Legume nodulation: successful symbiosis through short- and long-distance signalling
Mark Kinkema A , Paul T. Scott A and Peter M. Gresshoff A BA ARC Centre of Excellence for Integrative Legume Research, The University of Queensland, St Lucia, Brisbane, Qld 4072, Australia.
B Corresponding author. Email: p.gresshoff@uq.edu.au
Functional Plant Biology 33(8) 707-721 https://doi.org/10.1071/FP06056
Submitted: 17 March 2006 Accepted: 22 May 2006 Published: 2 August 2006
Abstract
Nodulation in legumes provides a major conduit of available nitrogen into the biosphere. The development of nitrogen-fixing nodules results from a symbiotic interaction between soil bacteria, commonly called rhizobia, and legume plants. Molecular genetic analysis in both model and agriculturally important legume species has resulted in the identification of a variety of genes that are essential for the establishment, maintenance and regulation of this symbiosis. Autoregulation of nodulation (AON) is a major internal process by which nodule numbers are controlled through prior nodulation events. Characterisation of AON-deficient mutants has revealed a novel systemic signal transduction pathway controlled by a receptor-like kinase. This review reports our present level of understanding on the short- and long-distance signalling networks controlling early nodulation events and AON.
Acknowledgments
We thank the Australian Research Council, the University of Queensland Strategic Research Fund and the Queensland State Government Smart State Initiative for funding under the Centre of Excellence Scheme. Special thanks are given to CILR members, especially Dr Attila Kereszt, for providing unpublished data and valued criticism.
Ané JM,
Kiss GB,
Riely BK,
Penmetsa RV, Oldroyd GE , et al.
(2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364–1367.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Apel K, Hirt H
(2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bauer WD
(1981) Infection of legumes by rhizobia. Annual Review of Plant Physiology 32, 407–449.
| Crossref | GoogleScholarGoogle Scholar |
Bersoult A,
Camut S,
Perhald A,
Kereszt A,
Kiss GB, Cullimore J
(2005) Expression of the Medicago truncatula DMI2 gene suggests roles of the symbiotic nodulation receptor kinase in nodules and during early nodule development. Molecular Plant–Microbe Interactions 18, 869–876.
| PubMed |
Bhuvaneswari TV,
Turgeon BG, Bauer WD
(1980) Early stages in the infection of soybean (Glycine max (L.) Merr.) by Rhizobium japonicum. I. Localization of infectible root cells. Plant Physiology 66, 1027–1031.
| PubMed |
Borisov AY,
Madsen LH,
Tsyganov VE,
Umehara Y, Voroshilova VA , et al.
(2003) The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiology 131, 1009–1017.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bradbury SM,
Peterson RL, Bowley SR
(1991) Interaction between three alfalfa nodulation genotypes and two Glomus species. New Phytologist 119, 115–120.
| Crossref | GoogleScholarGoogle Scholar |
Bright LJ,
Liang Y,
Mitchell DM, Harris JM
(2005) The LATD gene of Medicago truncatula is required for both nodule and root development. Molecular Plant–Microbe Interactions 18, 521–532.
| PubMed |
Buzas DM, Gresshoff PM
(2006) Short and long distance control of root development by LjHAR1 during the juvenile stage of Lotus japonicus. Journal of Plant Physiology ,
| PubMed |
Caba JM,
Recalde L, Ligero F
(1998) Nitrate-induced ethylene biosynthesis and the control of nodulation in alfalfa. Plant, Cell & Environment 21, 87–93.
| Crossref | GoogleScholarGoogle Scholar |
Caba JM,
Poveda JL,
Gresshoff PM, Ligero F
(1999) Differential sensitivity of nodulation to ethylene in soybean cv. Bragg and a supernodulating mutant. New Phytologist 142, 233–242.
| Crossref | GoogleScholarGoogle Scholar |
Caetano-Anollés G, Bauer WD
(1988) Feedback regulation of nodule formation in alfalfa. Planta 175, 546–557.
| Crossref | GoogleScholarGoogle Scholar |
Caetano-Anollés G, Gresshoff PM
(1990) Early induction of feedback regulatory responses governing nodulation in soybean. Plant Science 71, 69–81.
| Crossref | GoogleScholarGoogle Scholar |
Caetano-Anollés G, Gresshoff PM
(1991) Plant genetic control of nodulation. Annual Review of Microbiology 45, 345–382.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Caetano-Anollés G,
Lagares A, Bauer WD
(1990) Rhizobium meliloti exopolysaccharide mutants elicit feedback regulation of nodule formation in alfalfa. Plant Physiology 91, 368–374.
