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A salt stress-responsive cytokinin receptor homologue isolated from Medicago sativa nodules

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Abstract

A new cytokinin receptor homologue, MsHK1, was isolated from Medicago sativa root nodules. MsHK1 expression was induced in alfalfa seedlings by exogenous application of the cytokinin trans-zeatin. Transcript accumulation was detected in different plant organs. MsHK1 expression was induced by salt stress in alfalfa roots, leaves and nodules, and transcript accumulation in the vascular bundles pointed to a putative role in osmosensing for MsHK1 and/or other close cytokinin receptor homologues. Expression in the meristem and the invasion zone of the nodule suggest a role for cytokinin receptors in cytokinin sensing during nodule cell division and differentiation.

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Abbreviations

Asp:

aspartate

BAP:

6-benzyl aminopurine

CHASE:

cyclases/histidine kinases associated sensory extracellular

dpi:

days post-inoculation

His:

histidine

RACE:

rapid amplification of cDNA ends

UTR:

untranslated region

References

  • Bauer P, Crespi MD, Szecsi J, Allison LA, Schultze M, Ratet P, Kondorosi E, Kondorosi A (1994) Alfalfa Enod12 genes are differentially regulated during nodule development by Nod factors and Rhizobium invasion. Plant Physiol 105:585–592

    Article  PubMed  CAS  Google Scholar 

  • Casse F, Boucher C, Julliot JS, Michell M, Dénarié J (1979) Identification and characterization of large plasmids in Rhizobium meliloti using agarose gel electrophoresis. J Bacteriol 113:229–242

    CAS  Google Scholar 

  • Coba de la Peña T, Frugier F, McKhann HI, Bauer P, Brown S, Kondorosi A, Crespi M (1997) A carbonic anhydrase gene is induced in the nodule primordium and its cell-specific expresión is controlled by the presence of Rhizobium during development. Plant J 11:407–420

    Article  Google Scholar 

  • Cooper JB, Long SR (1994) Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6:215–225

    Article  PubMed  CAS  Google Scholar 

  • Crespi MD, Jurkevitch E, Poiret M, d’Aubenton-Carafa Y, Petrovics G, Kondorosi E, Kondorosi A (1994) enod40: a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO J 13:5099–5112

    PubMed  CAS  Google Scholar 

  • Dehio C, Bruijn FJ (1992) The early nodulin gene SrEnod2 from Sesbania rostrata is inducible by cytokinin. Plant J 2:117–128

    PubMed  CAS  Google Scholar 

  • Fang Y, Hirsch AM (1998) Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in transgenic alfalfa. Plant Physiol 116:53–68

    Article  PubMed  CAS  Google Scholar 

  • Ferguson BJ, Mathesius U (2003) Signaling interactions during nodule development. J Plant Growth Regul 22:47–72

    Article  CAS  Google Scholar 

  • Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Curr Opin Plant Biol 8:518–525

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680–2693

    Article  PubMed  CAS  Google Scholar 

  • Grefen C, Harter K (2004) Plant two-component systems: principles, functions, compexity and cross talk. Planta 219:733–742

    Article  PubMed  CAS  Google Scholar 

  • Haberer G, Kieber JJ (2002) Cytokinins: new insights into a classic phytohormone. Plant Physiol 128:354–362

    Article  PubMed  CAS  Google Scholar 

  • Hare PD, Cress WA, van Staden J (1997) The involvement of cytokinins in plant responses to environmental stress. Plant Growth Regul 23:79–103

    Article  CAS  Google Scholar 

  • Higuchi M, Pischke MS, Mähönen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, Helariutta Y, Sussman MR, Kakimoto T (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA 101:8821–8826

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa T, Boon-Chieng S, Mitaku S (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378–379

    Article  PubMed  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1938) The water culture method for growing plants without soil. Agricultural Experimental Station Circle No. 347. University of California. Berkley

    Google Scholar 

  • Hoth S, Ikeda Y, Morgante M, Wang X, Zuo J, Hanafey MK, Gaasterland T, Tingey SV, Chua NH (2003) Monitoring genome-wide changes in gene expression in response to endogenous cytokinin reveals targets in Arabidopsis thaliana. FEBS Lett 554:373–380

    Article  PubMed  CAS  Google Scholar 

  • Hutchison CE, Kieber JJ (2002) Cytokinin signaling in Arabidopsis. Plant Cell 14:S47–S59

    Article  PubMed  CAS  Google Scholar 

  • Hwang I, Sakakibara H (2006) Cytokinin biosynthesis and perception. Physiol Plant 126:528–538

