Key Points
-
Nod factors are oligosaccharide signalling molecules that are required for the establishment of nodule development. These signals activate several responses in the plant, including cytosolic Ca2+ fluxes and Ca2+ spiking in epidermal root-hair cells.
-
Mutations in a number of legume species define the genetic components that are involved in Nod-factor signalling. The proteins that are encoded by these genes can be placed in a signalling cascade relative to the cellular processes that are activated by Nod factor.
-
Some of the earliest-acting genes in this pathway encode receptor-like kinases with sugar-binding motifs in the extracellular domain. Mutations in these genes block all responses to Nod factor and this, coupled with the sequence homologies, suggests that their gene products probably function as the Nod-factor receptor.
-
Two genes downstream of the Nod-factor receptor are required for Ca2+ spiking and the maintenance of the Ca2+ flux. These genes encode a receptor-like kinase with leucine-rich-repeat domains in the extracellular domain and a protein with weak homology to cation channels.
-
Acting downstream of Ca2+ spiking, and potentially involved in the perception of this cellular response, is a chimeric Ca2+/calmodulin-dependent protein kinase. The recent cloning of the corresponding gene underlines the importance of Ca2+ in this signalling cascade.
Abstract
Several genes have recently been identified using legume mutants that are defective for nodulation signalling. The proteins they encode include novel types of receptor-like kinase that are predicted to recognize bacterial nodulation (Nod) factors, a leucine-rich-repeat receptor kinase, a putative ion channel and a predicted Ca2+/calmodulin-dependent protein kinase. The identification of these gene products provides new insights into the legume signalling responses to rhizobial signals.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Smil, V. Global population and the nitrogen cycle. Scientific American 277, 76–81 (1997).
Gage, D. J., Bobo, T. & Long, S. R. Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). J. Bacteriol. 178, 7159–7166 (1996).
Lodwig, E. M. et al. Amino-acid cycling drives nitrogen fixation in the legume–Rhizobium symbiosis. Nature 422, 722–726 (2003).
Perret, X., Staehelin, C. & Broughton, W. J. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64, 180–201 (2000).
Long, S. R. Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8, 1885–1898 (1996).
Fisher, R. F. & Long, S. R. Rhizobium–plant signal exchange. Nature 357, 655–660 (1992).
Downie, J. A. in The Rhizobiaceae (eds Spaink, H. P., Kondorosi, A. & Hooykaas, P. J. J.) 387–402 (Kluwer Academic Publishers, Dordrecht, 1998).
Denarie, J., Debelle, F. & Prome, J. C. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65, 503–535 (1996).
Long, S. R. Genes and signals in the Rhizobium–legume symbiosis. Plant Physiol. 125, 69–72 (2001).
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. 12, 829–832 (1999).
Van Brussel, A. A. N. et al. Induction of preinfection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium. Science 257, 70–72 (1992).
Esseling, J. J., Lhuissier, F. G. P. & Emons, A. M. C. Nod factor-induced root hair curling: continuous polar growth towards the point of nod factor application. Plant Physiol. 132, 1982–1988 (2003).
Pellock, B. J., Cheng, H. P. & Walker, G. C. Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides. J. Bacteriol. 182, 4310–4318 (2000).
Cheng, H. P. & Walker, G. C. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 180, 5183–5191 (1998).
Felle, H. H., Kondorosi, E., Kondorosi, A. & Schultze, M. The role of ion fluxes in Nod factor signalling in Medicago sativa. Plant J. 13, 455–463 (1998).
Felle, H. H., Kondorosi, E., Kondorosi, A. & Schultze, M. Elevation of the cytosolic free Ca2+ is indispensable for the transduction of the Nod factor signal in alfalfa. Plant Physiol. 121, 273–279 (1999).
Felle, H. H., Kondorosi, E., Kondorosi, A. & Schultze, M. Rapid alkalinization in alfalfa root hairs in response to rhizobial lipochitooligosaccharide signals. Plant J. 10, 295–301 (1996).
Kurkdjian, A. C. Role of the differentiation of root epidermal-cells in Nod factor (from Rhizobium meliloti)-induced root-hair depolarization of Medicago sativa. Plant Physiol. 107, 783–790 (1995).
Felle, H. H., Kondorosi, E., Kondorosi, A. & Schultze, M. Nod signal-induced plasma-membrane potential changes in alfalfa root hairs are differentially sensitive to structural modifications of the lipochitooligosaccharide. Plant J. 7, 939–947 (1995).
