Table A1.
Genes involved in regulation of arbuscular mycorrhiza and/or root nodule symbiosis.
| Genes | Organism | Structural characteristics | (putative) Localization | Mutants/transformed lines analyzed | phenotypes of the mutants/transformed lines | Involvement in | (putative) Function | References |
|---|---|---|---|---|---|---|---|---|
| (Ph)PDR1 | P. hybrida | ATP-binding cassette transporter subtype G (ABCG) | Plasma membrane | Transposon insertion mutant and KD RNAi lines in petunia plants; A. thaliana OE lines | Silenced lines: delay in AM colonization, strigolactone exudate levels affected; A. thaliana OE lines: higher tolerance to the synthetic strigolactone less retained into roots. | AM | Strigolactone exporter | Kretzschmar et al., 2012 |
| (Lj)NFR1/(Mt)LYK3 | L. japonicus/M. truncatula | LYK | Plasma membrane | (1,2,3) Mutants from a T-DNA insertion screen (Ljnfr1-1/Ljsym1-1, Ljnfr1-2/Ljsym1-2) (4) M. truncatula EMS-induced mutants B56/hcl-1, W1/hcl-2, AF3/hcl-3 (5) KD RNAi transformed roots. (6) M. truncatula EMS-induced mutants hcl-1, hcl-2, hcl-3, AC6/hcl-4/lyk3-4 | (1,2) Nod- phenotype, AM not affected (Ami+). (3) No root hair deformation, no root hair curling, no infection threads nor nodule primordia induced. (4) HCL stands for defective in root hair curling; only root hair deformation and reduced cortical cell division without meristematic cells. (5) Upon inoculation with a rhizobia strain mutated for the NF: root hair curling but decrease of IT number, ITs with a sac-like structure aborted in the root hair. (6) Concerning the fourth lyk3 mutant hcl-4: normal root hair curling observed, ITs with a sac-like shape and often aborted, few nodules. | RNS | NF receptor | (1) Schauser et al., 1998; (2) Wegel et al., 1998; (3) Radutoiu et al., 2003; (4) Catoira et al., 2001; (5) (Limpens et al., 2003); (6) Smit et al., 2007 |
| (Lj)NFR5/(Mt)NFP/(Pa)NFP | L. japonicus/M. truncatula/P. andersonii | LYK | Plasma membrane | (1,3,4,5) Mutant from a T-DNA insertion mutants screen (282-894/Ljnfr5-1/Ljsym5), Ac-TE insertion mutant (Ljnfr5-2), (2) EMS-induced mutant (EMS223/Ljnfr5-3/Ljsym25); (6,7) EMS-induced mutants (Mtnfp-1, Mtnfp-2), KD RNAi transformed roots; (8) KD RNAi transformed roots (PaNFP) | (1,2) Nod- phenotype. (1,3) Ami+ phenotypes. (2) (4, 5) Nod- phenotype and unresponsiveness to inoculation with M. loti or application of NF (no root hair deformation). (6,7) EMS-induced mutants: Nod- phenotype, absolutely no sign of RNS, even root hair deformation. (7) Silenced lines: ITs abortions in root hair cells, with sac-like structures. (8) Impairment of both RNS and AM. | RNS (and AM for P. andersonii) | NF receptor | (1) Schauser et al., 1998; (2) Szczyglowski et al., 1998 (3) Wegel et al., 1998; (4) Madsen et al., 2003; (5) Radutoiu et al., 2003; (6) Ben Amor et al., 2003; (7) Arrighi et al., 2006; (8) Op Den Camp et al., 2011 |
| (At)CERK1/(Os)CERK1 | A. thaliana/O. sativa | LYK | Plasma membrane | (1) KO transposon and T-DNA insertion mutants Atcerk1-1 and Atcerk1-2; (2,6) KO T-DNA insertion mutant Atcerk1-2; (3,4) KO T-DNA Atcerk1-2 and Atcerk1-3 mutants; (5) KD RNAi OsCERK1 lines | (1) No responses to chitin, including MAPK activation, ROS generation, and gene expression; impairment of disease resistance against the incompatible fungus Alternaria brassicicola. (2) Impairment of chitin-responsive genes, increase of fungal but not of bacterial growth (Erysiphe cichoracearum and Alternaria brassicicola; and Pto DC3000 respectively). (3) Enhanced growth of the virulent bacterial strain Pto DC3000 and the non-pathogenic strain Pto DC3000 hrcC. (4) Impairment of FRK1 induction after chitin and PGN treatment, as well as PGN-responsive genes. (5) Impairment of specific ROS generation and of phytoalexins accumulation. (6) Impairment of ROS generation, defense-related genes. | Defense | Chitin and PGN receptor | (1) Miya et al., 2007; (2) Wan et al., 2008; (3) Gimenez-Ibanez et al., 2009; (4) Willmann et al., 2011; (5) Shimizu et al., 2010; (6) Shinya et al., 2012 |
