{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T16:56:00Z","timestamp":1791219360749,"version":"4.1.0"},"reference-count":98,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2022,9,7]],"date-time":"2022-09-07T00:00:00Z","timestamp":1662508800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation (RSF)","doi-asserted-by":"publisher","award":["22-16-00064"],"award-info":[{"award-number":["22-16-00064"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation (RSF)","doi-asserted-by":"publisher","award":["19-29-05275_MK"],"award-info":[{"award-number":["19-29-05275_MK"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002261","name":"Russian Foundation for Basic Research (RFBR)","doi-asserted-by":"publisher","award":["22-16-00064"],"award-info":[{"award-number":["22-16-00064"]}],"id":[{"id":"10.13039\/501100002261","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002261","name":"Russian Foundation for Basic Research (RFBR)","doi-asserted-by":"publisher","award":["19-29-05275_MK"],"award-info":[{"award-number":["19-29-05275_MK"]}],"id":[{"id":"10.13039\/501100002261","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>The nature of plant\u2013fungi interaction at early stages of arbuscular mycorrhiza (AM) development is still a puzzling problem. To investigate the processes behind this interaction, we used the Medicago lupulina MlS-1 line that forms high-efficient AM symbiosis with Rhizophagus irregularis. AM fungus actively colonizes the root system of the host plant and contributes to the formation of effective AM as characterized by a high mycorrhizal growth response (MGR) in the host plant. The present study is aimed at distinguishing the alterations in the M. lupulina root metabolic profile as an indicative marker of effective symbiosis. We examined the root metabolome at the 14th and 24th day after sowing and inoculation (DAS) with low substrate phosphorus levels. A GS-MS analysis detected 316 metabolites. Results indicated that profiles of M. lupulina root metabolites differed from those in leaves previously detected. The roots contained fewer sugars and organic acids. Hence, compounds supporting the growth of mycorrhizal fungus (especially amino acids, specific lipids, and carbohydrates) accumulated, and their presence coincided with intensive development of AM structures. Mycorrhization determined the root metabolite profile to a greater extent than host plant development. The obtained data highlight the importance of active plant\u2013fungi metabolic interaction at early stages of host plant development for the determination of symbiotic efficiency.<\/jats:p>","DOI":"10.3390\/plants11182338","type":"journal-article","created":{"date-parts":[[2022,9,8]],"date-time":"2022-09-08T01:40:13Z","timestamp":1662601213000},"page":"2338","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["The Role of Medicago lupulina Interaction with Rhizophagus irregularis in the Determination of Root Metabolome at Early Stages of AM Symbiosis"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2231-6466","authenticated-orcid":false,"given":"Andrey P.","family":"Yurkov","sequence":"first","affiliation":[{"name":"Laboratory of Ecology of Symbiotic and Associative Rhizobacteria, All-Russia Research Institute for Agricultural Microbiology, Pushkin, 196608 St. Petersburg, Russia"},{"name":"Graduate School of Biotechnology and Food Science, Peter the Great St. Petersburg Polytechnic University, 194021 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5862-2676","authenticated-orcid":false,"given":"Roman K.","family":"Puzanskiy","sequence":"additional","affiliation":[{"name":"Faculty of Biology, St. Petersburg State University, 199034 St. Petersburg, Russia"},{"name":"Laboratory of Analytical Phytochemistry, Komarov Botanical Institute of the Russian Academy of Sciences, 197376 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexey A.","family":"Kryukov","sequence":"additional","affiliation":[{"name":"Laboratory of Ecology of Symbiotic and Associative Rhizobacteria, All-Russia Research Institute for Agricultural Microbiology, Pushkin, 196608 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anastasiia O.","family":"Gorbunova","sequence":"additional","affiliation":[{"name":"Laboratory of Ecology of Symbiotic and Associative Rhizobacteria, All-Russia Research Institute for Agricultural Microbiology, Pushkin, 196608 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tatyana R.","family":"Kudriashova","sequence":"additional","affiliation":[{"name":"Laboratory of Ecology of Symbiotic and Associative Rhizobacteria, All-Russia Research Institute for Agricultural