Arbuscular-Mycorrhizal Symbiosis in Medicago Regulated by the Transcription Factor MtbHLHm1;1 and the Ammonium Facilitator Protein MtAMF1;3
Abstract
:1. Introduction
2. Results
2.1. Both bHLHm1 and AMF Classes of Proteins Are Found in Mycorrhizal and Non-Inoculated Plants
2.2. MtbHLHm1;1 and MtAMF1;3 Are Differentially Expressed in Mycorrhizal and Unincoulated Roots
2.3. MtbHLHm1;1 Affects Mycorrhizal Arbuscule Abundance and AM Pi Responses in Roots
2.4. Cellular Localisation of MtbHLHm1;1 and MtAMF1;3 in AM Fungal Colonised Roots
2.5. MtbHLHm1;1 and MtAMF1;3 Influence Ammonium Transport in Yeast Cells
3. Discussion
3.1. MtbHLhm1;1 and MtAMF1;3 Are Required for the AM Fungal Symbiosis in Medicago
3.2. Loss of MtAMF1;3 Activity Disrupts Mycorrhizal Activity
4. Materials and Methods
4.1. Plant Materials, AM Fungi and Growth Conditions
4.2. Promoter GUS Reporter Analysis
4.3. Protein Localisation and Confocal Microscopy
4.4. Electromobility Shift Analysis
4.5. RNA Interference and Mycorrhizal Phenotype Analysis
4.6. Plant Biomass Measurements
4.7. RNA Extraction, cDNA Synthesis and Gene Expression Analysis
4.8. Yeast Mutant 26972c Complementation and 14C-Methylammonium Uptake
4.9. MtbHLHm1;1 and MtAMF1 Homology Search and Analysis of Phylogeny
4.10. Statistical Analysis
4.11. Accession Numbers
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Azcón-Aguilar, C.; Bago, B.; Barea, J.M. Saprophitic growth of AMF. In Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology, 2nd ed.; Varma, A., Hock, B., Eds.; Springer: Berlin/Heidelberg, Germany, 1999; pp. 391–407. [Google Scholar]
- Smith, S.E.; Read, D.J. Mycorrhizal Symbiosis, 3rd ed.; Academic Press: Amsterdam, The Netherlands, 2008; p. 815. [Google Scholar]
- Genre, A.; Chabaud, M.; Timmers, T.; Bonfante, P.; Barker, D. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 2005, 17, 3489–3499. [Google Scholar] [CrossRef]
- Pimprikar, P.; Gutjahr, C. Transcriptional regulation of arbuscular mycorrhiza development. Plant Cell Physiol. 2018, 59, 678–695. [Google Scholar] [CrossRef]
- Deng, J.; Zhu, F.G.; Liu, J.X.; Zhao, Y.F.; Wen, J.Q.; Wang, T.; Dong, J.L. Transcription Factor bHLH2 Represses CYSTEINE PROTEASE77 to Negatively Regulate Nodule Senescence. Plant Physiol. 2019, 181, 1683–1703. [Google Scholar] [CrossRef]
- Diedhiou, I.; Diouf, D. Transcription factors network in root endosymbiosis establishment and development. World J. Microb. Biot. 2018, 34, 37. [Google Scholar] [CrossRef]
- Godiard, L.; Lepage, A.; Moreau, S.; Laporte, D.; Verdenaud, M.; Timmers, T.; Gamas, P. MtbHLH1, a bHLH transcription factor involved in Medicago truncatula nodule vascular patterning and nodule to plant metabolic exchanges. New Phytol. 2011, 191, 391–404. [Google Scholar] [CrossRef]
- Chakraborty, S.; Valdes-Lopez, O.; Stonoha-Arther, C.; Ane, J.M. Transcription Factors Controlling the Rhizobium-Legume Symbiosis: Integrating Infection, Organogenesis and the Abiotic Environment. Plant Cell Physiol. 2022, 63, 1326–1343. [Google Scholar] [CrossRef]
- Lindsay, P.L.; Williams, B.N.; MacLean, A.; Harrison, M.J. A Phosphate-Dependent Requirement for Transcription Factors IPD3 and IPD3L During Arbuscular Mycorrhizal Symbiosis in Medicago truncatula. Mol. Plant-Microbe Interact. 2019, 32, 1277–1290. [Google Scholar] [CrossRef]