| (At)LYM2/(Os)CEBiP | A. thaliana/O. sativa | LYM | Plasma membrane | (1) OsCEBiP KO RNAi lines; (2) transposon insertion mutants lym2-2, lym2-3 | (1) Suppression of the specific ROS generation and impairment of gene responses induced by chitin. (2) No impairment of ROS generation. | Defense | Chitin receptor | (1) Kaku et al., 2006; (2) Shinya et al., 2012 |
| (At)LYK4 | A. thaliana | LYK | Plasma membrane | T-DNA insertion mutant lyk4 | Impairment of chitin-responsive genes, increase of fungal and bacterial growth (Alternaria brassicicola and Pto DC3000 respectively). | Defense | Chitin receptor | Wan et al., 2012 |
| (At)LYM1 | A. thaliana | LYM | Plasma membrane | (1) T-DNA insertion mutants lym1-1, lym1-2; (2) T-DNA insertion mutant lym1-1, transposon insertion mutant lym1-2 | Impairment of FRK1 induction after PGN treatment, as well as PGN-responsive genes; enhanced growth of Pto DC3000. (2) No impairment of ROS generation (lym1-2). | Defense | PGN receptor | (1) Willmann et al., 2011; (2) Shinya et al., 2012 |
| (At)LYM3 | A. thaliana | LYM | Plasma membrane | (1,2) cs lym3-1, lym3-2 | (1) Impairment of FRK1 induction after PGN treatment, as well as PGN-responsive genes; enhanced growth of Pto DC3000, Pto DC3000 hrcC- and the hypovirulent Pto DC3000 Δ avrPto/PtoB. (2) No impairment of ROS generation (lym3-1). | Defense | PGN receptor | (1) Willmann et al., 2011; (2) Shinya et al., 2012 |
| (Lj)SYMRK/(Ms)NORK/(Mt)DMI2 | L. japonicus/M. sativa/M. truncatula | LRR-RLK | Plasma membrane and IT | (1,2,7) L. japonicus EMS-induced mutant (EMS61/Ljsym21-2) and (1,3,4,7) mutants from a transposon/T-DNA insertion mutants screen (282-287/Ljsym2-1, cac41.5); (5,6) M. sativa MN-1008 mutant obtained from crosses between different cultivars; (8) M. truncatula KD RNAi transformed roots, transformed roots with the RNAi hairpin construct ENOD12::DMI2i, and 35S::DMI2-transformed roots from the TR25 mutant (lowering DMI2 activity in the nodule apex) | (1) Nod- phenotype. (2) Amplified swelling and branching, but no curling of root hairs when inoculated with M. loti. No more induction of the leghaemoglobin gene. (3,4) Coi- and Nod- phenotypes. (5,6,7) Myc- and Nod- phenotypes. (8) RNAi transformed roots: few nodules formed, in which ITs but few symbiosomes were observed; transformed roots with the RNAi hairpin or 35S::DMI2 constructs: more nodules formed, ITs growth amplified, with enlarged and branched ITs, but no symbiosomes observed, Fix- phenotype. | Common SYM pathway | Required for accommodation in both symbioses; positioned between NF perception and calcium spiking in the common SYM pathway | (1) Szczyglowski et al., 1998 (2) Stracke et al., 2002; (3) Schauser et al., 1998; (4) Wegel et al., 1998; (5) Caetano-Anollés and Gresshoff, 1991; (6) Endre et al., 2002; (7) Kistner et al., 2005; (8) Limpens et al., 2005 |