Ehrhardt, D. W., Atkinson, E. M. & Long, S. R. Depolarization of alfalfa root hair membrane-potential by Rhizobium meliloti Nod factors. Science 256, 998–1000 (1992).
Felle, H. H., Kondorosi, E., Kondorosi, A. & Schultze, M. How alfalfa root hairs discriminate between Nod factors and oligochitin elicitors. Plant Physiol. 124, 1373–1380 (2000).
Goedhart, J., Hink, M. A., Visser, A., Bisseling, T. & Gadella, T. W. J. In vivo fluorescence correlation microscopy (FCM) reveals accumulation and immobilization of Nod factors in root hair cell walls. Plant J. 21, 109–119 (2000).
Cardenas, L. et al. Rhizobium Nod factors induce increases in intracellular free calcium and extracellular calcium influxes in bean root hairs. Plant J. 19, 347–352 (1999).
Ehrhardt, D. W., Wais, R. & Long, S. R. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85, 673–681 (1996).
Walker, S. A., Viprey, V. & Downie, J. A. Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by Nod factors and chitin oligomers. Proc. Natl Acad. Sci. USA 97, 13413–13418 (2000). Reports the analysis of Ca2+ spiking and Ca2+ flux in P. sativum root hairs in response to Nod factors and chitin oligomers. It suggests a sequence of gene functions in Nod-factor signalling, on the basis of Ca2+ spiking and other phenotypes in nodulation-defective P. sativum mutants.
Shaw, S. L. & Long, S. R. Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiol. 131, 976–984 (2003). Shows that a low concentration of Nod factors can induce Ca2+ spiking, but higher concentrations are required to induce the Ca2+ flux. Mt DMI1 and Mt DMI2 mutants defective for Ca2+ spiking are shown to induce, but are unable to sustain, the Ca2+ flux.
Cardenas, L. et al. Ion changes in legume root hairs responding to Nod factors. Plant Physiol. 123, 443–451 (2000).
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 209, 207–212 (1999).
Foreman, J. et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446 (2003).
Shaw, S. L. & Long, S. R. Nod factor inhibition of reactive oxygen efflux in a host legume. Plant Physiol. 132, 2196–2204 (2003).
Santos, R., Herouart, D., Sigaud, S., Touati, D. & Puppo, A. Oxidative burst in alfalfa–Sinorhizobium meliloti symbiotic interaction. Mol. Plant Microbe Interact. 14, 86–89 (2001).
Ramu, S. K., Peng, H. M. & Cook, D. R. Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. Mol. Plant Microbe Interact. 15, 522–528 (2002).
Wais, R. J. et al. Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc. Natl Acad. Sci. USA 97, 13407–13412 (2000). Proposes an order of gene function in Nod-factor signalling in M. truncatula , on the basis of the analysis of Ca2+ spiking and other phenotypes in non-nodulating mutants.
Harris, J. M., Wais, R. & Long, S. R. Rhizobium-induced calcium spiking in Lotus japonicus. Mol. Plant Microbe Interact. 16, 335–341 (2003).
Wais, R. J., Keating, D. H. & Long, S. R. Structure–function analysis of nod factor-induced root hair calcium spiking in Rhizobium–legume symbiosis. Plant Physiol. 129, 211–224 (2002).
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. 128, 1390–1401 (2002).
Dolmetsch, R. E., Xu, K. L. & Lewis, R. S. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933–936 (1998).
Li, W. H., Llopis, J., Whitney, M., Zlokarnik, G. & Tsien, R. Y. Cell-permeant caged InsP3 ester shows that Ca2+ spike frequency can optimize gene expression. Nature 392, 936–941 (1998).
Allen, G. J. et al. A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411, 1053–1057 (2001).
Oldroyd, G. E. D., Mitra, R. M., Wais, R. J. & Long, S. R. Evidence for structurally specific negative feedback in the Nod factor signal transduction pathway. Plant J. 28, 191–199 (2001).
Pingret, J. L., Journet, E. P. & Barker, D. G. Rhizobium nod factor signaling: evidence for a G protein-mediated transduction mechanism. Plant Cell 10, 659–671 (1998).
Roche, P. et al. Molecular basis of symbiotic host specificity in Rhizobium meliloti — nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67, 1131–1143 (1991).