- Zanetti, M.E.; Ripodas, C.; Niebel, A. Plant NF-Y transcription factors: Key players in plant-microbe interactions, root development and adaptation to stress. Biochim. Biophys. Acta (BBA)-Gene Regul. Mech. 2017, 1860, 645–654. [Google Scholar] [CrossRef]
- Xue, L.; Klinnawee, L.; Zhou, Y.; Saridis, G.; Vijayakumar, V.; Brands, M.; Dörmann, P.; Gigolashvili, T.; Turck, F.; Bucher, M. AP2 transcription factor CBX1 with a specific function in symbiotic exchange of nutrients in mycorrhizal Lotus japonicus. Proc. Natl. Acad. Sci. USA 2018, 115, E9239–E9246. [Google Scholar] [CrossRef]
- Jiang, Y.; Xie, Q.; Wang, W.; Yang, J.; Zhang, X.; Yu, N.; Zhou, Y.; Wang, E. Medicago AP2-Domain Transcription Factor WRI5a Is a Master Regulator of Lipid Biosynthesis and Transfer during Mycorrhizal Symbiosis. Mol. Plant 2018, 11, 1344–1359. [Google Scholar] [CrossRef]
- Harrison, M.J.; Dewbre, G.R.; Liu, J. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 2002, 14, 2413–2429. [Google Scholar] [CrossRef]
- Karandashov, V.; Bucher, M. Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci. 2005, 10, 22–29. [Google Scholar] [CrossRef]
- Krajinski, F.; Courty, P.-E.; Sieh, D.; Franken, P.; Zhang, H.; Bucher, M.; Gerlach, N.; Kryvoruchko, I.; Zoeller, D.; Udvardi, M.; et al. The H+-ATPase HA1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis. Plant Cell 2014, 26, 1808–1817. [Google Scholar] [CrossRef]
- Bravo, A.; Brands, M.; Wewer, V.; Dörmann, P.; Harrison, M.J. Arbuscular mycorrhiza-specific enzymes FatM and RAM2 fine-tune lipid biosynthesis to promote development of arbuscular mycorrhiza. New Phytol. 2017, 214, 1631–1645. [Google Scholar] [CrossRef]
- Luginbuehl, L.H.; Menard, G.N.; Kurup, S.; Van Erp, H.; Radhakrishnan, G.V.; Breakspear, A.; Oldroyd, G.E.D.; Eastmond, P.J. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 2017, 356, 1175–1178. [Google Scholar] [CrossRef]
- Keymer, A.; Pimprikar, P.; Wewer, V.; Huber, C.; Brands, M.; Bucerius, S.L.; Delaux, P.-M.; Klingl, V.; Röpenack-Lahaye, E.v.; Wang, T.L.; et al. Lipid transfer from plants to arbuscular mycorrhiza fungi. eLife 2017, 6, e29107. [Google Scholar] [CrossRef]
- Liu, Y.; von Wirén, N. Ammonium as a signal for physiological and morphological responses in plants. J. Exp. Bot. 2017, 68, 2581–2592. [Google Scholar] [CrossRef]
- Xuan, Y.H.; Priatama, R.A.; Huang, J.; Je, B.I.; Liu, J.M.; Park, S.J.; Piao, H.L.; Son, D.Y.; Lee, J.J.; Park, S.H.; et al. Indeterminate domain 10 regulates ammonium-mediated gene expression in rice roots. New Phytol. 2013, 197, 791–804. [Google Scholar] [CrossRef]
- Pantoja, O. High affinity ammonium transporters: Molecular mechanism of action. Front. Plant Sci. 2012, 3, 34. [Google Scholar] [CrossRef]
- Wu, Y.; Yang, W.; Wei, J.; Yoon, H.; An, G. Transcription factor OsDOF18 controls ammonium uptake by inducing ammonium transporters in rice roots. Mol. Cells 2017, 40, 178–185. [Google Scholar] [CrossRef]
- Das, D.; Paries, M.; Hobecker, K.; Gigl, M.; Dawid, C.; Lam, H.M.; Zhang, J.H.; Chen, M.X.; Gutjahr, C. PHOSPHATE STARVATION RESPONSE transcription factors enable arbuscular mycorrhiza symbiosis. Nat. Commun. 2022, 13, 477. [Google Scholar] [CrossRef] [PubMed]
- Shi, J.C.; Zhao, B.Y.; Zheng, S.; Zhang, X.W.; Wang, X.L.; Dong, W.T.; Xie, Q.J.; Wang, G.; Xiao, Y.P.; Chen, F.; et al. A phosphate starvation response-centered network regulates mycorrhizal symbiosis. Cell 2021, 184, 5527. [Google Scholar] [CrossRef] [PubMed]
