Abstract
Nitrogen fixing bacteria, collectively referred to as rhizobia, are able to trigger the organogenesis of a new organ on legumes, the nodule. The morphogenetic trigger is a Rhizobium-produced lipochitin-oligosaccharide called the Nod factor, which is necessary, and in some legumes sufficient, for triggering nodule development in the absence of the bacterium. Because plant development is substantially influenced by plant hormones, it has been hypothesized that plant hormones (mainly the classical hormones abscisic acid, auxin, cytokinins, ethylene and gibberellic acid) regulate nodule development. In recent years, evidence has shown that Nod factors might act in legumes by changing the internal plant hormone balance, thereby orchestrating the nodule developmental program. In addition, many nonclassical hormonal signals have been found to play a role in nodule development, some of them similar to signals involved in animal development. These compounds include peptide hormones, nitric oxide, reactive oxygen species, jasmonic acid, salicylic acid, uridine, flavonoids and Nod factors themselves. Environmental factors, in particular nitrate, also influence nodule development by affecting the plant hormone status. This review summarizes recent findings on the involvement of classical and nonclassical signals during nodule development with the aim of illustrating the multiple interactions existing between these compounds that have made this area so complicated to analyze.
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References
N Arora F Skoog ON Alien (1959) ArticleTitleKinetin-induced pseudonodules on tobacco roots. Am J Bot 46 610–613 Occurrence Handle1:CAS:528:DyaF3cXivFGitA%3D%3D
S Asad Y Fang KL Wykoff AM Hirsch (1994) ArticleTitleIsolation and characterisation of cDNA and genomic clones of MsENOD40: transcripts are detected in meristematic cells of alfalfa. Protoplasma 183 10–23 Occurrence Handle1:CAS:528:DyaK2MXks1SmsLs%3D
R Atzorn A Crozier CT Wheeler G Sandberg (1988) ArticleTitleProduction of gibberellins and indole-3-acetic acid by Rhizobium phaseoli in relation to nodulation of Phaseolus vulgaris roots. Planta 175 532–538 Occurrence Handle1:CAS:528:DyaL1cXmt1KntL8%3D
J Badenoch-Jones CW Parker DS Letham (1987) ArticleTitlePhytohormones, Rhizobium mutants, and nodulation in legumes. VII. Identification and quantification of cytokinins in effective and ineffective pea root nodules using radioimmunoassay. J Plant Growth Regul 6 97–111 Occurrence Handle1:CAS:528:DyaL2sXltlSqtL8%3D
J Badenoch-Jones RE Summons BG Rolfe DS Letham (1984) ArticleTitlePhytohormones, Rhizobium mutants, and nodulation in legumes. IV. Auxin metabolites in pea root nodules. J Plant Growth Regul 3 23–39 Occurrence Handle1:CAS:528:DyaL2cXlsVOqsrs%3D
A Bano JE Harper RM Auge DS Neuman (2002) ArticleTitleChanges in phytohormone levels following inoculation of two soybean lines differing in nodulation. Funct Plant Biol 29 965–974 Occurrence Handle1:CAS:528:DC%2BD38XntFyqtLg%3D
A Bano JE Harper (2002) ArticleTitlePlant growth regulators and phloem exudates modulate root nodulation of soybean. Funct Plant Biol 29 1299–1307 Occurrence Handle1:CAS:528:DC%2BD38Xps1ygtL8%3D
A Bano JR Hillman (1986) ArticleTitleEffect of abscisic acid on nodule morphology, nitrogenase activity and H2 evolution in Faba vulgaris. Ann Bot 58 281–283 Occurrence Handle1:CAS:528:DyaL28XltlSrsrw%3D
P Bauer P Ratet MD Crespi M Schultze A Kondorosi (1996) ArticleTitleNod-factors and cytokinins induce similar cortical cell divisions, amyloplast deposition and MsENOD12A expression patterns in alfalfa roots. Plant J 10 91–105 Occurrence Handle1:CAS:528:DyaK28XltVamtrw%3D
N Benhamou A Asselin (1989) ArticleTitleAttempted localisation for a substrate for chitinases in plant cells reveals abundant N-acetyl-D-glucosamine residues in secondary walls. Biol Cell 67 341–350 Occurrence Handle1:CAS:528:DyaK3cXhtlKisb8%3D
RP Bhalerao J Eklof K Ljung A Marchant M Bennett G Sandberg (2002) ArticleTitleShoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J 29 325–332 Occurrence Handle1:CAS:528:DC%2BD38XhvFOitL8%3D Occurrence Handle11844109
DC Billington BT Golding SB Primrose (1979) ArticleTitleBiosynthesis of ethylene from methionine. Isolation of the putative intermediate 4-methylthio-2-oxobutanoate from culture fluids of bacteria and fungi. Biochem J 182 827–836 Occurrence Handle1:CAS:528:DyaL3cXhtVOjsLY%3D Occurrence Handle42392
I Blilou JA Ocampo JM Garcia-Garrido (1999) ArticleTitleResistance of pea roots to endomycorrhizal fungus or Rhizobium correlates with enhanced levels of endogenous salicylic acid. J Exp Bot 50 1663–1668 Occurrence Handle1:CAS:528:DyaK1MXntlyhu7o%3D
KJM Boot AAN van Brussel T Tak HP Spaink JW Kijne (1999) ArticleTitleLipochitin oligosaccharides from Rhizobium leguminosarum bv. viclae reduce auxin transport capacity in Vicia sativa subsp. nigra roots. Mol Plant-Microbe Interact 12 839–844 Occurrence Handle1:CAS:528:DyaK1MXmtl2gsr4%3D
DE Brown AM Rashotte AS Murphy J Normanly BW Tague WA Peer L Taiz GK Muday (2001) ArticleTitleFlavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126 524–535 Occurrence Handle1:CAS:528:DC%2BD3MXks1Gnu7s%3D Occurrence Handle11402184
P Bueno MJ Soto MP Rodríguez-Rosales J Sanjuan J Olivares JP Donaire (2001) ArticleTitleTime-course of lipoxygenase, antioxidant enzyme activities and H2O2 accumulation during the early stages of Rhizobium-legume symbiosis. New Phytol 152 91–96 Occurrence Handle1:CAS:528:DC%2BD3MXnvVyls70%3D
SP Burg EA Burg (1966) ArticleTitleThe interaction between auxin and ethylene and its role in plant growth. Proc Natl Acad Sci USA 55 262–269 Occurrence Handle1:CAS:528:DyaF28XoslOlsQ%3D%3D Occurrence Handle5220945
JM Caba ML Centeno B Fernandez PM Gresshoff F Ligero (2000) ArticleTitleInoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta 211 98–104 Occurrence Handle1:CAS:528:DC%2BD3cXjvVyhsLk%3D Occurrence Handle10923709
JM Caba L Poveda PM Gresshoff F Ligero (1999) ArticleTitleDifferential sensitivity of nodulation to ethylene in soybean cv. Bragg and a supernodulating mutant. New Phytol 142 233–242 Occurrence Handle1:CAS:528:DyaK1MXkslOmsr0%3D
JM Caba L Recalde F Ligero (1998) ArticleTitleNitrate-induced ethylene biosynthesis and the control of nodulation in alfalfa. Plant Cell Env 21 87–93 Occurrence Handle1:CAS:528:DyaK1cXitlCgsLY%3D
A Camas L Cardenas C Quinto M Lara (2002) ArticleTitleExpression of different calmodulin genes in bean (Phaseolus vulgaris L.): role of Nod factor on calmodulin gene regulation. Mol Plant-Microbe Interact 15 428–436 Occurrence Handle1:CAS:528:DC%2BD38XjslSit7o%3D Occurrence Handle12036273
BJ Carroll DL McNeil PM Gresshoff (1985) ArticleTitleIsolation and properties of soybean (Glycine max) mutants that nodulate in the presence of high nitrate concentrations. Proc Natl Acad Sci USA 82 4164–4166
GA Charbonneau W Newcomb (1985) ArticleTitleGrowth regulators in developing effective root nodules of the garden pea (Pisum sativum L.). Biochem Physiol Pflanzen 180 667–681 Occurrence Handle1:CAS:528:DyaL2MXlsFOms7k%3D