Ardourel, M. et al. Rhizobium meliloti lipooligosaccharide nodulation actors different structural requirements for bacterial entry into target root hair-cells and induction of plant symbiotic developmental responses. Plant Cell 6, 1357–1374 (1994).
Walker, S. A. & Downie, J. A. Entry of Rhizobium leguminosarum bv. viciae into root hairs requires minimal Nod factor specificity, but subsequent infection thread growth requires nodO or nodE. Mol. Plant Microbe Interact. 13, 754–762 (2000).
Spaink, H. P. et al. A novel highly unsaturated fatty-acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354, 125–130 (1991).
Sutton, J. M., Lea, E. J. A. & Downie, J. A. The nodulation-signaling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc. Natl Acad. Sci. USA 91, 9990–9994 (1994).
Firmin, J. L., Wilson, K. E., Carlson, R. W., Davies, A. E. & Downie, J. A. Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Mol. Microbiol. 10, 351–360 (1993).
Geurts, R. et al. Sym2 of pea is involved in a nodulation factor-perception mechanism that controls the infection process in the epidermis. Plant Physiol. 115, 351–359 (1997).
Geurts, R. & Franssen, H. Signal transduction in Rhizobium-induced nodule formation. Plant Physiol. 112, 447–453 (1996).
Ben Amor, B. et al. 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. 34, 495–506 (2003).
Madsen, E. B. et al. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637–640 (2003).
Radutoiu, S. et al. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585–592 (2003). Describes two L. japonicus genes ( Lj NFR1 and Lj Nfr5 ) that are thought to encode receptor kinases, which are predicted to recognize Nod factors.
Limpens, E. et al. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302, 630–633 (2003). Based on initial mapping work with P. sativum , this paper identifies a region in M. truncatula that encodes receptor kinases, and uses gene silencing to show that two of the genes Mt LYK3 and Mt LYK4 have a role in infection-thread initiation.
Steen, A. et al. Cell wall attachment of a widely distributed peptidoglycan binding domain is hindered by cell wall constituents. J. Biol. Chem. 278, 23874–23881 (2003).
Ponting, C. P., Aravind, L., Schultz, J., Bork, P. & Koonin, E. V. Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer. J. Mol. Biol. 289, 729–745 (1999).
Parniske, M. & Downie, J. A. Plant biology — locks, keys and symbioses. Nature 425, 569–570 (2003).
Esseling, J. J., Lhuissier, F. G. P. & Emons, A. M. C. A nonsymbiotic root hair tip growth phenotype on NORK-mutated legumes: implications for nodulation-factor-induced signaling and formation of a multifacteted root hair pocket for bacteria. Plant Cell 16, 933–944 (2004). Shows that root-hair deformation in legumes that are mutated in Mt DMI2 (or orthologous genes) might be altered because of a touch response. An alternative (branched) pathway for nodulation signalling is proposed in which early nodulation genes are on the pathway of gene induction but not root-hair deformation.
Catoira, R. et al. Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12, 1647–1665 (2000).
Duc, G., Trouvelot, A., Gianinazzipearson, V. & Gianinazzi, S. First report of non-mycorrhizal plant mutants (Myc−) obtained in pea (Pisum-sativum-L) and fababean (Vicia-faba L). Plant Science 60, 215–222 (1989).
Schneider, A. et al. Genetic mapping and functional analysis of a nodulation-defective mutant (sym19) of pea (Pisum sativum L.). Mol. Gen. Genet. 262, 1–11 (1999).
Schneider, A. et al. Mapping of the nodulation loci sym9 and sym10 of pea (Pisum sativum L.). Theor. Appl. Genet. 104, 1312–1316 (2002).
Albrecht, C., Geurts, R., Lapeyrie, F. & Bisseling, T. Endomycorrhizae and rhizobial Nod factors both require SYM8 to induce the expression of the early nodulin genes PsENOD5 and PsENOD12A. Plant J. 15, 605–614 (1998).
Mitra, R. M. et al. A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development:gene identification by transcript-based cloning. Proc. Natl Acad. Sci. USA 101, 4701–4705 (2004). A new method for transcript-based gene identification is used to isolate the Mt DMI3 gene, which encodes a probable Ca2+/CaM-dependent protein kinase, which is predicted to integrate Ca2+ spiking to activate gene induction in nodulation signalling.