Microbiology, Pushkin, 196608 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lidija M.","family":"Jacobi","sequence":"additional","affiliation":[{"name":"Laboratory of Ecology of Symbiotic and Associative Rhizobacteria, All-Russia Research Institute for Agricultural Microbiology, Pushkin, 196608 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrei P.","family":"Kozhemyakov","sequence":"additional","affiliation":[{"name":"Laboratory of Ecology of Symbiotic and Associative Rhizobacteria, All-Russia Research Institute for Agricultural Microbiology, Pushkin, 196608 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9576-1256","authenticated-orcid":false,"given":"Daria A.","family":"Romanyuk","sequence":"additional","affiliation":[{"name":"Laboratory of Ecology of Symbiotic and Associative Rhizobacteria, All-Russia Research Institute for Agricultural Microbiology, Pushkin, 196608 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ekaterina B.","family":"Aronova","sequence":"additional","affiliation":[{"name":"Graduate School of Biotechnology and Food Science, Peter the Great St. Petersburg Polytechnic University, 194021 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Galina S.","family":"Avdeeva","sequence":"additional","affiliation":[{"name":"Faculty of Biology, St. Petersburg State University, 199034 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2323-5235","authenticated-orcid":false,"given":"Vladislav V.","family":"Yemelyanov","sequence":"additional","affiliation":[{"name":"Faculty of Biology, St. Petersburg State University, 199034 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1778-2814","authenticated-orcid":false,"given":"Alexey L.","family":"Shavarda","sequence":"additional","affiliation":[{"name":"Laboratory of Analytical Phytochemistry, Komarov Botanical Institute of the Russian Academy of Sciences, 197376 St. Petersburg, Russia"},{"name":"Center for Molecular and Cell Technologies, St. Petersburg State University, 199034 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3657-2986","authenticated-orcid":false,"given":"Maria F.","family":"Shishova","sequence":"additional","affiliation":[{"name":"Faculty of Biology, St. Petersburg State University, 199034 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,9,7]]},"reference":[{"key":"ref_1","unstructured":"Smith, S.E., and Read, D.J. (2008). Mycorrhizal Symbiosis, Academic Press. [3rd ed.]."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1007\/s10886-012-0134-6","article-title":"Mycorrhiza-induced resistance and priming of plant defenses","volume":"38","author":"Jung","year":"2012","journal-title":"J. Chem. Ecol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1977","DOI":"10.3389\/fpls.2018.01977","article-title":"Increased silicon acquisition in bananas colonized by Rhizophagus irregularis MUCL 41833 reduces the incidence of Pseudocercospora fijiensis","volume":"9","author":"Gbongue","year":"2019","journal-title":"Front. Plant Sci."},{"key":"ref_4","first-page":"367","article-title":"Abiotic stresses and their effects on plant growth, yield and nutritional quality of agricultural produce","volume":"4","author":"Kumar","year":"2020","journal-title":"J. Sci. Food Agric."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e7495","DOI":"10.7717\/peerj.7495","article-title":"Metabolic alterations in pea leaves during arbuscular mycorrhiza development","volume":"7","author":"Shtark","year":"2019","journal-title":"PeerJ"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3886","DOI":"10.1038\/ncomms4886","article-title":"High specificity in plant leaf metabolic responses to arbuscular mycorrhiza","volume":"5","author":"Schweiger","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"721614","DOI":"10.3389\/fpls.2021.721614","article-title":"Arbuscular mycorrhizal symbiosis triggers major changes in primary metabolism together with modification of defense responses and signaling in both roots and leaves of Vitis vinifera","volume":"12","author":"Goddard","year":"2021","journal-title":"Front. Plant Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1758","DOI":"10.1111\/pce.13509","article-title":"Diverse Sorghum bicolor accessions show marked variation in growth and transcriptional responses to arbuscular mycorrhizal fungi","volume":"42","author":"Emmett","year":"2019","journal-title":"Plant Cell Environ."