C Charon C Johansson E Kondorosi A Kondorosi M Crespi (1997) ArticleTitle enod40 induces dedifferentiation and division of root cortical cells in legumes. Proc Natl Acad Sci USA 94 8901–8906 Occurrence Handle1:CAS:528:DyaK2sXltlWhtLo%3D Occurrence Handle11038563
C Charon C Sousa M Crespi A Kondorosi (1999) ArticleTitleAlteration of enod40 expression modifies Medicago truncatula root nodule development induced by Sinorhizobium meliloti. Plant Cell 11 1953–1965 Occurrence Handle1:CAS:528:DyaK1MXntFCgtL0%3D Occurrence Handle10521525
KK Chattopadhyay PS Basu (1989) ArticleTitleStudies on root nodules of leguminous trees: II. The bioproduction of different phytohormones in root nodules of Samanea saman (Jacq.) Merril and by its rhizobial symbiont. Biochem Physiol Pflanzen 184 387–394 Occurrence Handle1:CAS:528:DyaL1MXit1yltb0%3D
MJ Cho JE Harper (1993) ArticleTitleEffect of abscisic acid application on root isoflavonoid concentration and nodulation of wild type and nodulation-mutant soybean plants. Plant Soil 152 145–149
DB Collinge KM Kragh JD Mikkelsen KK Nielsen U Rasmussen K Vad (1993) ArticleTitlePlant chitinases. Plant J 3 31–40 Occurrence Handle1:CAS:528:DyaK3sXksVGitbc%3D Occurrence Handle8401605
B Compaan WC Yang T Bisseling H Franssen (2001) ArticleTitle ENOD40 expression in the pericycle precedes cortical cell division in Rhizobium-legume interaction and the highly conserved internal region of the gene does not encode a peptide. Plant Soil 230 1–8 Occurrence Handle1:CAS:528:DC%2BD3MXivFKjt70%3D
D Cook D Dreyer D Bonnet M Howell E Nony K VandenBosch (1995) ArticleTitleTransient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti. Plant Cell 7 43–55 Occurrence Handle1:CAS:528:DyaK2MXjsVyjsbw%3D Occurrence Handle7696879
JB Cooper SR Long (1994) ArticleTitleMorphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6 215–225 Occurrence Handle1:CAS:528:DyaK2cXlslWlsrY%3D Occurrence Handle12244237
JE Cooper R Rao (1992) ArticleTitleLocalised changes in flavonoid biosynthesis in roots of Lotus pendiculatus after infection by Rhizobium loti. Plant Physiol 100 444–450 Occurrence Handle1:CAS:528:DyaK38XmtlShsrY%3D Occurrence Handle16652981
V Corich S Goormachtig S Lievens M Van Montagu M Holsters (1998) ArticleTitlePatterns of ENOD40 gene expression in stem-borne nodules of Sesbania rostrata. Plant Mol Biol 37 67–76 Occurrence Handle1:CAS:528:DyaK1cXjtlajtLk%3D Occurrence Handle9620265
C Coronado JAS Zuanazzi C Sallaud JC Quirion R Esnault HP Husson A Kondorosi P Ratet (1995) ArticleTitleAlfalfa root flavonoid production is nitrogen regulated. Plant Physiol 108 533–542 Occurrence Handle1:CAS:528:DyaK2MXmtlaru7s%3D Occurrence Handle12228491
A Costacurta J Vanderleyden (1995) ArticleTitleSynthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21 1–18 Occurrence Handle7576148
M Crespi S Galvez (2000) ArticleTitleMolecular mechanisms in root nodule development. J Plant Growth Regul 19 155–166 Occurrence Handle1:CAS:528:DC%2BD3cXnvF2hurc%3D Occurrence Handle11038225
MD Crespi E Jurkevitch M Poiret Y d’Aubenton-Carafa G Petrovics E Kondorosi A Kondorosi (1994) ArticleTitle enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO J 13 5099–5112 Occurrence Handle1:CAS:528:DyaK2MXit1ektb8%3D Occurrence Handle7957074
M Cueto O Hernández-Perera R Martín ML Bentura J Rodrigo S Lamas MP Golvano (1996) ArticleTitlePresence of nitric oxide synthase activity in roots and root nodules of Lupinus albus. FEBS Lett 398 159–164 Occurrence Handle1:CAS:528:DyaK28Xnt1Kqsb4%3D Occurrence Handle8977098
JV Cullimore R Ranjeva JJ Bono (2001) ArticleTitlePerception of lipo-chitooligosaccharidic Nod factors in legumes. Trends Plant Sci 6 24–30 Occurrence Handle1:CAS:528:DC%2BD3MXlsFyrsbo%3D Occurrence Handle11164374
IB D’Agostino JJ Kieber (1999) ArticleTitleMolecular mechanisms of cytokinin action. Curr Opin Plant Biol 2 359–364 Occurrence Handle10508753
FD Dakora (1995) ArticleTitlePlant flavonoids - biological molecules for useful exploitation. Aust J Plant Physiol 22 87–99 Occurrence Handle1:CAS:528:DyaK2MXls1Kltbg%3D
TK Dangar PS Basu (1984) ArticleTitleSeasonal changes and metabolism of plant hormones in root nodules of Lens sp. Biol Plant 26 253–259 Occurrence Handle1:CAS:528:DyaL2cXmtVOlu78%3D
TK Dangar PS Basu (1987) ArticleTitleStudies on plant growth substances, IAA metabolism and nitrogenase activity in root nodules of Phaseolus aureus Roxb. var. mungo. Biol Plant 29 350–354 Occurrence Handle1:CAS:528:DyaL1cXhvFehtw%3D%3D
TK Dangar PS Basu (1991) ArticleTitleAbscisic acid production in culture by some rhizobium spp. of leguminous trees and pulses. Folia Microbiol 36 527–532 Occurrence Handle1:CAS:528:DyaK38XitFSrur4%3D
E Dantán-González Y Rosenstein C Quinto F Sánchez (2001) ArticleTitleActin monoubiquitylation is induced in plants in response to pathogens and symbionts. Mol Plant-Microbe Interac 14 1267–1273
J Davies J Zhang (1991) ArticleTitleRoot signals and the regulation of growth and development of plants in drying soil. Annu Rev Plant Physiol Plant Mol Biol 42 55–76 Occurrence Handle1:CAS:528:DyaK3MXltFSmsr8%3D
F de Billy C Grosjean S May M Bennett JV Cullimore (2001) ArticleTitleExpression studies on AUX1-like gens in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol Plant-Microbe Interact 14 267–277 Occurrence Handle1:CAS:528:DC%2BD3MXhsVKgsLw%3D Occurrence Handle11277424
C Dehio FJ de Bruijn (1992) ArticleTitleThe early nodulin gene SrEnod2 from Sesbania rostrata is 10 inducible by cytokinin. Plant J 2 117–128 Occurrence Handle1:CAS:528:DyaK3sXktVCquro%3D Occurrence Handle1303791
AJ DeJong J Cordewener F Lo Schiavo M Terzi J Vanderkerckove A van Kammen S de Vries (1992) ArticleTitleA carrot somatic embryo mutant is rescued by chitinase. Plant Cell 4 425–433 Occurrence Handle1:CAS:528:DyaK38XktVCgtrg%3D
AC Delves A Mathews DA Day AS Carter BJ Carroll PM Gresshoff (1986) ArticleTitleRegulation of soybean-Rhizobium nodule symbiosis by shoot and root factors. Plant Physiol 82 588–590 Occurrence Handle1:STN:280:DC%2BC3cnhslagtQ%3D%3D Occurrence Handle16665072
W D’Haeze M Holsters (2002) ArticleTitleNod factor structures, responses, and perception during initiation of nodule development. Glycobiol 12 79R–105R
MA Djordjevic U Mathesius T Arioli JJ Weinman E Gärtner (1997) ArticleTitleChalcone synthase gene expression in transgenic subterranean clover correlates with localised accumulation of flavonoids. Aust J Plant Physiol 24 119–132 Occurrence Handle1:CAS:528:DyaK2sXjs1Wrurs%3D
RC Dobert SB Rood DG Blevins (1992a) ArticleTitleGibberellins and the legume-Rhizobium symbiosis I. Endogenous gibberellins of Lima Bean (Phaseolus lunatus L.) stems and nodules. Plant Physiol 98 221–224 Occurrence Handle1:CAS:528:DyaK38Xht1CqurY%3D
RC Dobert SB Rood DG Blevins (1992b) ArticleTitleRhizobial-induced increase in internode length and identification of endogenous GAs of cowpea (Vigna unguiculata [L.] Walp) stems and nodules. J Plant Growth Regul 11 155–164 Occurrence Handle1:CAS:528:DyaK3sXjs1SgtA%3D%3D
RC Dobert SB Rood K Zanewich DG Blevins (1992c) ArticleTitleGibberellins and the legume-Rhizobium symbiosis III. Quantification of gibberellins from stems and nodules of Lima Bean and cowpea. Plant Physiol 100 1994–2001 Occurrence Handle1:CAS:528:DyaK3sXls1ejug%3D%3D