- Nouri, E.; Breuillin-Sessoms, F.; Feller, U.; Reinhardt, D. Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in Petunia hybrida. PLoS ONE 2014, 9, e90841. [Google Scholar] [CrossRef]
- Mäder, P.; Edenhofer, S.; Boller, T.; Wiemken, A.; Niggli, U. Arbuscular mycorrhizae in a long-term field trial comparing low-input (organic, biological) and high-input (conventional) farming systems in a crop rotation. Biol. Fertil. Soils 2000, 31, 150–156. [Google Scholar] [CrossRef]
- Govindarajulu, M.; Pfeffer, P.E.; Jin, H.; Abubaker, J.; Douds, D.D.; Allen, J.W.; Bucking, H.; Lammers, P.J.; Shachar-Hill, Y. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 2005, 435, 819–823. [Google Scholar] [CrossRef]
- Guether, M.; Neuhäuser, B.; Balestrini, R.; Dynowski, M.; Ludewig, U.; Bonfante, P. A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol. 2009, 150, 73–83. [Google Scholar] [CrossRef]
- Hodge, A.; Fitter, A.H. Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc. Natl. Acad. Sci. USA 2010, 107, 13754–13759. [Google Scholar] [CrossRef] [PubMed]
- Fellbaum, C.R.; Gachomo, E.W.; Beesetty, Y.; Choudhari, S.; Strahan, G.D.; Pfeffer, P.E.; Kiers, E.T.; Bucking, H. Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. USA 2012, 109, 2666–2671. [Google Scholar] [CrossRef]
- Smith, S.E.; Smith, F.A. Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 2011, 62, 227–250. [Google Scholar] [CrossRef]
- Kobae, Y.; Tamura, Y.; Takai, S.; Banba, M.; Hata, S. Localized Expression of Arbuscular Mycorrhiza-Inducible Ammonium Transporters in Soybean. Plant Cell Physiol. 2010, 51, 1411–1415. [Google Scholar] [CrossRef]
- Koegel, S.; Lahmidi, N.A.; Arnould, C.; Chatagnier, O.; Walder, F.; Ineichen, K.; Boller, T.; Wipf, D.; Wiemken, A.; Courty, P.E. The family of ammonium transporters (AMT) in Sorghum bicolor: Two AMT members are induced locally, but not systemically in roots colonized by arbuscular mycorrhizal fungi. New Phytol. 2013, 198, 853–865. [Google Scholar] [CrossRef] [PubMed]
- Breuillin-Sessoms, F.; Floss, D.S.; Gomez, S.K.; Pumplin, N.; Ding, Y.; Levesque-Tremblay, V.; Noar, R.D.; Daniels, D.A.; Bravo, A.; Eaglesham, J.B.; et al. Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter4 mutants is dependent on the ammonium transporter 2 family protein AMT2;3. Plant Cell 2015, 27, 1352–1366. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.P.; Zhou, W.Q.; Wu, J.D.; Xie, K.L.; Li, X.Y. LjAMT2;2 Promotes Ammonium Nitrogen Transport during Arbuscular Mycorrhizal Fungi Symbiosis in Lotus japonicus. Int. J. Mol. Sci. 2022, 23, 9522. [Google Scholar] [CrossRef] [PubMed]
- Chiasson, D.M.; Loughlin, P.C.; Mazurkiewicz, D.; Mohammadidehcheshmeh, M.; Fedorova, E.E.; Okamoto, M.; McLean, E.; Glass, A.D.M.; Smith, S.E.; Bisseling, T.; et al. Soybean SAT1 (Symbiotic Ammonium Transporter 1) encodes a bHLH transcription factor involved in nodule growth and NH4+ transport. Proc. Natl. Acad. Sci. USA 2014, 111, 4814–4819. [Google Scholar] [CrossRef] [PubMed]
- Kaiser, B.N.; Finnegan, P.M.; Tyerman, S.D.; Whitehead, L.F.; Bergersen, F.J.; Day, D.A.; Udvardi, M.K. Characterization of an ammonium transport protein from the peribacteroid membrane of soybean nodules. Science 1998, 281, 1202–1206. [Google Scholar] [CrossRef] [PubMed]