Caetano-Anollés G,
Paparozzi ET, Gresshoff PM
(1991) Mature nodules and root tips control nodulation in soybean. Journal of Plant Physiology 137, 389–396.
Calvert HE,
Pence MK,
Pierce M,
Malik NSA, Bauer WD
(1984) Anatomical analysis of the development and distribution of Rhizobium infections in soybean roots. Canadian Journal of Botany 62, 2375–2384.
Capoen W,
Goormachtig S,
De Rycke R,
Schroeyers K, Holsters M
(2005) SrSymRK, a plant receptor essential for symbiosome formation. Proceedings of the National Academy of Sciences USA 102, 10 369–10 374.
| Crossref | GoogleScholarGoogle Scholar |
Carroll BJ, Gresshoff PM
(1983) Nitrate inhibition of nodulation and nitrogen fixation in white clover. Zeitschrift fur Pflanzenphysiologie 110, 77–88.
Carroll BJ,
McNeil DL, Gresshoff PM
(1985a) Isolation and properties of soybean [Glycine max (L.) Merr.] mutants that nodulate in the presence of high nitrate concentrations. Proceedings of the National Academy of Sciences USA 82, 4162–4166.
| Crossref |
Carroll BJ,
McNeil DL, Gresshoff PM
(1985b) A supernodulation and nitrate tolerant symbiotic (nts) soybean mutant. Plant Physiology 78, 34–40.
| PubMed |
Casimiro I,
Beeckman T,
Graham N,
Bhalerao R,
Zhang H,
Casero P,
Sandberg G, Bennett MJ
(2003) Dissecting Arabidopsis lateral root development. Trends in Plant Science 8, 165–171.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Catford J-G,
Staehelin C,
Lerat S,
Piché Y, Vierheilig H
(2003) Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with nod factors. Journal of Experimental Botany 54, 1481–1487.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Catoira R,
Galera C,
De Billy F,
Penmetsa RV,
Journet E-P,
Maillet F,
Rosenberg C,
Cook D,
Gough C, Denarie J
(2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. The Plant Cell 12, 1647–1666.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chen W-M,
de Faria SM,
Straliotto R,
Pitard RM,
Simões Araùjo JL,
Chou J-H,
Chou Y-J,
Barrios E,
Prescott AR,
Elliott GN,
Sprent JI,
Young JPW, James EK
(2005) Proof that Burkholderia strains form effective symbioses with legumes: a study of novel Mimosa-nodulating strains from South America. Applied and Environmental Microbiology 71, 7461–7471.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Clark SE,
Williams RW, Meyerowitz EM
(1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575–585.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Delves AC,
Mathews A,
Day DA,
Carter AS,
Carroll BJ, Gresshoff PM
(1986) Regulation of the soybean-Rhizobium nodule symbiosis by shoot and root factors. Plant Physiology 82, 588–590.
| PubMed |
DeYoung BJ, Clark SE
(2001) Signaling through the CLV1 receptor complex. Plant Molecular Biology 46, 505–513.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
D’Haeze W,
De Rycke R,
Mathis R,
Goormachtig S,
Pagnotta S,
Verplancke C,
Capoen W, Holsters M
(2003) Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume. Proceedings of the National Academy of Sciences USA 100, 11789–11794.
| Crossref | GoogleScholarGoogle Scholar |
Duc G, Messager A
(1989) Mutagenesis of pea (Pisum sativum L.) and the isolation of mutants for nodulation and nitrogen fixation. Plant Science 60, 207–213.
| Crossref | GoogleScholarGoogle Scholar |
Duc G,
Trouvelot A,
Gianinazzi-Pearson V, Gianinazzi S
(1989) First report of non-mycorrhizal plant mutants (Myc–) obtained in pea (Pisum sativum L.) and faba bean (Vicia faba L.). Plant Science 60, 215–222.
| Crossref | GoogleScholarGoogle Scholar |
Durrant WE, Dong X
(2004) Systemic acquired resistance. Annual Review of Phytopathology 42, 185–209.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ehsan H,
Ray WK,
Phinney B,
Wang X,
Huber SC, Clouse SD
(2005) Interaction of Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase with a homolog of mammalian TGF-β receptor interacting protein. The Plant Journal 43, 251–261.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Endre G,
Kereszt A,
Kevei Z,
Mihacea S,
Kalo P, Kiss GB
(2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962–966.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fearn JC, LaRue TA
(1991) Ethylene inhibitors restore nodulation to sym5 mutants of Pisum sativum L. cv sparkle. Plant Physiology 96, 239–244.
