doi: 10.15389/agrobiology.2016.3.285eng

UDC 633.31/.37:631.461.52:57.052

Acknowledgements:
Supported by the Russian Scientific Foundation (project № 14-24-00135)

 

ROLE OF PHYTOHORMONES IN THE CONTROL OF SYMBIOTIC NODULE DEVELOPMENT IN LEGUME PLANTS. I. CYTOKININS (review)

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, Б
e-mail dol2helen@yahoo.com

Received March 18, 2016

 

The influence of cytokinins on nitrogen-fixing nodule development in legume plants, as well as the molecular mechanisms of this effect and interaction with components of signaling cascade activated by nodulation inductors, the bacterial signals Nod factors, are discussed in the review. Positive role of cytokinins was first shown in the experiments with their exogenous application to plants that resulted in spontaneous nodule formation on the roots of legume plants (K.R. Libbenga, P.A.A. Harkers, 1973). The experiments with bacterial strains defective in Nod factor biosynthesis, but producing the trans-zeatin, confirmed the assumption that cytokinins are involved in the control of nodule formation (J.B. Cooper, S.R. Long, 1994). As a result the nodule-like structures are developed expressing the symbiosis-specific early nodulin genes. At the present stage of research the identification of legume mutants defective in the genes encoding receptors to cytokinins allowed to provide evidence for the involvement of cytokinins in nodulation. The inhibition of nodule development was found in Medicago truncatula mutants defective in the cytokinin receptor gene CRE1 (cytokinin response1) and LHK1 (Lotus histidine kinase1) in Lotus japonicus (S. Gonzalez-Rizzo et al., 2006; J.D. Murray et al., 2007). Thus inhibition of plant susceptibility to cytokinins affected both the infection thread development and nodule formation. In contrast, the strengthening of the LHK1 and CRE1 gene function in L. japonicus and M. truncatula using a recombination approach, resulted in nodule-like structure formation in the absence of rhizobia (L. Tirichine et al., 2007; E. Ovchinnikova et al., 2011). The pathways of cytokinin biosynthesis and activation have been considered, as well as their perception and signal transduction. Cytokinin accumulation may be connected with the gene expression induction, that control the biosynthesis/activation of these hormones, but the molecular mechanisms of this activation remains to be seen. Analysis showed that cytokinins are involved in signal transduction from Nod factor after the stage controlled by one of the key regulators of the signaling pathway, the calcium calmodulin-dependent kinase. This suggests that activation of the receptor to cytokinins is dependent on Nod factors. The expression of the genes encoding transcription factors NSP2, ERN1 and NIN was significantly reduced in the mutants cre1 and lhk1, that allowed to conclude the activation of the receptor to cytokinins precedes the involvement of these transcription factors in signal transduction (L. Tirichine et al., 2007; J. Plet et al., 2011). The analysis has shown that cytokinins are involved in the control of early stages of organogenesis and infection development, but they are also important for nodule differentiation. In addition to local control of nodulation, cytokinins take participation in system control, i.e. in the autoregulation of nodulation. Therefore the cytokinins may play various roles in nodule development depending on their spatial and temporal activation.

Кeywords: legume-rhizobial symbiosis, cytokinins, Nod factors, nodules organogenesis, rhizobial infection.

 

Full article (Rus)

Full text (Eng)

 

