A dipeptide transporter from the arbuscular mycorrhizal fungus Rhizophagus irregularis is upregulated in the intraradical phase

Belmondo, Simone; Fiorilli, Valentina; Perez-Tienda, Jacob; Ferrol, Nuria; Marmeisse, Roland; Lanfranco, Luisa

doi:10.3389/fpls.2014.00436

Title: A dipeptide transporter from the arbuscular mycorrhizal fungus Rhizophagus irregularis is upregulated in the intraradical phase

Journal Article · Wed Sep 03 00:00:00 EDT 2014 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2014.00436· OSTI ID:1628261

Belmondo, Simone ^[1]; Fiorilli, Valentina ^[2]; Perez-Tienda, Jacob ^[3]; Ferrol, Nuria ^[3]; Marmeisse, Roland ^[4]; Lanfranco, Luisa ^[1]

University of Torino (Italy)
Consiglio Nazionale delle Ricerche, Torino (Italy)
Consejo Superior de Investigaciones Cientificas, Granada (Spain)
University of Torino (Italy); Université de Lyon, Villeurbanne (France)

Arbuscular mycorrhizal fungi (AMF), which form an ancient and widespread mutualistic symbiosis with plants, are a crucial but still enigmatic component of the plant micro biome. Nutrient exchange has probably been at the heart of the success of this plant-fungus interaction since the earliest days of plants on land. To characterize genes from the fungal partner involved in nutrient exchange, and presumably important for the functioning of the AM symbiosis, genome-wide transcriptomic data obtained from the AMF Rhizophagus irregularis were exploited. A gene sequence, showing amino acid sequence and transmembrane domains profile similar to members of the PTR2 family of fungal oligopeptide transporters, was identified and called RiPTR2. The functional properties of RiPTR2 were investigated by means of heterologous expression in Saccharomyces cerevisiae mutants defective in either one or both of its di/tripeptide transporter genes PTR2 and DAL5. These assays showed that RiPTR2 can transport dipeptides such as Ala-Leu, Ala-Tyr or Tyr-Ala. From the gene expression analyses it seems that RiPTR2 responds to different environmental clues when the fungus grows inside the root and in the extraradical phase.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Joint Genome Institute (JGI), Berkeley, CA (United States); Univ. of Torino (Italy)

Sponsoring Organization:: USDOE; Spanish Ministry of Economy and Competitiveness

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1628261

Journal Information:: Frontiers in Plant Science, Vol. 5; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (70)

