ABCDEFGHIJKLMNOPQRSTUVWXYZ
1
Gene Symbol
Phenotypic Defect
Reference
Protein class/Molecular function
Gene Name
Alternate names
Mutagen
Medicago Gene ID
ProbesetLotus Gene ID
Soybean Gene ID
Phaseolus Gene ID
Myc Phenotype
NotesReference
2
Infection
Nodule Organogenesis
Fixation
3
GmACPn/aNod+/-n/aWang et al., 2014Carrier proteinACYL CARRIER PROTEIN (ACP)RNAi
Medtr7g080390
Mtr.48571.1.S1_at
Lj1g3v2840250
Glyma.18G244300
Phvul.008G052400
n/a
Wang, J., Tóth, K., Tanaka, K., Nguyen, C.T., Yan, Z., Brechenmacher, L., Dahmen, J., Chen, M., Thelen, J.J., and Qiu, L. (2014). A soybean acyl carrier protein, GmACP, is important for root nodule symbiosis. Molecular Plant-Microbe Interactions 27, 415-423.
4
PvAGO5, GmAGO5
Inf-
Nod+/-, White++
n/aReyero-Saavedra et al., 2017
Multidomain protein (RNA silencing)
ARGONAUTE 5 (AGO5)RNAi
Medtr4g056430, Medtr4g056470
Mtr.45521.1.S1_at
Lj0g3v0169039.1
Glyma.12G083500
Phvul.011G088200
n/a
Reyero-Saavedra, M., Qiao, Z., Sánchez-Correa, M., Díaz-Pineda, M., Reyes, J., Covarrubias, A., Libault, M., and Valdés-López, O. (2017). Gene silencing of ARGONAUTE5 negatively affects the establishment of the legume-rhizobia symbiosis. Genes 8, 352.
5
LjAMSHInf+/-, Inf*Nod+/-Fix*Malolepszy et al., 2015
Enzyme (Metalloprotease; Deubiquitinating)
ASSOCIATED MOLECULE WITH THE SH3 DOMAIN OF STAM (AMSH)
LORE1
Medtr6g083940
Mtr.21924.1.S1_at; Mtr.21925.1.S1_s_at
Lj2g3v0721190
Glyma.07G093100
Phvul.003G094300
Myc+
Małolepszy, A., Urbański, D.F., James, E.K., Sandal, N., Isono, E., Stougaard, J., and Andersen, S.U. (2015). The deubiquitinating enzyme AMSH 1 is required for rhizobial infection and nodule organogenesis in Lotus japonicus. The Plant Journal 83, 719-731.
6
LjAMT1.1n/aNod++Fix+/-Rogato et al., 2008
Transporter (Ammonium)
AMMONIUM TRANSPORTER 1.1 (AMT1.1)
Antisense
Medtr1g045550
Mtr.10556.1.S1_at
Lj5g3v1314550, Lj0g3v0302059
Glyma.10G132300
Phvul.007G231700
n/a
Rogato, A., D’Apuzzo, E., Barbulova, A., Omrane, S., Stedel, C., Simon-Rosin, U., Katinakis, P., Flemetakis, M., Udvardi, M., and Chiurazzi, M. (2008). Tissue-specific down-regulation of LjAMT1; 1 compromises nodule function and enhances nodulation in Lotus japonicus. Plant molecular biology 68, 585.
7
PvANN1Inf+/-Nod+/-Fix+/-Carrasco-castilla et al., 2018
Membrane binding protein
ANNEXIN1 (ANN1)RNAi
Medtr8g038210
Mtr.14183.1.S1_at
Lj0g3v0203419
Glyma.13G199800
Phvul.011G209300
n/a
Carrasco-Castilla, J., Ortega-Ortega, Y., Jáuregui-Zúñiga, D., Juárez-Verdayes, M.A., Arthikala, M.-K., Monroy-Morales, E., Nava, N., Santana, O., Sánchez-López, R., and Quinto, C. (2018). Down-regulation of a Phaseolus vulgaris annexin impairs rhizobial infection and nodulation. Environmental and Experimental Botany 153, 108-119.
8
LjAPN1n/aNod+, Nod*Fix-Yamaya-Ito et al., 2018
Enzyme (Aspartyl protease)
ASPARTIC PEPTIDASE NODULE-INDUCED 1 (APN1)
Ljsym104
Somaclonal mutagenesis
Medtr0036s0070
Mtr.8869.1.S1_at
Lotus Chromosome 3 LC279017.1
Glyma.08G166200
Phvul.005G050500
n/a
Yamaya‐Ito, H., Shimoda, Y., Hakoyama, T., Sato, S., Kaneko, T., Hossain, M.S., Shibata, S., Kawaguchi, M., Hayashi, M., and Kouchi, H. (2018). Loss‐of‐function of ASPARTIC PEPTIDASE NODULE‐INDUCED 1 (APN 1) in Lotus japonicus restricts efficient nitrogen‐fixing symbiosis with specific Mesorhizobium loti strains. The Plant Journal 93, 5-16.
9
MtARF16aInf+/-Nod+n/aBreakspear et al., 2014
TF (Auxin responsive)
AUXIN RESPONSE FACTOR 16a (ARF16a)
Tnt1
Medtr1g094960
Mtr.39233.1.S1_at
Lj5g3v1812820
Glyma.10G210600
Phvul.007G095000
n/a
Breakspear, A., Liu, C., Roy, S., Stacey, N., Rogers, C., Trick, M., Morieri, G., Mysore, K.S., Wen, J., and Oldroyd, G.E. (2014). The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. The Plant Cell 26, 4680-4701.
10
GmARF8a/GmARF8b
n/aNod++n/aWang et al., 2015
TF (Auxin responsive)
AUXIN RESPONSE FACTOR 16a (ARF8a/ARF8b)
RNAi
Medtr5g076270, Medtr5g076270
Mtr.5139.1.S1_at, Mtr.5198.1.S1_at
Lj2g3v2475530
Glyma.14G208500, Glyma.02G239600
Phvul.008G242400
n/a
Wang, Y., Li, K., Chen, L., Zou, Y., Liu, H., Tian, Y., Li, D., Wang, R., Zhao, F., and Ferguson, B.J. (2015). MicroRNA167-directed regulation of the auxin response factors GmARF8a and GmARF8b is required for soybean nodulation and lateral root development. Plant physiology 168, 984-999.
11
MtARP3n/an/aFix*Gavrin et al., 2015
TF (Auxin responsive)
ACTIN RELATED PROTEIN (ARP2/ARP3)RNAi
Medtr8g089630
Mtr.13778.1.S1_at
Lj4g3v2717070
Glyma.05G172600
Phvul.002G253600
n/a
Gavrin, A., Jansen, V., Ivanov, S., Bisseling, T., and Fedorova, E. (2015). ARP2/3-Mediated Actin Nucleation Associated With Symbiosome Membrane Is Essential for the Development of Symbiosomes in Infected Cells of Medicago truncatula Root Nodules. Mol Plant Microbe Interact 28, 605-614.
12
LjARPC1Inf+/-
Nod++, White++
n/aHossain et al., 2012
Multiprotein complex subunit (Actin nucleator)
ACTIN-RELATED PROTEIN COMPONENT1 (ARPC1)
EMS
Medtr3g049070
Mtr.37170.1.S1_at
Lj6g3v0925910
Glyma.10G216300
Phvul.005G127400
Myc+
Hossain, M.S., Liao, J., James, E.K., Sato, S., Tabata, S., Jurkiewicz, A., Madsen, L.H., Stougaard, J., Ross, L., and Szczyglowski, K. (2012). Lotus japonicus ARPC1 is required for rhizobial infection. Plant physiology 160, 917-928.
13
PvBECLIN1n/aNod+/-n/aEstrada-Navarrete et al., 2016
Multiprotein complex subunit (Autophagy related)
AUTOPHAGY RELATED PROTEINRNAiMedtr3g018770
Mtr.9470.1.S1_at
Lj0g3v0261969
Glyma.11G153900
Phvul.005G029900
n/a
Estrada-Navarrete, G., Cruz-Mireles, N., Lascano, R., Alvarado-Affantranger, X., Hernández-Barrera, A., Barraza, A., Olivares, J.E., Arthikala, M.-K., Cárdenas, L., and Quinto, C. (2016). An autophagy-related kinase is essential for the symbiotic relationship between Phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi. The Plant Cell 28, 2326-2341.
