doi: 10.15389/agrobiology.2016.5.585eng

UDC 633.31/.37:631.461.52:57.052

Supported by the grant of the President of the Russian Federation (project HIII-6759.2016.4), the Russian Foundation for Basic Research (project № 14-04-01084-а) and Russian Science Foundation (project № 14-24-00135)



E.A. Dolgikh, A.N. Kirienko, I.V. Leppyanen, A.V. Dolgikh

All-Russian Research Institute for Agricultural Microbiology, Federal Agency of Scientific Organizations, 3, sh. Podbel’skogo, St. Petersburg, 196608 Russia,

Received January 25, 2016


This review refers to analysis of the modern data about the role of auxins in the regulation of nitrogen-fixing nodule development in the legume plants. The interaction of these hormones with cytokinins and components of signaling cascade activated by Nod factors during nodule organogenesis in legume plants with different types of nodules are discussed. Emphasis is being given to the participation of auxins in the control of initiation and early stages of nodule development. In early works the analysis of transgenic plants containing the fusions between promoters regulated by auxins and reporter genes, showed the accumulation of auxins in the places of nodule primordia development. It indicates a direct effect of these plant hormones on the process (U. Mathesius et al., 1998; C. Pacios-Bras et al., 2003). These studies became the basis for the suggestion that the auxin maximus in the cells giving later nodule primordia precedes these organs appearance. The creation of such peaks is dependent on Nod factors and cytokine response activation in plants, but it is differently regulated in legumes with determined (regulation of auxin biosynthesis) and non-determinated (control of auxin transport with flavonoids) type of nodules (A.P. Wasson et al., 2006; J. Plet et al., 2011; T. Suzaki et al., 2012). The effect of cytokinins on the auxin transport (auxin transporters PINs) during the formation of nodules has much in common with the participation of cytokinins in the control of lateral root development program, which may indicate an evolutionary relationship of two morphogenetic programs. In legume nodules and lateral roots development programs the initial stages have much in common, since both structures are formed as a result of the reactivation of differentiated root cells and have the features of structural similarity. However further divergence leads to the formation of structurally and functionally distinct organs that can be associated with unequal role that cytokinins and auxins play in controlling these processes. The review also examined the role of the balance of auxin and cytokinin hormones in determining the program of development of root cells. We discuss the experimental data using exogenous hormones, which showed that the founder-cells, giving rise to lateral roots, characterized by high plasticity of development processes, determined by the balance of auxins and cytokinins (L. Laplaze et al., 2007; Chatfield et al., 2013). However, an analysis of the data leads to the conclusion that the role of auxin in the control later stages nodulation in legumes is little investigated.

Keywords: legume-rhizobial symbiosis, auxins, phytohormonal balance, nodule organogenesis.


Full article (Rus)

Full text (Eng)