| (Lj)SIP2 | L. japonicus | MAPKK | Plasma membrane-associated and cytoplasm | KD RNAi transformed roots | Strong down-regulation of three marker genes for IT and nodule primordium formation; impairment of IT and nodulation formation. | RNS | Functional MAPKK interacting with SYMRK and that could be involved in the regulation of early symbiotic signal transduction and nodule organogenesis may be due to the inhibitory effect of SYMRK on its activity | Chen et al., 2012 |
| (Lj)SINA4 | L. japonicus | E3 ubiquitin ligase | Cytoplasm | OE transformed roots and OE transgenic lines | OE transformed roots: reduced SYMRK protein levels upon M. loti inoculation; OE transgenic lines: decrease of infection events and number of ITs, increase of white nodules, thick and branched ITs in both white and pink nodules, no or few bacteroids observed. | RNS | SYMRK turnover | Den Herder et al., 2012 |
| (Mt)PUB1 | M. truncatula | E3 ubiquitin ligase | Plasma membrane-associated | OE and KD RNAi transformed roots in the wild-type background and in the hcl-4 (lyk3-4) background | OE transformed roots: delay in nodulation observed; KD transformed roots (wt background): number of nodules strongly increased only upon S. meliloti mutant strains (nodL, nodFnodL: NF modified at the non-reducing end); KD transformed roots (hcl-4 background): impairment of nodulation and IT development observed in hcl-4 mutant overcame. | RNS* | Functional E3 ubiquitin ligase that interacts with LYK3 physically and functionally by regulating negatively infection and nodulation | Mbengue et al., 2010 |
| (Lj)SYMREM1/(Mt)SYMREM1 | L. japonicus/M. truncatula | Remorin | Host-derived membrane-associated with a localization to nodular ITs, more strongly at the tip where unwalled infection droplets form, and symbiosomes | (1) KD RNAi transformed roots, stable RNAi lines, Tnt1-transposon insertion mutants; (2) OE transformed roots | (1) RNAi transformed roots: no or few nodulation, often with small and white nodules, multiplication of IT formation, IT often aborted, highly branched or with a sac-like structure. Stable RNAi lines: enlargement of ITs and absence of symbiosome, suggesting a delay in rhizobia release into host cells; KO line: morphological change of nodule shape, enlarged and highly branched ITs, almost no symbiosomes formed. (2) Increase of mature nodules number but not in IT number. | RNS | Role in RNS accommodation and hypothesized to supervise localization, sorting and regulation of LjNFR1/MtLYK3, LjNFR5/MtNFP and LjSYMRK/MtDMI2 during RN symbiosis in plasma membrane sub-domains. | (1) Lefebvre et al., 2010; (2) Toth et al., 2012 |
| (Mt)HMGR1 | M. truncatula | 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase | Vesicle-like structures | Pharmacological inhibition and KD RNAi transformed roots | Pharmacological inhibition: decrease of nodule number; KD transformed roots: nodulation strongly decreased, with ITs and nodules development arrested at an early step, Fix- phenotype. | RNS* | HMGR1 activity is required for nodule development; four hypotheses were mentioned concerning the recruitment of HMGR1 by NORK and the link with the mevalonic acid (MVA) pathway | Kevei et al., 2007 |
| (Mt)FLOT2 | M. truncatula | Flotillin-like | Plasma membrane-associated microdomains | KD RNAi and amiRNA transformed roots | Few infection events, normal IT development but great part of small and white nodules; also decrease in primary root length as well as increase in lateral root length. | RNS | Required for IT initiation | Haney and Long, 2010 |
