., 2002, 15(2): 129-137 CrossRef
  24. Silverstein K.A., Graham M.A., Paape T.D., VandenBosch K.A. Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol., 2005, 138(2): 600-610 CrossRef
  25. Aerts A.M., Francois I.E., Cammue B.P., Thevissen K. The mode of antifungal action of plant, insect and human defensins. Cell. Mol. Life Sci., 2008, 65(13): 2069-2079 CrossRef
  26. Vaara M., Vaara T. Polycations as outer membrane-disorganizing agents. Antimicrobial Agents and Chemotherapy, 1983, 24(1): 114-122.
  27. Boman H.G. Peptide antibiotics and their role in innate immunity. Annu. Rev. Immunol., 1995, 13: 61-92 CrossRef
  28. Huang H.W. Molecular mechanism of antimicrobial peptides: The origin of cooperativity. BBA, 2006, 1758(9): 1292-1302 CrossRef
  29. Brogden K.A. Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol., 2005, 3(3): 238-250 CrossRef
  30. Sochacki K.A., Barns K.J., Bucki R., Weisshaar C. Real-time attack on single Escherichia coli cells by the human antimicrobial peptide LL-37. PNAS USA, 2011, 108(16): 77-81 CrossRef
  31. Teixeira V., Feio M.J., Bastos M. Role of lipids in the interaction of antimicrobial peptides with membranes. Prog. Lipid Res., 2012, 51(2): 149-177 CrossRef
  32. Van der Weerden N.L., Bleackley M.R., Anderson M.A. Properties and mechanisms of action of naturally occurring antifungal peptides. Cell. Mol. Life Sci., 2013, 70(19): 3545-3570 CrossRef
  33. Epand R.M., Vogel H.J. Diversity of antimicrobial peptides and their mode of action. Biochimica et Biophysica Acta Journal, 1999, 1462(1-2): 11-28.
  34. Graham M.A., Silverstein K.A., Cannon S.B., VandenBosch K.A. Computational identification and characterization of novel genes from legumes. Plant Physiol., 2004, 135(3): 1179-1197 CrossRef
  35. Silverstein K.A., Graham M.A., VandenBosch K.A. Novel paralogous gene families with potential function in legume nodules and seeds. Curr. Opin. Plant Biol., 2006, 9(2): 142-146 CrossRef
  36. Ganz T. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol., 2003, 3(9): 710-720 CrossRef
  37. Vriens K., Cammue B.P., Thevissen K. Antifungal plant defensins: mechanisms of action and production. Molecules, 2014, 19(8): 12280-12303 CrossRef
  38. Nagy K., Mikulass K.R., Vegh A.G., Kereszt A., Kondorosi E., Varo G., Szegletes Z. Interaction of cysteine-rich cationic antimicrobial peptides with intact bacteria and model membranes. Gen. Physiol. Biophys., 2015, 34(2): 135-144 CrossRef
  39. Nicolas P. Multifunctional host defense peptides: Intracellular-targeting antimicrobial peptides. FEBS Journal, 2009, 276(22): 6483-6496 CrossRef
  40. Guefrachi I., Nagymihaly M., Pislariu C.I., Van de Velde W., Ratet P., Mars M., Udvardi M.K., Kondorosi E., Mergaert P., Alunni B. Extreme specificity of NCR gene expression in Medicago truncatula. BMC Genomics, 2014, 15(1): 1-16 CrossRef
  41. Wang D., Griffitts J., Starker C., Fedorova E., Limpens E., Ivanov S., Bisseling T., Long S. A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science, 2010, 327(5969): 1126-1129 CrossRef
  42. Tiricz H., Szucs A., Farkas A., Pap B., Lima R.M., Maroti G., Kondo-
    rosi E., Kereszt A. Antimicrobial nodule-specific cysteine-rich peptides induce membrane depolarization-associated changes in the transcriptome of Sinorhizobium meliloti. Appl. Environ. Microbiol., 2013, 79(21): 6737-6746 CrossRef
  43. Durgo H., Klement E., Hunyadi-Gulyas E., Szucs A., Kereszt A., Medzihradszky K.F., Kondorosi E. Identification of nodule-specific cysteine-rich plant peptides in endosymbiotic bacteria. Proteomics, 2015, 15(13): 2291-2295 CrossRef
  44. Handler A.A., Lim J.E., Losick R. Peptide inhibitor of cytokinesis during sporulation in Bacillus subtilis. Mol. Microbiol., 2008, 68(3): 588-599 CrossRef
  45. Penterman J., Abo R.P., De Nisco N.J., Arnold M.F.F., Longhi R., Zan-
    da M., Walker G.C. Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis. PNAS USA, 2014, 111(9): 3561-3566 CrossRef
  46. Maroti G., Kondorosi E. Nitrogen-fixing Rhizobium-legume symbiosis: are polyploidy and host peptide-governed symbiont differentiation general principles of endosymbiosis? Front. Microbiol., 2014, 5: 1-6 CrossRef
  47. Farkas A., Maroti G., Durgo H., Gyorgypal Z., Lima R.M., Medzihradszky K.F., Kereszt A., Mergaert P., Kondorosi E. Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms. PNAS USA, 2014, 111(14): 5183-5188 CrossRef
  48. Haag A.F., Baloban M., Sani M., Kerscher B., Pierre O., Farkas A., Longhi R., Boncompagni E., Hérouart D., Dall’Angelo S., Kondo-
    rosi E., Zanda M., Mergaert P., Ferguson G.P. Protection of Sinorhizobium against host cysteine-rich antimicrobial peptides is critical for symbiosis. PLoS Biology, 2011, 9(10): e1001169 CrossRef
  49. Glazebrook J., Ichige A., Walker G.C. A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes and Development, 1993, 7(8): 1485-1497.
