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PLANT CELL 19 (4): 1221-1234

Copyright © 2007 by the American Society of Plant Physiologists.

An ERF Transcription Factor in Medicago truncatula That Is Essential for Nod Factor Signal Transduction[W]

Patrick H. Middletona,1, Júlia Jakabb,1, R. Varma Penmetsac,1, Colby G. Starkerd,2, Jake Dolld, Péter Kalóa,b, Radhika Prabhuc, John F. Marsha, Raka M. Mitrad, Attila Kereszte, Brigitta Dudasb, Kathryn VandenBoschf, Sharon R. Longd, Doug R. Cookc, Gyorgy B. Kissb,e, and Giles E.D. Oldroyda,3

a Department of Disease and Stress Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom
b Agricultural Biotechnology Centre, 2100 Gödöllo, Hungary
c Department of Plant Pathology, University of California, Davis, California 95616
d Department of Biological Sciences, Stanford University, Stanford, California 94305
e Institute of Genetics, Biological Research Center, 6726 Szeged, Hungary
f Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108

3 To whom correspondence should be addressed. E-mail giles.oldroyd{at}; fax 44-1603-450045.

Abstract: Rhizobial bacteria activate the formation of nodules on the appropriate host legume plant, and this requires the bacterial signaling molecule Nod factor. Perception of Nod factor in the plant leads to the activation of a number of rhizobial-induced genes. Putative transcriptional regulators in the GRAS family are known to function in Nod factor signaling, but these proteins have not been shown to be capable of direct DNA binding. Here, we identify an ERF transcription factor, ERF Required for Nodulation (ERN), which contains a highly conserved AP2 DNA binding domain, that is necessary for nodulation. Mutations in this gene block the initiation and development of rhizobial invasion structures, termed infection threads, and thus block nodule invasion by the bacteria. We show that ERN is necessary for Nod factor–induced gene expression and for spontaneous nodulation activated by the calcium- and calmodulin-dependent protein kinase, DMI3, which is a component of the Nod factor signaling pathway. We propose that ERN is a component of the Nod factor signal transduction pathway and functions downstream of DMI3 to activate nodulation gene expression.