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1007\/s00425-008-0877-z","article-title":"Overlapping expression patterns and differential transcript levels of phosphate transporter genes in arbuscular mycorrhizal, Pi-fertilised and phytohormone-treated Medicago truncatula roots","volume":"229","author":"Grunwald","year":"2009","journal-title":"Planta"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1111\/jipb.12609","article-title":"Nicotiana attenuata\u2019s capacity to interact with arbuscular mycorrhiza alters its competitive ability and elicits major changes in the leaf transcriptome","volume":"60","author":"Wang","year":"2018","journal-title":"J. Integr. Plant Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1104","DOI":"10.1104\/pp.102.019034","article-title":"Mapping of the proteome of barrel medic (Medicago truncatula)","volume":"131","author":"Watson","year":"2003","journal-title":"Plant Physiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"S145","DOI":"10.1002\/pmic.200500403","article-title":"A mass spectrometric approach to identify arbuscular mycorrhiza-related proteins in root plasma membrane fractions","volume":"6","author":"Valot","year":"2006","journal-title":"Proteomics"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00572-017-0789-5","article-title":"The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis","volume":"281","author":"Aloui","year":"2018","journal-title":"Mycorrhiza"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"e8991","DOI":"10.7717\/peerj.8991","article-title":"Proteomic analysis and interactions network in leaves of mycorrhizal and nonmycorrhizal sorghum plants under water deficit","volume":"8","author":"Winkler","year":"2020","journal-title":"PeerJ"},{"key":"ref_15","first-page":"e8888:1","article-title":"Distinct gene expression and secondary metabolite profiles for suboptimal mycorrhizal colonization in wild-type and the jasmonic acid deficient spr2 tomato mutant","volume":"8","author":"Winkler","year":"2020","journal-title":"PeerJ"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Kaur, S., and Suseela, V. (2020). Unraveling arbuscular mycorrhiza-induced changes in plant primary and secondary metabolome. Metabolites, 10.","DOI":"10.3390\/metabo10080335"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Yurkov, A.P., Puzanskiy, R.K., Avdeeva, G.S., Jacobi, L.M., Gorbunova, A.O., Kryukov, A.A., Kozhemyakov, A.P., Laktionov, Y.V., Kosulnikov, Y.V., and Romanyuk, D.A. (2021). Mycorrhiza-induced alterations in metabolome of Medicago lupulina leaves during symbiosis development. Plants, 10.","DOI":"10.3390\/plants10112506"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1111\/j.1469-8137.2007.02282.x","article-title":"Population-specific metabolic phenotypes of Arabidopsis lyrata ssp. petraea","volume":"177","author":"Davey","year":"2008","journal-title":"New Phytol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"4336","DOI":"10.1021\/jf904321p","article-title":"Seasonal changes in the metabolic fingerprint of 21 grass and legume cultivars studied by nuclear magnetic resonance-based metabolomics","volume":"58","author":"Bertram","year":"2010","journal-title":"J. Agric. Food Chem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1016\/j.phytochem.2010.02.001","article-title":"Metabolic classification of South American Ilex species by NMR-based metabolomics","volume":"71","author":"Kim","year":"2010","journal-title":"Phytochemistry"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1007\/s11306-009-0186-y","article-title":"Principal component and hierarchical clustering analysis of metabolites in destructive weeds; polygonaceous plants","volume":"6","author":"Miyagi","year":"2010","journal-title":"Metabolomics"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.pbi.2015.06.009","article-title":"Leaf metabolome in arbuscular mycorrhizal symbiosis","volume":"26","author":"Schweiger","year":"2015","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/0168-9452(89)90168-4","article-title":"Mutagenesis of pea Pisum sativum L. and the isolation of mutants for nodulation and nitrogen fixation","volume":"60","author":"Duc","year":"1989","journal-title":"Plant Sci."},{"key":"ref_24","first-page":"106","article-title":"Pea Pisum sativum L. mendelian genes controlling development of nitrogen-fixing nodules and arbuscular mycorrhiza","volume":"36","author":"Borisov","year":"2000","journal-title":"Czech J. Genet. Plant Breed."