14
GmBCH1/GmBCH2
n/aNod*Fix+/-Kim et al., 2013
Enzyme (Hydroxylase)
β-CAROTENE HYDROXYLASE (BCH1/BCH2)
RNAi
Medtr6g048440, Medtr7g085180
Mtr.33915.1.S1_at, Mtr.50032.1.S1_at
Lj5g3v1988680, Lj0g3v0299729, Lj1g3v3948070 (BCH2), Lj1g3v3948060 (BCH2)
Glyma.10G231200, Glyma.16G043300
Phvul.004G108900, Phvul.001G099900, Phvul.001G100100
n/a
Kim, Y.-K., Kim, S., Um, J.-H., Kim, K., Choi, S.-K., Um, B.-H., Kang, S.-W., Kim, J.-W., Takaichi, S., and Song, S.-B. (2013). Functional implication of β-carotene hydroxylases in soybean nodulation. Plant physiology 162, 1420-1433.
15
GmBEHL1n/aNod++n/aYan et al., 2018
TF (Brassinosteroid pathway)
BES1/BZR1 HOMOLOG LIKE1Artificial miRNA
Medtr5g019550
Mtr.43192.1.S1_at
Lj2g3v1803080
Glyma.01G178000
Phvul.002G026700, Phvul.002G026800
n/a
Yan, Q., Wang, L., and Li, X. (2018). GmBEHL1, a BES1/BZR1 family protein, negatively regulates soybean nodulation. Scientific reports 8, 7614.
16
MtBG2Inf++Nod++n/aGaudioso-Pedraza et al., 2018
Enzyme (Glucanase)
β-1,3 -GLUCANASE (BG2)RNAi
Medtr3g083580
Mtr.20928.1.S1_at
Lj4g3v2604040
Glyma.17G202900
Phvul.001G056400
n/a
Gaudioso-Pedraza, R., Beck, M., Frances, L., Kirk, P., Ripodas, C., Niebel, A., Oldroyd, G.E., Benitez-Alfonso, Y., and de Carvalho-Niebel, F. (2018). Callose-regulated symplastic communication coordinates symbiotic root nodule development. Current Biology 28, 3562-3577. e3566
17
MtBHLH1n/aNod+Fix+Laurence Godiard et al., 2011
TF (bHLH motif containing)
BASIC HELIX–LOOP–HELIX 1 (BHLH1)CRES-T
Medtr3g099620
Mtr.10993.1.S1_at
Lj1g3v1525930
Glyma.04G098400
Phvul.009G033800
n/a
Godiard, L., Lepage, A., Moreau, S., Laporte, D., Verdenaud, M., Timmers, T., and Gamas, P. (2011). MtbHLH1, a bHLH transcription factor involved in Medicago truncatula nodule vascular patterning and nodule to plant metabolic exchanges. New Phytologist 191, 391-404.
18
MtBHLH476Inf+Nod+/-Fix+Ariel et al.,2012
TF (bHLH motif containing)
BASIC HELIX–LOOP–HELIX 476 (BHLH476)
RNAi
Medtr5g014520
Mtr.253.1.S1_atLj2g3v1984620
Glyma.01G198100
Phvul.002G007400
n/a
Ariel, F., Brault-Hernandez, M., Laffont, C., Huault, E., Brault, M., Plet, J., Moison, M., Blanchet, S., Ichanté, J.L., and Chabaud, M. (2012). Two direct targets of cytokinin signaling regulate symbiotic nodulation in Medicago truncatula. The Plant Cell 24, 3838-3852.
19
PvBPS1Inf++Nod+/-n/aArthikala et al., 2018Unknown (DUF)BYPASS1 (BPS1)RNAiMedtr7g078700
Msa.1056.1.S1_at
Lj1g3v2752330
Glyma.18G237000
Phvul.008G059600
n/a
Arthikala, M.-K., Nanjareddy, K., and Lara, M. (2018). In BPS1 Downregulated Roots, the BYPASS1 Signal Disrupts the Induction of Cortical Cell Divisions in Bean-Rhizobium Symbiosis. Genes 9, 11.
20
MtBRI1n/aNod+/-, Nod*n/aCheng et al., 2017
Kinase (LRR-RLK)
BRASSINOSTEROID INSENSITIVE 1Tnt1
Medtr3g095100
Mtr.45830.1.S1_at
Lj1g3v1222370
Glyma.04G218300, Glyma.06G147600
Phvul.005G005900
n/a
Cheng, X., Gou, X., Yin, H., Mysore, K.S., Li, J., and Wen, J. (2017). Functional characterisation of brassinosteroid receptor MtBRI1 in Medicago truncatula. Scientific reports 7, 9327.
21
LjBRUSHInf+/-Nod+/- (C)n/aChiasson et al., 2018
Channel (Cations)
BRUSHLjcngcIVA1 GOFEMS-Tilling
Medtr5g007630
-Lj2g3v0632220
Glyma.09G168500
Phvul.004G143800
Myc++
Chiasson, D.M., Haage, K., Sollweck, K., Brachmann, A., Dietrich, P., and Parniske, M. (2017). A quantitative hypermorphic CNGC allele confers ectopic calcium flux and impairs cellular development. Elife 6, e25012.
22
LjBZFn/aNod++n/aNishimura et al., 2002
TF (bZIP domain containing)
BASIC LEUCINE ZIPPER FAMILY PROTEIN (BZF)
Ljsym77EMS
Medtr3g436010
Mtr.9651.1.S1_at
Lj6g3v0937020
Glyma.18G117100, Glyma.08G302500
Phvul.006G029200
n/a
Nishimura, R., Ohmori, M., Fujita, H., and Kawaguchi, M. (2002). 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 99, 15206-15210.
23
MtCAS31n/a
Nod+, Pink +/- (C)
Fix+/- (C)Li et al., 2018DehydrinCOLD ACCLIMATION SPECIFIC (CAS31)Tnt1
Medtr6g084640
Mtr.8651.1.S1_a_at
Lj2g3v0741950
Glyma.09G185500
-n/a
Li, X., Feng, H., Wen, J., Dong, J., and Wang, T. (2018). MtCAS31 Aids Symbiotic Nitrogen Fixation by Protecting the Leghemoglobin MtLb120-1 Under Drought Stress in Medicago truncatula. Front Plant Sci 9, 633.
24
MtCBS1Inf++Nod++Fix+/-Sinharoy et al., 2016
Enzyme (Synthase)
CYSTATHIONE BETASYNTHASE 1 (CBS1)
Tnt1
Medtr6g052300
Mtr.23516.1.S1_at
Lj6g3v1537040
Glyma.09G129700, Glyma.16G177500
Phvul.004G106300
n/a
Sinharoy, S., Torres-Jerez, I., Bandyopadhyay, K., Kereszt, A., Pislariu, C.I., Nakashima, J., Benedito, V.A., Kondorosi, E., and Udvardi, M.K. (2013). The C2H2 transcription factor regulator of symbiosome differentiation represses transcription of the secretory pathway gene VAMP721a and promotes symbiosome development in Medicago truncatula. Plant Cell 25, 3584-3601.
25
LjCCD7Inf+Nod+/-n/aLiu et. al., 2013
Enzyme (Oxidoreductase)
CAROTENOID CLEAVAGE DIOXYGENASE 7 (CCD7)
RNAiMedtr7g045370
Mtr.32038.1.S1_at
Lj0g3v0146209
Glyma.01G073200
Phvul.008G152801
n/a
Liu, J., Novero, M., Charnikhova, T., Ferrandino, A., Schubert, A., Ruyter-Spira, C., Bonfante, P., Lovisolo, C., Bouwmeester, H.J., and Cardinale, F. (2013). Carotenoid cleavage dioxygenase 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus. Journal of experimental botany 64, 1967-1981.
26
MtCCS52an/aNod+/-, Nod*Fix*Vinardell et al., 2003
Anaphase-promoting complex activator
CELL CYCLE SWITCH GENE encoding a 52 kDa protein (CCS 52a)
Antisense
Medtr4g102510
Msa.3010.1.S1_at; Mtr.12852.1.S1_at; Mtr.4030.1.S1_at
Lj4g3v1327590
Glyma.7G133000
Phvul.003G213700
n/a
Vinardell, J.M., Fedorova, E., Cebolla, A., Kevei, Z., Horvath, G., Kelemen, Z., Tarayre, S., Roudier, F., Mergaert, P., Kondorosi, A., and Kondorosi, E. (2003). Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. The Plant cell 15, 2093-2105.