P Doerner JE Jorgensen R You J Steppuhn C Lamb (1996) ArticleTitleRoot growth and cyclin control. Trends Plant Sci 1 211–212
DSH Drennan C Norton (1972) ArticleTitleThe effect of ethrel on nodulation in Pisum sativum L. Plant Soil 36 53–57 Occurrence Handle1:CAS:528:DyaE38XhtlKktrY%3D
J Dullaart LI Duba (1970) ArticleTitlePresence of gibberellin-like substances and their possible role in auxin bioproduction in root nodules and roots of Lupinus luteus L. Acta Bot Neerl 19 877–883 Occurrence Handle1:CAS:528:DyaE3MXht1Wgur4%3D
JV Dyachok AE Tobin NPJ Price S von Arnold (2000) ArticleTitleRhizobial Nod factors stimulate somatic embryo development in Picea abies. Plant Cell Rep 19 290–297 Occurrence Handle1:CAS:528:DC%2BD3cXjsVeitb4%3D
JV Dyachok M Wiweger L Kenne S von Arnold (2002) ArticleTitleEndogenous nod-factor-like signal molecules promote early somatic embryo development in Norway spruce. Plant Physiol 128 523–533 Occurrence Handle1:CAS:528:DC%2BD38XhsVSru7k%3D Occurrence Handle11842156
G Endre A Kereszt Z Kevei S Mihacea P Kalo GB Kiss (2002) ArticleTitleA receptor kinase gene regulating symbiotic nodule development. Nature 417 962–966 Occurrence Handle1:CAS:528:DC%2BD38XkvVagsbk%3D Occurrence Handle12087406
EM Estabrook C Sengupta-Gopalan (1991) ArticleTitleDifferential expression of phenylalanin ammonia-lyase and chalcone synthase during soybean nodule development. Plant Cell 3 299–308 Occurrence Handle1:CAS:528:DyaK3MXks1Grsbg%3D Occurrence Handle1840912
KB Evensen DG Blevins (1981) ArticleTitleDifferences in endogenous levels of gibberellin-like substances in nodules of Phaseolus lunatus L. plants inoculated with two Rhizobial strains. Plant Physiol 65 195–198
Y Fang AM Hirsch (1998) ArticleTitleStudying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in alfalfa. Plant Physiol 116 53–68 Occurrence Handle1:CAS:528:DyaK1cXkslCkug%3D%3D Occurrence Handle9449836
B Favery A Complainville JM Vinardell P Lecomte D Vaubert P Mergaert A Kondorosi E Kondorosi M Crespi P Abad (2002) ArticleTitleThe endosymbiosis-induced genes ENOD40 and CCS52a are involved in endoparasitic-nematode interactions in Medicago truncatula. Mol Plant-Microbe Interact 15 1008–1013 Occurrence Handle1:CAS:528:DC%2BD38XnvFGjtL4%3D Occurrence Handle12437298
JC Fearn TA LaRue (1991) ArticleTitleEthylene inhibitors restore nodulation to sym5 mutants of Pisum sativum L. cv Sparkle. Plant Physiol 96 239–244 Occurrence Handle1:CAS:528:DyaK3MXkt1Kju70%3D Occurrence Handle16668158
EE Fedorova ZK Al’zhapparova GY Zhiznevskaya EN Artemenko SF Izmailov (1992) ArticleTitlePhytohormones in soybean root nodules. Sov Plant Physiol 39 135–139
EE Fedorova GY Zhiznevskaya ZV Kalibernaya EN Artemenko SF Izmailov AV Gus’kov (2000) ArticleTitleIAA metabolism during development of symbiosis between Phaseolus vulgaris and Rhizobium phaseoli. Russ J Plant Physiol 47 203–206 Occurrence Handle1:CAS:528:DC%2BD3cXisVSit7k%3D
M Fedorova J van der Mortel PA Matsumoto J Cho CD Town K VandenBosch S Gnatt CP Vance (2002) ArticleTitleGenome-wide identification of nodule-specific transcripts in the model legume Medicago truncatula. Plant Physiol 130 519–537 Occurrence Handle1:CAS:528:DC%2BD38XotVKntrs%3D Occurrence Handle12376622
M Fernández-López S Goormachtig M Goa W D’Haeze M van Montagu M Holsters (1998) ArticleTitleEthylene-mediated phenotypic plasticity in root nodule development on Sesbania rostrate. Proc Natl Acad Sci USA 95 12724–12728 Occurrence Handle9770553
WW Fletcher JWS Alcorn JC Raymond (1959) ArticleTitleGibberellic acid and nodulation of legumes. Nature 184 1576 Occurrence Handle1:CAS:528:DyaF3cXmsVCrug%3D%3D
F Foucher E Kondorosi (2000) ArticleTitleCell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol 43 773–786 Occurrence Handle1:CAS:528:DC%2BD3cXosVGksbo%3D Occurrence Handle11089876
X Fu NP Harberd (2003) ArticleTitleAuxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421 740–743 Occurrence Handle1:CAS:528:DC%2BD3sXhsV2rtr8%3D Occurrence Handle12610625
AW Galston (1959) ArticleTitleGibberellins and nodulation. Nature 183 545 Occurrence Handle1:STN:280:DyaG1M%2Fmt1erug%3D%3D Occurrence Handle13632787
MA Gilles-González G González MF Perutz L Kiger MC Marden C Poyart (1994) ArticleTitleHeme-based sensors, exemplified by the kinase FixL, are a new class of heme protein with distinctive ligand binding and autoxidation. Biochem 33 8067–8073
N Goicoechea MC Antolín M Sánchez-Díaz (1997) ArticleTitleGas exchange is related to the hormone balance in mycorrhizal or nitrogen-fixing alfalfa subjected to drought. Physiol Plant 100 989–997 Occurrence Handle1:CAS:528:DyaK2sXlvFCiurk%3D
EM González L Gálvez C Arrese-Igor (2001a) ArticleTitleAbscisic acid induces a decline in nitrogen fixation that involves leghaemoglobin, but is independent of sucrose synthase activity. J Exp Bot 52 285–293
EM González L Gálvez M Royuela PM Aparicio-Tejo C Arrese-Igor (2001b) ArticleTitleInsights into the regulation of nitrogen fixation in pea nodules: lessons from drought, abscisic acid and increased photoassimilate availability. Agronomic 21 607–613
R González-Pasayo E Martinez-Romero (2000) ArticleTitleMultiresistance genes of Rhizobium etli CFN42. Mol Plant-Microbe Interact 13 572–577 Occurrence Handle10796024
G Goodlass KA Smith (1979) ArticleTitleEffects of ethylene on root extension and nodulation of pea (Pisum sativum L.) and white clover (Trifolium repens L.). Plant Soil 51 387–395 Occurrence Handle1:CAS:528:DyaE1MXltVGhtb8%3D
S Goormachtig M Alves-Ferreira M van Montague G Engler M Holsters (1997) ArticleTitleExpression of cell cycle genes during Sesbania rostrata stem nodule development. Mol Plant-Microbe Interact 10 316–325 Occurrence Handle1:CAS:528:DyaK2sXitlOhurg%3D Occurrence Handle9100377
A Goverse H Overmars J Engelbertink A Schots J Bakker J Helder (2000) ArticleTitleBoth induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. Mol Plant-Microbe Interact 13 1121–1129 Occurrence Handle1:CAS:528:DC%2BD3cXntVarsrY%3D Occurrence Handle11043473
PM Gresshoff A Mathews A Krotzky JE Olsson BJ Carroll AC Delves R Kosslak ER Applebaum DA Day (1988) Supernodulating and non-nodulating mutants of soybean. R Palacio DPS Verma (Eds) Molecular Genetics Of Plant-Microbe Interactions. APS Press St Paul MN 364–369
PM Gresshoff (1993) ArticleTitleMolecular-genetic analysis of nodulation genes in soybean. Plant Breed Rev 11 275–318
N Grobbelaar B Clarke MC Hough (1971) ArticleTitleThe nodulation and nitrogen fixation of isolated roots of Phaseolus vulgaris L. III. The effect of carbon dioxide and ethylene. Plant Soil (Spec Vol) 215–223
F Gubler R Kalla JK Roberts JV Jacobsen (1995) ArticleTitleGibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactions of a high-pl α-amylase gene promoter. Plant Cell 7 1879–1891 Occurrence Handle1:CAS:528:DyaK2MXpslOnsLw%3D Occurrence Handle8535141
FC Guinel RD Geil (2002) ArticleTitleA model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legumes and its use to understand the roles of ethylene in the establishment in these two symbioses. Can J Bot 80 695–720 Occurrence Handle1:CAS:528:DC%2BD38XntlSrsrY%3D
