The putative transporter MtUMAMIT14 participates in nodule formation in Medicago truncatula

Garcia, Kevin; Cloghessy, Kaylee; Cooney, Danielle R.; Shelley, Brett; Chakraborty, Sanhita; Kafle, Arjun; Busidan, Aymeric; Sonawala, Unnati; Collier, Ray; Jayaraman, Dhileepkumar; Ané, Jean-Michel; Pilot, Guillaume

doi:10.1038/s41598-023-28160-8

The putative transporter MtUMAMIT14 participates in nodule formation in Medicago truncatula

Journal Article · Mon Jan 16 00:00:00 EST 2023 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-023-28160-8· OSTI ID:2420741

Garcia, Kevin ^[1]; Cloghessy, Kaylee ^[2]; Cooney, Danielle R. ^[3]; Shelley, Brett ^[4]; Chakraborty, Sanhita ^[5]; Kafle, Arjun ^[3]; Busidan, Aymeric ^[4]; Sonawala, Unnati ^[4]; Collier, Ray ^[5]; Jayaraman, Dhileepkumar ^[5]; Ané, Jean-Michel ^[5]; Pilot, Guillaume ^[4]

North Carolina State University, Raleigh, NC (United States); North Carolina State Univ., Raleigh, NC (United States)
University of Notre Dame, IN (United States); Univ. of Wisconsin, Madison, WI (United States)
North Carolina State University, Raleigh, NC (United States)
Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)
Univ. of Wisconsin, Madison, WI (United States)

Transport systems are crucial in many plant processes, including plant–microbe interactions. Nodule formation and function in legumes involve the expression and regulation of multiple transport proteins, and many are still uncharacterized, particularly for nitrogen transport. Amino acids originating from the nitrogen-fixing process are an essential form of nitrogen for legumes. This work evaluates the role of MtN21 (henceforth MtUMAMIT14), a putative transport system from the MtN21/EamA-like/UMAMIT family, in nodule formation and nitrogen fixation in Medicago truncatula. To dissect this transporter’s role, we assessed the expression of MtUMAMIT14 using GUS staining, localized the corresponding protein in M. truncatula root and tobacco leaf cells, and investigated two independent MtUMAMIT14 mutant lines. Our results indicate that MtUMAMIT14 is localized in endosomal structures and is expressed in both the infection zone and interzone of nodules. Comparison of mutant and wild-type M. truncatula indicates MtUMAMIT14, the expression of which is dependent on the presence of NIN, DNF1, and DNF2, plays a role in nodule formation and nitrogen-fixation. While the function of the transporter is still unclear, our results connect root nodule nitrogen fixation in legumes with the UMAMIT family.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Florida, Gainesville, FL (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDA; USDOE Office of Science (SC)

Grant/Contract Number:: SC0018247

OSTI ID:: 2420741

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 13; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (78)