  1. Spaink H., Sheeley D.M., van Brussel A.A.N., Glushka J., York W.S., Tak T., Geiger O., Kennedy E., Reinhold N., Lugtenberg B.J.J. A novel highly unsaturated fatty acid moiety of lipooligosaccharide signals determines host specificity of Rhizobium. Nature, 1991, 354: 125-130 CrossRef
  2. Gonzalez-Rizzo S., Crespi M., Frugier F. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell, 2006, 18: 2680-2693 CrossRef
  3. Tirichine L., Sandal N., Madsen L.H., Radutoiu S., Albrektsen A.S., Sato S., Asamizu E., Tabata S., Stougaard J. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science, 2007, 315: 104-107 CrossRef
  4. Rightmyer A.P., Long S.R. Pseudonodule formation by wild-type and symbiotic mutant Medicago truncatula in response to auxin transport inhibitors. Mol. Plant Microbe Interact., 2011, 24: 1372-1384 CrossRef
  5. Plet J., Wasson A., Ariel F., Le Signor C., Baker D., Mathesius U., Crespi M., Frugier F. MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J., 2011, 65: 622-633 CrossRef
  6. Held M., Hou H., Miri M., Huynh C., Ross L., Hossain M.S., Sato S., Tabata S., Perry J., Wang T.L., Szczyglowski K. Lotus japonicus cytokinin receptors work partially redundantly to mediate nodule formation. Plant Cell, 2014, 26: 678-694 CrossRef
  7. Ferguson B.J., Mathesius U. Phytohormone regulation of legume-rhizobia interactions. J. Chem. Ecol., 2014, 201(40): 770-790 CrossRef
  8. van Zeijl1 A., Op den Camp R.H.M., Deinum E.E., Charnikhova T., Franssen H., Op den Camp H.J.M., Bouwmeester H., Kohlen W., Bisseling T., Geurts R. Rhizobium lipo-chitooligosaccharide signaling triggers accumulation of cytokinins in Medicago truncatula roots. Molecular Plant, 2015, 8(8): 1213-1226 CrossRef
  9. Kisiala A., Laffont C., Emery J.R.N., Frugier F. Bioactive cytokinins are selectively secreted by Sinorhizobium meliloti nodulating and nonodulating strains. Mol. Plant-Microbe Interact., 2013, 26: 1225-1231 CrossRef
  10. Frugier F., Kosuta S., Murray J.D., Crespi M., Szczyglowski K. Cytokinin: secret agent of symbiosis. Trends Plant Sci., 2008, 13: 115-120 CrossRef
  11. 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., 2011, 45: 119-144 CrossRef
  12. Libbenga K.R., Harkes P.A. Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum L. Planta, 1973, 114: 17-28 CrossRef
  13. Mathesius U. Auxin: at the root of nodule development? Funct. Plant Biol., 2008, 35: 651-668 CrossRef
  14. Allen E.K., Allen O.N., Newman A.S. Pseudonodulation of leguminous plants induced by 2-bromo-3,5-dichlorobenzoic acid. Am. J. Bot., 1953, 40: 429-435 CrossRef
  15. Hirsch A.M., Bhuvaneswari J.G., Torrey J.G., Bisseling T. Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. PNAS USA, 1989, 86: 1244-1248 CrossRef
  16. Long S.R. The Rhizobium-legume symbiosis: life together in the underground. Cell, 1989, 56: 203-214 CrossRef
  17. Mathesius U., Schlaman H.R., Spaink H.P., Sautter C., Rolfe B.G., Djordjevic M.A. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J., 1998, 14: 23-34 CrossRef
  18. Huo X.Y., Schnabel E., Hughes K., Frugoli J. RNAi phenotypes and the localization of a protein:GUS fusion imply a role for Medicago truncatula PIN genes in nodulation. Journal of Plant Growth Regulation, 2006, 25: 156-165 CrossRef
  19. Takanashi K., Sugiyama A., Yazaki K. Involvement of auxin distribution in root nodule development of Lotus japonicus. Planta, 2011, 234: 73-81 CrossRef
  20. Boot K.J.M., van Brussel A.A.N., Tak T., Spaink H.P., Kijne J.W. Lipochitin oligosaccharides from Rhizobium leguminosarum bv. viciae reduce auxin transport capacity in Vicia sativa subsp. nigra roots. Mol. Plant Microbe Interact., 1999, 12: 839-844 CrossRef
  21. van Noorden G.E., Kerim T., Goffard N., Wiblin R., Pellerone F.I., Rolfe B.G., Mathesius U. Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiol., 2007, 144: 1115-1131 CrossRef
  22. Wasson A.P., Pellerone F.I., Mathesius U. Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell, 2006, 18: 1617-1629 CrossRef
  23. Xiao T.T., Schilderink S., Moling S., Deinum E.E., Kondorosi E., Franssen H., Kulikova O., Niebel A., Bisseling T. Fate map of Medicago truncatula root nodules. Development, 2014, 141: 3517-3528 CrossRef
  24. Ng J.L.P., Hassan S., Truong T.T., Hocart C.H., Laffont C., Frugier F., Mathesius U. Flavonoids and auxin transport inhibitors rescue symbiotic nodulation in the Medicago truncatula cytokinin perception mutant cre1. The Plant Cell Preview, 2015, 27(8): 2210-2226 CrossRef
  25. Peer W.A., Bandyopadhyay A., Blakeslee J.J., Makam S.N., Chen R.J., Masson P.H., Murphy A.S. Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell, 2004, 16: 1898-1911 CrossRef
  26. Santelia D., Henrichs S., Vincenzetti V., Sauer M., Bigler L., Klein M., Bailly A., Lee Y., Friml J., Geisler M., Martinoia E. Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses. J. Biol. Chem., 2008, 283: 31218-31226 CrossRef
  27. Pacios-Bras C., Schlaman H.R., Boot K., Admiraal P., Langerak J.M., Stougaard J., Spaink H.P. Auxin distribution in Lotus japonicus during root nodule development. Plant Mol. Biol., 2003, 52: 1169-1180 CrossRef
  28. Subramanian S., Stacey G., Yu O. Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. The Plant Journal, 2006, 48: 261-273 CrossRef
  29. Suzaki T., Yano K., Ito M., Umehara Y., Suganuma N., Kawaguchi M. Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development, 2012, 139: 3997-4006 CrossRef