FC Guinel TA LaRue (1992) ArticleTitleEthylene inhibitors partly restore nodulation to pea mutant E107 (brz). Plant Physiol 99 515–518 Occurrence Handle1:CAS:528:DyaK38XkvVKqtr0%3D Occurrence Handle16668916
FC Guinel LL Sloetjes (2000) ArticleTitleEthylene is involved in the nodulation phenotype of Pisum sativum R50 (sym16), a pleiotropic mutant that nodulates poorly and has pale green leaves. J Exp Bot 51 885–894 Occurrence Handle1:CAS:528:DC%2BD3cXjsl2mt7o%3D Occurrence Handle10948214
H Gundlach MJ Müller TM Kutchan MH Zenk (1992) ArticleTitleJasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci USA 89 2389–2393 Occurrence Handle1:CAS:528:DyaK38XisFagsb8%3D Occurrence Handle11607285
B Hause W Maier O Miersch R Kramell D Strack (2002) ArticleTitleInduction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130 1213–1220 Occurrence Handle1:CAS:528:DC%2BD38XovVOmsrg%3D Occurrence Handle12427988
R Heidstra YC Yang Y Yalcin S Peck AM Emons A van Kammen T Bisseling (1997) ArticleTitleEthylene 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 Occurrence Handle1:CAS:528:DyaK2sXjs1Kls7o%3D Occurrence Handle9165125
IE Henson CT Wheeler (1976) ArticleTitleHormones in plants bearing nitrogen-fixing root nodules: the distribution of cytokinins in Vicia faba L. New Phytol 76 433–439 Occurrence Handle1:CAS:528:DyaE28XktFOitLs%3D
IE Henson CT Wheeler (1977) ArticleTitleHormones in plants bearing nitrogen-fixing root nodules: gibberellin-like substances in Alnus glutinosa (L.) gaertn. New Phytol 78 373–381 Occurrence Handle1:CAS:528:DyaE2sXhsFaksL4%3D
K Himanen E Boucheron S Vanneste JD Engler D Inzé T Beeckman (2002) ArticleTitleAuxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14 2339–2351 Occurrence Handle1:CAS:528:DC%2BD38XotFels70%3D Occurrence Handle12368490
AM Hirsch TV Bhuvaneswari JG Torrey T Bisseling (1989) ArticleTitleEarly nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci USA 86 1244–1248 Occurrence Handle1:CAS:528:DyaL1MXhvV2mtrs%3D Occurrence Handle16594017
AM Hirsch Y Fang S Asad Y Kapulnik (1997) ArticleTitleThe role of phytohormones in plant-microbe symbioses. Plant Soil 194 171–184 Occurrence Handle1:CAS:528:DyaK2sXnt1Wns7g%3D
AM Hirsch Y Fang (1994) ArticleTitlePlant hormones and nodulation: What’s the connection? Plant Mol Biol 26 5–9 Occurrence Handle1:CAS:528:DyaK2MXitVKnt7w%3D Occurrence Handle7948898
AM Hirsch (1992) ArticleTitleDevelopmental biology of legume nodulation. New Phytol 122 211–237
WJ Hunter (2001) ArticleTitleInfluence of root-applied epibrassinolide and carbenoxolone on the nodulation and growth of soybean (Glycine max L.) seedlings. J Agron Crop Sci 186 217–221 Occurrence Handle1:CAS:528:DC%2BD3MXnvVCru70%3D
P Hutangura U Mathesius BG Rolfe MEK Jones (1999) ArticleTitleAuxin 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. Aust J Plant Physiol 26 221–231 Occurrence Handle1:CAS:528:DyaK1MXktlKht7c%3D
M Jacobs PH Rubery (1988) ArticleTitleNaturally occurring auxin transport regulators. Science 241 346–349 Occurrence Handle1:CAS:528:DyaL1cXkvV2rs7s%3D Occurrence Handle17734864
V Jaiswal SJH Rizvi D Mukerji SN Mature (1981) ArticleTitleCytokinins in root nodules of Phaseolus mungo. Ann Bot 48 301–305 Occurrence Handle1:CAS:528:DyaL38XkvV2gtg%3D%3D
J Jelenska J Deckert E Kondorosi AB Legocki (2000) ArticleTitleMitotic B-type cyclins are differentially regulated by phytohormones and during yellow lupine nodule development. Plant Sci 150 29–39 Occurrence Handle1:CAS:528:DC%2BD3cXlsFWmsw%3D%3D
M Jiang J Zhang (2001) ArticleTitleEffect of abscisic acid and active oxygen species, antioxidant defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42 1265–1273 Occurrence Handle1:CAS:528:DC%2BD3MXos1Oms74%3D Occurrence Handle11726712
JI Jimenez-Zurdo F Frugier MD Crespi A Kondorosi (2000) ArticleTitleExpression profiles of 22 novel molecular markers for organogenetic pathways acting in alfalfa nodule development. Mol Plant-Microbe Interact 13 96–106 Occurrence Handle1:CAS:528:DC%2BD3cXislSgtw%3D%3D Occurrence Handle10656590
W Jinsart B Ternai GM Polya (1991) ArticleTitleInhibition of wheat embryo calcium-dependent protein kinase and avian light chanin kinase by flavonoids and related compounds. Biol Chem Hoppe-Seyler 372 819–827 Occurrence Handle1:CAS:528:DyaK38Xjs1Omug%3D%3D Occurrence Handle1772594
PCL John K Zhang C Cong L Diederich F Wightman (1993) ArticleTitlep34cdc2 related proteins in control of cell cycle progression, the switch between division and differentiation in tissue development, and stimulation of division by auxin and cytokinin. Aust J Plant Physiol 20 503–526 Occurrence Handle1:CAS:528:DyaK2cXhvVOiur8%3D
Y Kanayama Y Yamamoto (1990) ArticleTitleInhibition of nitrogen fixation in soybean plants supplied with nitrate II. Accumulation and properties of nitrosylleghemoglobin in nodules. Plant Cell Physiol 31 207–214 Occurrence Handle1:CAS:528:DyaK3cXhvFGgtr8%3D
H Katznelson SE Cole (1965) ArticleTitleProduction of gibberellin-like substances by bacteria and actinomycetes. Can J Microbiol 11 733–741 Occurrence Handle1:CAS:528:DyaF2MXksFKntLk%3D Occurrence Handle5861292
M Kawaguchi H Imaizumi-Anraku S Fukai K Syono (1996) ArticleTitleUnusual branching in the seedlings of Lotus japonicus - gibberellins reveal the nitrogen-sensitive cell divisions within the pericycle on roots. Plant Cell Physiol 37 461–470 Occurrence Handle1:CAS:528:DyaK28Xjs1yisLY%3D
D Ke ME Saltveit (1988) ArticleTitlePlant hormone interaction and phenolic metabolism in the regulation of russet spotting in iceberg lettuce. Plant Physiol 88 1136–1140 Occurrence Handle1:CAS:528:DyaL1MXnsVWjtQ%3D%3D Occurrence Handle16666434
C Kistner M Parniske (2002) ArticleTitleEvolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7 511–518 Occurrence Handle1:CAS:528:DC%2BD38Xotlyltbs%3D Occurrence Handle12417152
R Kneer AA Poulev A Olesinski I Raskin (1999) ArticleTitleCharacterization of the elicitor-induced biosynthesis and secretion of genestein from roots of Lupinus luteus L. J Exp Bot 50 1553–1559 Occurrence Handle1:CAS:528:DyaK1MXms1Ogt74%3D
H Koltai M Dhandaydham C Opperman J Thomas D Bird (2001) ArticleTitleOverlapping plant signal transduction pathways induced by a parasitic nematode and a rhizobial endosymbiont. Mol Plant-Microbe Interact 14 1168–1177 Occurrence Handle1:CAS:528:DC%2BD3MXnsVeltLs%3D Occurrence Handle11605956
E Kondorosi B Hoffmann G Endre L Börge C Koncz D Dudits J Szecsi G Kiss A Kondorosi (1993) Involvement of hormones in nodule initiation: auxin sensitivity and hormone balance affect nodulation of Medicago. R Palacios J Mora E Newton (Eds) New Horizons in Nitrogen Fixation Kluwer Academic Publishers Dordrecht, The Netherlands 357
H Kouchi S Hata (1993) ArticleTitleIsolation and characterisation of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Gent 238 106–119 Occurrence Handle1:CAS:528:DyaK3sXlslOltLw%3D
H Kouchi K Takane RB So JK Ladha PM Reddy (1999) ArticleTitleRice ENOD40: isolation and expression analysis in rice and transgenic soybean root nodules. Plant J 18 121–129 Occurrence Handle1:CAS:528:DyaK1MXjs1ansbY%3D Occurrence Handle10363365