Quantification on the LightCycler Rasmussen, Randy Rapid Cycle Real-Time PCR https://doi.org/10.1007/978-3-642-59524-0_3	book	January 2001
The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont Tisserant, E.; Kohler, A.; Dozolme-Seddas, P. New Phytologist, Vol. 193, Issue 3 https://doi.org/10.1111/j.1469-8137.2011.03948.x	journal	November 2011
AtPTR1, a plasma membrane peptide transporter expressed during seed germination and in vascular tissue of Arabidopsis: Peptide transporter of Arabidopsis Dietrich, Daniela; Hammes, Ulrich; Thor, Kathrin The Plant Journal, Vol. 40, Issue 4 https://doi.org/10.1111/j.1365-313X.2004.02224.x	journal	September 2004
The molecular components of the extracellular protein-degradation pathways of the ectomycorrhizal fungus Paxillus involutus Shah, Firoz; Rineau, Francois; Canbäck, Björn New Phytologist, Vol. 200, Issue 3 https://doi.org/10.1111/nph.12425	journal	July 2013
Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance Kuzyakov, Yakov; Xu, Xingliang New Phytologist, Vol. 198, Issue 3 https://doi.org/10.1111/nph.12235	journal	March 2013
Uptake of organic nitrogen by plants: Tansley review Näsholm, Torgny; Kielland, Knut; Ganeteg, Ulrika New Phytologist, Vol. 182, Issue 1 https://doi.org/10.1111/j.1469-8137.2008.02751.x	journal	February 2009
Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis Fellbaum, C. R.; Gachomo, E. W.; Beesetty, Y. Proceedings of the National Academy of Sciences, Vol. 109, Issue 7 https://doi.org/10.1073/pnas.1118650109	journal	January 2012
A family of oligopeptide transporters is required for growth of Candida albicans on proteins [Correction] Molecular Microbiology, Vol. 62, Issue 3, p. 916-916 https://doi.org/10.1111/j.1365-2958.2006.05388.x	journal	September 2006
Oligopeptide transport and regulation of extracellular proteolysis are required for growth of Aspergillus fumigatus on complex substrates but not for virulence: Oligopeptide transporters of A. fumigatus Hartmann, Thomas; Cairns, Timothy C.; Olbermann, Patrick Molecular Microbiology, Vol. 82, Issue 4 https://doi.org/10.1111/j.1365-2958.2011.07868.x	journal	October 2011
Structural and functional characterization of AtPTR3, a stress-induced peptide transporter of Arabidopsis Karim, Sazzad; Lundh, Dan; Holmström, Kjell-Ove Journal of Molecular Modeling, Vol. 11, Issue 3 https://doi.org/10.1007/s00894-005-0257-6	journal	May 2005
Nitrogen transfer in the arbuscular mycorrhizal symbiosis Govindarajulu, Manjula; Pfeffer, Philip E.; Jin, Hairu Nature, Vol. 435, Issue 7043 https://doi.org/10.1038/nature03610	journal	June 2005
Genome-scale model reconstruction of the methylotrophic yeast Ogataea polymorpha Liebal, Ulf Winfried; Fabry, Brigida A.; Ravikrishnan, Aarthi RWTH Aachen University https://doi.org/10.18154/rwth-2021-02761	text	January 2021
Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material Leigh, Joanne; Hodge, Angela; Fitter, Alastair H. New Phytologist, Vol. 181, Issue 1 https://doi.org/10.1111/j.1469-8137.2008.02630.x	journal	September 2008
A Phosphate Transporter from Medicago truncatula Involved in the Acquisition of Phosphate Released by Arbuscular Mycorrhizal Fungi Harrison, Maria J.; Dewbre, Gary R.; Liu, Jinyuan The Plant Cell, Vol. 14, Issue 10 https://doi.org/10.1105/tpc.004861	journal	September 2002
Characterization of an Amino Acid Permease from the Endomycorrhizal Fungus Glomus mosseae Cappellazzo, Gilda; Lanfranco, Luisa; Fitz, Michael Plant Physiology, Vol. 147, Issue 1 https://doi.org/10.1104/pp.108.117820	journal	March 2008
AtPTR1 and AtPTR5 Transport Dipeptides in Planta Komarova, Nataliya Y.; Thor, Kathrin; Gubler, Adrian Plant Physiology, Vol. 148, Issue 2 https://doi.org/10.1104/pp.108.123844	journal	August 2008
Characterization of a CuZn superoxide dismutase gene in the arbuscular mycorrhizal fungus Glomus intraradices González-Guerrero, Manuel; Oger, Elodie; Benabdellah, Karim Current Genetics, Vol. 56, Issue 3 https://doi.org/10.1007/s00294-010-0298-y	journal	April 2010