Levy, J. et al. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361–1364 (2004). Positional cloning was used to identify the Mt DMI3 gene, which encodes a probable Ca2+/CaM-dependent protein kinase, which is predicted to integrate Ca2+ spiking to activate gene induction in nodulation signalling.
Stracke, S. et al. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959–962 (2002).
Endre, G. et al. A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962–966 (2002).
Dangl, J. L. & Jones, J. D. G. Plant pathogens and integrated defence responses to infection. Nature 411, 826–833 (2001).
Ane, J.-M. et al. A novel protein required for bacterial and fungal symbioses in legumes. Science 303, 1364–1367 (2004). The essential nodulation signalling gene Mt DMI1 was identified by positional cloning and encodes a membrane protein that is predicted to have cation selectivity.
den Hartog, M., Musgrave, A. & Munnik, T. Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation. Plant J. 25, 55–65 (2001).
den Hartog, M., Verhoef, N. & Munnik, T. Nod factor and elicitors activate different phospholipid signaling pathways in suspension-cultured alfalfa cells. Plant Physiol. 132, 311–317 (2003).
Miles, G. P., Samuel, M. A., Jones, A. M. & Ellis, B. E. Mastoparan rapidly activates plant MAP kinase signaling independent of heterotrimeric G proteins. Plant Physiol. 143, 1332–1336 (2004).
Tucker, E. B. & Boss, W. F. Mastoparan-induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol. 111, 459–467 (1996).
Takahashi, K., Isobe, M. & Muto, S. Mastoparan induces an increase in cytosolic calcium ion concentration and subsequent activation of protein kinases in tobacco suspension culture cells. Biochim. Biophys. Acta 1401, 339–346 (1998).
Patil, S., Takezawa, D. & Poovaiah, B. W. Chimeric plant calcium/calmodulin-dependent protein-kinase gene with a neural visinin-like calcium-binding domain. Proc. Natl Acad. Sci. USA 92, 4897–4901 (1995).
Liu, Z. H., Xia, M. & Poovaiah, B. W. Chimeric calcium/calmodulin-dependent protein kinase in tobacco: differential regulation by calmodulin isoforms. Plant Mol. Biol. 38, 889–897 (1998).
Oldroyd, G. E. D. & Long, S. R. Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod factor signaling. Plant Physiol. 131, 1027–1032 (2003).
Kneen, B. E., Weeden, N. F. & Larue, T. A. Non-nodulating mutants of Pisum sativum (L) cv. sparkle. J. Heredity 85, 129–133 (1994).
Borisov, A. Y. et al. The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiol. 131, 1009–1017 (2003).
Schauser, L., Roussis, A., Stiller, J. & Stougaard, J. A plant regulator controlling development of symbiotic root nodules. Nature 402, 191–195 (1999).
Catoira, R. et al. The HCL gene of Medicago truncatula controls Rhizobium-induced root hair curling. Development 128, 1507–1518 (2001).
Harrison, M. J. Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 361–389 (1999).
Hodge, A., Campbell, C. D. & Fitter, A. H. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413, 297–299 (2001).
Soltis, D. E. et al. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen-fixation in angiosperms. Proc. Natl Acad. Sci. USA 92, 2647–2651 (1995).
Kistner, C. & Parniske, M. Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci. 7, 511–518 (2002).
Journet, E. P. et al. Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol. Plant Microbe Interact. 14, 737–748 (2001).
van Rhijn, P. et al. 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. Proc. Natl Acad. Sci. USA 94, 5467–5472 (1997).
Gualtieri, G. & Bisseling, T. The evolution of nodulation. Plant Mol. Biol. 42, 181–194 (2000).
Bonfante, P. et al. The Lotus japonicus LjSym4 gene is required for the successful symbiotic infection of root epidermal cells. Mol. Plant Microbe Interact. 13, 1109–1120 (2000).
Schauser, L. et al. Symbiotic mutants deficient in nodule establishment identified after T-DNA transformation of Lotus japonicus. Mol. Gen. Genet. 259, 414–423 (1998).
Szczyglowski, K. et al. Nodule organogenesis and symbiotic mutants of the model legume Lotus japonicus. Mol. Plant Microbe Interact. 11, 684–697 (1998).
Kawaguchi, M. et al. Root, root hair, and symbiotic mutants of the model legume Lotus japonicus. Mol. Plant Microbe Interact. 15, 17–26 (2002).