27
MtCDC16n/aNod++Fix+Kuppusamy et al.,2009
Anaphase-promoting complex component
CELL DIVISION CYCLE16 (CDC16)RNAi
Medtr8g058380
Mtr.51354.1.S1_at
Lj0g3v0096099
Glyma.06G228700
Phvul.011G165500
n/a
Kuppusamy, K.T., Ivashuta, S., Bucciarelli, B., Vance, C.P., Gantt, J.S., and VandenBosch, K.A. (2009). Knockdown of CELL DIVISION CYCLE16 reveals an inverse relationship between lateral root and nodule numbers and a link to auxin in Medicago truncatula. Plant physiology 151, 1155-1166.
28
MtCDPK1Inf*Nod+/-n/aIvashuta et al.,2005
Enzyme (Calcium dependent Kinase)
CALCIUM DEPENDANT PROTEIN KINASE 1 (CDPK1)
RNAiMedtr5g022030
Mtr.249.1.S1_s_at
Lj2g3v1695240
Glyma.01G166100, Glyma.11G077300
Phvul.002G108700
Myc+/-
Ivashuta, S., Liu, J., Liu, J., Lohar, D.P., Haridas, S., Bucciarelli, B., VandenBosch, K.A., Vance, C.P., Harrison, M.J., and Gantt, J.S. (2005). RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. The Plant Cell 17, 2911-2921.
29
LjCHIT5Inf+/-Nod+, Pink +/-Fix+/-Malolepszy et al., 2018
Enzyme (Glycosyl hydrolase)
CHITINASE 5 (CHIT5)LORE1
Medtr1g013150
Mtr.42876.1.S1_at
Lj5g3v0525260
Glyma.17G217000, Glyma.14G110700
Phvul.001G046400
n/a
Malolepszy, A., Kelly, S., Sørensen, K.K., James, E.K., Kalisch, C., Bozsoki, Z., Panting, M., Andersen, S.U., Sato, S., and Tao, K. (2018). A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis. Elife 7, e38874.
30
MtCHRn/aNod+/-n/aZhang et al., 2009
Enzyme (Oxidoreductase)
CHALCONE REDUCTASE (CHR)RNAi
Medtr5g097910
Mtr.15678.1.S1_s_at
Lj2g3v3339170, Lj0g3v0328269, 8 other homologs
Glyma.02G307300
Phvul.008G287200
n/a
Wasson, A.P., Pellerone, F.I., and Mathesius, U. (2006). Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. The Plant Cell 18, 1617-1629.
31
MtCHSn/aNod+/-n/aZhang et al., 2009
Enzyme (Synthase)
CHALCONE SYNTHASE (CHS)RNAi
Medtr7g084300
Msa.3134.1.S1_at
Lj4g3v2603590
Glyma.19G105100
Phvul.001G083000
n/a
Zhang, J., Subramanian, S., Stacey, G., and Yu, O. (2009). Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. The Plant Journal 57, 171-183.
32
LjCIP73Inf+/-Nod+/-n/aKang et al., 2011
Unknown (Scythe_N Ubiquitin-like domain containing)
CCAMK INTERACTING PROTEIN OF APPROXIMATELY 73 KDa (CIP73)
RNAi
Medtr4g116370
Mtr.7126.1.S1_at
Lj4g3v1970880
Glyma.17G106000
Phvul.003G173700
n/a
Kang, H., Zhu, H., Chu, X., Yang, Z., Yuan, S., Yu, D., Wang, C., Hong, Z., and Zhang, Z. (2011). A novel interaction between CCaMK and a protein containing the Scythe_N ubiquitin-like domain in Lotus japonicus. Plant physiology 155, 1312-1324.
33
LjCKX3Inf+/-Nod+/-n/aReid et al., 2016
Enzyme (Oxidoreductase)
CYTOKININ OXIDASE/DEHYDROGENASE 3 (CKX3)
LORE1
Medtr2g039410
Mtr.14413.1.S1_at
Lj5g3v0692300
Glyma.09G063900, Glyma.15G140000
Phvul.009G231700
Myc+
Reid, D.E., Heckmann, A.B., Novák, O., Kelly, S., and Stougaard, J. (2016). CYTOKININ OXIDASE/DEHYDROGENASE3 maintains cytokinin homeostasis during root and nodule development in Lotus japonicus. Plant physiology 170, 1060-1074.
34
LjCLC1n/aNod+/-n/aWang et al., 2015
Protein (Endocytosis)
CLATHARIN HEAVY CHAIN1RNAi
Medtr3g070940
Mtr.41546.1.S1_at
Lj6g3v0497300
Glyma.02G258200, Glyma.14G058300
Phvul.008G222800
n/a
Wang, C., Zhu, M., Duan, L., Yu, H., Chang, X., Li, L., Kang, H., Feng, Y., Zhu, H., Hong, Z., and Zhang, Z. (2015). Lotus japonicus Clathrin Heavy Chain1 Is Associated with Rho-Like GTPase ROP6 and Involved in Nodule Formation. Plant Physiology 167, 1497-1510.
35
LjCLE-RS1n/aNod++n/aNishida et al., 2018
Peptide (Signaling)
CLAVATA3/ENDOSPERM SURROUNDING REGION12 (CLE12/CLE13)
CLE-RS1/CLE-RS2 (root signal), RIC1/RIC2 (rhizobium induced CLE)
CRSISPR/Cas9
Medtr4g079630
Mtr.19172.1.S1_at
Lj0g3v0000559.1
Glyma.13G368300
Phvul.011G135900
n/a
Nishida, H., Tanaka, S., Handa, Y., Ito, M., Sakamoto, Y., Matsunaga, S., Betsuyaku, S., Miura, K., Soyano, T., and Kawaguchi, M. (2018). A NIN-LIKE PROTEIN mediates nitrate-induced control of root nodule symbiosis in Lotus japonicus. Nature communications 9, 499.
36
LjCLE-RS2n/aNod++n/aNishida et al., 2018
Peptide (Signaling)
CLAVATA3/ENDOSPERM SURROUNDING REGION12 (CLE12/CLE13)
CRSISPR/Cas9
Medtr4g079610
Mtr.19174.1.S1_at
AP010911.1
Glyma.06G284100
Phvul.011G135900
n/a
Nishida, H., Tanaka, S., Handa, Y., Ito, M., Sakamoto, Y., Matsunaga, S., Betsuyaku, S., Miura, K., Soyano, T., and Kawaguchi, M. (2018). A NIN-LIKE PROTEIN mediates nitrate-induced control of root nodule symbiosis in Lotus japonicus. Nature communications 9, 499.
37
LjCLV2n/aNod++n/aKrusell et al., 2011
Receptor-like protein (LRR-RLP)
CLAVATA 2 (CLV2)Pssym28RNAi
Medtr7g079550
Mtr.34002.1.S1_s_at
Lj2g3v0743220
Glyma.09G251800
Phvul.008G055400
Myc++ (tomato)
Krusell, L., Sato, N., Fukuhara, I., Koch, B.E., Grossmann, C., Okamoto, S., Oka‐Kira, E., Otsubo, Y., Aubert, G., and Nakagawa, T. (2011). The Clavata2 genes of pea and Lotus japonicus affect autoregulation of nodulation. The Plant Journal 65, 861-871.
38
MtCNGC15aInf+/-Nod+/-n/aCharpentier et al., 2016
Channel (Cations)
CYCLIC NUCLEOTIDE GATED CHANNELS 15A (CNGC15a)
Tnt1, RNAi
Medtr1g064240
Mtr.50460.1.S1_at
Lj5g3v0659940
Glyma.13G141000, Glyma.10G053900
Phvul.007G148700
Myc+/-
Charpentier, M., Sun, J., Martins, T.V., Radhakrishnan, G.V., Findlay, K., Soumpourou, E., Thouin, J., Véry, A.-A., Sanders, D., and Morris, R.J. (2016). Nuclear-localized cyclic nucleotide–gated channels mediate symbiotic calcium oscillations. Science 352, 1102-1105.
39
MtCNGC15bInf+/-Nod+/-n/aCharpentier et al., 2016
Channel (Cations)
CYCLIC NUCLEOTIDE GATED CHANNELS 15B (CNGC 15b)
Tnt1, RNAi
Medtr4g058730
-Lj0g3v0103009
Glyma.12G076800
Phvul.011G080800
Myc+/-
Charpentier, M., Sun, J., Martins, T.V., Radhakrishnan, G.V., Findlay, K., Soumpourou, E., Thouin, J., Véry, A.-A., Sanders, D., and Morris, R.J. (2016). Nuclear-localized cyclic nucleotide–gated channels mediate symbiotic calcium oscillations. Science 352, 1102-1105.