The expression of GintPT, the phosphate transporter of Rhizophagus irregularis, depends on the symbiotic status and phosphate availability Fiorilli, Valentina; Lanfranco, Luisa; Bonfante, Paola Planta, Vol. 237, Issue 5 https://doi.org/10.1007/s00425-013-1842-z	journal	January 2013
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis Bonfante, Paola; Genre, Andrea Nature Communications, Vol. 1, Issue 1 https://doi.org/10.1038/ncomms1046	journal	July 2010
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
Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots Guttenberger, Martin Planta, Vol. 211, Issue 3 https://doi.org/10.1007/s004250000324	journal	August 2000
Amino Acid Uptake in Arbuscular Mycorrhizal Plants Whiteside, Matthew D.; Garcia, Maria O.; Treseder, Kathleen K. PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0047643	journal	October 2012
ThPTR2, a di/tri-peptide transporter gene from Trichoderma harzianum Vizcaíno, J. A.; Cardoza, R. E.; Hauser, M. Fungal Genetics and Biology, Vol. 43, Issue 4 https://doi.org/10.1016/j.fgb.2005.12.003	journal	April 2006
Organic N molecules in the soil solution: what is known, what is unknown and the path forwards Warren, Charles R. Plant and Soil, Vol. 375, Issue 1-2 https://doi.org/10.1007/s11104-013-1939-y	journal	October 2013
A novel fungal family of oligopeptide transporters identified by functional metatranscriptomics of soil eukaryotes Damon, Coralie; Vallon, Laurent; Zimmermann, Sabine The ISME Journal, Vol. 5, Issue 12 https://doi.org/10.1038/ismej.2011.67	journal	June 2011
Peptide uptake in the ectomycorrhizal fungus Hebeloma cylindrosporum: characterization of two di- and tripeptide transporters (HcPTR2A and B) Benjdia, Mariam; Rikirsch, Enno; Muller, Tobias New Phytologist, Vol. 170, Issue 2 https://doi.org/10.1111/j.1469-8137.2006.01672.x	journal	April 2006
Intraspecific variation in use of different organic nitrogen sources by the ectomycorrhizal fungus Hebeloma cylindrosporum Guidot, Alice; Verner, Marie-Christine; Debaud, Jean-Claude Mycorrhiza, Vol. 15, Issue 3 https://doi.org/10.1007/s00572-004-0318-1	journal	August 2004
Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis Tisserant, E.; Malbreil, M.; Kuo, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 50 https://doi.org/10.1073/pnas.1313452110	journal	November 2013
GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices Pérez-Tienda, Jacob; Testillano, Pilar S.; Balestrini, Raffaella Fungal Genetics and Biology, Vol. 48, Issue 11 https://doi.org/10.1016/j.fgb.2011.08.003	journal	November 2011
Seasonal variation in soluble soil carbon and nitrogen across a grassland productivity gradient Farrell, Mark; Hill, Paul W.; Farrar, John Soil Biology and Biochemistry, Vol. 43, Issue 4 https://doi.org/10.1016/j.soilbio.2010.12.022	journal	April 2011
The rapid generation of mutation data matrices from protein sequences Jones, David T.; Taylor, William R.; Thornton, Janet M. Bioinformatics, Vol. 8, Issue 3 https://doi.org/10.1093/bioinformatics/8.3.275	journal	January 1992
Organic nitrogen Schmidt, Susanne; Näsholm, Torgny; Rentsch, Doris New Phytologist, Vol. 203, Issue 1 https://doi.org/10.1111/nph.12851	journal	May 2014
Multiplicity and regulation of genes encoding peptide transporters in Saccharomyces cerevisiae Hauser, Melinda; Narita, Vanny; Donhardt, Amy M. Molecular Membrane Biology, Vol. 18, Issue 1 https://doi.org/10.1080/09687680010029374	journal	January 2001
Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs Minet, Michele; Dufour, Marie-Elisabeth; Lacroute, Francois The Plant Journal, Vol. 2, Issue 3 https://doi.org/10.1111/j.1365-313x.1992.00417.x	journal	May 1992
Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level Krüger, Manuela; Krüger, Claudia; Walker, Christopher New Phytologist, Vol. 193, Issue 4 https://doi.org/10.1111/j.1469-8137.2011.03962.x	journal	December 2011