| (Mt)FLOT4 | M. truncatula | Flotillin-like | Plasma membrane-associated microdomains | KD RNAi and amiRNA transformed roots | Few infection events, ITs largely aborted in root hair, great part of small and white nodules; also increase in the number of secondary lateral roots. | RNS | Required for IT initiation and development | Haney and Long, 2010 |
| (Mt)MSBP1 | M. truncatula | Membrane-bound steroid-binding protein | Nuclear membranes and surrounding ER | Transformed roots with KD RNAi lines | KD lines: frequency of mycorrhizal colonization unchanged but infection sites often aborted. In case of successful infection sites, septated hyphae and collapsed arbuscules observed. | AM | Sterol homeostasis | Kuhn et al., 2010 |
| (Lj)CASTOR and (Lj)POLLUX/(Mt)DMI1 | L. japonicus/M. truncatula | Ion channel | Nuclear membranes, (5) preferentially the inner nuclear membrane | (3,4,5,6) EMS-induced mutant (EMS1749/Ljsym4-2); (2,3,4,5,6) mutant from a T-DNA insertion screen (282-227/Ljsym4-1); (1,5,6) EMS-induced mutant (EMS46/Ljsym22-1); (5) EMS-induced mutant, T-DNA insertion mutants, somaclonal variation-induced mutants; (7,9) EMS-induced mutants (dmi1-1/C71, dmi1-2/B129); (8,9) fast neutron bombardment-induced mutant (dmi1-4) | (1) Nod- phenotype. (2) Coi- phenotype. (3,6) Nod- phenotype. No root hair curling, no IT. (3,4,6) Myc- phenotype for Ljsym4-2, rare infection events and delay in arbuscule formation for Ljsym4-1 and Ljsym22-1. (5) No penetration of endosymbionts, with no root hairs curling neither calcium spiking during RNS, and abortion of infection attempts in AM. (7,8) Nod- phenotype. | Common SYM pathway | Cation channel that could trigger a potassium influx at the nuclear envelope and be involved in a compensatory mechanism with the release of Ca2+ during calcium spiking around the nucleus | (1) Szczyglowski et al., 1998 (2) Wegel et al., 1998; (3) Bonfante et al., 2000; (4) Novero et al., 2002; (5) Imaizumi-Anraku et al., 2005; (6) Kistner et al., 2005; (7) Catoira et al., 2000; (8) Ané et al., 2004 |
| (Lj)NUP85 | L. japonicus | Nucleoporin | Nuclear membranes | EMS-induced mutants (1,3,4,5,6) EMS76/Ljsym24-1/Ljnup85-1, (3,2,7) EMS1-1E/Ljnup85-2/Ljsym73 (3,7) EMS1-6F/Ljnup85-3/Ljsym85 | (1) Nod- phenotype for Ljsym24. (2) Low nodulation and Ami+. (3) Nod- and Myc- phenotypes for Ljsym24 and Ljsym85; low nodulation for Ljsym73. (4) No ITs, low nodulation with Fix- phenotype, arbuscule formation delayed. (6) Nod- Ami- phenotypes. (5) Root hair deformation but impairment of calcium spiking. (7) Root hair branching after NF treatment, few ITs, no calcium spiking recorded, Coi- phenotype. Less AM and RNS impairments at reduced temperatures. | Common SYM pathway | NPC component | (1) Szczyglowski et al., 1998 (2) Kawaguchi et al., 2002; (3) Kawaguchi et al., 2005; (4) Kistner et al., 2005; (5) Miwa et al., 2006; (6) Sandal et al., 2006; (7) Saito et al., 2007 |
| (Lj)NUP133 | L. japonicus | Nucleoporin | Nuclear membranes | T-DNA insertion mutants (1,3,4) 5371-22/nup133-1/Ljsym3-1, (1,2,4) 2557-1/nup133-2/Ljsym3-2; (4) nup133-4/Ljsym45; (3,4) EMS-induced mutant EMS247/nup133-3/Ljsym3-3 | (1) Nod- and Coi- phenotypes for Ljsym3-2. (2) Coi- phenotype. (3) No ITs, low nodulation with Fix- phenotype, Coi- phenotype, rarely arbuscules formation observed but strongly delayed. (4) No calcium spiking recorded for Ljsym3-1; for several Ljnup133 mutants root hair swelling and branching, but not root hair curling, few ITs, strong defects in nodule development, from no nodules formed to small ineffective nodules (Fix- phenotype) with almost no infected cells. Less AM and RNS impairments at reduced temperatures. | Common SYM pathway | NPC component | (1) Schauser et al., 1998; (2) Wegel et al., 1998; (3) Kistner et al., 2005; (4) Kanamori et al., 2006 |