The CCAAT box-binding transcription factor NF-YA1 controls rhizobial infection.
P. Laporte, A. Lepage, J. Fournier, O. Catrice, S. Moreau, M.-F. Jardinaud, J.-H. Mun, E. Larrainzar, D. R. Cook, P. Gamas, et al. (2014)
J. Exp. Bot. 65, 481-494
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Lotus japonicus Cytokinin Receptors Work Partially Redundantly to Mediate Nodule Formation.
M. Held, H. Hou, M. Miri, C. Huynh, L. Ross, M. S. Hossain, S. Sato, S. Tabata, J. Perry, T. L. Wang, et al. (2014)
PLANT CELL 26, 678-694
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The C2H2 Transcription Factor REGULATOR OF SYMBIOSOME DIFFERENTIATION Represses Transcription of the Secretory Pathway Gene VAMP721a and Promotes Symbiosome Development in Medicago truncatula.
S. Sinharoy, I. Torres-Jerez, K. Bandyopadhyay, A. Kereszt, C. I. Pislariu, J. Nakashima, V. A. Benedito, E. Kondorosi, and M. K. Udvardi (2013)
PLANT CELL 25, 3584-3601
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Rhizobial and Mycorrhizal Symbioses in Lotus japonicus Require Lectin Nucleotide Phosphohydrolase, Which Acts Upstream of Calcium Signaling.
N. J. Roberts, G. Morieri, G. Kalsi, A. Rose, J. Stiller, A. Edwards, F. Xie, P. M. Gresshoff, G. E. D. Oldroyd, J. A. Downie, et al. (2013)
Plant Physiology 161, 556-567
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Medicago truncatula ERN Transcription Factors: Regulatory Interplay with NSP1/NSP2 GRAS Factors and Expression Dynamics throughout Rhizobial Infection.
M. R. Cerri, L. Frances, T. Laloum, M.-C. Auriac, A. Niebel, G. E. D. Oldroyd, D. G. Barker, J. Fournier, and F. de Carvalho-Niebel (2012)
Plant Physiology 160, 2155-2172
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A Phaseolus vulgaris NADPH Oxidase Gene is Required for Root Infection by Rhizobia.
J. Montiel, N. Nava, L. Cardenas, R. Sanchez-Lopez, M.-K. Arthikala, O. Santana, F. Sanchez, and C. Quinto (2012)
Plant Cell Physiol. 53, 1751-1767
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Rapid Phosphoproteomic and Transcriptomic Changes in the Rhizobia-legume Symbiosis.
C. M. Rose, M. Venkateshwaran, J. D. Volkening, P. A. Grimsrud, J. Maeda, D. J. Bailey, K. Park, M. Howes-Podoll, D. den Os, L. H. Yeun, et al. (2012)
Mol. Cell. Proteomics 11, 724-744
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Two Direct Targets of Cytokinin Signaling Regulate Symbiotic Nodulation in Medicago truncatula.
F. Ariel, M. Brault-Hernandez, C. Laffont, E. Huault, M. Brault, J. Plet, M. Moison, S. Blanchet, J. L. Ichante, M. Chabaud, et al. (2012)
PLANT CELL 24, 3838-3852
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Transcriptional Responses toward Diffusible Signals from Symbiotic Microbes Reveal MtNFP- and MtDMI3-Dependent Reprogramming of Host Gene Expression by Arbuscular Mycorrhizal Fungal Lipochitooligosaccharides.
L. F. Czaja, C. Hogekamp, P. Lamm, F. Maillet, E. A. Martinez, E. Samain, J. Denarie, H. Kuster, and N. Hohnjec (2012)
Plant Physiology 159, 1671-1685
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A Medicago truncatula Tobacco Retrotransposon Insertion Mutant Collection with Defects in Nodule Development and Symbiotic Nitrogen Fixation.
C. I. Pislariu, J. D. Murray, J. Wen, V. Cosson, R. R. D. Muni, M. Wang, V. A. Benedito, A. Andriankaja, X. Cheng, I. T. Jerez, et al. (2012)
Plant Physiology 159, 1686-1699
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The Small GTPase ROP6 Interacts with NFR5 and Is Involved in Nodule Formation in Lotus japonicus.
D. Ke, Q. Fang, C. Chen, H. Zhu, T. Chen, X. Chang, S. Yuan, H. Kang, L. Ma, Z. Hong, et al. (2012)
Plant Physiology 159, 131-143
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WUSCHEL-RELATED HOMEOBOX5 Gene Expression and Interaction of CLE Peptides with Components of the Systemic Control Add Two Pieces to the Puzzle of Autoregulation of Nodulation.
M. A. Osipova, V. Mortier, K. N. Demchenko, V. E. Tsyganov, I. A. Tikhonovich, L. A. Lutova, E. A. Dolgikh, and S. Goormachtig (2012)
Plant Physiology 158, 1329-1341
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LegumeIP: an integrative database for comparative genomics and transcriptomics of model legumes.
J. Li, X. Dai, T. Liu, and P. X. Zhao (2012)
Nucleic Acids Res. 40, D1221-D1229
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Laser Microdissection Unravels Cell-Type-Specific Transcription in Arbuscular Mycorrhizal Roots, Including CAAT-Box Transcription Factor Gene Expression Correlating with Fungal Contact and Spread.
C. Hogekamp, D. Arndt, P. A. Pereira, J. D. Becker, N. Hohnjec, and H. Kuster (2011)
Plant Physiology 157, 2023-2043
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A Novel Interaction between CCaMK and a Protein Containing the Scythe_N Ubiquitin-Like Domain in Lotus japonicus.
H. Kang, H. Zhu, X. Chu, Z. Yang, S. Yuan, D. Yu, C. Wang, Z. Hong, and Z. Zhang (2011)
Plant Physiology 155, 1312-1324
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A C Subunit of the Plant Nuclear Factor NF-Y Required for Rhizobial Infection and Nodule Development Affects Partner Selection in the Common Bean-Rhizobium etli Symbiosis.
M. E. Zanetti, F. A. Blanco, M. P. Beker, M. Battaglia, and O. M. Aguilar (2010)
PLANT CELL 22, 4142-4157
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The B-3 Ethylene Response Factor MtERF1-1 Mediates Resistance to a Subset of Root Pathogens in Medicago truncatula without Adversely Affecting Symbiosis with Rhizobia.
J. P. Anderson, J. Lichtenzveig, C. Gleason, R. P. Oliver, and K. B. Singh (2010)
Plant Physiology 154, 861-873
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How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground.
H. Kouchi, H. Imaizumi-Anraku, M. Hayashi, T. Hakoyama, T. Nakagawa, Y. Umehara, N. Suganuma, and M. Kawaguchi (2010)
Plant Cell Physiol. 51, 1381-1397