| PubMed |
Felle HH,
Kondorosi É,
Kondorosi Á, Schultze M
(1998) The role of ion fluxes in Nod factor signalling in Medicago sativa. The Plant Journal 13, 455–463.
| Crossref | GoogleScholarGoogle Scholar |
Ferguson BJ,
Ross JJ, Reid JB
(2005) Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiology 138, 2396–2405.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fernández-López M,
Goormachtig S,
Gao M,
D’Haeze W,
Van Montagu M, Holsters M
(1998) Ethylene-mediated phenotypic plasticity in root nodule development on Sesbania rostrata. Proceedings of the National Academy of Sciences USA 95, 12 724–12 728.
Gabriel DW, Rolfe BG
(1990) Working models of specific recognition in plant–microbe interactions. Annual Review of Phytopathology 28, 365–391.
| Crossref | GoogleScholarGoogle Scholar |
Gage DJ
(2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiology and Molecular Biology Reviews 68, 280–300.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
George MLC, Robert FM
(1991) Autoregulatory response of Phaseolus vulgaris L. to symbiotic mutants of Rhizobium leguminosarum bv. phaseoli. Applied and Environmental Microbiology 57, 2687–2692.
| PubMed |
Goodlass G, Smith KA
(1979) Effects of ethylene on root extension and nodulation of pea (Pisum sativum L.) and white clover (Trifolium repens L.). Plant and Soil 51, 387–395.
| Crossref | GoogleScholarGoogle Scholar |
Goormachtig S,
Capoen W,
James EK, Holsters M
(2004) Switch from intracellular to intercellular invasion during water stress-tolerant legume nodulation. Proceedings of the National Academy of Sciences USA 101, 6303–6308.
| Crossref | GoogleScholarGoogle Scholar |
Graham PH, Vance CP
(2003) Legumes: importance and constraints to greater use. Plant Physiology 131, 872–877.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gresshoff PM
(1993) Molecular genetic analysis of nodulation genes in soybean. Plant Breeding Reviews 11, 275–318.
Grobbelaar N,
Clarke B, Hough MC
(1971) The nodulation and nitrogen fixation of isolated roots of Phaseolus vulgaris L. Plant and Soil Special Vol., 215–223.
Guinel FC, LaRue TA
(1992) Ethylene inhibitors partly restore nodulation to pea mutant E107 (brz). Plant Physiology 99, 515–518.
| PubMed |
Hattan J,
Kanamoto H,
Takemura M,
Yokota A, Kohchi T
(2004) Molecular characterization of the cytoplasmic interacting protein of the receptor kinase IRK expressed in the inflorescence and root apices of Arabidopsis. Bioscience, Biotechnology, and Biochemistry 68, 2598–2606.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Heidstra R,
Geurts R,
Franssen H,
Spaink HP,
van Kammen A, Bisseling T
(1994) Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiology 105, 787–797.
| PubMed |
Heidstra R,
Nilsen G,
Martinez-Abarca F,
van Kammen A, Bisseling T
(1997a) Nod factor-induced expression of leghemoglobin to study the mechanism of NH4NO3 inhibition on root hair deformation. Molecular Plant–Microbe Interactions 10, 215–220.
| PubMed |
Heidstra R,
Yang WC,
Yalcin Y,
Peck S,
Emons A,
Van Kammen A, Bisseling T
(1997b) Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction. Development 124, 1781–1787.
| PubMed |
Hinson K
(1975) Nodulation responses from nitrogen applied to soybean half-root systems. Agronomy Journal 67, 799–804.
Hirsch AM,
Bhuvaneswari TV,
Torrey JG, Bisseling T
(1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proceedings of the National Academy of Sciences of the United States of America 86, 1244–1248.
| Crossref |
PubMed |
Hunter WJ
(1993) Ethylene production by root nodules and effect of ethylene on nodulation in Glycine max. Applied and Environmental Microbiology 59, 1947–1950.
| PubMed |
Hutangura P,
Mathesius U,
Jones MGK, Rolfe BG
(1999) Auxin induction is a trigger for root gall formation caused by root-knot nematodes in white clover and is associated with the activation of the flavonoid pathway. Australian Journal of Plant Physiology 26, 221–231.