REFERENCES

  1. Schultze M., Kondorosi A. Regulation of symbiotic root nodule development. Annu. Rev. Genet., 1998, 32: 33-57 CrossRef
  2. Phillips D.A., Torrey J.G. Studies on cytokinin production by Rhizobium. Plant Physiol., 1972, 49: 11-15 CrossRef
  3. Sturtevant D.B., Taller B.J. Cytokinin production by Bradyrhizobium japonicum. Plant Physiol., 1989, 89: 1247-1252 CrossRef
  4. Thimann K.V. On the physiology of the formation of nodules on legume roots. PNAS USA, 1936, 22: 511-514 CrossRef
  5. Morris R.O. Genes specifying auxin and cytokinin biosynthesis in prokaryotes. In: Plant hormones. P.J. Davies (ed.). KAP, Dordrecht, 1995, E20: 318-339 CrossRef
  6. Sachs T., Thimann K. The role of auxins and cytokinins in the release of buds from dominance. Am. J. Bot., 1967, 54(1): 136-144 CrossRef
  7. Tanaka M., Takei K., Kojima M., Sakakibara H., Mori H. Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. The Plant Journal, 2006, 45(6): 1028-1036 CrossRef
  8. Werner T., Motyka V., Strnad M., Schmülling T. Regulation of plant growth by cytokinin. PNAS USA, 2008, 98(18): 10487-10492 CrossRef
  9. Werner T., Köllmer I., Bartrina I., Holst K., Schmülling T. New insights into the biology of cytokinin degradation. Plant Biology, 2006, 8(3): 371-381 CrossRef
  10. Sakakibara H. Cytokinins: activity, biosynthesis, and translocation. Annu. Rev. Plant Biol., 2006, 57: 431-449 CrossRef
  11. Syono K., Newcomb W., Torrey J.G. Cytokinin production in relation to the development of pea root nodules. Can. J. Bot., 1976, 54: 2155-2162 CrossRef
  12. Newman J.D., Diebold R.J., Schultz B.W., Noel K.D. Infection of soybean and pea nodules by Rhizobium spp. purine auxotrophs in the presence of 5-aminoimidazole-4-carboxamide riboside. J. Bacteriol., 1994, 176: 3286-3294 (PMCID: PMC205499).
  13. 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
  14. Truchet G., Roche P., Lerouge P., Vasse J., Camut S., Debilly F., Prome J.C., Denarie J. Sulphatedlipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature, 1991, 351: 670-673 CrossRef
  15. Stokkermans T.J.W., Peters N.K. Bradyrhizobium elkanii lipo-oligosaccharide signals induce complete nodule structures on Glycine soja Siebold et. Zucc. Planta, 1994, 193: 413-420 CrossRef
  16. Cárdenas L., Domínguez J., Quinto C., López-Lara I.M., Lugtenberg B.J., Spaink H.P., Rademaker G.J., Haverkamp J., Thomas-Oates J.E. Isolation, chemical structures and biological activity of the lipo-chitin oligosaccharide nodulation signals from Rhizobium etli. Plant Mol. Biol., 1995, 29(3): 453-464 CrossRef
  17. Ritsema T., Lugtenberg B.J., Spaink H.P. Acyl-acyl carrier protein is a donor of fatty acids in the NodA-dependent step in biosynthesis of lipochitin oligosaccharides by rhizobia. J. Bacteriol., 1997, 179(12): 4053-4055 (PMCID: PMC179219).
  18. Corvera A., Promé D., Promé J.-C., Martínez-Romero E., Romero D. The nolL gene from Rhizobium etli determines nodulation efficiency by mediating the acetylation of the fucosyl residue in the Nodulation factor. Mol. Plant-Microbe Interact., 1999, 12(3): 236-246 CrossRef
  19. Perret X., Staehelin C., Broughton W.J. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Res., 2000, 64(1): 180-201 CrossRef
  20. Denarie J., Debelle F., Prome J.C. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem., 1996, 65: 503-535 CrossRef
  21. Long S.R. Rhizobium symbiosis: Nod factors in perspective. Plant Cell, 1996, 8: 1885-1898 CrossRef
  22. Madsen E.B., Madsen L.H., Radutoiu S., Olbryt M., Rakwalska M., Szcyglowski K., Sato S., Kaneko T., Tabata S., Sandal N., Stougaard J. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature, 2003, 425: 637-640 CrossRef
  23. Radutoiu S., Madsen L.H., Madsen E.B., Felle H.H., Umehara Y., Gronlund M., Sato S., Nakamura Y., Tabata S., Sandal N., Stougaard J. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature, 2003, 425: 569-570 CrossRef
  24. Ben Amor B., Shaw S.L., Oldroyd G.E.D., Maillet F., Penmetsa R., Cook D., Long S.R., Denarie J., Gough C. The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J., 2003, 34: 1-12 CrossRef
  25. Arrighi J.-F., Barre A., ben Amor B., Bersoult A., Soriano L.C., Mirabells R., de Carvalho-Niebel F., Journet E.-P., Gherardi M., Huguet T., Geurts R., Denarie J., Rouge P., Gough C. The Medicago trancatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol., 2006, 142: 265-279 CrossRef