40
MtCNGC15cInf+/-Nod+/-n/aCharpentier et al., 2016
Channel (Cations)
CYCLIC NUCLEOTIDE GATED CHANNELS 15C (CNGC 15c)
Tnt1, RNAi
Medtr2g094860
Mtr.32319.1.S1_at
Lj3g3v1089390, Lj3g3v1089380
Glyma.12G175000
Phvul.005G133900
Myc+/-
Charpentier, M., Sun, J., Martins, T.V., Radhakrishnan, G.V., Findlay, K., Soumpourou, E., Thouin, J., Véry, A.-A., Sanders, D., and Morris, R.J. (2016). Nuclear-localized cyclic nucleotide–gated channels mediate symbiotic calcium oscillations. Science 352, 1102-1105.
41
MtCOPT1n/aNod+n/aSenovilla et al., 2018
Transporter (Copper)
COPPER TRASPORTER 1 (COPT1)Tnt1
Medtr4g019870
Mtr.42937.1.S1_s_at
Lj0g3v0091689.1
Glyma.18G191300
Phvul.008G113200
n/a
Senovilla, M., Castro‐Rodríguez, R., Abreu, I., Escudero, V., Kryvoruchko, I., Udvardi, M.K., Imperial, J., and González‐Guerrero, M. (2018). Medicago truncatula COPPER TRANSPORTER 1 (Mt COPT 1) delivers copper for symbiotic nitrogen fixation. New Phytologist 218, 696-709.
42
MtCP6n/aNod+/-, Nod*Fix++Pierre et al., 2014
Enzyme (Cysteine protease)
CYSTEINE PROTEINASE 6 (CP6)RNAi
Medtr4g079800
Mtr.45750.1.S1_at
Lj3g3v1642060
Glyma.12G127200
Phvul.011G132100
n/a
Pierre, O., Hopkins, J., Combier, M., Baldacci, F., Engler, G., Brouquisse, R., Hérouart, D., and Boncompagni, E. (2014). Involvement of papain and legumain proteinase in the senescence process of Medicago truncatula nodules. New Phytologist 202, 849-863.
43
MtCPK3n/aNod++n/aGargantini et al., 2006
Enzyme (Calcium dependent Kinase)
CALCIUM DEPENDANT PROTEIN KINASE 3 (CPK3)
RNAiMedtr3g051770
Mtr.37994.1.S1_at
Lj2g3v3164080
Glyma.08G316500
Phvul.006G043700
n/a
Gargantini, P.R., Gonzalez‐Rizzo, S., Chinchilla, D., Raices, M., Giammaria, V., Ulloa, R.M., Frugier, F., and Crespi, M.D. (2006). A CDPK isoform participates in the regulation of nodule number in Medicago truncatula. The Plant Journal 48, 843-856.
44
MtCRA2n/aNod+/-n/aHuault et al., 2014
Enzyme (Kinase; LRR-RLK)
COMPACT ROOT ARCHITECTURE 2 (CRA2)
Tnt1
Medtr3g110840
Mtr.38398.1.S1_at
Lj1g3v2096140
Glyma.06G090700, Glyma.04G088700
Phvul.009G114400
n/a
Huault, E., Laffont, C., Wen, J., Mysore, K.S., Ratet, P., Duc, G., and Frugier, F. (2014). Local and systemic regulation of plant root system architecture and symbiotic nodulation by a receptor-like kinase. PLoS Genetics 10, e1004891.
45
MtCRE1 (L.O.F)Inf++Nod+/-n/aGonzalez-Rizzo et al., 2006
Enzyme (Histidine kinase)
CYTOKININ RESPONSE 1 (CRE1)
Ljlhk1 (lotus histidine kinase), Ljlhk1 (lotus histidine kinase), spontaneous nodule formation (Ljsnf2) gof
RNAi
Medtr8g106150
Mtr.45840.1.S1_at
Lj4g3v3113830
Glyma.05G241600
Phvul.002G324900
Myc+
Gonzalez-Rizzo, S., Crespi, M., and Frugier, F. (2006). The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. The Plant Cell 18, 2680-2693.
46
LjCRE1 (G.O.F)Inf+/-
White++ (spontaneous)
n/aTirichine et al., 2007
Enzyme (Histidine kinase)
CYTOKININ RESPONSE 1 (CRE1)
hit1 (hyperinfected1)
EMS
Medtr8g106150
Mtr.45840.1.S1_at
Lj4g3v3113830
Glyma.05G241600
Phvul.002G324900
n/a
Tirichine, L., Sandal, N., Madsen, L.H., Radutoiu, S., Albrektsen, A.S., Sato, S., Asamizu, E., Tabata, S., and Stougaard, J. (2007). A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315, 104-107.
47
MtCRNn/aNod++n/aCrook et al., 2016PseudokinaseCORYNE (CRN)Tnt1
Medtr7g020850
Mtr.35355.1.S1_at
Lj1g3v3137890
Glyma.08G257700, Glyma.18G282100
Phvul.008G019200
n/a
Crook, A.D., Schnabel, E.L., and Frugoli, J.A. (2016). The systemic nodule number regulation kinase SUNN in Medicago truncatula interacts with MtCLV2 and MtCRN. The Plant Journal 88, 108-119.
48
LjCYCLOPS (MtIPD3)
Inf-Nod*n/aYano et al., 2008
Transcriptional activator
INTERACTING PROTEIN DMI 3LjcyclopsEMS-Tilling
Medtr5g026850
Mtr.42174.1.S1_at, Mtr.29567.1.S1_at, Mtr.3453.1.S1_s_at
Lj2g3v1549600
Glyma.01G149500
Phvul.002G128600
Myc+/-
Yano, K., Yoshida, S., Müller, J., Singh, S., Banba, M., Vickers, K., Markmann, K., White, C., Schuller, B., and Sato, S. (2008). CYCLOPS, a mediator of symbiotic intracellular accommodation. Proceedings of the National Academy of Sciences 105, 20540-20545.
49
MtIPD3LInf-Nod-n/aJin et al., 2018
Transcriptional activator
INTERACTING PROTEIN DMI 3 LIKE(IPD3/IPD3L)
Tnt1
MT35v5_contig_51603_1
----Myc+
Jin, Y., Liu, H., Luo, D., Yu, N., Dong, W., Wang, C., Zhang, X., Dai, H., Yang, J., and Wang, E. (2016). DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nature Communications 7, 12433.
50
MtCYP15an/aNod*Fix*Sheokand S., et al., 2005
Enzyme (Cysteine protease)
CYSTEINE PROTEASE 15a (CYP15a)AntisenseMedtr1g023210
Mtr.12217.1.S1_at
Lj1g3v2140860
Glyma.17G254900
Phvul.001G009900
n/a
Sheokand, S., Dahiya, P., Vincent, J., and Brewin, N. (2005). Modified expression of cysteine protease affects seed germination, vegetative growth and nodule development in transgenic lines of Medicago truncatula. Plant Science 169, 966-975.
51
MtDELLA1Inf+/-Nod+/-n/aFonouni-Farde et al., 2016; Jin et al., 2016
Transcriptional regulator (D-E-L-L-A motif)
DELLA 1PsLATnt1
Medtr3g065980
Mtr.31658.1.S1_s_at
Lj6g3v0433880.1
Glyma.11G216500, Glyma.18G040000
Phvul.001G230500
n/a (Myc+/- della1 della 2)
Fonouni-Farde, C., Tan, S., Baudin, M., Brault, M., Wen, J., Mysore, K.S., Niebel, A., Frugier, F., and Diet, A. (2016). DELLA-mediated gibberellin signalling regulates Nod factor signalling and rhizobial infection. Nature communications 7, 12636.; Jin, Y., Liu, H., Luo, D., Yu, N., Dong, W., Wang, C., Zhang, X., Dai, H., Yang, J., and Wang, E. (2016). DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nature Communications 7, 12433.