Imaizumi-Anraku H,
Takeda N,
Charpentier M,
Perry J, Miwa H , et al.
(2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433, 527–531.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jacobs M, Rubery PH
(1988) Naturally occuring auxin transport regulators. Science 241, 346–349.
Jacobsen E, Feenstra WJ
(1984) A new pea mutant with efficient nodulation in the presence of nitrate. Plant Science Letters 33, 337–344.
| Crossref | GoogleScholarGoogle Scholar |
Jamet A,
Sigaud S,
Van de Sype G,
Puppo A, Hérouart D
(2003) Expression of the bacterial catalase genes during Sinorhizobium meliloti–Medicago sativa symbiosis and their crucial role during the infection process. Molecular Plant–Microbe Interactions 16, 217–225.
| PubMed |
Kalo P,
Gleason C,
Edwards A,
Marsh J, Mitra RM , et al.
(2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308, 1786–1789.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kanamori N,
Madsen LH,
Radutoiu S,
Frantescu M, Quistgaard EMH , et al.
(2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proceedings of the National Academy of Sciences USA 103, 359–364.
| Crossref | GoogleScholarGoogle Scholar |
Kaothien P,
Ok SH,
Shuai B,
Wengier D,
Cotter R,
Kelley D,
Kiriakopolos S,
Muschietti J, McCormick S
(2005) Kinase partner protein interacts with LePRK1 and LePRK2 receptor kinases and plays a role in polarized pollen tube growth. The Plant Journal 42, 492–503.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Karlova R,
Boeren S,
Russinova E,
Aker J,
Vervoort J, de Vries S
(2006) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes BRASSINOSTEROID-INSENSITIVE1. The Plant Cell 18, 626–638.
| Crossref |
PubMed |
Kistner C,
Winzer T,
Pitzschke A,
Mulder L, Sato S , et al.
(2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. The Plant Cell 17, 2217–2229.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Koltai H,
Dhandaydham M,
Oppermann CH,
Thomas J, Bird D
(2001) Overlapping plant signal transduction pathways induced by a parasitic nematode and a rhizobial endosymbiont. Molecular Plant–Microbe Interactions 14, 1168–1177.
| PubMed |
Kosslak RM, Bohlool BB
(1984) Suppression of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side. Plant Physiology 75, 125–130.
| PubMed |
Krusell L,
Madsen LH,
Sato S,
Aubert G, Genua A , et al.
(2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420, 422–426.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lamb C, Dixon RA
(1997) The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251–275.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lawson CGR,
Carroll BJ, Gresshoff PM
(1988) Alleviation of nitrate inhibition of soybean nodulation by high inoculum does not involve bacterial nitrate metabolism. Plant and Soil 110, 123–127.
| Crossref | GoogleScholarGoogle Scholar |
Lee KH, La Rue T
(1992) Exogenous ethylene inhibits nodulation of Pisum sativum L. cv sparkle. Plant Physiology 100, 1759–1763.
| PubMed |
Lévy J,
Bres C,
Geurts R,
Chalhoub B, Kulikova O , et al.
(2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361–1364.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Li J,
Wen J,
Lease KA,
Doke JT,
Tax FE, Walker JC
(2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213–222.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ligero F,
Lluch C, Olivares J
(1986) Evolution of ethylene from roots of Medicago sativa plants inoculated with Rhizobium meliloti. Journal of Plant Physiology 125, 361–365.
Ligero F,
Lluch C, Olivares J
(1987) Evolution of ethylene from roots and nodulation rate of alfalfa (Medicago sativa L.) plants inoculated with Rhizobium meliloti as affected by the presence of nitrate. Journal of Plant Physiology 129, 461–467.
Ligero F,
Caba JM,
Lluch C, Olivares J
(1991) Nitrate inhibition of nodulation can be overcome by the ethylene inhibitor aminoethoxyvinylglycine. Plant Physiology 97, 1221–1225.
| PubMed |
Ligero F,
Poveda JL,
Gresshoff PM, Caba JM
(1999) Nitrate-and inoculation-enhanced ethylene biosynthesis in soybean roots as a possible mediator of nodulation control. Journal of Plant Physiology 154, 482–488.