    Article  CAS  Google Scholar 

  • Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060–1063

    Article  PubMed  CAS  Google Scholar 

  • Ito Y, Kurata N (2006) Identification and characterization of cytokinin-signalling gene families in rice. Gene 382:57–65

    Article  PubMed  CAS  Google Scholar 

  • Jimenez-Zurdo JI, Frugier F, Crespi MD, Kondorosi A (2000) Expression profiles of 22 novel molecular markers for organogenetic pathways acting in alfalfa nodule development. Mol Plant-Microbe Interact 13:96–106

    Article  PubMed  CAS  Google Scholar 

  • Kakimoto T (2003) Perception and signal transduction of cytokinins. Annu Rev Plant Physiol Plant Mol Biol 54:605–627

    CAS  Google Scholar 

  • Kiba T, Naitou T, Koizumi N, Yamashino T, Sakakibara H, Mizuno T (2005) Combinatorial microarray analysis revealing Arabidopsis genes implicated in cytokinin responses through the His→Asp phosphorelay circuitry. Plant Cell Physiol 46:339–355

    Article  PubMed  CAS  Google Scholar 

  • Kim HJ, Ryu H, Hong SH, Woo HR, Lim PO, Lee IC, Sheen J, Nam HG, Hwang I (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci USA 103:814–819

    Article  PubMed  CAS  Google Scholar 

  • Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DM (2004) Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses. Plant J 38:203–214

    Article  PubMed  CAS  Google Scholar 

  • Mähönen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, Helariutta Y (2000) A novel two-component hybrid molecule regulates vascular morphogenesis in the Arabidopsis root. Genes Dev 14:2938–2943

    Article  PubMed  Google Scholar 

  • Mathesius U, Charon C, Rolfe BG, Kondorosi A, Crespi M (2000) 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 13:617–628

    Article  PubMed  CAS  Google Scholar 

  • Mizuno T (1998) His-Asp phosphotransfer signal transduction. J Biochem 123:555–563

    PubMed  CAS  Google Scholar 

  • Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118

    Article  PubMed  CAS  Google Scholar 

  • Mulder L, Hogg B, Bersoult A, Cullimore JV (2005) Integration of signalling pathways in the establishment of the legume-rhizobia symbiosis. Physiol Plant 123:207–218

    Article  CAS  Google Scholar 

  • Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315:101–104

    Article  PubMed  CAS  Google Scholar 

  • Newcomb W, Syono K, Torrey JG (1976) Development of an ineffective pea root nodule: morphogenesis, fine structure, and cytokinin biosynthesis. Can J Bot 55:1891–1907

    Google Scholar 

  • Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377

    Article  PubMed  CAS  Google Scholar 

  • Oldroyd GED (2007) Nodules and hormones. Science 315:52–53

    Article  PubMed  CAS  Google Scholar 

  • Papon N, Clastre M, Andreu F, Gantet P, Rideau M, Crèche J (2002) Expression analysis in plant and cell suspensions of CrCKR1, a cDNA encoding a histidine kinase receptor homologue in Catharanthus roseus (L.) G. Don. J Exp Bot 53:1989–1990

    Article  PubMed  CAS  Google Scholar 

  • Pareek A, Singh A, Kumar M, Kushwaha HR, Lynn AM, Singla-Pareek SL (2006) Whole-genome analysis of Oryza sativa reveals similar architecture of two-component signaling machinery with Arabidopsis. Plant Physiol 142:380–397

    Article  PubMed  CAS  Google Scholar 

  • Parkinson JS, Kofoid EC (1992) Communication modules in bacterial signaling proteins. Annu Rev Genet 26:71–111

    Article  PubMed  CAS  Google Scholar 

  • Pas J, von Grotthuss M, Wyrwicz LS, Rychlewski L, Barcizewski J (2004) Structure prediction, evolution and ligand interaction of CHASE domain. FEBS Lett 576:287–290

    Article  PubMed  CAS  Google Scholar 

  • Pay A, Heberle-Bors E, Hirt H (1992) An alfalfa cDNA encodes a protein with homology to translationally controlled human tumor protein. Plant Mol Biol 19:501–503

    Article  PubMed  CAS  Google Scholar 

  • Rashotte AM, Carson SDB, To JPC, Kieber JJ (2003) Expression profiling of cytokinin action in Arabidopsis. Plant Physiol 132:1998–2011

    Article  PubMed  CAS  Google Scholar 

  • Reiser V, Raitt D, Saito H (2003) Yeast osmosensor Sln1 and plant cytokinin receptor Cre1 respond to changes in turgor pressure. J Cell Biol 161:1035–1040

    Article  PubMed  CAS  Google Scholar 

  • Riefler M, Novak O, Strnad M, Shmülling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54