A family of oligopeptide transporters is required for growth of Candida albicans on proteins Reuss, Oliver; Morschhauser, Joachim Molecular Microbiology, Vol. 60, Issue 3 https://doi.org/10.1111/j.1365-2958.2006.05136.x	journal	May 2006
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods Tamura, K.; Peterson, D.; Peterson, N. Molecular Biology and Evolution, Vol. 28, Issue 10 https://doi.org/10.1093/molbev/msr121	journal	May 2011
Harnessing Natural Diversity to Probe Metabolic Pathways Homann, Oliver R.; Cai, Houjian; Becker, Jeffrey M. PLoS Genetics, Vol. preprint, Issue 2005 https://doi.org/10.1371/journal.pgen.0010080.eor	journal	January 2005
Single Nucleus Genome Sequencing Reveals High Similarity among Nuclei of an Endomycorrhizal Fungus Lin, Kui; Limpens, Erik; Zhang, Zhonghua PLoS Genetics, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pgen.1004078	journal	January 2014
Characterization of a general amino acid permease from Hebeloma cylindrosporum Wipf, Daniel; Benjdia, Mariam; Tegeder, Mechthild FEBS Letters, Vol. 528, Issue 1-3 https://doi.org/10.1016/S0014-5793(02)03271-4	journal	August 2002
Identification of differentially expressed genes from Trichoderma harzianum during growth on cell wall of Fusarium solani as a tool for biotechnological application Vieira, Pabline Marinho; Coelho, Alexandre Siqueira Guedes; Steindorff, Andrei Stecca BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-177	journal	January 2013
Nitrogen Mineralization: Challenges of a Changing Paradigm Schimel, Joshua P.; Bennett, Jennifer Ecology, Vol. 85, Issue 3 https://doi.org/10.1890/03-8002	journal	March 2004
Arbuscular Mycorrhizas and N Acquisition by Plants Lanfranco, Luisa; Guether, Mike; Bonfante, Paola Ecological Aspects of Nitrogen Metabolism in Plants https://doi.org/10.1002/9780470959404.ch3	book	March 2011
Arbuscular mycorrhiza on root-organ cultures Fortin, J. André; Bécard, Guillaume; Declerck, Stéphane Canadian Journal of Botany, Vol. 80, Issue 1 https://doi.org/10.1139/b01-139	journal	January 2002
Molecular insights into proton coupled peptide transport in the PTR family of oligopeptide transporters Newstead, Simon Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1850, Issue 3 https://doi.org/10.1016/j.bbagen.2014.05.011	journal	March 2015
Isolation and characterization of a Saccharomyces cerevisiae peptide transport gene Perry, J. R.; Basrai, M. A.; Steiner, H. Y. Molecular and Cellular Biology, Vol. 14, Issue 1 https://doi.org/10.1128/mcb.14.1.104-115.1994	journal	January 1994
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Kinetics of NH 4 + uptake by the arbuscular mycorrhizal fungus Rhizophagus irregularis Pérez-Tienda, J.; Valderas, A.; Camañes, G. Mycorrhiza, Vol. 22, Issue 6 https://doi.org/10.1007/s00572-012-0452-0	journal	July 2012
Nutritional exchanges in the arbuscular mycorrhizal symbiosis: Implications for sustainable agriculture Fitter, A. H.; Helgason, T.; Hodge, A. Fungal Biology Reviews, Vol. 25, Issue 1 https://doi.org/10.1016/j.fbr.2011.01.002	journal	March 2011
Bigger may be better in soil N cycling: Does rapid acquisition of small l-peptides by soil microbes dominate fluxes of protein-derived N in soil? Hill, Paul W.; Farrell, Mark; Jones, Davey L. Soil Biology and Biochemistry, Vol. 48 https://doi.org/10.1016/j.soilbio.2012.01.023	journal	May 2012
An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material Hodge, Angela; Campbell, Colin D.; Fitter, Alastair H. Nature, Vol. 413, Issue 6853 https://doi.org/10.1038/35095041	journal	September 2001
Effect of the arbuscular mycorrhizal fungus Glomus fasciculatum on the uptake of amino nitrogen by Lolium perenne Cliquet, Jean Bernard; Murray, Philip J.; Boucaud, Jean New Phytologist, Vol. 137, Issue 2 https://doi.org/10.1046/j.1469-8137.1997.00810.x	journal	October 1997
Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Minet, M.; Dufour, Me; Lacroute, F. The Plant Journal, Vol. 2, Issue 3 https://doi.org/10.1046/j.1365-313X.1992.t01-38-00999.x	journal	May 1992
Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages Giovannetti, M.; Sbrana, C.; Avio, L. New Phytologist, Vol. 125, Issue 3 https://doi.org/10.1111/j.1469-8137.1993.tb03907.x	journal	November 1993
A Versatile Monosaccharide Transporter That Operates in the Arbuscular Mycorrhizal Fungus Glomus sp Is Crucial for the Symbiotic Relationship with Plants Helber, Nicole; Wippel, Kathrin; Sauer, Norbert The Plant Cell, Vol. 23, Issue 10 https://doi.org/10.1105/tpc.111.089813	journal	October 2011
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
Fenpropimorph and fenhexamid impact phosphorus translocation by arbuscular mycorrhizal fungi Zocco, Domenico; Van Aarle, Ingrid M.; Oger, Elodie Mycorrhiza, Vol. 21, Issue 5 https://doi.org/10.1007/s00572-010-0344-0	journal	November 2010
Regulation of Amino Acid, Nucleotide, and Phosphate Metabolism in Saccharomyces cerevisiae Ljungdahl, Per O.; Daignan-Fornier, Bertrand Genetics, Vol. 190, Issue 3 https://doi.org/10.1534/genetics.111.133306	journal	March 2012
The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems Lipson, David; Näsholm, Torgny Oecologia, Vol. 128, Issue 3 https://doi.org/10.1007/s004420100693	journal	August 2001
Harnessing Natural Diversity to Probe Metabolic Pathways Homann, Oliver R.; Cai, Houjian; Becker, Jeffrey M. PLoS Genetics, Vol. 1, Issue 6 https://doi.org/10.1371/journal.pgen.0010080	journal	December 2005
Mycorrhizal Fungi: Their Habitats and Nutritional Strategies Kubicek, Christian P.; Druzhinina, Irina S. Environmental and Microbial Relationships https://doi.org/10.1007/978-3-540-71840-6_14	book	January 2007
Native Arbuscular Mycorrhizal Inoculum Modulates Growth, Oxidative Metabolism and Alleviates Salinity Stresses in Legume Species Karima, Bencherif; Amima, Hasbaya; Ahlam, Misoumi Current Microbiology, Vol. 80, Issue 2 https://doi.org/10.1007/s00284-022-03145-4	journal	January 2023
Changes in arbuscular mycorrhizal associations and fine root traits in sites under different plant successional phases in southern Brazil Zangaro, Waldemar; de Assis, Rafael Leandro; Rostirola, Leila Vergal Mycorrhiza, Vol. 19, Issue 1 https://doi.org/10.1007/s00572-008-0202-5	journal	September 2008
Genome-wide identification, structural analysis and expression profiles of GRAS gene family in orchardgrass Xu, Xiaoheng; Feng, Guangyan; Huang, Linkai Molecular Biology Reports, Vol. 47, Issue 3 https://doi.org/10.1007/s11033-020-05279-9	journal	February 2020
Laser Microdissection Reveals That Transcripts for Five Plant and One Fungal Phosphate Transporter Genes Are Contemporaneously Present in Arbusculated Cells Balestrini, Raffaella; Gómez-Ariza, Jorge; Lanfranco, Luisa Molecular Plant-Microbe Interactions®, Vol. 20, Issue 9 https://doi.org/10.1094/mpmi-20-9-1055	journal	September 2007
A Symbiotic Sugar Transporter in the Arbuscular Mycorrhizal Fungus Glomus sp Eckardt, Nancy A. The Plant Cell, Vol. 23, Issue 10 https://doi.org/10.1105/tpc.111.231010	journal	October 2011
Roles of Different Peptide Transporters in Nutrient Acquisition in Candida albicans Dunkel, Nico; Hertlein, Tobias; Franz, Renate Eukaryotic Cell, Vol. 12, Issue 4 https://doi.org/10.1128/ec.00008-13	journal	February 2013
Differential Regulation and Substrate Preferences in Two Peptide Transporters of Saccharomyces cerevisiae Cai, Houjian; Hauser, Melinda; Naider, Fred Eukaryotic Cell, Vol. 6, Issue 10 https://doi.org/10.1128/ec.00257-06	journal	August 2007
The Ubiquitin Ligase Ubr11 Is Essential for Oligopeptide Utilization in the Fission Yeast Schizosaccharomyces pombe Kitamura, Kenji; Nakase, Mai; Tohda, Hideki Eukaryotic Cell, Vol. 11, Issue 3 https://doi.org/10.1128/ec.05253-11	journal	January 2012
Isolation and characterization of a Saccharomyces cerevisiae peptide transport gene. Perry, J. R.; Basrai, M. A.; Steiner, H. Y. Molecular and Cellular Biology, Vol. 14, Issue 1 https://doi.org/10.1128/mcb.14.1.104	journal	January 1994