Limpens E,
Franken C,
Smit P,
Willemse J,
Bisseling T, Geurts R
(2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302, 630–633.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Loh J, Stacey G
(2003) Nodulation gene regulation in Bradyrhizobium japonicum: a unique integration of global regulatory circuits. Applied and Environmental Microbiology 69, 10–17.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Loh JT,
Yuen-Tsai JPY,
Stacey MG,
Lohar D,
Welborn A, Stacey G
(2001) Population density-dependent regulation of the Bradyrhizobium japonicum nodulation genes. Molecular Microbiology 42, 37–46.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lohar DP, Bird DMcK
(2003) Lotus japonicus: A new model to study root-parasitic nematodes. Plant & Cell Physiology 44, 1176–1184.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Madsen EB,
Madsen LH,
Radutoiu S,
Olbryt M, Rakwalska M , et al.
(2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637–640.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Malik NSA,
Calvert HE, Bauer WD
(1987) Nitrate induced regulation of nodule formation in soybean. Plant Physiology 84, 266–271.
| PubMed |
Mathesius U
(2003) Conservation and divergence of signalling pathways between roots and soil microbes — the Rhizobium–legume symbiosis compared to the development of lateral roots, mycorrhizal interactions and nematode-induced galls. Plant and Soil 255, 105–119.
| Crossref | GoogleScholarGoogle Scholar |
Mathesius U,
Bayliss C,
Weinman JJ,
Schlaman HRM,
Spaink HP,
Rolfe BG,
McCully ME, Djordjevic MA
(1998a) Flavonoids synthesized in cortical cells during nodule initiation are early developmental markers in white clover. Molecular Plant–Microbe Interactions 11, 1223–1232.
Mathesius U,
Schlaman HRM,
Spaink HP,
Sautter C,
Rolfe BG, Djordjevic MA
(1998b) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. The Plant Journal 14, 23–34.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mathesius U,
Weinman JJ,
Rolfe BG, Djordjevic MA
(2000) Rhizobia can induce nodules in white clover by ‘hijacking’ mature cortical cells activated during lateral root development. Molecular Plant–Microbe Interactions 13, 170–182.
| PubMed |
Mathews A,
Carroll BJ, Gresshoff PM
(1989) Development of Bradyrhizobium infections in a supernodulating and non-nodulating mutant of soybean (Glycine max (L.) Merr). Protoplasma 150, 40–47.
| Crossref | GoogleScholarGoogle Scholar |
McCallum CM,
Comai L,
Greene EA, Henikoff S
(2000) Targeted screening for induced mutations. Nature Biotechnology 18, 455–457.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Meixner C,
Ludwig-Müller J,
Miersch O,
Gresshoff P,
Staehelin C, Vierheilig H
(2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222, 709–715.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mitra RM,
Gleason CA,
Edwards A,
Hadfield J,
Downie JA,
Oldroyd GE, Long SR
(2004a) A Ca2+ / calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proceedings of the National Academy of Sciences USA 101, 4701–4705.
| Crossref | GoogleScholarGoogle Scholar |
Mitra RM,
Shaw SL, Long SR
(2004b) Six nonnodulating plant mutants defective for Nod factor-induced transcriptional changes associated with the legume–rhizobia symbiosis. Proceedings of the National Academy of Sciences USA 101, 10 217–10 222.
| Crossref | GoogleScholarGoogle Scholar |
Morris AC, Djordjevic MA
(2006) The Rhizobium leguminosarum biovar trifolii ANU794 induces novel developmental responses on the subterranean clover cultivar Woogenellup. Molecular Plant–Microbe Interactions 19, 471–479.
| PubMed |
Nakagawa T, Kawaguchi M
(2006) Shoot-applied MeJA suppresses root nodulation in Lotus japonicus. Plant & Cell Physiology 47, 176–180.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nam KH, Li J
(2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203–212.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nam KH, Li J
(2004) The Arabidopsis transthyretin-like protein is a potential substrate of BRASSINOSTEROID-INSENSITIVE 1. The Plant Cell 16, 2406–2417.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nishimura R,
Hayashi M,
Wu GJ,
Kouchi H, Imaizumi-Anraku H , et al.