52
MtDELLA2Inf+/-Nod+/-n/aFonouni-Farde et al., 2016; Jin et al., 2016
Transcriptional regulator (D-E-L-L-A motif)
DELLA 2PsCRYTnt1
MT35v5_contig_52215_1
-
Lj4g3v2436020.1
Glyma.05G140400, Glyma.08G095800
Phvul.003G291500
n/a (Myc+/- della1 della 2)
Fonouni-Farde, C., Tan, S., Baudin, M., Brault, M., Wen, J., Mysore, K.S., Niebel, A., Frugier, F., and Diet, A. (2016). DELLA-mediated gibberellin signalling regulates Nod factor signalling and rhizobial infection. Nature communications 7, 12636.; Jin, Y., Liu, H., Luo, D., Yu, N., Dong, W., Wang, C., Zhang, X., Dai, H., Yang, J., and Wang, E. (2016). DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nature Communications 7, 12433.
53
MtDELLA3Inf+/-Nod+/-n/aFonouni-Farde et al., 2016; Jin et al., 2016
Transcriptional regulator (D-E-L-L-A motif)
DELLA 3Tnt1
MT35v5_contig_55897_1
-
Lj6g3v0959470.1
Glyma.04G150500, Glyma.06G213100, Glyma.10G190200, Glyma.20G200500
Phvul.007G131200
n/a
Fonouni-Farde, C., Tan, S., Baudin, M., Brault, M., Wen, J., Mysore, K.S., Niebel, A., Frugier, F., and Diet, A. (2016). DELLA-mediated gibberellin signalling regulates Nod factor signalling and rhizobial infection. Nature communications 7, 12636.; Jin, Y., Liu, H., Luo, D., Yu, N., Dong, W., Wang, C., Zhang, X., Dai, H., Yang, J., and Wang, E. (2016). DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nature Communications 7, 12433.
54
MtDMEInf+
Nod+, Nod*, White++
Fix+/-Carine Satgé et al., 2016
Enzyme (DNA glycosylase)
DEMETER (DME)RNAi
Medtr1g492760
-Lj5g3v1769410
Glyma.20G188300
Phvul.007G223600
n/a
Satge, C., Moreau, S., Sallet, E., Lefort, G., Auriac, M.-C., Rembliere, C., Cottret, L., Gallardo, K., Noirot, C., and Jardinaud, M.-F. (2016). Reprogramming of DNA methylation is critical for nodule development in Medicago truncatula. Nature plants 2, 16166.
55
MtDMI1(LjPOLLUX)
Inf-Nod-Fix-Ane et al., 2004
Channel (Cations)
DOES NOT MAKE Infections 1 (DMI1)
Ljcastor, Ljpollux, Pssym8
EMS mutagenesis, Tnt1 (Peiter et al., 2007)
Medtr2g005870
Mtr.124.1.S1_s_at; Mtr.19417.1.S1_at
Lj6g3v2275020, Lj6g3v2275010
Glyma.12G167300
Phvul.006G218700
Myc-
Ané, J.-M., Kiss, G.B., Riely, B.K., Penmetsa, R.V., Oldroyd, G.E., Ayax, C., Lévy, J., Debellé, F., Baek, J.-M., and Kalo, P. (2004). Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364-1367.
56
LjCASTORInf-Nod-n/aImaizumi-Anraku et al., 2005
Channel (Cations)
DOES NOT MAKE Infections 1 (DMI1)EMS- Tilling--
Lj6g3v2275020, Lj6g3v2275010
Glyma.12G167300
Phvul.006G218700
Myc-
Imaizumi-Anraku, H., Takeda, N., Charpentier, M., Perry, J., Miwa, H., Umehara, Y., Kouchi, H., Murakami, Y., Mulder, L., and Vickers, K. (2005). Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433, 527.
57
LjSYMRKInf-Nod-Fix-Stracke et al., 2002
Enzyme (Kinase; LRR-RLK)
SYMBIOTIC RECEPTOR KINASE (SYMRK)/DOES NOT MAKE Infections 2 (DMI2)
Ljsymrk (symbiotic receptor kinase), Msnork (nodulation receptor kinase; Pssym19
EMS mutagenesis, LATER: y ray, Tnt1
Medtr5g030920
Mtr.51192.1.S1_at
Lj2g3v1467920
Glyma.01G020100, Glyma.09G202300
Phvul.002G143400, Phvul.002G116200
Myc-
Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T., Tabata, S., Sandal, N., Stougaard, J., and Szczyglowski, K. (2002). A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959.
58
MtCCaMK (L.O.F)
Inf-Nod-Fix-Levy et al., 2004; Mitra et al., 2004
Kinase (Calcium/Calmodulin dependent)
CALCIUM CALMODULIN KINASE (CCaMK)/DOES NOT MAKE Infections 3 (DMI3)
Pssym9
EMS mutagenesis
Medtr8g043970
Mtr.8930.1.S1_at
Lj3g3v1739280
Glyma.15G222300
Phvul.011G186900
Myc-
Lévy, J., Bres, C., Geurts, R., Chalhoub, B., Kulikova, O., Duc, G., Journet, E.-P., Ané, J.-M., Lauber, E., and Bisseling, T. (2004). A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361-1364.; Mitra, R.M., Gleason, C.A., Edwards, A., Hadfield, J., Downie, J.A., Oldroyd, G.E., and Long, S.R. (2004). A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proceedings of the National Academy of Sciences 101, 4701-4705.
59
LjCCaMK (G.O.F)Inf-
White++ (spontaneous)
n/aTirichine et al., 2006
Kinase (Calcium/Calmodulin dependent)
CALCIUM CALMODULIN KINASE (CCaMK)/DOES NOT MAKE Infections 3 (DMI3)
Lsnf1 (spontaneous nodule formation1)
EMS mutagenesis
Medtr8g043970
Mtr.8930.1.S1_at
Lj3g3v1739280
Glyma.15G222300
Phvul.011G186900
n/a
Tirichine, L., Imaizumi-Anraku, H., Yoshida, S., Murakami, Y., Madsen, L.H., Miwa, H., Nakagawa, T., Sandal, N., Albrektsen, A.S., and Kawaguchi, M. (2006). Deregulation of a Ca 2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441, 1153.
60
MtDNF1n/aNod*, White++Fix-, Fix*Wang et al., 2010; Van de Velde et al., 2010
Signal peptidase complex subunit
DEFECTIVE IN Nitrogen Fixation1 (DNF1)FNBMedtr3g027890
Mtr.43876.1.S1_at
Lj1g3v4931800
Glyma.10G156000
Phvul.001G228900
n/a
Wang, D., Griffitts, J., Starker, C., Fedorova, E., Limpens, E., Ivanov, S., Bisseling, T., and Long, S. (2010). A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327, 1126-1129., Van de Velde, W., Zehirov, G., Szatmari, A., Debreczeny, M., Ishihara, H., Kevei, Z., Farkas, A., Mikulass, K., Nagy, A., and Tiricz, H. (2010). Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327, 1122-1126.
61
MtDNF2n/a
Nod++, White++
Fix-, Fix*Bourcy et al., 2014
Enzyme (Phosphatidylinositol phospholipase C‐like)
DEFECTIVE IN Nitrogen Fixation2 (DNF2)FNB, Tnt1
Medtr4g085800
Mtr.630.1.S1_at-
Glyma.02G102700
Phvul.003G048300
n/a
Bourcy, M., Brocard, L., Pislariu, C.I., Cosson, V., Mergaert, P., Tadege, M., Mysore, K.S., Udvardi, M.K., Gourion, B., and Ratet, P. (2013). Medicago truncatula DNF2 is a PI‐PLC‐XD‐containing protein required for bacteroid persistence and prevention of nodule early senescence and defense‐like reactions. New Phytologist 197, 1250-1261.
62
MtDNF4n/aNod*, White++Fix*Kim et al., 2015
Peptide (Cysteine-rich)
DEFECTIVE IN Nitrogen Fixation4 (DNF4)NCR211FNB
Medtr4g035705
----n/a
Kim, M., Chen, Y., Xi, J., Waters, C., Chen, R., and Wang, D. (2015). An antimicrobial peptide essential for bacterial survival in the nitrogen-fixing symbiosis. Proceedings of the National Academy of Sciences 112, 15238-15243.
63
MtDNF7n/aNod*, White++Fix-, Fix*Horvath et al, 2015
Peptide (Cysteine-rich)
DEFECTIVE IN Nitrogen Fixation7 (DNF7)NCR167FNBMedtr7g029760
Mtr.3210.1.S1_at
---n/a
Horváth, B., Domonkos, Á., Kereszt, A., Szűcs, A., Ábrahám, E., Ayaydin, F., Bóka, K., Chen, Y., Chen, R., and Murray, J.D. (2015). Loss of the nodule-specific cysteine rich peptide, NCR169, abolishes symbiotic nitrogen fixation in the Medicago truncatula dnf7 mutant. Proceedings of the National Academy of Sciences 112, 15232-15237.