  50. Ichige A., Walker G.C. Genetic analysis of the Rhizobium meliloti bacA gene: functional interchangeability with the Escherichia coli sbmA gene and phenotypes of mutants. J. Bacteriol., 1997, 179(1): 209-216.
  51. Ferguson G.P., Jansen A., Marlow V.L., Walker G.C. BacA-mediated bleomycin sensitivity in Sinorhizobium meliloti is independent of the unusual lipid A modification. J. Bacteriol., 2006, 188(8): 3143-3148 CrossRef
  52. Marlow V.L., Haag A.F., Kobayashi H., Fletcher V., Scocchi M., Wal-
    ker G.C., Ferguson G.P. Essential role for the BacA protein in the uptake of a truncated eukaryotic peptide in Sinorhizobium meliloti. J. Bacteriol., 2009, 191(5): 1519-1527 CrossRef
  53. Karunakaran R., Haag A.F., East A.K., Ramachandran V.K., Prell J., James E.K., Scocchi M., Ferguson G.P., Poole P.S. BacA is essential for bacteroid development in nodules of galegoid, but not phaseoloid, legumes. J. Bacteriol., 2010, 192(11): 2920-2928 CrossRef
  54. Wehmeier S., Arnold M.F, Marlow V.L., Aouida M., Myka K.K., Fletcher V., Benincasa M., Scocchi M., Ramotar D., Ferguson G.P. Internalization of a thiazole-modified peptide in Sinorhizobium meliloti occurs by BacA-dependent and -independent mechanisms. Microbiology, 2010, 156: 2702-2713 CrossRef
  55. Crook M.B., Lindsay D.P., Biggs M.B., Bentley J.S., Price J.C., Cle-
    ment S.C., Clement M.J., Long S.R., Griffitts J.S. Rhizobial plasmids that cause impaired symbiotic nitrogen fixation and enhanced host invasion. Mol. Plant-Microbe Interact., 2012, 25(8): 1026-1033 CrossRef
  56. Price P.A., Tanner H.R., Dillon B.A., Shabab M., Walker G.C., Griffitts J.S. Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility. PNAS USA, 2015, 112(49): 15244-15249 CrossRef
  57. Silipo A., Vitiello G., Gully D., Sturiale L., Chaintreuil C., Fardoux J., Gargani D., Lee H.-I., Kulkarni G., Busset N., Marchetti R., Palmigiano A., Moll H., Engel R., Lanzetta R., Paduano L., Parrilli M., Chang W.-S., Holst O., Newman D.K., Garozzo D., D’Errico G., Giraud E., Molinaro A. Covalently linked hopanoid-lipid A improves outer-membrane resistance of a Bradyrhizobium symbiont of legumes. Nat. Commun., 2014, 5: 5106 CrossRef
  58. Kulkarni G., Busset N., Molinaro A., Gargani D., Chaintreuil C., Silipo A., Giraud E., Newman D.K. Specific hopanoid classes differentially affect free-living and symbiotic states of Bradyrhizobium diazoefficiens. MBio Jounal, 2015, 6(5): e01251-15 CrossRef
  59. Alunni B., Kevei Z., Redondo-Nieto M., Kondorosi A., Mergaert P., Kondorosi E. Genomic organization and evolutionary insights on GRP and NCR genes, two large nodule-specific gene families in Medicago truncatula. Mol. Plant-Microbe Interact., 2007, 20(9): 1138-1148 CrossRef
  60. Kim M., Chen Y., Xi J., Waters C., Chen R., Wang D. An antimicrobial peptide essential for bacterial survival in the nitrogen-fixing symbiosis. PNAS USA, 2015, 112(49): 15238-15243 CrossRef
  61. Horváth B., Domonkos Á., Kereszt A., Szucs A., Ábrahám E., Ayaydin F., Bóka K., Chen Y., Chen R., Murray J.D., Udvardi M.K., Kondorosi É., Kaló P. Loss of the nodule-specific cysteine rich peptide, NCR169, abolishes symbiotic nitrogen fixation in the Medicago truncatula dnf7 mutant. PNAS USA, 2015, 112(49): 15232-15237 CrossRef
  62. Lang C., Long S.R. Transcriptomic analysis of Sinorhizobium meliloti and Medicago truncatula symbiosis using nitrogen fixation-deficient nodules. Molecular Plant-Microbe Interactions, 2015, 28(8): 856-868 CrossRef
  63. Alunni B., Gourion B. Terminal bacteroid differentiation in the legume-rhizobium symbiosis: nodule-specific cysteine-rich peptides and beyond. New Phytologist, 2016, 211(2): 411-417 CrossRef
  64. Klyukova M.S. Kharakteristika semeistva genov, kodiruyushchikh NCR-peptidy, u gorokha posevnogo (Pisum sativum L.). Magisterskaya dissertatsia [Characterization of gene family encoding NCR peptides in pea (Pisum sativum L.). Magister Thesis]. St. Petersburg, 2016 (in Russ.).
  65. Oono R., Denison R.F. Comparing symbiotic efficiency between swollen versus nonswollen rhizobial bacteroids. Plant Physiol., 2010, 154(3): 1541-1548 CrossRef

 

back