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NENA, a Lotus japonicus Homolog of Sec13, Is Required for Rhizodermal Infection by Arbuscular Mycorrhiza Fungi and Rhizobia but Dispensable for Cortical Endosymbiotic Development.
M. Groth, N. Takeda, J. Perry, H. Uchida, S. Draxl, A. Brachmann, S. Sato, S. Tabata, M. Kawaguchi, T. L. Wang, et al. (2010)
PLANT CELL 22, 2509-2526
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CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically.
V. Mortier, G. Den Herder, R. Whitford, W. Van de Velde, S. Rombauts, K. D'haeseleer, M. Holsters, and S. Goormachtig (2010)
Plant Physiology 153, 222-237
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Plant flotillins are required for infection by nitrogen-fixing bacteria.
C. H. Haney and S. R. Long (2010)
PNAS 107, 478-483
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Legume Transcription Factor Genes: What Makes Legumes So Special?.
M. Libault, T. Joshi, V. A. Benedito, D. Xu, M. K. Udvardi, and G. Stacey (2009)
Plant Physiology 151, 991-1001
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A Nuclear-Targeted Cameleon Demonstrates Intranuclear Ca2+ Spiking in Medicago truncatula Root Hairs in Response to Rhizobial Nodulation Factors.
B. J. Sieberer, M. Chabaud, A. C. Timmers, A. Monin, J. Fournier, and D. G. Barker (2009)
Plant Physiology 151, 1197-1206
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Large-Scale Analysis of Putative Soybean Regulatory Gene Expression Identifies a Myb Gene Involved in Soybean Nodule Development.
M. Libault, T. Joshi, K. Takahashi, A. Hurley-Sommer, K. Puricelli, S. Blake, R. E. Finger, C. G. Taylor, D. Xu, H. T. Nguyen, et al. (2009)
Plant Physiology 151, 1207-1220
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LIN, a Novel Type of U-Box/WD40 Protein, Controls Early Infection by Rhizobia in Legumes.
E. Kiss, B. Olah, P. Kalo, M. Morales, A. B. Heckmann, A. Borbola, A. Lozsa, K. Kontar, P. Middleton, J. A. Downie, et al. (2009)
Plant Physiology 151, 1239-1249
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A Small GTPase of the Rab Family Is Required for Root Hair Formation and Preinfection Stages of the Common Bean-Rhizobium Symbiotic Association.
F. A. Blanco, E. Peltzer Meschini, M. E. Zanetti, and O. M. Aguilar (2009)
PLANT CELL 21, 2797-2810
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Calcium Spiking Patterns and the Role of the Calcium/Calmodulin-Dependent Kinase CCaMK in Lateral Root Base Nodulation of Sesbania rostrata.
W. Capoen, J. Den Herder, J. Sun, C. Verplancke, A. De Keyser, R. De Rycke, S. Goormachtig, G. Oldroyd, and M. Holsters (2009)
PLANT CELL 21, 1526-1540
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GRAS Proteins Form a DNA Binding Complex to Induce Gene Expression during Nodulation Signaling in Medicago truncatula.
S. Hirsch, J. Kim, A. Munoz, A. B. Heckmann, J. A. Downie, and G. E.D. Oldroyd (2009)
PLANT CELL 21, 545-557
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Nodulation Signaling in Legumes Depends on an NSP1-NSP2 Complex.
N. A. Eckardt (2009)
PLANT CELL 21, 367
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Antiquity and Function of CASTOR and POLLUX, the Twin Ion Channel-Encoding Genes Key to the Evolution of Root Symbioses in Plants.
C. Chen, C. Fan, M. Gao, and H. Zhu (2009)
Plant Physiology 149, 306-317
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How CYCLOPS keeps an eye on plant symbiosis.
W. Capoen and G. Oldroyd (2008)
PNAS 105, 20053-20054
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De Novo Organ Formation from Differentiated Cells: Root Nodule Organogenesis.
M. Crespi and F. Frugier (2008)
Science Signaling 1, re11
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Abscisic Acid Coordinates Nod Factor and Cytokinin Signaling during the Regulation of Nodulation in Medicago truncatula.
Y. Ding, P. Kalo, C. Yendrek, J. Sun, Y. Liang, J. F. Marsh, J. M. Harris, and G. E.D. Oldroyd (2008)
PLANT CELL 20, 2681-2695
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EFD Is an ERF Transcription Factor Involved in the Control of Nodule Number and Differentiation in Medicago truncatula.
T. Vernie, S. Moreau, F. de Billy, J. Plet, J.-P. Combier, C. Rogers, G. Oldroyd, F. Frugier, A. Niebel, and P. Gamas (2008)
PLANT CELL 20, 2696-2713
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A Positive Regulatory Role for LjERF1 in the Nodulation Process Is Revealed by Systematic Analysis of Nodule-Associated Transcription Factors of Lotus japonicus.
E. Asamizu, Y. Shimoda, H. Kouchi, S. Tabata, and S. Sato (2008)
Plant Physiology 147, 2030-2040
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Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes.
S. Kosuta, S. Hazledine, J. Sun, H. Miwa, R. J. Morris, J. A. Downie, and G. E. D. Oldroyd (2008)
PNAS 105, 9823-9828
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The Transcription Factor MtSERF1 of the ERF Subfamily Identified by Transcriptional Profiling Is Required for Somatic Embryogenesis Induced by Auxin Plus Cytokinin in Medicago truncatula.
F. R. Mantiri, S. Kurdyukov, D. P. Lohar, N. Sharopova, N. A. Saeed, X.-D. Wang, K. A. VandenBosch, and R. J. Rose (2008)
Plant Physiology 146, 1622-1636
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Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant.
K. M. Jones, N. Sharopova, D. P. Lohar, J. Q. Zhang, K. A. VandenBosch, and G. C. Walker (2008)
PNAS 105, 704-709
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AP2-ERF Transcription Factors Mediate Nod Factor Dependent Mt ENOD11 Activation in Root Hairs via a Novel cis-Regulatory Motif.
A. Andriankaja, A. Boisson-Dernier, L. Frances, L. Sauviac, A. Jauneau, D. G. Barker, and F. de Carvalho-Niebel (2007)
PLANT CELL 19, 2866-2885
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