    Article  PubMed  CAS  Google Scholar 

  • Romanov GA, Lomin SN, Schmülling T (2006) Biochemical characteristics and ligand-binding properties of Arabidopsis cytokinin receptor AHK3 compared to CRE1/AHK4 as revealed by a direct binding assay. J Exp Bot 57:4051–4058

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Short KC, Torrey JG (1972) Cytokinins in seedling roots of pea. Plant Physiol 49:155–160

    Article  PubMed  CAS  Google Scholar 

  • Spíchal L, Rakova NY, Riefler M, Mizuno T, Romanov GA, Sornad M, Schmülling T (2004) Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3, differ in their ligand specificity in a bacterial assay. Plant Cell Physiol 45:1299–1305

    Article  PubMed  Google Scholar 

  • Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Miwa K, Ishikawa K, Yamada H, Aiba H, Mizuno T (2001) The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinins. Plant Cell Physiol 42:107–113

    Article  PubMed  CAS  Google Scholar 

  • Syono K, Newcomb W, Torrey JG (1976) Cytokinin production in relation to the development of pea root nodules. Can J Bot 54:2155–2162

    CAS  Google Scholar 

  • Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107

    Article  PubMed  CAS  Google Scholar 

  • Ueguchi C, Koizumi H, Suzuki T, Mizuno T (2001a) Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol 42:231–235

    Article  PubMed  CAS  Google Scholar 

  • Ueguchi C, Sato S, Kato T, Tabata S (2001b) The AHK4 gene involved in the cytokinin-signaling pathway as a direct receptor molecule in Arabidopsis thaliana. Plant Cell Physiol 42:751–755

    Article  PubMed  CAS  Google Scholar 

  • Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743–1754

    Article  PubMed  CAS  Google Scholar 

  • Vasse J, de Billy F, Camut S, Truchet G (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol 172:4295–4306

    PubMed  CAS  Google Scholar 

  • Verdoy D, Coba de la Peña T, Redondo FJ, Lucas MM, Pueyo JJ (2006) Trangenic Medicago truncatula plants that accumulate proline display nitrogen-fixing activity with enhanced tolerante to osmotic stress. Plant Cell Environ 29:1913–1923

    Article  PubMed  CAS  Google Scholar 

  • Vincent JM (1970) A manual for the practical study of root-nodule bacteria. IBP Handbook No. 15. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K, Miwa K, Yamashino T, Mizuno T (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42:1017–1023

    Article  PubMed  CAS  Google Scholar 

  • Yonekura-Sakakibara K, Kojima M, Yamaya T, Sakakibara H (2004) Molecular characterization of cytokinin-responsive histidine kinases in maize: differential ligand preferences and response to cis-zeatin. Plant Physiol 134:1654–1661

    Article  PubMed  CAS  Google Scholar 

  • Zhao XC, Schaller GE (2004) Effect of salt and osmotic stress upon expression of the ethylene receptor ETR1 in Arabidopsis thaliana. FEBS Lett 562:189–192

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank C. Mark for editorial assistance. This work was supported by the Comunidad de Madrid (fellowship to T.C.P. and grant to J.J.P.), the CSIC and the European Social Fund (postdoctoral contract to T.C.P.), and the Spanish Ministry of Education and Science (grant to J.J.P.). The Department of Immunology and Oncology was founded and is supported by the Spanish National Research Council (CSIC) and by Pfizer.

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Authors and Affiliations

  1. Department of Plant Physiology and Ecology, Instituto de Recursos Naturales, Centro de Ciencias Medioambientales, CSIC, Serrano 115-bis, 28006, Madrid, Spain

    Teodoro Coba de la Peña, Claudia B. Cárcamo, M. Mercedes Lucas & José J. Pueyo

  2. Department of Immunology and Oncology, Centro Nacional de Biotecnología, CSIC, Darwin 3, UAM Campus de Cantoblanco, 28049, Madrid, Spain

    Luis Almonacid, Angel Zaballos & Dimitrios Balomenos

Authors
  1. Teodoro Coba de la Peña
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  2. Claudia B. Cárcamo
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  3. Luis Almonacid
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  4. Angel Zaballos
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  5. M. Mercedes Lucas
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  6. Dimitrios Balomenos
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  7. José J. Pueyo
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Correspondence to José J. Pueyo.

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Coba de la Peña, T., Cárcamo, C.B., Almonacid, L. et al. A salt stress-responsive cytokinin receptor homologue isolated from Medicago sativa nodules. Planta 227, 769–779 (2008). https://doi.org/10.1007/s00425-007-0655-3

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