  30. Suzaki T., Ito M., Kawaguchi M. Genetic basis of cytokinin and auxin functions during root nodule development. Front. Plant Sci., 2013, 4: 42 CrossRef
  31. Benková E., Michniewicz M., Sauer M., Teichmann T., Seifertová D., Jürgens G., Friml J. Local, efflux dependent auxin gradients as a common module for plant organ formation. Cell, 2003, 115: 591-602 CrossRef
  32. Petrásek J., Friml J. Auxin transport routes in plant development. Development, 2009, 136: 2675-2688 CrossRef
  33. Pernisová M., Klíma P., Horák J., Válková M., Malbeck J., Soucek P., Reichman P., Hoyerová K., Dubová J., Friml J., Zazímalová E., He-
    játko J. Cytokinins modulate auxin induced organogenesis in plants via regulation of the auxin efflux. PNAS USA, 2009, 106: 3609-3614 CrossRef
  34. Ruzicka K., Simásková M., Duclercq J., Petrásek J., Zazímalová E., Simon S., Friml J., Van Montagu M.C.E., Benková E. Cytokinin regulates root meristem activity via modulation of the polar auxin transport. PNAS USA, 2009, 106: 4284-4289 CrossRef
  35. Marhavý P., Bielach A., Abas L., Abuzeineh A., Duclercq J., Tanaka H., Parezová M., Petrášek J., Friml J., Kleine-Vehn J., Benková E. Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev. Cell, 2011, 21: 796-804 CrossRef
  36. Marhavý P., Duclercq J., Weller B., Feraru E., Bielach A., Offringa R., Friml J., Schwechheimer C., Murphy A., Benková E. Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Curr. Biol., 2014, 24: 1031-1037 CrossRef
  37. Laplaze L., Benkova E., Casimiro I., Maes L., Vanneste S., Swarup R., Weijers D., Calvo V., Parizot B., Herrera-Rodriguez M.B., Offringa R., Graham N., Doumas P., Friml J., Bogusz D., Beeckman T., Bennett M. Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell, 2007, 19(12): 3889-3900 CrossRef
  38. Dello Ioio R., Linhares F.S., Scacchi E., Casamitjana-Martinez E., Heidstra R., Costantino P., Sabatini S. Cytokinins determine Arabidopsis root meristem size by controlling cell differentiation. Curr. Biol., 2007, 17: 678-682 CrossRef
  39. Moubayidin L., Perilli S., Dello Ioio R., Di Mambro R., Costanti-
    no P., Sabatini S. The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr. Biol., 2010, 20: 1138-1143 CrossRef
  40. De Smet I., Tetsumura T., De Rybel B., Frei dit Frey N., Laplaze L., Casimiro I., Swarup R., Naudts M., Vanneste S., Audenaert D., Inzé D., Bennett M.J., Beeckman T. Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development, 2007, 134: 681-690 CrossRef
  41. Overvoorde P., Fukaki H., Beeckman T. Auxin control of root development. Cold Spring Harbor Perspectives in Biology, 2010, 2: a001537 CrossRef
  42. Chatfield S.P., Capron R., Severino A., Penttila P.-A., Alfred S., Nah-
    al H., Provart N.J. Incipient stem cell niche conversion in tissue culture: using a systems approach to probe early events in WUSCHEL dependent conversion of lateral root primordia into shoot meristems. The Plant Journal, 2013, 73: 798-813 CrossRef
  43. Casimiro I., Marchant A., Bhalerao R.P., Beeckman T., Dhooge S., Swarup R., Graham N., Inzé D., Sandberg G., Casero P.J., Bennett M.J. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell, 2001, 13: 843-852 CrossRef
  44. Dubrovsky J.G., Colón-Carmona A., Rost T.L., Doerner P.W. Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta, 2001, 214: 30-36 CrossRef
  45. Péret B., de Rybel B., Casimiro I., Benkova I., Swarup R., Laplaze L., Beeckman T., Bennett M.J. Arabidopsis lateral root development: an emerging story. Trends Plant Sci., 2009, 14: 399-408 CrossRef
  46. Benková E., Bielach A. Lateral root organogenesis — from cell to organ. Curr. Opin. Plant Biol., 2010, 13: 677-683 CrossRef
  47. Op den Camp R.H., De Mita S., Lillo A., Cao Q., Limpens E., Bisseling T., Geurts R. A phylogenetic strategy based on a legume-specific whole genome duplication yields symbiotic cytokinin type-A response regulators. Plant Physiol., 2011, 157: 2013-2022 CrossRef
  48. Soyano T., Hayashi M. Transcriptional networks leading to symbiotic nodule organogenesis. Curr. Opin. Plant Biol., 2014, 20: 146-154 CrossRef
  49. Oláh B., Brière C., Bécard G., Dénarié J., Gough C. Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J., 2005, 44: 195-207 CrossRef
  50. Maillet F., Poinsot V., André O., Puech-Pagès V., Haouy A., Gueuni-
    er M., Cromer L., Giraudet D., Formey D., Niebel A., Martinez E.A., Driguez H., Bécard G., Dénarié J. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature, 2011, 469: 58-63 CrossRef
  51. Penmetsa R.V., Cook D.R. A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science, 1997, 275: 527-530 CrossRef
  52. Penmetsa R.V., Uribe P., Anderson J., Lichtenzveig J., Gish J.C., Nam Y.W., Engstrom E., Xu K., Sckisel G., Pereira M., Baek J.M., Lopez-Meyer M., Long S.R., Harrison M.J., Singh K.B., Kiss G.B., Cook D.R. The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. Plant J., 2008, 55: 580-595 CrossRef
  53. Larrainzar E., Riely B.K., Kim S.C., Carrasquilla-Garcia N., Yu H.-Y., Hwang H.-J., Oh M., Kim G.B., Surendrarao A.K., Chasman D., Siahpirani A.F., Penmetsa R., Lee G.-S., Kim N., Roy S., Jeong-Hwan Mun L.-H., Cook D.R. Deep sequencing of the Medicago truncatula root transcriptome reveals a massive and early interaction between nodulation factor and ethylene signals. Plant Physiol., 2015, 169: 233-265 CrossRef