  26. Smit P., Limpens E., Geurts R., Fedorova E., Dolgikh E., Gough C., Bisseling T. Medicago LYK3 an entry receptor in rhizobial Nod factor signaling. Plant Physiol., 2007, 145(1): 183-191 CrossRef
  27. Oldroyd G.E.D., Downie J.A. Coordinating nodule morphogenesis with Rhizobial infection in legumes. Annu. Rev. Plant Biol., 2008, 59: 519-546 CrossRef
  28. Ehrhardt D.W., Atkinson E.M., Long S.R. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science, 1992, 256(5059): 998-1000 CrossRef
  29. Ehrhardt D.W., Wais R., Long S.R. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell, 1996, 85(5): 673-681 CrossRef
  30. Harris J.M., Wais R., Long S.R. Rhizobium-induced calcium spiking in Lotus japonicus. Mol. Plant-Microbe Interact., 2003, 16: 335-341 CrossRef
  31. Felle H.H., Kondorosi E., Kondorosi A., Schultze M. Nod factors modulate the concentration of cytosolic free calcium differently in growing and non-growing root hairs of Medicago sativa L. Planta, 1999, 209: 207-212 CrossRef
  32. Engstrom E.M., Ehrhardt D.W., Mitra R.M., Long S.R. Pharmacological analysis of Nod factor-induced calcium spiking in Medicago truncatula: evidence for the requirement of type IIA calcium pumps and phosphoinositide signaling. Plant Physiol., 2002, 128: 1390-1401 CrossRef
  33. Charron D., Pingret J.L., Chabaud M., Journet E.P., Barker D.G. Pharmacological evidence that multiple phospholipid signaling pathways link Rhizobium nodulation factor perception in Medicago truncatula root hairs to intracellular responses, including Ca2+ spiking and specific ENOD gene expression. Plant Physiol., 2004, 136: 3582-3593 CrossRef
  34. Van Brussel A.A.N., Bakhuizen R., Van Spronsen P.C., Spaink H.P., Tak T., Lugtenberg B.J.J., Kijne J.W. Induction of preinfection thread structures in the leguminous host plant by mitogeniclipooligosaccharides of Rhizobium. Science, 1992, 257: 70-72 CrossRef
  35. de Ruijter N.C.A., Bisseling T., Emons A.M.C. Rhizobium Nod factors induce an increase in sub-apical fine bundles of actin filaments in Vicia sativa root hairs within minutes. Mol. Plant Microbe Interact., 1999, 12: 829-832 CrossRef
  36. Timmers A.C.J., Auriac M.-C., Truche G. Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development, 1999, 126: 3617-3628 (PMID: 10409507).
  37. Lerouge P., Roche P., Faucher C., Maillet F., Truchet G., Prome J.C., Denarie J. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature, 1990, 19: 781-784 CrossRef
  38. Horvath B., Heidstra R., Lados M., Moerman M., Spaink H.P., Prome J.-C., Van Kammen A., Bisseling T. Lipo-oligosaccharides of Rhizobium induce infection related early nodulin gene expression in pea root hairs. Plant J., 1993, 4: 727-733 CrossRef
  39. Bauer P., Ratet P., Crespi M., Schultze M., Kondorosi A. Nod factors and cytokinins induce similar cortical cell division, amyloplast deposition and MsEnod12A expression patterns in alfalfa roots. Plant J., 1996, 10: 91-105 CrossRef
  40. Downie J.A., Walker S.A. Plant responses to nodulation factors. Curr. Opin. Plant Biol., 1999, 2: 483-489 CrossRef
  41. Marsh J.F., Rakocevic A., Mitra R.M., Brocard L., Sun J., Eschstruth A., Long S.R., Schultze M., Pascal Ratet P., Oldroyd G.E.D. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmo-dulin-dependent protein kinase. Plant Physiol., 2007, 144: 324-335 CrossRef
  42. Schauser L., Wieloch W., Stougaard J. A plant regulator controlling development of symbiotic root nodules. Nature, 1999, 402: 191-195 CrossRef
  43. de Billy F., Grosjean C., May S., Bennett M., Cullimore J. Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol. Plant-Microbe Interact., 2001, 14(3): 267-277 CrossRef
  44. Pate J.S., Gunning B.E.S., Briarty L.G. Ultrastructure and functioning of the transport system of the leguminous root nodule. Planta, 1969, 85: 11-34 CrossRef
  45. 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
  46. Sprent J.I., Embrapa J.I. Root nodule anatomy, type of export product and evolutionary origin in some Leguminosae. Plant Cell Environ., 1979, 3: 35-43 CrossRef
  47. Crespi M., Frugier F. De novo organ formation from a differentiated cells: root nodule organogenesis. Sci. Signal., 2008, 1(49): re11 CrossRef