(2002a) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420, 426–429.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nishimura R,
Ohmori M,
Fujita H, Kawaguchi M
(2002b) A lotus basic leucine zipper protein with a RING-finger motif negatively regulates the developmental program of nodulation. Proceedings of the National Academy of Sciences USA 99, 15 206–15 210.
| Crossref | GoogleScholarGoogle Scholar |
Nishimura R,
Ohmori M, Kawaguchi M
(2002c) The novel symbiotic phenotype of enhanced-nodulating mutant of Lotus japonicus: astray mutant is an early nodulating mutant with wider nodulation zone. Plant & Cell Physiology 43, 853–859.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nukui N,
Ezura H,
Yuhashi K-I,
Yasuta T, Minamisawa K
(2000) Effects of ethylene precursor and inhibitors for ethylene biosynthesis and perception on nodulation in Lotus japonicus and Macroptilium atropurpureum. Plant & Cell Physiology 41, 893–897.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nukui N,
Ezura H, Minamisawa K
(2004) Transgenic Lotus japonicus with an ethylene receptor gene Cm-ERS1/H70A enhances formation of infection threads and nodule primordia. Plant & Cell Physiology 45, 427–435.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nutman PS
(1948) Physiological studies on nodule formation I. The relation between nodulation and lateral root formation in red clover. Annals of Botany 12, 81–96.
Nutman PS
(1952) Studies on the physiology of nodule formation. III. Experiments on the excision of root-tips and nodules. Annals of Botany 16, 80–102.
Oka-Kira E,
Tateno K,
Miura K,
Haga T, Hayashi M , et al.
(2005) klavier (klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction. The Plant Journal 44, 505–515.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Olah B,
Brière C,
Bécaud G,
Dénarié J, Gough C
(2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1 / DMI2 signalling pathway. The Plant Journal 44, 195–207.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Oldroyd GED
(2001) Dissecting symbiosis: developments in Nod factor signal transduction. Annals of Botany 87, 709–718.
| Crossref | GoogleScholarGoogle Scholar |
Oldroyd GED,
Engstrom EM, Long SR
(2001) Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. The Plant Cell 13, 1835–1849.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pacios-Bras C,
Schlaman HRM,
Boot K,
Admiraal P,
Langerak JM,
Stougaard J, Spaink HP
(2003) Auxin distribution in Lotus japonicus during root nodule development. Plant Molecular Biology 52, 1169–1180.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Park SJ, Buttery BR
(1988) Nodulation mutants of white bean (Phaseolus vulgaris L.) induced by ethyl-methane sulfonate. Canadian Journal of Plant Science 68, 199–202.
Penmetsa RV, Cook DR
(1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275, 527–530.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Penmetsa RV,
Frugoli JA,
Smith LS,
Long SR, Cook DR
(2003) Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiology 131, 998–1008.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Peters NK, Crist-Estes DK
(1989) Nodule formation is stimulated by the ethylene inhibitor aminoethoxyvinylglycine. Plant Physiology 91, 690–693.
| PubMed |
Pierce M, Bauer WD
(1983) A rapid regulatory response governing nodulation in soybean. Plant Physiology 73, 286–290.
| PubMed |
Postma JG,
Jacobsen E, Feenstra WJ
(1988) Three pea mutants with an altered nodulation studied by genetic analysis and grafting. Journal of Plant Physiology 132, 424–430.
Price GD,
Mohapatra SS, Gresshoff PM
(1984) Structure of nodules formed by Rhizobium strain ANU289 in the non-legume Parasponia and legume siratro (Macroptilium atropurpureum). Botanical Gazette (Chicago, Ill.) 145, 444–451.
| Crossref | GoogleScholarGoogle Scholar |
Radutoiu S,
Madsen LH,
Madsen EB,
Felle HH, Umehara Y , et al.
(2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585–592.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ramu SK,
Peng H-M, Cook DR
(2002) Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. Molecular Plant–Microbe Interactions 15, 522–528.
| PubMed |
Rienties IM,
Vink J,
Borst JW,
Russinova E, de Vries SC
(2005) The Arabidopsis SERK1 protein interacts with the AAA-ATPase AtCDC48, the 14–3-3 protein GF14λ and the PP2C phosphatase KAPP. Planta 221, 394–405.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sagan M, Duc G
(1996) Sym28 and Sym29, two new genes involved in regulation of nodulation in pea (Pisum sativum L.). Symbiosis 20, 229–245.