64
MtEFDInf++Nod++n/aVernie et al., 2008
TF (Ethylene response factor)
ETHYLENE RESPONSE FACTOR REQUIRED FOR NODULE DIFFERENTIATION (EFD)
Deletion TILLING
Medtr4g008860
Mtr.41581.1.S1_at
Lj3g3v0014470
Glyma.08G216600, Glyma.07G025800
Phvul.010G159500
Myc+
Vernié, T., Moreau, S., De Billy, F., Plet, J., Combier, J.-P., Rogers, C., Oldroyd, G., Frugier, F., Niebel, A., and Gamas, P. (2008). EFD is an ERF transcription factor involved in the control of nodule number and differentiation in Medicago truncatula. The Plant Cell 20, 2696-2713.
65
MtSKL(LjEIN2a)Inf++Nod++n/aPenmetsa et al., 2008NRAMP ProteinETHYLENE INSENSITIVE 2 (EIN2a)Mtskl (sickle)EMS
Medtr0041s0030
Mtr.9302.1.S1_at
Lj1g3v4590690
Glyma.03G181400
Phvul.001G177500
Myc++
Varma Penmetsa, R., Uribe, P., Anderson, J., Lichtenzveig, J., Gish, J.C., Nam, Y.W., Engstrom, E., Xu, K., Sckisel, G., and Pereira, M. (2008). The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. The Plant Journal 55, 580-595.
66
LjEIN2bInf++Nod++Fix-/-Reid et al., 2018NRAMP ProteinETHYLENE INSENSITIVE 2 (EIN2a/EIN2b)LORE1--Lj5g3v0659810
Glyma.13G145100, Glyma.10G058300
Phvul.007G150600
n/a
Reid, D., Liu, H., Kelly, S., Kawaharada, Y., Mun, T., Andersen, S.U., Desbrosses, G., and Stougaard, J. (2018). Dynamics of ethylene production in response to compatible Nod factor. Plant physiology 176, 1764-1772.
67
LjENOD40-1/ENOD40-2
Inf+Nod+/-n/aKumagai et al., 2006PeptideEARLY NODULIN 40RNAi
MT4Noble_057132, Medtr8g069785
-Lj3g3v3599510
Glyma.01G028500
Phvul.002G064232
n/a
Kumagai, H., Kouchi, H., Kinoshita, E., and Ridge, R.W. (2006). RNAi Knock-Down of ENOD40 s Leads to Significant Suppression of Nodule Formation in Lotus japonicus. Plant and Cell Physiology 47, 1102-1111.
68
GmENOD93n/aNod+/-, Nod*n/aYan et al., 2015
Membrane protein
EARLY NODULIN 93LORE1---
Glyma.06G247600
-n/a
Yan, Z., Hossain, M.S., Arikit, S., Valdés‐López, O., Zhai, J., Wang, J., Libault, M., Ji, T., Qiu, L., and Meyers, B.C. (2015). Identification of microRNAs and their mRNA targets during soybean nodule development: functional analysis of the role of miR393j‐3p in soybean nodulation. New Phytologist 207, 748-759.
69
LjEPR3Inf+/-, Inf*Nod*n/aKawaharada et al., 2015
Enzyme (Kinase; LysM-RLK)
EXOPOLYSACCHARIDE RECEPTOR (EPR3)
Ljlys3, Ljexo277,MtLYK10
LORE1
Medtr5g033490
Mtr.25148.1.S1_at
Lj2g3v1415410
Glyma.08G283300
Phvul.002G059500, Pv03g003063700
n/a
Kawaharada, Y., Kelly, S., Nielsen, M.W., Hjuler, C.T., Gysel, K., Muszyński, A., Carlson, R., Thygesen, M.B., Sandal, N., and Asmussen, M. (2015). Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 523, 308.
70
LjERF1n/aNod+/-n/aAsamizu et al., 2008
TF (Ethylene responsive)
ETHYLENE RESPONSE FACTOR 1 (ERF1)RNAiMedtr1g074370
Mtr.39861.1.S1_at
Lj5g3v1167370
Glyma.20G203700
Phvul.007G127800
n/a
Asamizu, E., Shimoda, Y., Kouchi, H., Tabata, S., and Sato, S. (2008). A positive regulatory role for LjERF1 in the nodulation process is revealed by systematic analysis of nodule-associated transcription factors of Lotus japonicus. Plant physiology 147, 2030-2040.
71
MtERN1Inf+/-, Inf*Nod-, Nod*n/aMiddleton et al., 2007
TF (Ethylene responsive)
ETHYLENE RESPONSE FACTOR REQUIRED FOR NODULATION1 (ERN1)
Mtbit1 (branched Infection thread, poodle
Fast Neutron mutagenesis
Medtr7g085810
Mtr.7556.1.S1_at
Lj1g3v3975310
Glyma.19G113100
Phvul.001G111800
Myc+
Middleton, P.H., Jakab, J., Penmetsa, R.V., Starker, C.G., Doll, J., Kaló, P., Prabhu, R., Marsh, J.F., Mitra, R.M., and Kereszt, A. (2007). An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. The Plant Cell 19, 1221-1234.
72
MtERN2Inf+, Inf*Nod+, Nod*Fix+, Fix*Cerri et al., 2016
TF (Ethylene responsive)
ETHYLENE RESPONSE FACTOR REQUIRED FOR NODULATION2 (ERN2)
TILLING, Tnt1
Medtr6g029180
Mtr.43947.1.S1_at
-
Glyma.16G154100, Glyma.02G072800
Phvul.001G160100
Myc+
Cerri, M.R., Frances, L., Kelner, A., Fournier, J., Middleton, P.H., Auriac, M.-C., Mysore, K.S., Wen, J., Erard, M., and Barker, D.G. (2016). The symbiosis-related ERN transcription factors act in concert to coordinate rhizobial host root infection. Plant physiology 171, 1037-1054.
73
MtEXO70H4Inf+/-, Inf*Nod+n/aLiu et al., 2019
Membrane protein (Exocyst complex subunit)
EXOCYST70H4Tnt1Medtr4g062330
Mtr.21216.1.S1_at
Lj0g3v0313429
Glyma.11G144600, Glyma.12G075200
Phvul.011G068800, Phvul.L003900
n/a
Liu, C.W, Breakspear, A., Stacey, N., Findlay, K., Nakashima A., Ramakrishnan, K., Endre, A., de Carvalho-Niebel, F., Oldroyd, G.E.D, Udvardi, M.K., Fournier, J., Murray, J.D The infectosome is required for polar growth of rhizobial infection threads Nature Comms. 2019
74
GmEXPB2n/aNod+/-, Nod*Fix+/-Li et al., 2015Expansinβ-EXPANSIN B2 (EXPB2)RNAi
Medtr0118s0070
Mtr.33549.1.S1_at
Lj5g3v0642670.1
Glyma.10G122300
Phvul.008G144100
n/a
Li, X., Zhao, J., Tan, Z., Zeng, R., and Liao, H. (2015). GmEXPB2, a cell wall β-expansin, affects soybean nodulation through modifying root architecture and promoting nodule formation and development. Plant Physiology 169, 2640-2653.
75
LjFEN1Inf+Nod*Fix-Hakoyama et al., 2009
Enzyme (Homocitrate Synthase)
FAIL IN ENLARGEMENT of infection CELLS (FEN1)
EMS mutagenesis
--
Lj1g3v3690180, Lj1g3v3690020
Glyma.19g120400, Glyma.19g120600, Glyma.03g005700
Phvul.007G004600
n/a
Hakoyama, T., Niimi, K., Watanabe, H., Tabata, R., Matsubara, J., Sato, S., Nakamura, Y., Tabata, S., Jichun, L., and Matsumoto, T. (2009). Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation. Nature 462, 514.
76
MtFER2n/aNod+Fix+/-Dhanushkodi et al., 2018
Protein complex (Iron scavenging)
FERRITINS (FER2/FER3)RNAi
Medtr5g083170
Mtr.12355.1.S1_at
Lj2g3v2806680
Glyma.02G262500
Phvul.001G245700
n/a
Dhanushkodi, R., Matthew, C., McManus, M.T., and Dijkwel, P.P. (2018). Drought-induced senescence of Medicago truncatula nodules involves serpin and ferritin to control proteolytic activity and iron levels. New Phytol 220, 196-208.