L Krusell LH Madsen S Sato G Aubert A Genua K Szczyglowski G Due T Kaneko S Tabata F de Bruijn E Pajuelo N Sandals J Stougaard (2002) ArticleTitleShoot control of root development and nodulation is mediated by a receptor kinase. Nature 420 422–426 Occurrence Handle1:CAS:528:DC%2BD38XptFCis7w%3D Occurrence Handle12442170
CGR Lawson BG Rolfe MA Djordjevic (1996) ArticleTitle Rhizobium inoculation induces condition-dependent changes in the flavonoid composition of root exudates from Trifolium subterraneum. Aust J Plant Physiol 23 93–101 Occurrence Handle1:CAS:528:DyaK28XhslanurY%3D
KH Lee TA LaRue (1992a) ArticleTitlePleiotropic effects of sym-17: a mutation in Pisum sativum L. cv Sparkle causes decreased nodulation, altered root and shoot growth, and increased ethylene production. Plant Physiol 100 1326–1333 Occurrence Handle1:CAS:528:DyaK3sXhvFCruw%3D%3D
KH Lee TA LaRue (1992b) ArticleTitleEthylene as a possible mediator of light- and nitrate-induced inhibition of nodulation of Pisum sativum L. cv Sparkle. Plant Physiol 100 1334–1338 Occurrence Handle1:CAS:528:DyaK3sXhvFCqsg%3D%3D
KH Lee TA LaRue (1992c) ArticleTitleExogenous ethylene inhibits nodulation of Pisum sativum L. cv 7 Sparkle. Plant Physiol 100 1759–1763 Occurrence Handle1:CAS:528:DyaK3sXnslWqsQ%3D%3D
TT Lee (1971) ArticleTitleCytokinin-controlled indoleacetic acid oxidase isoenzymes in tobacco callus cultures. Plant Physiol 47 181–185 Occurrence Handle1:CAS:528:DyaE3MXos1Kntg%3D%3D Occurrence Handle16657590
FGP Lhuissier NCA De Ruijter BJ Sieberer JJ Esseling AMC Emons (2001) ArticleTitleTime course of cell biological events evoked in legume root hairs by Rhizobium Nod factors: state of the art. Ann Bot 87 289–302 Occurrence Handle1:CAS:528:DC%2BD3MXht1artbk%3D
B Lian X Zhou M Miransari DL Smith (2000) ArticleTitleEffects of salicylic acid on the development and root nodulation of soybean seedlings. J Agron Crop Sci 185 187–192 Occurrence Handle1:CAS:528:DC%2BD3cXns1Gku78%3D
KR Libbenga PAA Harkes (1973) ArticleTitleInitial proliferation of cortical cells in the formation of root nodules in Pisum sativum L. Planta 114 17–28
KR Libbenga F van Iren RJ Bogers MF Schraag-Lamers (1973) ArticleTitleThe role of hormones and gradients in the initiation of cortex proliferation and nodule formation in Pisum sativum L. Planta 114 29–39 Occurrence Handle1:CAS:528:DyaE2cXnvFSnsw%3D%3D
F Ligero JM Caba C Lluch J Olivares (1991) ArticleTitleNitrate inhibition of nodulation can be overcome in the presence of the ethylene inhibitor, aminoethoxyvinylglycine. Plant Physiol 97 1221–1225 Occurrence Handle1:CAS:528:DyaK38XhvVGjsA%3D%3D Occurrence Handle16668512
F Ligero C Lluch J Olivares (1986) ArticleTitleEvolution of ethylene from roots of Medicago sativa plants inoculated with Rhizobium meliloti. J Plant Physiol 125 361–365 Occurrence Handle1:CAS:528:DyaL2sXhsFOlsg%3D%3D
E Logemann SC Wu J Schroder E Schmelzer IE Somssich K Hahlbrock (1995) ArticleTitleGene activation by UV light, fungal elicitor or fungal infection in Petroselinum crispum is correlated with repression of cell cycle-related genes. Plant J 8 865–876 Occurrence Handle1:CAS:528:DyaK28XosFahsA%3D%3D Occurrence Handle8580959
M-A Lorteau BJ Ferguson FC Guinel (2001) ArticleTitleEffects of cytokinin on ethylene production and nodulation in pea (Pisum sativum) cv. Sparkle. Physiol Plant 112 421–428 Occurrence Handle1:CAS:528:DC%2BD3MXlt1Kru70%3D Occurrence Handle11473700
CM Markwei TA LaRue (1997) ArticleTitlePhenotypic characterization of sym 21, a gene conditioning shoot-controlled inhibition of nodulation in Pisum sativum cv Sparkle. Physiol Plant 100 927–932 Occurrence Handle1:CAS:528:DyaK2sXlvFCitbc%3D
F Martinez-Abarca JA Herrera-Cervara P Bueno J Sanjuan T Bisseling J Olivares (1998) ArticleTitleInvolvement of salicylic acid in the establishment of the Rhizobium meliloti-alfalfa symbiosis. Mol Plant-Microbe Interact 11 153–155 Occurrence Handle1:CAS:528:DyaK1cXmsFWhsQ%3D%3D
CS Maskell JF Gibson PJ Dart (1977) ArticleTitleElectron-paramagnetic-resonance studies of leghaemoglobins from soya-beans and cowpea root nodules. Biochem J 167 435–445
U Mathesius (2001) ArticleTitleFlavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. J Exp Bot 52 419–426 Occurrence Handle1:CAS:528:DC%2BD3MXjs1ajsr4%3D Occurrence Handle11326048
U Mathesius C Bayliss JJ Weinman HRM Schlaman HP Spaink BG Rolfe ME McCully MA Djordjevic (1998b) ArticleTitleFlavonoids synthesised in cortical cells during nodule initiation are early developmental markers in white clover. Mol Plant-Microbe Interac 11 1223–1232 Occurrence Handle1:CAS:528:DyaK1cXnslyltbw%3D
U Mathesius C Charon BG Rolfe A Kondorosi M Crespi (2000) ArticleTitleTemporal 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 Occurrence Handle1:CAS:528:DC%2BD3cXjsFensbc%3D Occurrence Handle10830261
U Mathesius G Keijzers SHA Natera JJ Weinman MA Djordjevic BG Rolfe (2001) ArticleTitleEstablishment of a root proteome reference map for the model legume Medicago truncatula using the EST database for peptide mass fingerprinting. Proteomics 1 1424–1440 Occurrence Handle1:CAS:528:DC%2BD3MXpt1Gisro%3D Occurrence Handle11922602
U Mathesius HRM Schlaman HP Spaink C Sautter BG Rolfe MA Djordjevic (1998a) ArticleTitleAuxin transport inhibition precedes nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14 23–34 Occurrence Handle1:CAS:528:DyaK1cXjtV2is7o%3D
C Mathieu S Moreau P Frendo A Puppo MJ Davies (1998) ArticleTitleDirect detection of radicals in intact soybean nodules: presence of nitric oxide-leghemoglobin complexes. Free Radic Biol Med 24 1242–1249 Occurrence Handle1:CAS:528:DyaK1cXjsFWhtrY%3D Occurrence Handle9626580
HI McKhann F Frugier G Petrovics T Coba de la Peña E Jurkevitch S Brown E Kondorosi A Kondorosi M Crespi (1997) ArticleTitleCloning of a WD-repeat-containing gene from alfalfa (Medicago saliva): a role in hormone-mediated cell division? Plant Mol Biol 34 771–780 Occurrence Handle1:CAS:528:DyaK2sXlvFyrsbg%3D Occurrence Handle9278167
RB Mellor DB Collinge (1995) ArticleTitleA simple model based on known plant defence reactions is sufficient to explain most aspects of nodulation. J Exp Bot 46 1–18 Occurrence Handle1:CAS:528:DyaK2MXjslKiurk%3D
MG Mes (1959) ArticleTitleInfluence of gibberellic acid and photoperiod on the growth, flowering nodulation and nitrogen assimilation of Vicia villosa. Nature 184 2035–2036 Occurrence Handle1:CAS:528:DyaF3cXmvFSntg%3D%3D
E Miklashevichs H Rohrig J Schell J Schmidt (2001) ArticleTitlePerception and signal transduction of rhizobial NOD factors. Crit Rev Plant Sci 20 373–394 Occurrence Handle1:CAS:528:DC%2BD3MXmsVOnuro%3D
E Minami H Kouchi JR Cohn T Ogawa G Stacey (1996) ArticleTitleExpression of the early nodulin, ENOD40, in soybean roots in response to various lipo-chitin signal molecules. Plant J 10 23–32 Occurrence Handle1:CAS:528:DyaK28XltVamsbg%3D Occurrence Handle8758977
GK Muday A DeLong (2001) ArticleTitlePolar auxin transport: controlling where and how much. Trends Plant Sci 6 535–542 Occurrence Handle1:CAS:528:DC%2BD3MXovFGksLc%3D Occurrence Handle11701382
Y Murakami-Mizukami Y Yamamoto S Yamaki (1991) ArticleTitleAnalysis of indole acetic acid and abscisic acid contents in nodules of soybean plants bearing VA Mycorrhizas. Soil Sci Plant Nutr 37 291–298 Occurrence Handle1:CAS:528:DyaK3MXmt1ygt78%3D