Sagan M, Gresshoff PM
(1996) Developmental mapping of nodulation events in Pea (Pisum sativum L.) using supernodulating plant genotypes and bacterial variability reveals both plant and Rhizobium control of nodulation regulation. Plant Science 117, 167–179.
| Crossref | GoogleScholarGoogle Scholar |
Santos R,
Hérouart D,
Sigaud S,
Touati D, Puppo A
(2001) Oxidative burst in alfalfa–Sinorhizobium meliloti symbiotic interaction. Molecular Plant–Microbe Interactions 14, 86–89.
| PubMed |
Sargent L,
Huang SZ,
Rolfe BG, Djordjevic MA
(1987) Split root assays using Trifolium subterraneum shows that Rhizobium infection induces a systemic response that can inhibit nodulation of another invasive Rhizobium strain. Applied and Environmental Microbiology 53, 1611–1619.
| PubMed |
Schauser L,
Roussis A,
Stiller J, Stougaard J
(1999) A plant regulator controlling development of symbiotic root nodules. Nature 402, 191–195.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schmidt JS,
Harper JE,
Hoffman TK, Bent AF
(1999) Regulation of soybean nodulation independent of ethylene signaling. Plant Physiology 119, 951–959.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schnabel E,
Journet EP,
de Carvalho-Niebel F,
Duc G, Frugoli J
(2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Molecular Biology 58, 809–822.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schlaman HRM,
Horvath B,
Vigenboom E,
Okker RGH, Lugtenberg BJJ
(1991) Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum biovar vicae. Journal of Bacteriology 173, 4277–4287.
| PubMed |
Searle IR,
Men AE,
Laniya TS,
Buzas DM,
Iturbe-Ormaetxe I,
Carroll BJ, Gresshoff PM
(2003) Long-distance signaling in nodulation directed by a clavata1-like receptor kinase. Science 299, 109–112.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shah K,
Gadella TWJ,
van Erp H,
Hecht V, de Vries SC
(2001) Subcellular localization and oligomerization of the Arabidopsis thaliana somatic embryogenesis receptor kinase 1 protein. Journal of Molecular Biology 309, 641–655.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sharma VK,
Carles C, Fletcher JC
(2003) Maintenance of stem cell populations in plants. Proceedings of the National Academy of Sciences USA 100, 11 823–11 829.
| Crossref | GoogleScholarGoogle Scholar |
Shaw SL, Long SR
(2003a) Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiology 131, 976–984.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shaw SL, Long SR
(2003b) Nod factor inhibition of reactive oxygen efflux in a host legume. Plant Physiology 132, 2196–2204.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shrihari PC,
Sakamoto K,
Inubushi K, Akao S
(2000) Interaction between supernodulating or non-nodulating mutants of soybean and two arbuscular mycorrhizal fungi. Mycorrhiza 10, 101–106.
| Crossref | GoogleScholarGoogle Scholar |
Smit P,
Raedts J,
Portyanko V,
Debelle F,
Gough C,
Bisseling T, Geurts R
(2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308, 1789–1791.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Solaiman MZ,
Senoo K,
Kawaguchi M,
Imaizumi-Anraku H,
Akao S,
Tanaka A, Obata H
(2000) Characterization of mycorrhizas formed by Glomus sp. on roots of hypernodulating mutants of Lotus japonicus. Journal of Plant Research 113, 443–448.
| Crossref | GoogleScholarGoogle Scholar |
Soltis DE,
Soltis PS,
Morgan DR,
Swensen SM,
Mullin BC,
Dowd JM, Martin PG
(1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences USA 92, 2647–2651.
| Crossref |
Spaink HP
(2000) Root nodulation and infection factors produced by rhizobial bacteria. Annual Review of Microbiology 54, 257–288.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stacey G,
Libault M,
Brechenmacher L,
Wan J, May GD
(2006) Genetics and functional genomics of legume nodulation. Current Opinion in Plant Biology 9, 110–121.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stracke S,
Kistner C,
Yoshida S,
Mulder L, Sato S , et al.
(2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959–962.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Suganuma N,
Yamauchi H, Yamamoto K
(1995) Enhanced production of ethylene by soybean roots after inoculation with Bradyrhizobium japonicum. Plant Science 111, 163–168.
| Crossref | GoogleScholarGoogle Scholar |
Tang W,
Ezcurra I,
Muschietti J, McCormick S
(2002) A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. The Plant Cell 14, 2277–2287.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thimann KV
(1936) On the physiology of the formation of nodules on legume roots. Proceedings of the National Academy of Sciences USA 22, 511–514.
| Crossref |
Timmers ACJ,
Auriac M-C, Truchet G
(1999) Refined analysis of early symbiotic steps of the Rhizobium–Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126, 3617–3628.
