Abstract
Several phytohormones have been reported to positively or negatively regulate the formation of nitrogen-fixing nodules in Lotus japonicus and other legumes. Auxin is important for root nodulation and required for cortical cell division. Because auxin accumulation was observed in the root of the L. japonicus mutant spontaneous nodule formation 2 (snf2), which has a gain-of-function mutation in a putative cytokinin receptor, it appears that auxin acts downstream of cytokinin signaling. Activation of cytokinin signaling is involved in the induction of root nodule formation. Ethylene, gibberellin (GA), and abscisic acid (ABA) inhibit the cortical cell divisions induced by cytokinin. ABA regulates nitrogen fixation activity through the control of nitric oxide levels. Though jasmonic acid (JA) is known as a negative regulator of nodulation, recent data suggest that it functions as a positive regulator over a certain range of concentrations. The increase in salicylic acid (SA) levels normally triggered as a defense response does not occur upon infection with compatible symbionts. LjCCD7-silenced L. japonicus plants, which were expected to have reduced concentrations of strigolactone, produced fewer nodules than the controls, suggesting that strigolactone promotes nodule formation in L. japonicus.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Bano A, Harper JE (2002) Plant growth regulators and phloem exudates modulate root nodulation of soybean. Funct Plant Biol 29:1299–1307
Cho M-J, Harper JE (1993) Effect of abscisic acid application on root isoflavonoid concentration and nodulation of wild-type and nodulation-mutant soybean plants. Plant Soil 152:145–149
Cooper JB, Long SR (1994) Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-Zeatin secretion. Plant Cell 6:215–225
Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci USA 92:4114–4119
de Billy F, Grosjean C, May S et al (2001) Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol Plant Microbe Interact 14:267–277
Dill A, Thomas SG, Hu J et al (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16:1392–1405
Ding Y, Kalo P, Yendrek C et al (2008) Abscisic acid coordinates Nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell 20:2681–2695
Ferguson BJ, Foo E, Ross JJ et al (2011) Relationship between gibberellin, ethylene and nodulation in Pisum sativum. New Phytol 189:829–842
Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 234:1073–1081
Foo E, Yoneyama K, Hugill C et al (2013) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6:76–87
González EM, Galvaz L, Arrese-Igor C (2001) Abscisic acid induces a decline in nitrogen fixation that involves leghaemoglobin, but is independent of sucrose synthase activity. J Exp Bot 52:285–293
Gresshoff PM (2003) Post-genomic insights into nodulation. Genome Biol 4:201
Gresshoff PM, Lohar D, Chan PK et al (2009) Genetic analysis of ethylene regulation of legume nodulation. Plant Sign Behav 4:818–823
Grichko VP, Glick BR (2000) Identification of DNA sequences that regulate the expression of the Enterobacter cloacae UW4 1-aminocyclopropane-1-carboxylic acid deaminase gene. Can J Microbiol 46:1159–1165
Heckmann AB, Sandal N, Bek AS et al (2011) Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol Plant Microbe Interact 24:1385–1395
Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem 42:1825–1831
Kaneko T, Nakamura Y, Sato S et al (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7:331–338
Kinkema M, Gresshoff PM (2008) Investigation of downstream signals of the soybean autoregulation of nodulation receptor kinase GmNARK. Mol Plant Microbe Interact 21:1337–1348
Krusell L, Madsen LH, Sato S et al (2002) Shoot control of root development is mediated by a receptor-like kinase. Nature 420:422–426
Lee KH, LaRue TA (1992) Exogenous ethylene inhibits nodulation of Pisum sativum L. cv Sparkle. Plant Physiol 100:1759–1763
Liu J, Novero M, Chamikhova T et al (2013) CAROTENOID CLEAVAGE DIOXYGENASE 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus. J Exp Bot 64:1967–1981
Lohar DP, Schaff JE, Laskey JG et al (2004) Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J 38:203–214
Lohar D, Stiller J, Kam J et al (2009) Ethylene insensitivity conferred by a mutated Arabidopsis ethylene receptor gene alters nodulation in transgenic Lotus japonicus. Ann Bot 104:277–285
Mabood F, Souleimanov A, Smith DL (2006) Jasmonates induce Nod factor production by Bradyrhizobium japonicum. Plant Physiol Biochem 44:759–765
Maekawa T, Maekawa-Yoshikawa M, Takeda N et al (2009) Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant J 58:183–194
MartÃnez-Abarca F, Herrera-Cervera JA, Bueno P et al (1998) Involvement of salicylic acid in the establishment of the Rhizobium meliloti-alfalfa symbiosis. Mol Plant Microbe Interact 11:153–155
McGinnis KM, Thomas SG, Soule JD et al (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120–1130