77
MtFER3n/aNod+Fix+/-Dhanushkodi et al., 2018
Protein complex (Iron scavenging)
FERRITINS (FER2/FER3)RNAi
Medtr4g014540
Msa.1670.1.S1_at
Lj3g3v1378250
Glyma.03G050100
Phvul.010G065600
n/a
Dhanushkodi, R., Matthew, C., McManus, M.T., and Dijkwel, P.P. (2018). Drought-induced senescence of Medicago truncatula nodules involves serpin and ferritin to control proteolytic activity and iron levels. New Phytol 220, 196-208.
78
MtFLOT2Inf+/-Nod+/-Fix+/-Haney et al., 2010
Membrane protein
FLOTILLIN 2 (FLOT2)RNAi
Medtr3g106420
-Lj1g3v1854330
Glyma.06G065600
Phvul.009G090700
n/a
Haney, C.H., and Long, S.R. (2010). Plant flotillins are required for infection by nitrogen-fixing bacteria. Proc Natl Acad Sci U S A 107, 478-483.
79
MtFLOT4Inf+/-Nod+/-Fix+/-Haney et al., 2010
Membrane protein
FLOTILLIN 4 (FLOT4)RNAi
Medtr3g106430
Mtr.11786.S1_at
Lj0g3v0315989,
Glyma.06G065600
Phvul.009G090700
n/a
Haney, C.H., and Long, S.R. (2010). Plant flotillins are required for infection by nitrogen-fixing bacteria. Proc Natl Acad Sci U S A 107, 478-483.
80
MtFNSIIn/aNod+/-n/aZhang et al., 2009
Enzyme (Synthase)
FLAVONE SYNTHASE (FNSII)RNAiMedtr7g027960
Mtr.1299.1.S1_s_at
-
Glyma.13G173500
Phvul.003G074000
n/a
Zhang, J., Subramanian, S., Stacey, G., and Yu, O. (2009). Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. The Plant Journal 57, 171-183.
81
GmFWL1n/aNod+/-n/aLibault et al., 2010MtGA2ox10
Unknown (PLAC8 domain containing)
FRUIT WEIGHT 2.2-LIKE 1 (FWL1)RNAi
Medtr6g084940
-
Chromosome location AP004536.1
Glyma.09G187000
Phvul.003G292900
n/a
Libault, M., Zhang, X.C., Govindarajulu, M., Qiu, J., Ong, Y.T., Brechenmacher, L., Berg, R.H., Hurley‐Sommer, A., Taylor, C.G., and Stacey, G. (2010). A member of the highly conserved FWL (tomato FW2. 2‐like) gene family is essential for soybean nodule organogenesis. The Plant Journal 62, 852-864.
82
MtGA2ox10Inf+/-Nod+/-, Nod*n/aKim et al., 2019
Enzyme (Oxidase)
GIBERELLIC ACID 20-OXIDASECRISPR/Cas9
Medtr4g074130
-Lj3g3v3500200
Glyma.11G104800, Glyma.12G029800
Phvul.011G032800
n/a
Kim, G.-B., Son, S.-U., Yu, H.-J., and Mun, J.-H. (2019). MtGA2ox10 encoding C20-GA2-oxidase regulates rhizobial infection and nodule development in Medicago truncatula. Scientific Reports 9, 5952.
83
GmGαn/aNod++n/aChoudhury and Pandey, 2015
Heterotrimeric G-protein complex subunit
Soybean heterotrimeric G PROTEINS (Ga)
RNAi
Medtr1g015750
Mtr.5675.1.S1_s_at
Lj5g3v0433470
Glyma.17G226700
Phvul.001G092700
n/a
Choudhury, S.R., and Pandey, S. (2015). Phosphorylation-dependent regulation of G-protein cycle during nodule formation in soybean. The Plant Cell 27, 3260-3276.
84
LjGLB1Inf+/-Nod+/-Fix+/-Fukudome et al., 2016
Oxygen carrier hemoprotein
non-symbiotic Class 1 HAEMOGLOBIN 1 (GLB1)
LORE1, TILLING
Medtr4g068860
Msa.878.1.S1_at
Lj4g3v0353440
Glyma.11G121800
Phvul.011G048700
n/a
Fukudome, M., Calvo-Begueria, L., Kado, T., Osuki, K.-i., Rubio, M.C., Murakami, E.-i., Nagata, M., Kucho, K.-i., Sandal, N., and Stougaard, J. (2016). Hemoglobin LjGlb1-1 is involved in nodulation and regulates the level of nitric oxide in the Lotus japonicus–Mesorhizobium loti symbiosis. Journal of experimental botany 67, 5275-5283.
85
GmGβ1/GmGβ2/GmGβ3/GmGβ4
n/aNod+/-, Nod*Fix*Choudhury and Pandey, 2013
Heterotrimeric G-protein complex subunit
Soybean heterotrimeric G PROTEINS (GmGβ1/GmGβ2/GmGβ3/GmGβ4)
RNAi
Medtr3g116500
Mtr.10712.1.S1_at
Lj1g3v3407660(GmGβ3); Lj1g3v3407660 (GmGβ2)
GmGβ1 (Glyma.12G043900), GmGβ2 (Glyma.11G118500), GmGβ3 (Glyma.06G013000), GmGβ4 (Glyma.04G013100)
Phvul.011G045900
n/a
Choudhury, S.R., and Pandey, S. (2013). Specific subunits of heterotrimeric G proteins play important roles during nodulation in soybean. Plant physiology 162, 522-533.
86
GmGγ1/GmGγ2/GmGγ3/GmGγ4/GmGγ5/GmGγ6/GmGγ7/GmGγ8/GmGγ9,GmGγ10
n/aNod+/-, Nod*Fix*Choudhury and Pandey, 2013
Heterotrimeric G-protein complex subunit
Soybean heterotrimeric G PROTEINS (GmGγ1/GmGγ2/GmGγ3/GmGγ4/GmGγ5/GmGγ6/GmGγ7/GmGγ8/GmGγ9,GmGγ10)
RNAi
Medtr1g071100
Mtr.7374.1.S1_at
Lj5g3v1014880 (GmGy1)
GmGγ1 (Glyma.10G03610), GmGγ2 (Glyma.02G16190), GmGγ3 (Glyma.20G33390), GmGγ4 (Glyma.10G32215), GmGγ5 (Glyma.11G18050), GmGγ6 (Glyma.14G17060), GmGγ7 (Glyma.17G29590), GmGγ8 (Glyma.15G19630), GmGγ9 (Glyma.17G05640), and GmGγ10 (Glyma.07G04510)
Phvul.007G175700
n/a
Choudhury, S.R., and Pandey, S. (2013). Specific subunits of heterotrimeric G proteins play important roles during nodulation in soybean. Plant physiology 162, 522-533.
87
LjHIPn/aNod++n/aKang et al., 2015
Molecular chaperone protein
HSC/HSP70 INTERACTING PROTEIN (HIP)
RNAi
Medtr4g102390
Mtr.40545.1.S1_a_at
Lj4g3v1327390
Glyma.05G051600, Glyma.17G133600
Phvul.003G214200
n/a
Kang, H., Xiao, A., Huang, X., Gao, X., Yu, H., He, X., Zhu, H., Hong, Z., and Zhang, Z. (2015). A Lotus japonicus cochaperone protein interacts with the ubiquitin-like domain protein CIP73 and plays a negative regulatory role in nodulation. Molecular Plant-Microbe Interactions 28, 534-545.
88
MtHMGR1Inf-Nod-n/aKevei et al., 2007
Enzyme (Oxidoreductase)
3-HYDROXY-3-METHYLGLUTARYL COENZYME A REDUCTASE 1 (HMGR1)
RNAi
Medtr5g026460
Mtr.40156.1.S1_at
Lj2g3v1574250.1
Glyma.01G156700
Phvul.006G008200
n/a
Kevei, Z., Lougnon, G., Mergaert, P., Horváth, G.V., Kereszt, A., Jayaraman, D., Zaman, N., Marcel, F., Regulski, K., and Kiss, G.B. (2007). 3-Hydroxy-3-methylglutaryl coenzyme A reductase1 interacts with NORK and is crucial for nodulation in Medicago truncatula. The Plant Cell 19, 3974-3989.