A Murphy WA Peer L Taiz (2000) ArticleTitleRegulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211 315–324 Occurrence Handle1:CAS:528:DC%2BD3cXlsVWqs7o%3D Occurrence Handle10987549
W Newcomb K Syono JG Torrey (1976) ArticleTitleDevelopment of an ineffective pea root nodule: morphogenesis, fine structure, and cytokinin biosynthesis. Can J Bot 55 1891–1907
R Nishimura M Hayashi GJ Wu H Kouchi H Imaizumi-Anraku Y Murakami S Kawasaki S Akao M Ohmori N Nagasawa K Harada M Kawaguchi (2002a) ArticleTitleHAR1 mediates systemic regulation of symbiotic organ development. Nature 420 426–429 Occurrence Handle1:CAS:528:DC%2BD38XptFCis7k%3D
R Nishimura M Ohmori H Fujita M Kawaguchi (2002b) ArticleTitleA lotus basic leucine zipper protein with a RING-finger motif negatively regulates the developmental program of nodulation. Proc Natl Acad Sci USA 99 15206–15210 Occurrence Handle1:CAS:528:DC%2BD38Xpt1yqtLY%3D
R Nishimura M Ohmori M Kawaguchi (2002c) ArticleTitleThe novel symbiotic phenotype of enhanced-nodulating mutant of Lotus japonicus: astray mutant is an early nodulating mutant with wider nodulation zone. Plant Cell Physiol 43 853–859 Occurrence Handle1:CAS:528:DC%2BD38XmsFOktbY%3D
N Nukui H Ezura K-I Yuhashi T Yasuta K Minamisawa (2000) ArticleTitleEffects of ethylene precursor and inhibitors for ethylene biosynthesis and perception on nodulation in Lotus japonicus and Macroptilium atropurpureum. Plant Cell Physiol 41 893–897 Occurrence Handle1:CAS:528:DC%2BD3cXlt1WlurY%3D Occurrence Handle10965947
PS Nutman (1952) ArticleTitleStudies on the physiology of nodule formation III. Experiments on the excision of root-tips and nodules. Ann Bot 16 79–101 Occurrence Handle1:CAS:528:DyaG38XitlOksA%3D%3D
V Oke SR Long (1999) ArticleTitleBacterial genes induced within the nodule during the Rhizobium-legume symbiosis. Mol Microbiol 32 837–849 Occurrence Handle1:CAS:528:DyaK1MXjs1ent7k%3D Occurrence Handle10361286
GED Oldroyd EM Engstrom SR Long (2001) ArticleTitleEthylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell 13 1835–1849 Occurrence Handle1:CAS:528:DC%2BD3MXmsFKiu70%3D Occurrence Handle11487696
RV Penmetsa DR Cook (1997) ArticleTitleA legume ethylene-insensitive mutant hyperinfected by its Rhizobium symbiont. Science 275 527–530 Occurrence Handle1:CAS:528:DyaK2sXnvVekuw%3D%3D Occurrence Handle8999796
NK Peters DK Chris-Estes (1989) ArticleTitleNodule formation is stimulated by the ethylene inhibitor, aminoethoxyvinylglycine. Plant Physiol 91 690–693 Occurrence Handle1:CAS:528:DyaK3cXkslem Occurrence Handle16667088
DA Phillips JG Torrey (1970) ArticleTitleCytokinin production by Rhizobium japonicum. Physiol Plant 23 1057–1063 Occurrence Handle1:CAS:528:DyaE3MXivFWnsA%3D%3D
DA Phillips JG Torrey (1972) ArticleTitleStudies on cytokinin production by Rhizobium. Plant Physiol 49 11–15 Occurrence Handle1:CAS:528:DyaE38XktlOltg%3D%3D Occurrence Handle16657888
DA Phillips (1971) ArticleTitleAbscisic acid inhibition of root nodule initiation in Pisum sativum. Planta 100 181–190 Occurrence Handle1:CAS:528:DyaE38XitFyksw%3D%3D
H Porta P Rueda-Benitez F Campos JM Colmenaro-Flores JM Colorado MJ Carmona AA Covarrubias M Rocha-Sosa (1999) ArticleTitleAnalysis of lipoxygenase mRNA accumulation in the common bean (Phaseolus vulgaris L.) during development and under stress conditions. Plant Cell Physiol 40 850–858 Occurrence Handle1:CAS:528:DyaK1MXlsVOhsbw%3D Occurrence Handle10555305
A Puppo B Halliwell (1988) ArticleTitleGeneration of hydroxyl radicals by soybean nodule leghaemoglobin. Planta 173 405–410 Occurrence Handle1:CAS:528:DyaL1cXht1Ojtbc%3D
W Rademacher (1994) ArticleTitleGibberellin formation in microorganisms. Plant Growth Regul 15 303–314 Occurrence Handle1:CAS:528:DyaK2MXis1Cgurw%3D
M Radley (1961) ArticleTitleGibberellin-like substances in plants. Nature 191 684–685 Occurrence Handle1:CAS:528:DyaF38Xpt1yq Occurrence Handle13738974
SK Ramu HM Peng DR Cook (2002) ArticleTitleNod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. Mol Plant-Microbe Interac 15 522–528 Occurrence Handle1:CAS:528:DC%2BD38XktlSntr0%3D
MP Ramanujam V Abdul Jaleel G Kumaravelu (1998) ArticleTitleEffect of salicylic acid on nodulation, nitrogenous compounds and related enzymes of Vigna mungo. Biol Plant 41 307–311 Occurrence Handle1:CAS:528:DyaK1cXotVGksbY%3D
K Recourt AJ van Tunen LA Mur AAN van Brussel BJJ Lugtenberg JW Kijne (1992) ArticleTitleActivation of flavonoid biosynthesis in roots of Vicia sativa subsp. nigra plants by inoculation with Rhizobium leguminosarum biovar viciae. Plant Mol Biol 19 211–220
JR Redmond M Batley MA Djordjevic RW Innes PL Keumpel BG Rolfe (1986) ArticleTitleFlavones induce expression of nod genes in Rhizobium. Nature 323 632–635 Occurrence Handle1:CAS:528:DyaL2sXivVehtw%3D%3D
M Regvar N Gogala P Zalar (1996) ArticleTitleEffects of jasmonic acid on mycorrhizal Allium sativum. New Phytol 134 703–707 Occurrence Handle1:CAS:528:DyaK2sXls1yitA%3D%3D
B Relic X Perret MT Estrada-Garcia J Kopcinska W Golinowski H Krishnan SG Pueppke WJ Broughton (1994) ArticleTitleNod factors of Rhizobium are the key to the legume door. Mol Microbiol 13 171–178 Occurrence Handle1:CAS:528:DyaK2cXltVeqtL0%3D Occurrence Handle7984092
C Rice-Evans (2001) ArticleTitleFlavonoid antioxidants. Curr Med Chem 8 797–807 Occurrence Handle1:CAS:528:DC%2BD3MXjsVChtbc%3D Occurrence Handle11375750
RW Ridge GL Bender BG Rolfe (1992) ArticleTitleNodule-like structures induced on roots of wheat seedlings by addition of the synthetic auxin 2,4-dichlorophenoxyacetic acid and the effects of microorganisms. Aust J Plant Physiol 19 481–492 Occurrence Handle1:CAS:528:DyaK3sXjs1Sitg%3D%3D
LF Roddam WR Lewis-Henderson MA Djordjevic (2002) ArticleTitleTwo novel chromosomal loci influence cultivar-specific nodulation failure in the interaction between strain ANU794 and subterranean clover cv. Woogenellup. Funct Plant Biol 29 473–483 Occurrence Handle1:CAS:528:DC%2BD38XktF2ht7c%3D
C Rodrigez-Barrueco F Bermudez de Castro (1973) ArticleTitleCytokinin-induced pseudonodules on Alnus glutinosa. Physiol Plant 29 277–280
C Rodriguez-Barrueco C Miguel LMS Palni (1979) ArticleTitleCytokinins in root nodules of the nitrogen-fixing non-legume Myrica gale L. Z Pflanzenphysiol 95 275–278 Occurrence Handle1:CAS:528:DyaE1MXmtVOntrY%3D
H Röhrig J Schmidt E Miklashevichs J Schell M John (2002) ArticleTitleSoybean ENOD40 encodes two peptides that bind to sucrose synthase. Proc Natl Acad Sci USA 99 1915–1920 Occurrence Handle11842184
E Rojo R Solano JJ Sánchez-Serrano (2003) ArticleTitleInteractions between signalling compounds involved in plant defence. J Plant Growth Regul 22 22–22
JJ Ross DP O’Neil JJ Smith HJ Kerckhoffs RC Elliot (2000) ArticleTitleEvidence that auxin promotes gibberellin A1 biosynthesis in pea. Plant J 21 547–552 Occurrence Handle1:CAS:528:DC%2BD3cXjsVeru7g%3D Occurrence Handle10758505
JJ Ross (1998) ArticleTitleEffects of auxin transport inhibitors on gibberellin in pea. J Plant Growth Regul 17 141–146 Occurrence Handle1:CAS:528:DyaK1cXms1Ght74%3D
JA Ryals UH Neuenschwander MG Willits A Molina H-Y Steiner MD Hunt (1996) ArticleTitleSystemic acquired resistance. Plant Cell 8 1809–1819 Occurrence Handle1:CAS:528:DyaK28Xmsl2murw%3D Occurrence Handle12239363