- Vargas, R.C.; García-Salcedo, R.; Tenreiro, S.; Teixeira, M.C.; Fernandes, A.R.; Ramos, J.; Sá-Correia, I. Saccharomyces cerevisiae multidrug resistance transporter Qdr2 is implicated in potassium uptake, providing a physiological advantage to quinidine-stressed cells. Eukaryot. Cell 2007, 6, 134–142. [Google Scholar] [CrossRef] [PubMed]
- Dias, P.J.; Sá-Correia, I. The drug:H(+) antiporters of family 2 (DHA2), siderophore transporters (ARN) and glutathione:H(+) antiporters (GEX) have a common evolutionary origin in hemiascomycete yeasts. BMC Genom. 2013, 14, 901. [Google Scholar] [CrossRef]
- Schmitz, A.M.; Harrison, M.J. Signaling events during initiation of arbuscular mycorrhizal symbiosis. J. Integr. Plant Biol. 2014, 56, 250–261. [Google Scholar] [CrossRef]
- Streng, A.; op den Camp, R.; Bisseling, T.; Geurts, R. Evolutionary origin of Rhizobium Nod factor signaling. Plant Signal. Behav. 2011, 6, 1510–1514. [Google Scholar] [CrossRef]
- Sohlenkamp, C.; Shelden, M.; Howitt, S.; Udvardi, M. Characterization of Arabidopsis AtAMT2, a novel ammonium transporter in plants. FEBS Lett. 2000, 467, 273–278. [Google Scholar] [CrossRef]
- Simon-Rosin, U.; Wood, C.; Udvardi, M.K. Molecular and cellular characterisation of LjAMT2; 1, an ammonium transporter from the model legume Lotus japonicus. Plant Mol. Biol. 2003, 51, 99–108. [Google Scholar] [CrossRef] [PubMed]
- Couturier, J.; Montanini, B.; Martin, F.; Brun, A.; Blaudez, D.; Chalot, M. The expanded family of ammonium transporters in the perennial poplar plant. New Phytol. 2007, 174, 137–150. [Google Scholar] [CrossRef] [PubMed]
- Straub, D.; Ludewig, U.; Neuhäuser, B. A nitrogen-dependent switch in the high affinity ammonium transport in Medicago truncatula. Plant Mol. Biol. 2014, 86, 485–494. [Google Scholar] [CrossRef]
- Javot, H.l.n.; Penmetsa, R.V.; Terzaghi, N.; Cook, D.R.; Harrison, M.J. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. USA 2007, 104, 1720–1725. [Google Scholar] [CrossRef] [PubMed]
- Barker, D.G.; Bianchi, S.; Blondon, F.; Dattée, Y.; Duc, G.; Essad, S.; Flament, P.; Gallusci, P.; Génier, G.; Guy, P.; et al. Medicago truncatula, a model plant for studying the molecular genetics of the Rhizobium-legume symbiosis. Plant Mol. Biol. Rep. 1990, 8, 40–49. [Google Scholar] [CrossRef]
- Mohammadi-Dehcheshmeh, M.; Ebrahimie, E.; Tyerman, S.; Kaiser, B. A novel method based on combination of semi-in vitro and in vivo conditions in Agrobacterium rhizogenes-mediated hairy root transformation of Glycine species. Vitr. Cell. Dev. Biol. Plant 2013, 50, 282–291. [Google Scholar] [CrossRef]
- Livak, K.J.; Schmittgen, T.D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef]
- Balzergue, C.; Puech-Pagès, V.; Bécard, G.; Rochange, S.F. The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. J. Exp. Bot. 2011, 62, 1049–1060. [Google Scholar] [CrossRef]
- Balzergue, C.; Chabaud, M.; Barker, D.G.; Becard, G.; Rochange, S.F. High phosphate reduces host ability to develop arbuscular mycorrhizal symbiosis without affecting root calcium spiking responses to the fungus. Front. Plant Sci. 2013, 4, 426. [Google Scholar] [CrossRef]
- Vierheilig, H.; Coughlan, A.P.; Wyss, U.; Piche, Y. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl. Environ. Microbiol. 1998, 64, 5004–5007. [Google Scholar] [CrossRef]
- McGonigle, T.P.; Miller, M.H.; Evans, D.G.; Fairchild, G.L.; Swan, J.A. A new method which gives an objective measure of colonization of roots by vesicular—Arbuscular mycorrhizal fungi. New Phytol. 1990, 115, 495–501. [Google Scholar] [CrossRef] [PubMed]