89
GmIFS1/GmIFS2n/aNod+/-n/aSubramanian et al., 2006
Enzyme (Synthase)
ISOFLAVONE SYNTHASE (IFS)RNAi
Medtr4g088160, Medtr4g088170, Medtr4g088195
Mtr.10492.1.S1_x_at, Mtr.40276.1.S1_at, Mtr.30765.1.S1_at
Lj4g3v0486150, Lj4g3v0485100, Lj4g3v0485090
Glyma.07G202300, Glyma.13G173500
Phvul.003G051700, Phvul.003G051800, Phvul.003G074000
n/a
Subramanian, S., Stacey, G., and Yu, O. (2006). Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. The Plant Journal 48, 261-273.
90
LjIGN1n/aNod+, Nod*Fix-, Fix*Kumagai et al., 2007
Membrane protein (Ankyrin-repeat domain)
INEFFECTIVE GREENISH NODULE 1 (IGN1)
Somatic mutation
Medtr7g100430
Mtr.11594.1.S1_at
Lj5g3v2288700
Glyma.20G241200, Glyma.10G291900
Phvul.007G008900
n/a
Kumagai, H., Hakoyama, T., Umehara, Y., Sato, S., Kaneko, T., Tabata, S., and Kouchi, H. (2007). A novel ankyrin-repeat membrane protein, IGN1, is required for persistence of nitrogen-fixing symbiosis in root nodules of Lotus japonicus. Plant Physiology 143, 1293-1305.
91
GmINS1n/aNod+/-Fix+/-Li et al., 2018
Cell wall component (b-expansin)
INCREASING NODULE SIZE 1 (INS1)RNAiMedtr1g032730
Mtr.32987.1.S1_at
Lj0g3v0264009
Glyma.07G172000
Phvul.003G016300
n/a
Li, X., Zheng, J., Yang, Y., and Liao, H. (2018a). INCREASING NODULE SIZE1 expression is required for normal rhizobial symbiosis and nodule development. Plant physiology 178, 1233-1248.
92
LjIPT3n/aNod++n/aSasaki et al., 2014
Enzyme (Transferase)
ISOPENTENYL TRANSFERASE (IPT3)LORE1
Medtr1g072540
Mtr.12113.1.S1_at
Lj5g3v0962690.1
Glyma.10G025300
Phvul.007G170100
n/a
Sasaki, T., Suzaki, T., Soyano, T., Kojima, M., Sakakibara, H., and Kawaguchi, M. (2014). Shoot-derived cytokinins systemically regulate root nodulation. Nature Communications 5, 4983.
93
LjKLVn/aNod++, Nod*n/aMiyazawa et al., 2010
Enzyme (Kinase; LRR-RLK)
KLAVIER (KLV)
Ion Beam Mutagenesis
Medtr6g015265, Medtr6g015190
Mtr.43460.1.S1_at, Mtr.9737.1.S1_at
Lj1g3v3023720
Glyma.18G267000, Glyma.13G056200
Phvul.004G037600
n/a
Miyazawa, H., Oka-Kira, E., Sato, N., Takahashi, H., Wu, G.-J., Sato, S., Hayashi, M., Betsuyaku, S., Nakazono, M., and Tabata, S. (2010). The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development 137, 4317-4325.
94
MtKNAT3/MtKNAT5/MtKNAT9/MtKNAT10
Inf+Nod+, Nod*n/aDi Giacomo et al., 2017
TF (KNOX Homeodomain)
KNOTTED-1 LIKE TAKE HOMEDOMAIN proteins (KNAT3/KNAT5/KNAT9/KNAT10)
RNAi
Medtr1g012960, Medtr3g106400, Medtr4g116545, Medtr2g461240
Lj1g3v1853300, Lj0g3v0268639, Lj6g3v1088990
Glyma.14G112400 (KNAT3), Glyma.04G064100 (KNAT5), Glyma.06G065200 (KNAT5), Glyma.17G104800 (KNAT9), Glyma.15G202200 (KNAT10)
Phvul.009G090500, Phvul.003G174900, Phvul.009G209500
n/a
Di Giacomo, E., Laffont, C., Sciarra, F., Iannelli, M.A., Frugier, F., and Frugis, G. (2017). KNAT3/4/5‐like class 2 KNOX transcription factors are involved in Medicago truncatula symbiotic nodule organ development. New Phytologist 213, 822-837.
95
LjLANInf-Nod+/-Fix+/-Suzaki et al., 2019
Multiprotein complex
LACK OF SYMBIONT ACCOMMODATION (LAN)
EMS, LORE1, CRISPR/Cas9
Medtr3g116260
Mtr.51430.1.S1_at
Lj3g3v3487860
Glyma.04G123300
Phvul.002G127500
Myc+/-
Suzaki, T., Takeda, N., Nishida, H., Hoshino, M., Ito, M., Misawa, F., Handa, Y., Miura, K., and Kawaguchi, M. (2019). LACK OF SYMBIONT ACCOMMODATION controls intracellular symbiont accommodation in root nodule and arbuscular mycorrhizal symbiosis in Lotus japonius. PLoS genetics 15, e1007865.
96
MtLAX2n/aNod+/-n/aRoy et al., 2017
Transporter (Auxin influx)
LIKE-AUX1 (LAX2)Tnt1
Medtr7g067450
Mtr.41246.1.S1_at
Lj0g3v0304149
Glyma.07G147000
Phvul.008G106300
Myc+
Roy, S., Robson, F., Lilley, J., Liu, C.-W., Cheng, X., Wen, J., Walker, S., Sun, J., Cousins, D., and Bone, C. (2017). MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis. Plant Physiology 174, 326-338.
97
LjLB1/LjLB2/LjLB3
Inf+Nod+Fix-Ott et al., 2005
Oxygen carrier hemoprotein
LEGHEMOGLOBIN (LB1/LB2/LB3)RNAi--
Lj5g3v0035290, Lj5g3v0035290, Lj5g3v0465970
--n/a
Ott, T., van Dongen, J.T., Gu, C., Krusell, L., Desbrosses, G., Vigeolas, H., Bock, V., Czechowski, T., Geigenberger, P., and Udvardi, M.K. (2005). Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Current biology 15, 531-535.
98
MtLIN, LjLINInf+/-, Inf*Nod*, White++n/aYano et al., 2009; Kiss et al., 2009
Enzyme (Ligase)
LUMPY InfectionS (LIN)LjcerberusEMS
Medtr1g090320
-Lj5g3v1697430
Glyma.10G194500
Phvul.007G136300
Myc+/-
Yano, K., Yoshida, S., Müller, J., Singh, S., Banba, M., Vickers, K., Markmann, K., White, C., Schuller, B., and Sato, S. (2008). CYCLOPS, a mediator of symbiotic intracellular accommodation. Proceedings of the National Academy of Sciences 105, 20540-20545., Kiss, E., Oláh, B., Kaló, P., Morales, M., Heckmann, A.B., Borbola, A., Lózsa, A., Kontár, K., Middleton, P., and Downie, J.A. (2009). LIN, a novel type of U-box/WD40 protein, controls early infection by rhizobia in legumes. Plant physiology 151, 1239-1249.
99
LjLNPInf-Nod-n/aRoberts et al., 2013
Enzyme (Hydrolase)
LECTIN NUCLEOTIDE PHOSPHOHYDROLASE (LNP)
Antisense
Medtr7g085150
Mtr.14668.1.S1_at
Lj1g3v3948070
Glyma.16G043300
Phvul.001G099900
Myc+/-
Roberts, N.J., Morieri, G., Kalsi, G., Rose, A., Stiller, J., Edwards, A., Xie, F., Gresshoff, P.M., Oldroyd, G.E., and Downie, J.A. (2013). Rhizobial and mycorrhizal symbioses in Lotus japonicus require lectin nucleotide phosphohydrolase, which acts upstream of calcium signaling. Plant physiology 161, 556-567.
100
MtLOG1n/aNod+/-n/aMortier et al., 2014
Enzyme (Hydrolase), cytokinin riboside 5′‐monophosphate phosphoribohydrolases
LONELYGUY1 (LOG1)RNAi
Medtr0041s0100
Mtr.39530.1.S1_s_at
Lj1g3v4580630
Glyma.03G181300
Phvul.001G177400
n/a
Mortier, V., Wasson, A., Jaworek, P., De Keyser, A., Decroos, M., Holsters, M., Tarkowski, P., Mathesius, U., and Goormachtig, S. (2014). Role of LONELY GUY genes in indeterminate nodulation on Medicago truncatula. New Phytologist 202, 582-593.