| PubMed |
Truchet G,
Roche P,
Lerouge P,
Vasse J,
Camut S,
Debilly F,
Prome JC, Dénarié J
(1991) Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351, 670–673.
| Crossref | GoogleScholarGoogle Scholar |
van Brussel AAN,
Bakhuizen R,
van Spronsen PC,
Spaink HP,
Tak T,
Lugtenberg BJJ, Kijne JW
(1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257, 70–72.
van Loon LC,
Bakker PA, Pieterse CMJ
(1998) Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology 36, 453–483.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
van Noorden GE,
Ross JJ,
Reid JB,
Rolfe BG, Mathesius U
(2006) Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiology 140, 1494–1506.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
van Spronsen PC,
Tak T,
Rood AMM,
van Brussel AAN,
Kijne JW, Boot KJM
(2003) Salicylic acid inhibits indeterminate-type nodulation but not determinate-type nodulation. Molecular Plant–Microbe Interactions 16, 83–91.
| PubMed |
Vasse J,
de Billy F, Truchet G
(1993) Abortion of infection during the Rhizobium meliloti–alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. The Plant Journal 4, 555–566.
| Crossref | GoogleScholarGoogle Scholar |
Vessey JK,
Pawlowski K, Bergman B
(2005) Root-based N2-fixing symbioses: legumes, actinorhizal plants, Parasponia sp. and cycads. Plant and Soil 266, 205–230.
| Crossref | GoogleScholarGoogle Scholar |
Vierheilig H,
Garcia-Garrido JM,
Wyss U, Piché Y
(2000a) Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biology & Biochemistry 32, 589–595.
| Crossref | GoogleScholarGoogle Scholar |
Vierheilig H,
Maier W,
Wyss U,
Samson J,
Strack D, Piché Y
(2000b) Cyclohexenone derivative- and phosphate-levels in split root systems and their role in the systemic suppression of mycorrhization in precolonized barley plants. Journal of Plant Physiology 157, 593–599.
Wais RJ,
Galera C,
Oldroyd G,
Catoira R,
Penmetsa RV,
Cook D,
Gough C,
Denarie J, Long SR
(2000) Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proceedings of the National Academy of Sciences USA 97, 13 407–13 412.
| Crossref | GoogleScholarGoogle Scholar |
Walker SA,
Viprey V, Downie JA
(2000) Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by Nod factors and chitin oligomers. Proceedings of the National Academy of Sciences USA 97, 13 413–13 418.
| Crossref | GoogleScholarGoogle Scholar |
Walter M,
Chaban C,
Schütze K,
Batistic O, Weckermann K , et al.
(2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. The Plant Journal 40, 428–438.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Weerasinghe R,
Bird DMcK, Allen NS
(2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proceedings of the National Academy of Sciences USA 102, 3147–3152.
| Crossref | GoogleScholarGoogle Scholar |
Wopereis J,
Pajuelo E,
Dazzo FB,
Jiang Q,
Gresshoff PM,
de Bruijn FJ,
Stougaard J, Szczyglowski K
(2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. The Plant Journal 23, 97–114.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wu C,
Dickstein R,
Carry AJ, Norris JH
(1996) The auxin transport inhibitor N-(1-Naphthyl)phthalamic acid elicits pseudonodules on non-nodulating mutants of white sweet clover. Plant Physiology 110, 501–510.
| PubMed |
Xie Z-P,
Staehelin C,
Vierheilig H,
Wiemken A,
Jabbouri S,
Broughton WJ,
Vögeli-Lange R, Boller T
(1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybean. Plant Physiology 108, 1519–1525.
| PubMed |
Xie Z-P,
Staehelin C,
Wiemken A, Boller T
(1996) Ethylene responsiveness of soybean cultivars characterized by leaf senescence, chitinase induction and nodulation. Journal of Plant Physiology 149, 690–694.
Xie Z-P,
Muller J,
Wiemken A,
Broughton WJ, Boller T
(1998) Nod factors and tri-iodobenzoic acid stimulate mycorrhizal colonization and affect carbohydrate partitioning in mycorrhizal roots of Lablab purpureus. New Phytologist 139, 361–366.
| Crossref | GoogleScholarGoogle Scholar |
Yamamoto E,
Caglar H, Knap HT
(2000) Molecular characterization of two soybean homologs of Arabidopsis thaliana CLAVATA1 from the wild type and fasciation mutant. Biochimica et Biophysica Acta 1491, 333–340.
| PubMed |