- Bhattacharyya, J.; Chowdhury, A.H.; Ray, S.; Jha, J.K.; Das, S.; Gayen, S.; Chakraborty, A.; Mitra, J.; Maiti, M.K.; Basu, A.; et al. Native polyubiquitin promoter of rice provides increased constitutive expression in stable transgenic rice plants. Plant Cell Rep. 2012, 31, 271–279. [Google Scholar] [CrossRef]
- Marini, A.M.; Springael, J.Y.; Frommer, W.B.; Andre, B. Cross-talk between ammonium transporters in yeast and interference by the soybean SAT1 protein. Mol. Microbiol. 2000, 35, 378–385. [Google Scholar] [CrossRef]
- Pao, S.S.; Paulsen, I.T.; Saier, M.H., Jr. Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 1998, 62, 1–34. [Google Scholar] [CrossRef] [PubMed]
- Gbelska, Y.; Krijger, J.J.; Breunig, K.D. Evolution of gene families: The multidrug resistance transporter genes in five related yeast species. FEMS Yeast Res. 2006, 6, 345–355. [Google Scholar] [CrossRef] [PubMed]
- Sá-Correia, I.; dos Santos, S.C.; Teixeira, M.C.; Cabrito, T.R.; Mira, N.P. Drug:H+ antiporters in chemical stress response in yeast. Trends Microbiol. 2009, 17, 22–31. [Google Scholar] [CrossRef]
- Gaude, N.; Bortfeld, S.; Duensing, N.; Lohse, M.; Krajinski, F. Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J. 2012, 69, 510–528. [Google Scholar] [CrossRef]
- Karas, B.; Amyot, L.; Johansen, C.; Sato, S.; Tabata, S.; Kawaguchi, M.; Szczyglowski, K. Conservation of Lotus and Arabidopsis Basic Helix-Loop-Helix Proteins Reveals New Players in Root Hair Development. Plant Physiol. 2009, 151, 1175–1185. [Google Scholar] [CrossRef]
- Breuillin, F.; Schramm, J.; Hajirezaei, M.; Ahkami, A.; Favre, P.; Druege, U.; Hause, B.; Bucher, M.; Kretzschmar, T.; Bossolini, E.; et al. Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J. 2010, 64, 1002–1017. [Google Scholar] [CrossRef]
- Kobae, Y.; Ohmori, Y.; Saito, C.; Yano, K.; Ohtomo, R.; Fujiwara, T. Phosphate treatment strongly inhibits new arbuscule development but not the maintenance of arbuscule in mycorrhizal rice roots. Plant Physiol. 2016, 171, 566–579. [Google Scholar] [CrossRef]
- Zeng, H.Q.; Wang, G.P.; Zhang, Y.Q.; Hu, X.Y.; Pi, E.X.; Zhu, Y.Y.; Wang, H.Z.; Du, L.Q. Genome-wide identification of phosphate-deficiency-responsive genes in soybean roots by high-throughput sequencing. Plant Soil. 2016, 398, 207–227. [Google Scholar] [CrossRef]
- Kobae, Y. Dynamic Phosphate Uptake in Arbuscular Mycorrhizal Roots Under Field Conditions. Front. Environ. Sci. 2019, 6, 159. [Google Scholar] [CrossRef]
- Trejo, D.; Banuelos, J.; Gavito, M.E.; Sangabriel-Conde, W. High phosphorus fertilization reduces mycorrhizal colonization and plant biomass of three cultivars of pineapple. Terra Lat. 2020, 38, 853–858. [Google Scholar] [CrossRef]
- Zhang, S.Y.; Nie, Y.Y.; Fan, X.N.; Wei, W.; Chen, H.; Xie, X.A.; Tang, M. A transcriptional activator from Rhizophagus irregularis regulates phosphate uptake and homeostasis in AM symbiosis during phosphorous starvation. Front. Microbiol. 2023, 13, 1114089. [Google Scholar] [CrossRef] [PubMed]
- Tanaka, Y.; Yano, K. Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ. 2005, 28, 1247–1254. [Google Scholar] [CrossRef]
- Koegel, S.; Boller, T.; Lehmann, M.F.; Wiemken, A.; Courty, P.E. Rapid nitrogen transfer in the Sorghum bicolor-Glomus mosseae arbuscular mycorrhizal symbiosis. Plant Signal. Behav. 2013, 8, e25229. [Google Scholar] [CrossRef]