P Salzer H Corbiere T Boller (1999) ArticleTitleHydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradicies. Planta 208 319–325 Occurrence Handle1:CAS:528:DyaK1MXjtlOgtbk%3D
JL Salzwedel FB Dazzo (1993) ArticleTitlepSym nod gene influence on elicitation of peroxidase activity from white clover and pea roots by rhizobia and their cell-free supernatants. Mol Plant-Microbe Interect 6 127–134 Occurrence Handle1:CAS:528:DyaK3sXitlSjtLo%3D
R Santos D Hérouart A Puppo D Touati (2000) ArticleTitleCritical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis. Mol Microbiol 38 750–759 Occurrence Handle1:CAS:528:DC%2BD3MXitFOr Occurrence Handle11115110
R Santos D Hérouart S Sigaud D Touati A Puppo (2001) ArticleTitleOxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol Plant-Microbe Interact 14 86–89 Occurrence Handle1:CAS:528:DC%2BD3MXot1Og Occurrence Handle11194876
T Sato H Fujikaki N Ohtake K Sueyoshi T Takahashi A Sato T Ohyama (2002) ArticleTitleEffect of exogenous salicylic acid on nodule formation of hypernodulating mutant and wild type of soybean. Soil Sci Plant Nutr 48 413–420 Occurrence Handle1:CAS:528:DC%2BD38XltFOrt7o%3D
B Scheres HI McKhann A Zalensky M Lobler T Bisseling AM Hirsch (1992) ArticleTitleThe PsENOD12 gene is expressed at two different sites in Afghanistan pea pseudonodules induced by auxin transport inhibitors. Plant Physiol 100 1649–1655 Occurrence Handle1:CAS:528:DyaK3sXnslWntA%3D%3D Occurrence Handle16653180
HRM Schlaman AA Gisel NEM Quaedvlieg GV Bloemberg BJJ Lugtenberg JW Kijne I Potrykus HP Spaink C Sautter (1997) ArticleTitleChitin oligosaccharides can induce cortical cell division in roots of Vicia sativa when delivered by ballistic microtargeting. Development 124 4887–4895 Occurrence Handle1:CAS:528:DyaK1cXit1Kisw%3D%3D Occurrence Handle9428425
J Schmid H Röhrig M John U Wienecke G Stacey C Koncz J Schell (1993) ArticleTitleAlteration of plant growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules. Plant J 4 651–658
JS Schmidt JE Harper TK Hoffman AF Bent (1999) ArticleTitleRegulation of soybean nodulation independent of ethylene signalling. Plant Physiol 119 951–959 Occurrence Handle1:CAS:528:DyaK1MXhvFymtbc%3D Occurrence Handle10069833
PE Schmidt WJ Broughton D Werner (1994) ArticleTitleNod-factors of Bradyrhizobium japonicum and Rhizobium sp. NGR234 induce flavonoid accumulation in soybean root exudate. Mol Plant-Microbe Interact 7 384–390 Occurrence Handle1:CAS:528:DyaK2cXlsFaqu70%3D
IR Searle AE Men T Laniya DM Buzas I Iturbe-Ormaetxe BJ Carroll PM Gresshoff (2003) ArticleTitleLong-distance signalling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299 109–112 Occurrence Handle1:CAS:528:DC%2BD38XpvVensLo%3D Occurrence Handle12411574
G Sinvany Y Kapulnik S Wininger H Badani E Jurkevitch (2002) ArticleTitleThe early nodulin enod40 is induced by, and also promotes arbuscular mycorrhizal root colonization. Physiol Mol Plant Pathol 60 103–109 Occurrence Handle1:CAS:528:DC%2BD38XktVyjsbo%3D
G Smit CC de Koster J Schripsema HP Spaink AA van Brussel JW Kijne (1995) ArticleTitleUridine, a 5 cell division factor in pea roots. Plant Mol Biol 29 869–873 Occurrence Handle1:CAS:528:DyaK28XitF2lsw%3D%3D Occurrence Handle8541512
C Sousa C Johansson C Charon H Manyani C Sautter A Kondorosi M Crespi (2001) ArticleTitleTranslational and structural requirements of the early nodulin gene enod40, a short-open reading frame-containing RNA, for elicitation of a cell-specific growth response in the alfalfa root cortex. Mol Cell Biol 21 354–366 Occurrence Handle1:CAS:528:DC%2BD3MXptVSk Occurrence Handle11113209
HP Spaink AHM Wijfjes TB Vanvliet JW Kijne BJJ Lugtenberg (1993) ArticleTitleRhizobial lipo-oligosaccharide signals and their role in plant morphogenesis. Are analogous lipophilic chitin derivatives produced by the plant? Aust J Plant Physiol 20 381–392 Occurrence Handle1:CAS:528:DyaK2cXhsFyktro%3D
HP Spaink (1999) Flavonoids as regulators of plant development: new insights from studies of plant-rhizobia interactions. R Verpoorte K Downum J Romeo (Eds) Recent Advances in Phytochemistry Interactions of Plants and Microorganisms vol. 32 167–178
G Stacey N Shibuya (1997) ArticleTitleChitin recognition in rice and legumes. Plant Soil 194 161–169 Occurrence Handle1:CAS:528:DyaK2sXnt1Wns78%3D
C Staehelin C Charon T Boller M Crespi A Kondorosi (2001) ArticleTitle Medicago truncatula plants overexpressing the early nodulin gene enod40 exhibit accelerated mycorrhizal colonization and enhanced formation of arbuscules. Proc Natl Acad Sci USA 98 15366–15371 Occurrence Handle1:CAS:528:DC%2BD38XpsVGm Occurrence Handle11752473
C Staehelin J Granado J Muller A Wiemken RB Mellor G Felix M Regenaas WJ Broughton T Boller (1994) ArticleTitlePerception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proc Natl Acad Sci USA 91 2196–2200 Occurrence Handle1:CAS:528:DyaK2cXitFalur0%3D Occurrence Handle8134372
HA Stafford (1997) ArticleTitleRoles of flavonoids in symbiotic and defence functions in legume roots. Bot Rev 63 27–39
G Stenlid (1976) ArticleTitleEffects of flavonoids on the polar transport of auxins. Physiol Plant 38 262–266 Occurrence Handle1:CAS:528:DyaE2sXosVKhuw%3D%3D
LC Stephenson TW Bunker WE Dubbs HD Grimes (1998) ArticleTitleSpecific soybean lipoxygenases localize to discrete subcellular compartments and their mRNAs are differentially regulated by source-sink status. Plant Physiol 116 923–933 Occurrence Handle1:CAS:528:DyaK1cXitVKqu78%3D Occurrence Handle9501125
J Stougaard (2001) ArticleTitleGenetics and genomics of root symbiosis. Curr Opin Plant Biol 4 328–335 Occurrence Handle1:CAS:528:DC%2BD3MXksVyktL0%3D Occurrence Handle11418343
S Stracke C Kistner S Yoshida L Mulder S Sato T Kaneko S Tabata N Sandal J Stougaard K Szczyglowski M Parniske (2002) ArticleTitleA plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417 959–962 Occurrence Handle1:CAS:528:DC%2BD38XkvVagsbg%3D Occurrence Handle12087405
JG Streeter (1988) ArticleTitleInhibition of legume nodule formation and N2 fixation by nitrate. Crit Rev Plant Sci 7 1–23 Occurrence Handle1:CAS:528:DyaL1MXnt1CgtQ%3D%3D
N Suganuma H Yamauchi K Yamamoto (1995) ArticleTitleEnhanced production of ethylene by soybean roots after inoculation with Bradyrhizobium japonicum. Plant Sci 111 163–168 Occurrence Handle1:CAS:528:DyaK2MXptVemur4%3D
JC Suttle (1988) ArticleTitleEffect of ethylene treatment on polar IAA transport, net IAA uptake and specific binding of N-1-naphthylphthalamic acid in tissues and microsomes isolated from etiolated pea epicotyls. Plant Physiol 88 795–799 Occurrence Handle1:CAS:528:DyaL1MXkslOm Occurrence Handle16666386
K Syono W Newcomb JG Torrey (1976) ArticleTitleCytokinin production in relation to the development of pea root nodules. Can J Bot 54 2155–2162 Occurrence Handle1:CAS:528:DyaE28XlsFKlsbo%3D
KV Thimann (1936) ArticleTitleOn the physiology of the formation of nodules on legumes roots. Proc Natl Acad Sci USA 22 511–513 Occurrence Handle1:CAS:528:DyaA2sXjvVektw%3D%3D Occurrence Handle16577735