| (Lj)NENA | L. japonicus | Nucleoporin | Nuclear membranes | EMS-induced mutants nena-1 to nena-5, C6+ ion beam irradiated mutant nena-6 | Coi- phenotype, rare successful colonization with normal arbuscules, no root hair infection, Nod- phenotype (nena-1 and nena-2) to few nodules (nena-3), impairment of calcium spiking (nena-1). No symbiotic defects for nena-4 and nena-5. Less AM and RNS impairments at reduced temperatures. | Common SYM pathway | NPC component proposed to be involved in import to the nucleus of proteins required for calcium spiking | Groth et al., 2010 |
| (Mt)MCA8 | M. truncatula | SERCA-type calcium ATPase | Nuclear membranes and ER | KD RNAi transformed roots | Silenced lines affected in NF-induced calcium spiking but no defects in nodulation, reduced AM colonization, with several aborted penetration attempts, and strongly reduced arbuscules and vesicles. | AM and RNS | Required for calcium oscillations with reloading nuclear envelope and ER lumen in calcium | Capoen et al., 2011 |
| (Mt)SYP132 | M. truncatula | Syntaxin | Plasma membrane, IT, unwalled droplets and symbiosome | – | – | RNS | Vesicle trafficking during IT/symbiosome formation | Catalano et al., 2004, 2007; Limpens et al., 2009; Ivanov et al., 2012 |
| (Mt)VAMP721d and (Mt)VAMP721e | M. truncatula | SNARE | Vesicles closed to unwalled droplets, near or on membranes of developing symbiosomes; over PAM, in particular thin branches | KD RNAi transformed roots concerning both VAMP721d and VAMP721e | Impairment of symbiosome formation, with numerous nodular ITs but no or rare symbiosomes observed, “unwalled droplets” actually with a thin cell wall, and impairment of arbuscule formation, stopped before mature arbuscule development | AM and RNS | Common symbiotic regulators in exocytotic vesicle trafficking | Ivanov et al., 2012 |
| (Mt)DNF1 | M. truncatula | 22-kD subunit (SPC22) of the signal peptidase complex (SPC) | ER-like structures | Fast neutron bombardment mutants | (1) Accumulation of nodule-specific cysteine-rich (NCR) peptides in the ER. (2) No terminal differentiation of bacteroids, Fix-phenotype. | RNS | Proper secretion of components involved in functional symbiosomes | (1) Van De Velde et al., 2010; (2) Wang et al., 2010b |
| (Ph)PAM1/(Mt)VAPYRIN | P. hybrida/M. truncatula | MSP and ANK domains | Cytoplasm, mobile spherical structures, nucleus | (1,2) Transposon mutants; (3) KD RNAi transformed roots; (4) four fast-neutron mutants, tansposon mutant lines | (1,2,3,5) Difficulties to penetrate epidermis cells, no functional arbuscules found. (4) Normal root hair curling, but numerous infection events, abnormal IT development and small, white and uninfected nodules | AM and RNS | Role in RNS and AM fungal accommodation, acting downstream of the calcium signal of the common SYM pathway, may be involved in membrane and/or cargo trafficking | (1) Sekhara Reddy et al., 2007; (2) Feddermann et al., 2010; (3) Pumplin et al., 2010; (4) Murray et al., 2011 |
Ami, AM infection; Coi-, Absence of cortex invasion; Fix-, defective in nitrogen fixation; KD, Knockdown; KO, Knockout; Myc-, Non-mycorrhizal; Nod-, Non-nodulating; OE, Overexpression; PGN, peptidoglycan; Pto DC3000, Pseudomonas syringae pathovar tomato strain DC3000; RNAi, RNA interference; ROS, Reactive oxygen species
*
up-regulated during AM.