- Koegel, S.; Brulé, D.; Wiemken, A.; Boller, T.; Courty, P.-E. The effect of different nitrogen sources on the symbiotic interaction between Sorghum bicolor and Glomus intraradices: Expression of plant and fungal genes involved in nitrogen assimilation. Soil. Biol. Biochem. 2015, 86, 159–163. [Google Scholar] [CrossRef]
- Fahraeus, G. The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen. Microbiol. 1957, 16, 374–381. [Google Scholar] [CrossRef]
- Mankin, S.L.; Hill, D.S.; Olhoft, P.M.; Toren, E.; Wenck, A.R.; Nea, L.; Xing, L.; Brown, J.A.; Fu, H.; Ireland, L.; et al. Disarming and sequencing of Agrobacterium rhizogenes strain K599 (NCPPB2659) plasmid pRi2659. Vitr. Cell. Dev. Biol. Plant 2007, 43, 521–535. [Google Scholar] [CrossRef]
- Limpens, E.; Ramos, J.; Franken, C.; Raz, V.; Compaan, B.; Franssen, H.; Bisseling, T.; Geurts, R. RNA interference in Agrobacterium rhizogenes-transformed roots of Arabidopsis and Medicago truncatula. J. Exp. Bot. 2004, 55, 983–992. [Google Scholar] [CrossRef]
- Limpens, E.; Mirabella, R.; Fedorova, E.; Franken, C.; Franssen, H. Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc. Natl. Acad. Sci. USA 2005, 102, 10375. [Google Scholar] [CrossRef] [PubMed]
- Deguchi, Y.; Banba, M.; Shimoda, Y.; Chechetka, S.A.; Suzuri, R.; Okusako, Y.; Ooki, Y.; Toyokura, K.; Suzuki, A.; Uchiumi, T.; et al. Transcriptome profiling of Lotus japonicus roots during arbuscular mycorrhiza development and comparison with that of nodulation. DNA Res. 2007, 14, 117–133. [Google Scholar] [CrossRef] [PubMed]
- Trouvelot, A. Mesure du taux de mycorhization VA d’un systeme radiculaire. Recherche de methodes d’estimation ayant une significantion fonctionnelle. In Physiological and Genetical Aspects of Mycorrhizae; INRA: Paris, France, 1986; pp. 217–221. [Google Scholar]
- Ivanov, S.; Fedorova, E.E.; Limpens, E.; De Mita, S.; Genre, A.; Bonfante, P.; Bisseling, T. Rhizobium–legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc. Natl. Acad. Sci. USA 2012, 109, 8316–8321. [Google Scholar] [CrossRef] [PubMed]
- Gietz, D.; St.Jean, A.; Woods, R.A.; Schiestl, R.H. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 1992, 20, 1425. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ovchinnikova, E.; Chiasson, D.; Wen, Z.; Wu, Y.; Tahaei, H.; Smith, P.M.C.; Perrine-Walker, F.; Kaiser, B.N. Arbuscular-Mycorrhizal Symbiosis in Medicago Regulated by the Transcription Factor MtbHLHm1;1 and the Ammonium Facilitator Protein MtAMF1;3. Int. J. Mol. Sci. 2023, 24, 14263. https://doi.org/10.3390/ijms241814263
Ovchinnikova E, Chiasson D, Wen Z, Wu Y, Tahaei H, Smith PMC, Perrine-Walker F, Kaiser BN. Arbuscular-Mycorrhizal Symbiosis in Medicago Regulated by the Transcription Factor MtbHLHm1;1 and the Ammonium Facilitator Protein MtAMF1;3. International Journal of Molecular Sciences. 2023; 24(18):14263. https://doi.org/10.3390/ijms241814263
Chicago/Turabian StyleOvchinnikova, Evgenia, David Chiasson, Zhengyu Wen, Yue Wu, Hero Tahaei, Penelope M. C. Smith, Francine Perrine-Walker, and Brent N. Kaiser. 2023. "Arbuscular-Mycorrhizal Symbiosis in Medicago Regulated by the Transcription Factor MtbHLHm1;1 and the Ammonium Facilitator Protein MtAMF1;3" International Journal of Molecular Sciences 24, no. 18: 14263. https://doi.org/10.3390/ijms241814263