Murray JD, Karas BJ, Sato S et al (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315:101–104
Nakagawa T, Kawaguchi M (2006) Shoot-applied MeJA suppresses root nodulation in Lotus japonicus. Plant Cell Physiol 47:176–180
Nakatsukasa-Akune M, Yamashita K, Shimoda Y et al (2005) Suppression of root nodule formation by artificial expression of the TrEnodDR1 (coat protein of white clover cryptic virus 1) gene in Lotus japonicus. Mol Plant Microbe Interact 18:1069–1080
Nishimura R, Hayashi M, Wu GJ et al (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–429
Nukui N, Ezura H, Yuhashi K et al (2000) Effects of ethylene precursor and inhibitors for ethylene biosynthesis and perception on nodulation in Lotus japonicus and Macroptilium atropurpureum. Plant Cell Physiol 41:893–897
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 Physiol 45:427–435
Oldroyd GE, Engstrom EM, Long SR (2001) Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell 13:1835–1849
Op den Camp RH, De Mita S, Lillo A et al (2011) A phylogenetic strategy based on a legume-specific whole genome duplication yields symbiotic cytokinin type-A response regulators. Plant Physiol 157:2013–2022
Pacios-Bras C, Schlaman HR, Boot K et al (2003) Auxin distribution in Lotus japonicus during root nodule development. Plant Mol Biol 52:1169–1180
Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275:527–530
Penmetsa RV, Frugoli JA, Smith LS et al (2003) Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol 131:998–1008
Penmetsa RV, Uribe P, Anderson J et al (2008) The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. Plant J 55:580–595
Phillips DA (1971) Abscisic acid inhibition of root nodule initiation in Pisum sativum. Planta 100:181–190
Rosas S, Soria R, Correa N et al (1998) Jasmonic acid stimulates the expression of nod genes in Rhizobium. Plant Mol Biol 38:1161–1168
Schmidt JS, Harper JE, Hoffman TK et al (1999) Regulation of soybean nodulation independent of ethylene signaling. Plant Physiol 119:951–960
Seo HS, Li J, Lee S-Y et al (2007) The hypernodulating nts mutation induces jasmonate synthetic pathway in soybean leaves. Mol Cells 24:185–193
Shimoda Y, Shimoda-Sasakura F, Kucho K et al (2009) Overexpression of class 1 plant hemoglobin genes enhances symbiotic nitrogen fixation activity between Mesorhizobium loti and Lotus japonicus. Plant J 57:254–263
Soto MJ, Fernández-Aparicio M, Castellanos-Morales V et al (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42:383–385
Stacey G, McAlvin CB, Kim SY et al (2006) Effects of endogenous salicylic acid on nodulation in the model legumes Lotus japonicus and Medicago truncatula. Plant Physiol 141:1473–1481
Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J 48:261–273
Sun J, Cardoza V, Mitchell DM et al (2006) Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J 46:961–970
Suzaki T, Yano K, Ito M et al (2012) Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development 139:3997–4006
Suzuki A, Akune M, Kogiso M et al (2004) Control of nodule number by the phytohormone abscisic acid in the roots of two leguminous species. Plant Cell Physiol 45:914–922
Suzuki A, Suriyagoda L, Shigeyama T et al (2011) Lotus japonicus nodulation is photomorphogenetically controlled by sensing the red/far red (R/FR) ratio through jasmonic acid (JA) signaling. Proc Natl Acad Sci USA 108:16837–16842
Takanashi K, Sugiyama A, Yazaki K (2011) Involvement of auxin distribution in root nodule development of Lotus japonicus. Planta 234:73–81
Thimann KV (1936) On the physiology of the formation of nodules on legumes roots. Proc Natl Acad Sci USA 22:511–514
Tirichine L, Sandal N, Madsen LH et al (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107
Tominaga A, Nagata M, Futsuki K et al (2009) Enhanced nodulation and nitrogen fixation in the abscisic acid low-sensitive mutant enhanced nitrogen fixation1 of Lotus japonicus. Plant Physiol 151:1965–1976
Trinchant JC, Rigaud J (1982) Nitrite and nitric oxide as inhibitors of nitrogenase from soybean bacteroids. Appl Environ Microbiol 44:1385–1388
Uchiumi T, Ohwada T, Itakura M et al (2004) Expression islands clustered on the symbiosis island of the Mesorhizobium loti genome. J Bacteriol 186:2439–2448
van Spronsen PC, Tak T, Rood AMM et al (2003) Salicylic acid inhibits indeterminate-type nodulation but not determinate-type nodulation. Mol Plant Microbe Interact 16:83–91
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Suzuki, A. (2014). Hormone Regulation of Root Nodule Formation in Lotus. In: Tabata, S., Stougaard, J. (eds) The Lotus japonicus Genome. Compendium of Plant Genomes. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-44270-8_9
Download citation
DOI: https://doi.org/10.1007/978-3-662-44270-8_9
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-662-44269-2
Online ISBN: 978-3-662-44270-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)