Cited By (10)

To trade in the field: the molecular determinants of arbuscular mycorrhiza nutrient exchange Salvioli di Fossalunga, Alessandra; Novero, Mara Chemical and Biological Technologies in Agriculture, Vol. 6, Issue 1 https://doi.org/10.1186/s40538-019-0150-7	journal	June 2019
The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis Aloui, Achref; Recorbet, Ghislaine; Lemaître-Guillier, Christelle Mycorrhiza, Vol. 28, Issue 1 https://doi.org/10.1007/s00572-017-0789-5	journal	July 2017
RiPEIP1, a gene from the arbuscular mycorrhizal fungus Rhizophagus irregularis, is preferentially expressed in planta and may be involved in root colonization Fiorilli, Valentina; Belmondo, Simone; Khouja, Hassine Radhouane Mycorrhiza, Vol. 26, Issue 6 https://doi.org/10.1007/s00572-016-0697-0	journal	April 2016
In silico analysis of fungal small RNA accumulation reveals putative plant mRNA targets in the symbiosis between an arbuscular mycorrhizal fungus and its host plant Silvestri, Alessandro; Fiorilli, Valentina; Miozzi, Laura BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5561-0	journal	March 2019
Role of Arbuscular Mycorrhizal Fungi in the Nitrogen Uptake of Plants: Current Knowledge and Research Gaps Bücking, Heike; Kafle, Arjun Agronomy, Vol. 5, Issue 4 https://doi.org/10.3390/agronomy5040587	journal	December 2015
Fungal and plant gene expression in the Tulasnella calospora - Serapias vomeracea symbiosis provides clues about nitrogen pathways in orchid mycorrhizas Fochi, Valeria; Chitarra, Walter; Kohler, Annegret New Phytologist, Vol. 213, Issue 1 https://doi.org/10.1111/nph.14279	journal	November 2016
Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks Wipf, Daniel; Krajinski, Franziska; Tuinen, Diederik New Phytologist, Vol. 223, Issue 3 https://doi.org/10.1111/nph.15775	journal	April 2019
Resolving the ‘nitrogen paradox’ of arbuscular mycorrhizas : fertilization with organic matter brings considerable benefits for plant nutrition and growth : Enhanced plant growth with the AM symbiosis Thirkell, Tom J.; Cameron, Duncan D.; Hodge, Angela Plant, Cell & Environment, Vol. 39, Issue 8 https://doi.org/10.1111/pce.12667	journal	February 2016
Virus-Induced Gene Silencing Using Tobacco Rattle Virus as a Tool to Study the Interaction between Nicotiana attenuata and Rhizophagus irregularis Groten, Karin; Pahari, Nabin T.; Xu, Shuqing PLOS ONE, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pone.0136234	journal	August 2015
Contrasting Nitrogen Fertilisation Rates Alter Mycorrhizal Contribution to Barley Nutrition in a Field Trial Thirkell, Tom; Cameron, Duncan; Hodge, Angela Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01312	journal	October 2019

Similar Records

Identification of Populus Small RNAs Responsive to Mutualistic Interactions With Mycorrhizal Fungi, Laccaria bicolor and Rhizophagus irregularis

Journal Article · Mon Mar 18 00:00:00 EDT 2019 · Frontiers in Microbiology · OSTI ID:1628261

Mewalal, Ritesh; Yin, Hengfu; Hu, Rongbin; +6 more

High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis

Journal Article · Mon Jan 22 00:00:00 EST 2018 · New Phytologist · OSTI ID:1628261

Chen, Eric C. H.; Morin, Emmanuelle; Beaudet, Denis; +15 more

Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi

Journal Article · Mon Mar 01 00:00:00 EST 2021 · The ISME Journal · OSTI ID:1628261

Emmett, Bryan D.; Lévesque-Tremblay, Véronique; Harrison, Maria J.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
54 ENVIRONMENTAL SCIENCES
arbuscular mycorrhizal fungi
organic nitrogen
dipeptide transporter
Rhizophagus irregularis
symbiosis

Title: A dipeptide transporter from the arbuscular mycorrhizal fungus Rhizophagus irregularis is upregulated in the intraradical phase

Citation Formats

References (70)

Cited By (10)

Similar Records

Related Subjects