  48. Endre G., Kereszt A., Kevei Z., Mihacea S., Kalo P., Kiss G.B. A receptor kinase gene regulating symbiotic nodule development. Nature, 2002, 417: 962-966 CrossRef
  49. Ane J.-M., Kiss G.B., Riely B.K., Penmetsa R., Oldroyd G.E.D., Ayax C., Levy J., Debelle F., Baek J.-M., Kalo P., Rosenberg C., Roe B.A., Long S.R., Denarie J., Cook D.R.. Medicago trancatula DMI1 required for bacterial and fungal symbioses in legumes. Science, 2004, 303: 1364-1367 CrossRef
  50. Oldroyd G.E., Downie J.A. Nuclear calcium changes at the core of symbiosis signalling. Curr. Opin. Plant Biol., 2006, 9: 351-357 CrossRef
  51. Smit P., Raedts J., Portyanko V., Debelle F., Gough C., Bisseling T., Geurts R. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science, 2005, 308: 1789-1790 CrossRef
  52. Yano K., Tansengco M.L., Hio T., Higashi K., Murooka Y., Imaizumi-Anraku H., Kawaguchi M., Hayashi M. New nodulation mutants responsible for infection thread development in Lotus japonicus. Mol. Plant-Microbe Interact., 2006, 19(7): 801-810 CrossRef
  53. Andriankaja A., Boisson-Dernie A., Frances L., Sauviac L., Jauneau A., Barker D.G., de Carvalho-Niebel F. AP2-ERF transcription factors mediate Nod factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell, 2007, 19: 2866-2885 CrossRef
  54. Middleton P.H., Jakab J., Penmetsa R.V., Starker C.G., Doll J., Kaló P., Prabhu R., Marsh J.F., Mitra R.M., Kereszt A., Dudas B., Van den Bosch K., Long S.R., Cook D.R., Kiss G.B., Oldroyd G.E. An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell, 2007, 19: 1221-1234 CrossRef
  55. Libbenga K.R., Harkes P.A.A. Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum L. Planta, 1973, 114: 17-28 CrossRef
  56. Fang Y., Hirsch A.M. Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in transgenic alfalfa. Plant Physiol., 1998, 116: 53-68 CrossRef
  57. Cooper J.B., Long S.R. Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell, 1994, 6: 215-225 CrossRef
  58. Mathesius U., Charon C., Rolfe B.G., Kondorosi A., Crespi M. Temporal and spatial order of events during the induction of cortical cell divisions in white clover by Rhizobium leguminosarum bv trifolii inoculation or localized cytokinin addition. Mol. Plant-Microbe Interact., 2000, 13: 617-628 CrossRef
  59. Lorteau M.-A., Ferguson B.J., Guinel F.C. Effects of cytokinin on ethylene production and nodulation in pea (Pisum sativum) cv. Sparkle. Physiologia Plantarum, 2001, 112: 421-428 CrossRef
  60. Heckmann A.B., Sandal N., Bek A.S., Madsen L.H., Jurkiewicz A., Nielsen M.W., Tirichine L., Stougaard J. Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol. Plant-Microbe Interact., 2011, 24(11): 1385-1395 CrossRef
  61. van Rhijn P., Fang Y., Galili S., Shaul O., Atzmon N., Wininger S., Eshed Y., Lum M., Li Y., To V., Fujishig N., Kapulnik Y., Hirsch A.M. Expression of early nodulin genes in alfalfa mycorrhizae indicates that signal transduction pathways used in forming arbuscular mycorrhizae and Rhizobium-induced nodules may be conserved. PNAS USA, 1997, 94: 5467-5472 CrossRef
  62. Lohar D.P., Schaff J.E., Laskey J.G., Kieber J.J., Bilyeu K.D., Bird D.M. Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J., 2004, 38: 203-214 CrossRef
  63. 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
  64. 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
  65. Murray J., Karas B., Ross L., Brachmann A., Wagg C., Geil R., Perry J., Nowakowski K., MacGillivary M., Held M., Stougaard J., Peterson L., Parniske M., Szczyglowski K. Genetic suppressors of the Lotus japonicus har1-1 hypernodulation phenotype. Mol. Plant-Microbe Interact., 2006, 19(10): 1082-1091 CrossRef
  66. Murray J.D., Karas B.J., Sato S., Tabata S., Amyot L., Szczyglowski K. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science, 2007, 315: 101-104 CrossRef
  67. Inoue T., Higuchi M., Hashimoto Y., Seki M., Kobayashi M., Kato T., Tabata S., Shinozaki K., Kakimoto T. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature, 2001, 409: 1060-1063 CrossRef
  68. Suzuki T., Miwa K., Ishikawa K., Yamada H., Aiba H., Mizuno T. The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinins. Plant Cell Physiol., 2001, 42: 107-113 CrossRef