GA Thurber JR Douglas AW Galston (1958) ArticleTitleInhibitory effects of gibberellins on nodulation in dwarf beans, Phaseolous vulgaris. Nature 181 1082–1083 Occurrence Handle1:CAS:528:DyaG1cXpvFyjtA%3D%3D
JC Trinchant J Rigaud (1982) ArticleTitleNitrite and nitric oxide as inhibitors of nitrogenase from soybean bacteroids. Appl Environ Microbiol 44 1385–1388 Occurrence Handle1:CAS:528:DyaL3sXjtFajtg%3D%3D Occurrence Handle16346155
EW Triplett JJ Heitholt KB Evensen DG Blevins (1981) ArticleTitleIncrease in internode length in Paseolus lunatus L. caused by inoculation with a nitrate reductase-deficient strain of Rhizobium sp. Plant Physiol 67 1–4 Occurrence Handle1:CAS:528:DyaL3MXotVemtA%3D%3D Occurrence Handle16661605
G Truchet DG Barker S Camut F de Billy J Vasse T Huguet (1989) ArticleTitleAlfalfa nodulation in the absence of Rhizobium. Mol Gen Genet 219 65–68 Occurrence Handle1:CAS:528:DyaK3cXlt1CjtQ%3D%3D
G Truchet P Roche P Lerouge J Vasse S Camut F de Billy J-C Promé J Dénarié (1991) ArticleTitleSulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351 670–673 Occurrence Handle1:CAS:528:DyaK3MXltlWmsbo%3D
RE Tully P van Berkum KW Lovins DL Keister (1998) ArticleTitleIdentification and sequencing of a cytochrome P450 gene cluster from Bradyrhizobium japonicum. Biochim Biophys Acta 1398 243–255 Occurrence Handle1:CAS:528:DyaK1cXkt1yiurc%3D Occurrence Handle9655913
AAN van Brussel T Tak KJM Boot JW Kijne (2002) ArticleTitleAutoregulation of root nodule formation: signals of both symbiotic partners studied in a split-root system of Vicia sativa subsp. nigra. Mol Plant-Microbe Interact 15 341–349 Occurrence Handle1:CAS:528:DC%2BD38XivV2mt7o%3D Occurrence Handle12026172
PPG van der Holst HRM Schlaman HP Spaink (2001) ArticleTitleProteins involved in the production and perception of oligosaccharides in relation to plant and animal development. Curr Opin Struct Biol 11 608–616 Occurrence Handle1:CAS:528:DC%2BD3MXntlyisLs%3D Occurrence Handle11785763
PC van Spronsen AAN van Brussel JW Kijne (1995) ArticleTitleNod-factors produced by Rhizobium leguminosarum biovar. viciae induce ethylene-related changes in root cortical cells of Vicia sativa subsp. nigra. Eur J Cell Biol 68 463–469 Occurrence Handle1:STN:280:DyaK283ksFyjtw%3D%3D Occurrence Handle8690027
PC van Spronsen T Tak AMM Rood AAN van Brussel JW Kijne KJM Boot (2003) ArticleTitleSalicylic acid inhibits indeterminant-type nodulation but not determinant-type nodulation. Mol Plant Microbe Interact 16 83–91 Occurrence Handle1:CAS:528:DC%2BD38XpvVWgs7c%3D Occurrence Handle12580285
WAT van Workum AAN van Brussel T Tak CA Wijffelman JW Kijne (1995) ArticleTitleEthylene prevents nodulation of Vicia sativa ssp. nigra by exopolysaccharide-deficient mutants of Rhizobium leguminosarum bv. viciae. Mol Plant Microbe Interact 8 278–285 Occurrence Handle1:CAS:528:DyaK2MXls1Okurc%3D
BV Vardhini SSR Rao (1999) ArticleTitleEffect of brassinosteroids on nodulation and nitrogenase activity in groundnut (Arachis hypogaea L.). Plant Growth Regul 28 165–167 Occurrence Handle1:CAS:528:DyaK1MXmsFWht7g%3D
J Vasse F de Billy G Truchet (1993) ArticleTitleAbortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. Plant J 4 555–566
KL-C Wang H Li JR Ecker (2002) ArticleTitleEthylene biosynthesis and signalling networks. Plant Cell S131 S131–S151
SH Watts CT Wheeler JR Hillman AMM Berrie A Crozier VB Math (1983) ArticleTitleAbscisic acid in the nodulated root system of Alnus glutinosa. New Phytol 95 203–208 Occurrence Handle1:CAS:528:DyaL2cXjsFGm
CT Wheeler IE Henson ME McLaughlin (1979) ArticleTitleHormones in plants bearing actinomycete root nodules. Bot Gaz 140S 52–57
PM Williams M Sicardi De Mallorca (1982) ArticleTitleAbscisic acid and gibberellin-like substances in roots and root nodules of Glycine max. Plant Soil 65 19–26 Occurrence Handle1:CAS:528:DyaL38Xkt1Sktb0%3D
JP Wisniewski CD Gardner NJ Brewin (1999) ArticleTitleIsolation of lipoxygenase cDNA clones from pea nodule mRNA. Plant Mol Biol 39 775–783 Occurrence Handle1:CAS:528:DyaK1MXjtFSqs7g%3D Occurrence Handle10350091
JP Wisniewski EA Rathbun JP Knox NJ Brewin (2000) ArticleTitleInvolvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum. Mol Plant Microbe Interact 13 413–420 Occurrence Handle1:CAS:528:DC%2BD3cXitFOksb4%3D Occurrence Handle10755304
J Wopereis E Pajuelo FB Dazzo Q Jiang PM Gresshoff FJ de Bruijn J Stougaard K Szczyglowski (2000) ArticleTitleShort root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J 23 97–114 Occurrence Handle1:CAS:528:DC%2BD3cXlvFWnsrg%3D Occurrence Handle10929105
C Wu R Dickstein AJ Cary JH Norris (1996) ArticleTitleThe auxin transport inhibitor N-(1-naphthyl)phthalamic acid elicits pseudonodules on non-nodulating mutants of white sweetclover. Plant Physiol 110 501–510 Occurrence Handle1:CAS:528:DyaK28XhtF2msr8%3D Occurrence Handle12226200
WC Yang C de Blank I Maskiene H Hirt J Bakker A van Kammen H Franssen T Bisseling (1994) ArticleTitle Rhizobium Nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cell cycle is only completed in primordium formation. Plant Cell 6 1415–1426 Occurrence Handle1:CAS:528:DyaK2MXhvV2is78%3D Occurrence Handle7994175
WC Yang P Katinakis P Hendriks A Smolders F de Vries J Spee A van Kammen T Bisseling H Franssen (1993) ArticleTitleCharacterisation of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. Plant J 3 573–585 Occurrence Handle1:CAS:528:DyaK3sXltFSgtL4%3D Occurrence Handle8220464
K-I Yuhashi N Ichikawa H Ezura S Akao Y Minakawa N Nukui T Yasuta K Minamisawa (2000) ArticleTitleRhizobitoxine production by Bradyrhizobium elkanii enhances nodulation and competitiveness on Macroptilium atropurpureum. Appl Environ Microbiol 66 2658–2663 Occurrence Handle1:CAS:528:DC%2BD3cXjvFWnsbg%3D Occurrence Handle10831453
SAJ Zaat AAN van Brussel T Tak BJJ Lugtenberg JW Kijne (1989) ArticleTitleThe ethylene-inhibitor aminoethoxyvinylglycine restores normal nodulation by Rhizobium leguminosarum biovar. viciae on Vicia saliva subsp. nigra by suppressing the ‘Thick and short roots’ phenotype. Planta 177 141–150 Occurrence Handle1:CAS:528:DyaL1MXhvV2mtb4%3D
H Zhang A Jennings PW Barlow BG Forde (1999) ArticleTitleDual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96 6529–6534 Occurrence Handle1:CAS:528:DyaK1MXksFKktbc%3D Occurrence Handle10339622
JAS Zuanazzi PH Clergeot J-C Quirion HP Husson A Kondorosi P Ratet (1998) ArticleTitleProduction of Sinorhizobium meliloti nod gene activation and repressor flavonoids from Medicago sativa roots. Mol Plant Microbe Interact 11 784–794 Occurrence Handle1:CAS:528:DyaK1cXkslWht7o%3D
Acknowledgements
Due to the vast size of the topic, the authors have undoubtedly omitted some researchers’ work, for which we apologize. Financial support was provided to BJF by the Tasmanian International Research Scholarship and the Thomas Crawford Memorial Research Scholarship, both of the University of Tasmania, and to UM by the Australian Research Council.
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Ferguson, B., Mathesius, U. Signaling Interactions During Nodule Development . J Plant Growth Regul 22, 47–72 (2003). https://doi.org/10.1007/s00344-003-0032-9
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DOI: https://doi.org/10.1007/s00344-003-0032-9