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Hairy roots ? a short cut to transgenic root nodules Hansen, J�rgen; J�rgensen, Jan-Elo; Stougaard, Jens Plant Cell Reports, Vol. 8, Issue 1 https://doi.org/10.1007/BF00735768	journal	May 1989
Medicago truncatula syntaxin SYP132 defines the symbiosome membrane and infection droplet membrane in root nodules Catalano, Christina M.; Czymmek, Kirk J.; Gann, Janine G. Planta, Vol. 225, Issue 3 https://doi.org/10.1007/s00425-006-0369-y	journal	August 2006
An RNA-Seq transcriptome analysis revealing novel insights into aluminum tolerance and accumulation in tea plant Li, Yong; Huang, Jie; Song, Xiaowei Planta, Vol. 246, Issue 1 https://doi.org/10.1007/s00425-017-2688-6	journal	April 2017
NTR1 encodes a high affinity oligopeptide transporter in Arabidopsis Rentsch, Doris; Laloi, Maryse; Rouhara, Ila FEBS Letters, Vol. 370, Issue 3 https://doi.org/10.1016/0014-5793(95)00853-2	journal	August 1995
Amino acid transport in plants Fischer, W. Trends in Plant Science, Vol. 3, Issue 5 https://doi.org/10.1016/S1360-1385(98)01231-X	journal	May 1998
Amino Acid Export in Developing Arabidopsis Seeds Depends on UmamiT Facilitators Müller, Benedikt; Fastner, Astrid; Karmann, Julia Current Biology, Vol. 25, Issue 23 https://doi.org/10.1016/j.cub.2015.10.038	journal	December 2015
NODULE INCEPTION Recruits the Lateral Root Developmental Program for Symbiotic Nodule Organogenesis in Medicago truncatula Schiessl, Katharina; Lilley, Jodi L. S.; Lee, Tak Current Biology, Vol. 29, Issue 21 https://doi.org/10.1016/j.cub.2019.09.005	journal	November 2019
The way out and in: phloem loading and unloading of amino acids Tegeder, Mechthild; Hammes, Ulrich Z. Current Opinion in Plant Biology, Vol. 43 https://doi.org/10.1016/j.pbi.2017.12.002	journal	June 2018
Take a Trip Through the Plant and Fungal Transportome of Mycorrhiza Garcia, Kevin; Doidy, Joan; Zimmermann, Sabine D. Trends in Plant Science, Vol. 21, Issue 11 https://doi.org/10.1016/j.tplants.2016.07.010	journal	November 2016
Endoribonuclease-Based Two-Component Repressor Systems for Tight Gene Expression Control in Plants Liang, Yan; Richardson, Sarah; Yan, Jingwei ACS Synthetic Biology, Vol. 6, Issue 5 https://doi.org/10.1021/acssynbio.6b00295	journal	February 2017
A Golden Gate Modular Cloning Toolbox for Plants Engler, Carola; Youles, Mark; Gruetzner, Ramona ACS Synthetic Biology, Vol. 3, Issue 11 https://doi.org/10.1021/sb4001504	journal	February 2014
A plant regulator controlling development of symbiotic root nodules Schauser, Leif; Roussis, Andreas; Stiller, Jiri Nature, Vol. 402, Issue 6758 https://doi.org/10.1038/46058	journal	November 1999
Amino-acid cycling drives nitrogen fixation in the legume–Rhizobium symbiosis Lodwig, E. M.; Hosie, A. H. F.; Bourdès, A. Nature, Vol. 422, Issue 6933 https://doi.org/10.1038/nature01527	journal	April 2003
The Medicago genome provides insight into the evolution of rhizobial symbioses Young, Nevin D.; Debellé, Frédéric; Oldroyd, Giles E. D. Nature, Vol. 480, Issue 7378 https://doi.org/10.1038/nature10625	journal	November 2011
Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein Shaner, Nathan C.; Campbell, Robert E.; Steinbach, Paul A. Nature Biotechnology, Vol. 22, Issue 12 https://doi.org/10.1038/nbt1037	journal	November 2004
Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis Ranocha, Philippe; Dima, Oana; Nagy, Réka Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3625	journal	October 2013
Nodule cysteine-rich peptides maintain a working balance during nitrogen-fixing symbiosis Pan, Huairong; Wang, Dong Nature Plants, Vol. 3, Issue 5 https://doi.org/10.1038/nplants.2017.48	journal	May 2017
High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method Gietz, R. Daniel; Schiestl, Robert H. Nature Protocols, Vol. 2, Issue 1 https://doi.org/10.1038/nprot.2007.13	journal	January 2007
Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants Oldroyd, Giles E. D. Nature Reviews Microbiology, Vol. 11, Issue 4 https://doi.org/10.1038/nrmicro2990	journal	March 2013
The drug/metabolite transporter superfamily: The DMT superfamily Jack, Donald L.; Yang, Nelson M.; H. Saier, Milton European Journal of Biochemistry, Vol. 268, Issue 13 https://doi.org/10.1046/j.1432-1327.2001.02265.x	journal	July 2001
Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids Prell, J.; White, J. P.; Bourdes, A. Proceedings of the National Academy of Sciences, Vol. 106, Issue 30 https://doi.org/10.1073/pnas.0903653106	journal	July 2009
Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation Ivanov, S.; Fedorova, E. E.; Limpens, E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 21 https://doi.org/10.1073/pnas.1200407109	journal	May 2012
NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production Soyano, Takashi; Hirakawa, Hideki; Sato, Shusei Proceedings of the National Academy of Sciences, Vol. 111, Issue 40 https://doi.org/10.1073/pnas.1412716111	journal	September 2014
Detailed characterization of the UMAMIT proteins provides insight into their evolution, amino acid transport properties, and role in the plant Zhao, Chengsong; Pratelli, Réjane; Yu, Shi Journal of Experimental Botany, Vol. 72, Issue 18 https://doi.org/10.1093/jxb/erab288	journal	July 2021
UMAMIT14 is an amino acid exporter involved in phloem unloading in Arabidopsis roots Besnard, Julien; Pratelli, Réjane; Zhao, Chengsong Journal of Experimental Botany, Vol. 67, Issue 22 https://doi.org/10.1093/jxb/erw412	journal	November 2016
Arabidopsis UMAMIT24 and 25 are amino acid exporters involved in seed loading Besnard, Julien; Zhao, Chengsong; Avice, Jean-Christophe Journal of Experimental Botany, Vol. 69, Issue 21 https://doi.org/10.1093/jxb/ery302	journal	August 2018
MEGA11: Molecular Evolutionary Genetics Analysis Version 11 Tamura, Koichiro; Stecher, Glen; Kumar, Sudhir Molecular Biology and Evolution, Vol. 38, Issue 7 https://doi.org/10.1093/molbev/msab120	journal	April 2021
Amino Acid Export in Plants: A Missing Link in Nitrogen Cycling Okumoto, Sakiko; Pilot, Guillaume Molecular Plant, Vol. 4, Issue 3 https://doi.org/10.1093/mp/ssr003	journal	May 2011
MtExpress, a Comprehensive and Curated RNAseq-based Gene Expression Atlas for the Model Legume Medicago truncatula Carrere, Sebastien; Verdier, Jerome; Gamas, Pascal Plant and Cell Physiology, Vol. 62, Issue 9 https://doi.org/10.1093/pcp/pcab110	journal	July 2021
Medicago truncatula IPD3 Is a Member of the Common Symbiotic Signaling Pathway Required for Rhizobial and Mycorrhizal Symbioses Horváth, Beatrix; Yeun, Li Huey; Domonkos, Ágota Molecular Plant-Microbe Interactions, Vol. 24, Issue 11 https://doi.org/10.1094/MPMI-01-11-0015	journal	November 2011
Use of a Subtractive Hybridization Approach to Identify New Medicago truncatula Genes Induced During Root Nodule Development Gamas, Pascal Molecular Plant-Microbe Interactions, Vol. 9, Issue 4 https://doi.org/10.1094/MPMI-9-0233	journal	January 1996
Saprophytic Intracellular Rhizobia in Alfalfa Nodules Timmers, Antonius C. J.; Soupène, Eric; Auriac, Marie-Christine Molecular Plant-Microbe Interactions®, Vol. 13, Issue 11 https://doi.org/10.1094/MPMI.2000.13.11.1204	journal	November 2000
Agrobacterium rhizogenes -Transformed Roots of Medicago truncatula for the Study of Nitrogen-Fixing and Endomycorrhizal Symbiotic Associations Boisson-Dernier, Aurélien; Chabaud, Mireille; Garcia, Fernand Molecular Plant-Microbe Interactions®, Vol. 14, Issue 6 https://doi.org/10.1094/MPMI.2001.14.6.695	journal	June 2001
Nitrogen Fixation Mutants of Medicago truncatula Fail to Support Plant and Bacterial Symbiotic Gene Expression Starker, Colby G.; Parra-Colmenares, Adriana L.; Smith, Lucinda Plant Physiology, Vol. 140, Issue 2 https://doi.org/10.1104/pp.105.072132	journal	January 2006