  69. Ovchinnikova E., Journet E.-P., Chabaud M., Cosson V., Ratet P., Duc G., Fedorova E., Wei Liu W., Rik Op den Camp R., Zhukov V., Tikhonovich I., Borisov A., Bisseling T., Limpens E. IPD3 controls the formation of nitrogen-fixing symbiosomes in pea and Medicago spp. Mol. Plant-Microbe Interact., 2011, 24(11): 1333-1344 CrossRef
  70. 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
  71. 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
  72. Lohar D.P., Sharopova N., Endre G., Peñuela S., Samac D., Town C., Silverstein K.A., VandenBosch K.A. Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol., 2006, 140: 221-234 CrossRef
  73. 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
  74. 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
  75. Breakspear A., Liu C., Roy S., Stacey N., Rogers C., Trick M., Morieri G., Mysore K.S., Wen J., Oldroyd G.E.D., Downie J.A., Murray J.D. The root hair «infectome» of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for Auxin signaling in rhizobial infection. Plant Cell, 2014, 26: 4680-4701 CrossRef
  76. Genre A., Russo G. Does a common pathway transduce symbiotic signals in plant—microbe interactions? Front. Plant Sci., 2016, 7: A96 CrossRef
  77. Madsen L.H., Tirichine L., Jurkiewicz A., Sullivan J.T., Heckmann A.B., Bek A.S. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat. Commun., 2010, 1: 1-10 CrossRef
  78. Hayashi T., Banba M., Shimoda Y., Kouchi H., Hayashi M., Imaizumi-Anraku H. A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J., 2010, 63: 141-154 CrossRef
  79. Ariel F., Brault-Hernandez M., Laffont C., Huault E., Brault M., Plet J., Moison M., Blanchet S., Ichanté J.L., Chabaud M., Carrere S., Crespi M., Chan R.L., Frugier F. Two direct targets of cytokinin signaling regulate symbiotic nodulation in Medicago truncatula. Plant Cell, 2012, 24: 3838-3852 CrossRef
  80. Mok D.W., Mok M.C. Cytokinin metabolism and action. Annu. Rev. Plant Physiol. Plant Mol. Biol., 2001, 52: 89-118 CrossRef
  81. Costacurta A., Vanderleyden J. Synthesis of phytohormones by plant associated bacteria. Crit. Rev. Microbiol., 1995, 21: 1-18 CrossRef
  82. Miyawaki K., Tarkowski P., Matsumoto-Kitano M., Kato T., Sato S., Tarkowska D., Tabata S., Sandberg G., Kakimoto T. Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. PNAS USA, 2006, 103(44): 16598-16603 CrossRef
  83. Takei K., Yamaya T., Sakakibara H. Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-zeatin. J. Biol. Chem., 2004, 279(40): 41866-41872 CrossRef
  84. Kurakawa T., Ueda N., Maekawa M., Kobayashi K., Kojima M., Nagato Y., Sakakibara H., Kyozuka J. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature, 2007, 445(7128): 652-655 CrossRef
  85. 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. Mol. Plant, 2015, 8(8): 1213-1226 CrossRef
  86. Azarakhsh M., Kirienko A.N., Zhukov V., Lebedeva M.A., Dolgikh E.A., Lutova L.A. KNOTTED1-LIKE HOMEOBOX 3: a new regulator of symbiotic nodule development. J. Exp. Bot., 2015, 66(22): 7181-7195 CrossRef
  87. Mortier V., Wasson A., Jaworek P., De Keyser A., Decroos M., Holsters M., Tarkowski P., Mathesius U., Goormachtig S. Role of LONELY GUY genes in indeterminate nodulation on Medicago truncatula. New Phytologist, 2014, 202(2): 582-593 CrossRef
  88. Hirose N., Takei K. Regulation of cytokinin biosynthesis, compartmentalization and translocation. J. Exp. Bot., 2008, 59(1): 75-83 CrossRef
  89. Chen Y., Chen W., Li X., Jiang H., Wu P., Xia K., Yang Y., Wu G. Knockdown of LjIPT3 influences nodule development in Lotus japonicus. Plant Cell Physiol., 2014, 55(1): 183-193 CrossRef
  90. Kisiala A., Laffont C., Emery J.R.N., Frugier F. Bioactive cytokinins are selectively secreted by Sinorhizobium meliloti nodulating and nonnodulating strains. Mol. Plant-Microbe Interact., 2013, 26: 1225-1231 CrossRef
  91. Sasaki T., Suzaki T., Soyano T., Kojima M., Sakakibara H., Kawaguchi M. Shoot-derived cytokinins systemically regulate root nodulation. Nature, 2014, 5: 4983 CrossRef
  92. Mortier V., DeWever E., Vuylsteke M., Holsters M., Goormachtig S. Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling. Plant J., 2012, 70: 367-376 CrossRef
  93. Soyano T., Hirakawa H., Sato S., Hayashi M., Kawaguchi M. Nodule inception creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production. PNAS USA, 2014, 111: 14607-14612 CrossRef

back