Kosuta, S. et al. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol. 131, 952–962 (2003).
Chabaud, M., Venard, C., Defaux-Petras, A., Becard, G. & Barker, D. G. Targeted inoculation of Medicago truncatula in vitro root cultures reveals MtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi. New Phytol. 156, 265–273 (2002).
De Koninck, P. & Schulman, H. Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 279, 227–230 (1998).
Putney, J. W. Calcium signaling: up, down, up, down ... what's the point? Science 279, 191–192 (1998).
Meyer, T., Hanson, P. I., Stryer, L. & Schulman, H. Calmodulin trapping by calcium-calmodulin dependent protein kinase. Science 256, 1199–1202 (1992).
Takezawa, D., Ramachandiran, S., Paranjape, V. & Poovaiah, B. W. Dual regulation of a chimeric plant serine threonine kinase by calcium and calcium calmodulin. J. Biol. Chem. 271, 8126–8132 (1996).
Sathyanarayanan, P. V., Cremo, C. R. & Poovaiah, B. W. Plant chimeric Ca2+/calmodulin-dependent protein kinase role of the neural visinin-like domain in regulating autophosphorylation and calmodulin affinity. J. Biol. Chem. 275, 30417–30422 (2000).
Sathyanarayanan, P. V., Siems, W. F., Jones, J. P. & Poovaiah, B. W. Calcium-stimulated autophosphorylation site of plant chimeric calcium/calmodulin-dependent protein kinase. J. Biol. Chem. 276, 32940–32947 (2001).
Wais, R. J., Wells, D. H. & Long, S. R. Analysis of differences between Sinorhizobium meliloti 1021 and 2011 strains using the host calcium spiking response. Mol. Plant Microbe Interact. 15, 1245–1252 (2002).
Acknowledgements
We would like to thank S. Walker for providing unpublished images and our colleagues for helpful discussions. The authors are supported by grants from the Biotechnology and Biosciences Research Council and the Royal Society (to G.E.D.O.).
Author information
Authors and Affiliations
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Related links
Related links
DATABASES
Interpro
FURTHER INFORMATION
Glossary
- BACTEROID
-
A terminally differentiated form of rhizobial bacteria that reside inside the nodule and fix nitrogen.
- SYMBIOSOME
-
A bacteroid that is surrounded by a specialized plant membrane, and that is the site of nitrogen fixation and nutrient exchange.
- FLAVANOID
-
A phenolic compound that is produced by the plant and that activates symbiotic responses in free-living rhizobial bacteria.
- LysM DOMAIN
-
A domain that is proposed to be involved in binding β1–4-linked N-acetylglucosamine residues.
- PEPTIDOGLYCAN
-
A proteinacious polysaccharide that is found in bacterial cell walls.
- CHITIN
-
A polysaccharide that is made up of β1–4-linked N-acetyl glucosamine residues and is found in arthropod exoskeleton and some plants and fungi.
- SYNTENIC
-
A region of the genome that is conserved between different species.
- MYCORRHIZAE
-
Fungal species that form symbiotic interactions with plants and that assist in the uptake of nutrients from the soil.
- BRASSINOSTEROIDS
-
A group of naturally occurring plant polyhydroxysteroids that function as plant hormones.
- CLAVATA RECEPTOR
-
A receptor that is involved in meristematic identity.
- VISININ
-
A Ca2+-binding protein in animals.
Rights and permissions
About this article
Cite this article
Oldroyd, G., Downie, J. Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5, 566–576 (2004). https://doi.org/10.1038/nrm1424
Issue Date:
DOI: https://doi.org/10.1038/nrm1424
This article is cited by
-
Amelioration of NaCl stress on germination, growth, and nitrogen fixation of Vicia faba at isosmotic Na–Ca combinations and Rhizobium
Planta (2024)
-
Deciphering the role of SPL12 and AGL6 from a genetic module that functions in nodulation and root regeneration in Medicago sativa
Plant Molecular Biology (2022)
-
Nitrogen fixation capacity and metabolite responses to phosphorus in soybean nodules
Symbiosis (2022)
-
Computational characterizations of GDP-mannose 4,6-dehydratase (NoeL) Rhizobial proteins
Current Genetics (2021)
-
The cell-surface protein composition of a coral symbiont, Breviolum psygmophilum, reveals a mechanism for host specificity and displays dynamic regulation during temperature stress
Marine Biology (2020)