Medicago truncatula NIN Is Essential for Rhizobial-Independent Nodule Organogenesis Induced by Autoactive Calcium/Calmodulin-Dependent Protein Kinase Marsh, John F.; Rakocevic, Alexandra; Mitra, Raka M. Plant Physiology, Vol. 144, Issue 1 https://doi.org/10.1104/pp.106.093021	journal	March 2007
Siliques Are Red1 from Arabidopsis Acts as a Bidirectional Amino Acid Transporter That Is Crucial for the Amino Acid Homeostasis of Siliques Ladwig, Friederike; Stahl, Mark; Ludewig, Uwe Plant Physiology, Vol. 158, Issue 4 https://doi.org/10.1104/pp.111.192583	journal	February 2012
A Medicago truncatula Tobacco Retrotransposon Insertion Mutant Collection with Defects in Nodule Development and Symbiotic Nitrogen Fixation Pislariu, Catalina I.; D. Murray, Jeremy; Wen, JiangQi Plant Physiology, Vol. 159, Issue 4 https://doi.org/10.1104/pp.112.197061	journal	June 2012
A Positive Regulator of Nodule Organogenesis, NODULE INCEPTION, Acts as a Negative Regulator of Rhizobial Infection in Lotus japonicus Yoro, Emiko; Suzaki, Takuya; Toyokura, Koichi Plant Physiology, Vol. 165, Issue 2 https://doi.org/10.1104/pp.113.233379	journal	April 2014
Physiological Responses and Gene Co-Expression Network of Mycorrhizal Roots under K ⁺ Deprivation Garcia, Kevin; Chasman, Deborah; Roy, Sushmita Plant Physiology, Vol. 173, Issue 3 https://doi.org/10.1104/pp.16.01959	journal	February 2017
The Nitrate Transporter Family Protein LjNPF8.6 Controls the N-Fixing Nodule Activity Valkov, Vladimir Totev; Rogato, Alessandra; Alves, Ludovico Martins Plant Physiology, Vol. 175, Issue 3 https://doi.org/10.1104/pp.17.01187	journal	September 2017
NIN Acts as a Network Hub Controlling a Growth Module Required for Rhizobial Infection Liu, Cheng-Wu; Breakspear, Andrew; Guan, Dian Plant Physiology, Vol. 179, Issue 4 https://doi.org/10.1104/pp.18.01572	journal	February 2019
Transport of Organic Solutes in Phloem and Xylem of a Nodulated Legume Pate, John S.; Atkins, Craig A.; Hamel, Kathy Plant Physiology, Vol. 63, Issue 6 https://doi.org/10.1104/pp.63.6.1082	journal	June 1979
MedicagoN2-Fixing Symbiosomes Acquire the Endocytic Identity Marker Rab7 but Delay the Acquisition of Vacuolar Identity Limpens, Erik; Ivanov, Sergey; van Esse, Wilma The Plant Cell, Vol. 21, Issue 9 https://doi.org/10.1105/tpc.108.064410	journal	September 2009
A Rab1 GTPase Is Required for Transport between the Endoplasmic Reticulum and Golgi Apparatus and for Normal Golgi Movement in Plants Batoko, Henri; Zheng, Huan-Quan; Hawes, Chris The Plant Cell, Vol. 12, Issue 11 https://doi.org/10.1105/tpc.12.11.2201	journal	November 2000
Four Genes of Medicago truncatula Controlling Components of a Nod Factor Transduction Pathway Catoira, Romy; Galera, Christine; de Billy, Francoise The Plant Cell, Vol. 12, Issue 9 https://doi.org/10.1105/tpc.12.9.1647	journal	September 2000
The NIN Transcription Factor Coordinates Diverse Nodulation Programs in Different Tissues of the Medicago truncatula Root Vernié, Tatiana; Kim, Jiyoung; Frances, Lisa The Plant Cell, Vol. 27, Issue 12 https://doi.org/10.1105/tpc.15.00461	journal	December 2015
Ex vitro composite plants: an inexpensive, rapid method for root biology Collier, Ray; Fuchs, Beth; Walter, Nathalie The Plant Journal, Vol. 43, Issue 3 https://doi.org/10.1111/j.1365-313X.2005.02454.x	journal	July 2005
Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula Tadege, Million; Wen, Jiangqi; He, Ji The Plant Journal, Vol. 54, Issue 2 https://doi.org/10.1111/j.1365-313X.2008.03418.x	journal	April 2008
Walls are thin 1 (WAT1), an Arabidopsis homolog of Medicago truncatula NODULIN21, is a tonoplast-localized protein required for secondary wall formation in fibers: Tonoplastic WAT1 and secondary wall formation Ranocha, Philippe; Denancé, Nicolas; Vanholme, Ruben The Plant Journal, Vol. 63, Issue 3 https://doi.org/10.1111/j.1365-313X.2010.04256.x	journal	May 2010
Soybean ureide transporters play a critical role in nodule development, function and nitrogen export: Nitrogen transport in soybean nodules Collier, Ray; Tegeder, Mechthild The Plant Journal, Vol. 72, Issue 3 https://doi.org/10.1111/j.1365-313X.2012.05086.x	journal	August 2012
Utility of the P19 suppressor of gene‐silencing protein for production of therapeutic antibodies in Nicotiana expression hosts Garabagi, Freydoun; Gilbert, Erin; Loos, Andreas Plant Biotechnology Journal, Vol. 10, Issue 9 https://doi.org/10.1111/j.1467-7652.2012.00742.x	journal	September 2012
Adaptation of Medicago truncatula to nitrogen limitation is modulated via local and systemic nodule developmental responses Jeudy, Christian; Ruffel, Sandrine; Freixes, Sandra New Phytologist, Vol. 185, Issue 3 https://doi.org/10.1111/j.1469-8137.2009.03103.x	journal	December 2009
Local and systemic N signaling are involved in Medicago truncatula preference for the most efficient Sinorhizobium symbiotic partners Laguerre, Gisèle; Heulin‐Gotty, Karine; Brunel, Brigitte New Phytologist, Vol. 195, Issue 2 https://doi.org/10.1111/j.1469-8137.2012.04159.x	journal	May 2012
Hormone modulation of legume‐rhizobial symbiosis Liu, Huan; Zhang, Chi; Yang, Jun Journal of Integrative Plant Biology, Vol. 60, Issue 8 https://doi.org/10.1111/jipb.12653	journal	June 2018
RTP1 encodes a novel endoplasmic reticulum (ER)‐localized protein in Arabidopsis and negatively regulates resistance against biotrophic pathogens Pan, Qiaona; Cui, Beimi; Deng, Fengyan New Phytologist, Vol. 209, Issue 4 https://doi.org/10.1111/nph.13707	journal	October 2015
Source and sink mechanisms of nitrogen transport and use Tegeder, Mechthild; Masclaux-Daubresse, Céline New Phytologist, Vol. 217, Issue 1 https://doi.org/10.1111/nph.14876	journal	November 2017
Medicago truncatula Ferroportin2 mediates iron import into nodule symbiosomes Escudero, Viviana; Abreu, Isidro; Tejada‐Jiménez, Manuel New Phytologist, Vol. 228, Issue 1 https://doi.org/10.1111/nph.16642	journal	May 2020
The functional characterization of LjNRT2.4 indicates a novel, positive role of nitrate for an efficient nodule N ₂ ‐fixation activity Valkov, Vladimir Totev; Sol, Stefano; Rogato, Alessandra New Phytologist, Vol. 228, Issue 2 https://doi.org/10.1111/nph.16728	journal	July 2020
Nutrient demand and fungal access to resources control the carbon allocation to the symbiotic partners in tripartite interactions of Medicago truncatula: Carbon allocation in tripartite interactions Kafle, Arjun; Garcia, Kevin; Wang, Xiurong Plant, Cell & Environment, Vol. 42, Issue 1 https://doi.org/10.1111/pce.13359	journal	August 2018
MtMOT1.2 is responsible for molybdate supply to Medicago truncatula nodules Gil‐Díez, Patricia; Tejada‐Jiménez, Manuel; León‐Mediavilla, Javier Plant, Cell & Environment, Vol. 42, Issue 1 https://doi.org/10.1111/pce.13388	journal	July 2018
An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing Roux, Brice; Rodde, Nathalie; Jardinaud, Marie-Françoise The Plant Journal, Vol. 77, Issue 6 https://doi.org/10.1111/tpj.12442	journal	February 2014
Functional characterization and physiological roles of the single Shaker outward K⁺ channel in Medicago truncatula Drain, Alice; Thouin, Julien; Wang, Limin The Plant Journal, Vol. 102, Issue 6 https://doi.org/10.1111/tpj.14697	journal	March 2020
Legumes Symbioses: Absence of Nod Genes in Photosynthetic Bradyrhizobia Giraud, Eric; Moulin, Lionel; Vallenet, David Science, Vol. 316, Issue 5829 https://doi.org/10.1126/science.1139548	journal	June 2007
Cloning and nucleotide sequencing of Rhizobium meliloti aminotransferase genes: an aspartate aminotransferase required for symbiotic nitrogen fixation is atypical Watson, R. J.; Rastogi, V. K. Journal of Bacteriology, Vol. 175, Issue 7 https://doi.org/10.1128/jb.175.7.1919-1928.1993	journal	April 1993
Getting around the legume nodule: I. The structure of the peripheral zone in four nodule types Guinel, Frédérique C. Botany, Vol. 87, Issue 12 https://doi.org/10.1139/B09-074	journal	December 2009
Getting around the legume nodule: II. Molecular biology of its peripheral zone and approaches to study its vasculature Guinel, Frédérique C. Botany, Vol. 87, Issue 12 https://doi.org/10.1139/B09-075	journal	December 2009
Proton-Coupled Sugar and Amino Acid Transporters in Plants Bush, D. R. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 44, Issue 1 https://doi.org/10.1146/annurev.pp.44.060193.002501	journal	June 1993
Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis Gomez, S. Karen; Javot, Hélène; Deewatthanawong, Prasit BMC Plant Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2229-9-10	journal	January 2009
Very bright orange fluorescent plants: endoplasmic reticulum targeting of orange fluorescent proteins as visual reporters in transgenic plants Mann, David GJ; Abercrombie, Laura L.; Rudis, Mary R. BMC Biotechnology, Vol. 12, Issue 1 https://doi.org/10.1186/1472-6750-12-17	journal	January 2012
Disruption of the Lotus japonicus transporter LjNPF2.9 increases shoot biomass and nitrate content without affecting symbiotic performances Sol, Stefano; Valkov, Vladimir Totev; Rogato, Alessandra BMC Plant Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12870-019-1978-5	journal	August 2019
Fate map of Medicago truncatula root nodules Xiao, T. T.; Schilderink, S.; Moling, S. Development, Vol. 141, Issue 18 https://doi.org/10.1242/dev.110775	journal	September 2014
Rhizobium meliloti Genes Encoding Catabolism of Trigonelline Are Induced under Symbiotic Conditions Boivin, Catherine; Camut, Sylvie; Malpica, Carlos A. The Plant Cell, Vol. 2, Issue 12 https://doi.org/10.2307/3869336	journal	December 1990
MtMTP2-Facilitated Zinc Transport Into Intracellular Compartments Is Essential for Nodule Development in Medicago truncatula León-Mediavilla, Javier; Senovilla, Marta; Montiel, Jesús Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00990	journal	July 2018
Interaction and Regulation of Carbon, Nitrogen, and Phosphorus Metabolisms in Root Nodules of Legumes Liu, Ailin; Contador, Carolina A.; Fan, Kejing Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01860	journal	December 2018
Metabolic and Transcriptional Reprogramming in Developing Soybean (Glycine max) Embryos Collakova, Eva; Aghamirzaie, Delasa; Fang, Yihui Metabolites, Vol. 3, Issue 2 https://doi.org/10.3390/metabo3020347	journal	May 2013
Multiple Autoregulation of Nodulation (AON) Signals Identified through Split Root Analysis of Medicago truncatula sunn and rdn1 Mutants Kassaw, Tessema; Jr., William; Frugoli, Julia Plants, Vol. 4, Issue 2 https://doi.org/10.3390/plants4020209	journal	April 2015
Disruption of the Lotus japonicus transporter LjNPF2.9 increases shoot biomass and nitrate content without affecting symbiotic performances Sol, Stefano; Valkov, Vladimir; Rogato, Alessandra figshare https://doi.org/10.6084/m9.figshare.c.4650596	collection	January 2019

Similar Records

MtSWEET11, a Nodule-Specific Sucrose Transporter of Medicago truncatula

Journal Article · Sun Mar 27 20:00:00 EDT 2016 · Plant Physiology (Bethesda) · OSTI ID:1438839

Temporal change in chromatin accessibility predicts regulators of nodulation in Medicago truncatula

Journal Article · Tue Nov 08 19:00:00 EST 2022 · BMC Biology · OSTI ID:1975673

Related Subjects

58 GEOSCIENCES
Science & Technology - Other Topics

The putative transporter MtUMAMIT14 participates in nodule formation in Medicago truncatula

Citation Formats

References (78)

Similar Records

Related Subjects