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Shtark, O., Puzanskiy, R., Avdeeva, G., Yemelyanov, V., Shavarda, A., Romanyuk, D., Kliukova, M., Kirpichnikova, A., Tikhonovich, I., and Zhukov, V. (2021). Metabolic alterations in Pisum sativum roots during plant growth and arbuscular mycorrhiza development. Plants, 10.","DOI":"10.3390\/plants10061033"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/0168-9452(95)04229-N","article-title":"Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula Gaertn. after \u03b3-ray mutagenesis","volume":"111","author":"Sagan","year":"1995","journal-title":"Plant Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.phytochem.2007.06.032","article-title":"Metabolite profiling of mycorrhizal roots of Medicago truncatula","volume":"69","author":"Schliemann","year":"2008","journal-title":"Phytochemistry"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1134\/S1062360415050082","article-title":"Development of arbuscular mycorrhiza in highly responsive and mycotrophic host plant\u2014Black medick (Medicago lupulina L.)","volume":"46","author":"Yurkov","year":"2015","journal-title":"Russ. J. Dev. Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1094\/MPMI.1998.11.9.933","article-title":"Mycorrhiza mutants of Lotus japonicus define genetically independent steps during symbiotic infection","volume":"11","author":"Wegel","year":"1998","journal-title":"MPMI"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/0168-9452(96)04427-5","article-title":"A nodulation (Nod+\/Fix\u2212) mutant of Phaseolus vulgaris L. has nodulelike structures lacking peripherial vascular bundles (Pvb\u2212) and is resistant to mycorrhizal infection (Myc\u2212)","volume":"118","author":"Shiztliffe","year":"1996","journal-title":"Plant Sci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/0031-9422(94)00538-5","article-title":"Identification of a yellow pigment formed in maize roots upon mycorrhizal colonization","volume":"38","author":"Klingner","year":"1995","journal-title":"Phytochemistry"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1094\/MPMI.1998.11.10.1017","article-title":"Cell defense responses assosiated with localized and systemic resistance to Phitophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus","volume":"11","author":"Cordier","year":"1998","journal-title":"MPMI"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1111\/j.1365-313X.2007.03175.x","article-title":"A petunia mutant affected in intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi","volume":"51","author":"Reddy","year":"2007","journal-title":"Plant J."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"952","DOI":"10.1016\/j.cub.2017.06.042","article-title":"Understanding the arbuscule at the heart of endomycorrhizal symbioses in plants","volume":"27","author":"Luginbuehl","year":"2017","journal-title":"Curr. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"5341","DOI":"10.1128\/AEM.71.9.5341-5347.2005","article-title":"Dependence of arbuscular-mycorrhizal fungi on their plant host for palmitic acid synthesis","volume":"71","author":"Trepanier","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1151","DOI":"10.1111\/tpj.12706","article-title":"A set of fluorescent protein-based markers expressed from constitutive and arbuscular mycorrhiza-inducible promoters to label organelles, membranes and cytoskeletal elements in Medicago truncatula","volume":"80","author":"Ivanov","year":"2014","journal-title":"Plant J."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1007\/s00374-002-0539-4","article-title":"Host plant benefit from association with arbuscular mycorrhizal fungi: Variation due to differences in size of mycelium","volume":"36","author":"Hart","year":"2002","journal-title":"Biol. Fertil. Soils"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"672","DOI":"10.1111\/nph.17994","article-title":"Root metabolome of plant-arbuscular mycorrhizal symbiosis mirrors the mutualistic or parasitic mycorrhizal phenotype","volume":"234","author":"Kaur","year":"2022","journal-title":"New Phytol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1111\/j.1469-8137.2004.01039.x","article-title":"Functional diversity in arbuscular mycorrhizal (AM) symbioses: The contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake","volume":"162","author":"Smith","year":"2004","journal-title":"New Phytol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1111\/j.1469-8137.2006.01935.x","article-title":"Functional biology of plant phosphate uptake at root and mycorrhiza interfaces","volume":"173","author":"Bucher","year":"2007","journal-title":"New Phytol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"598","DOI":"10.3389\/fmicb.2015.00598","article-title":"Metabolic transition in mycorrhizal tomato roots","volume":"6","author":"Rivero","year":"2015","journal-title":"Front. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1479","DOI":"10.1002\/jsfa.5919","article-title":"Mycorrhizal technology and phosphorus in the production of primary and secondary metabolites in cebil (Anadenanthera colubrina (Vell.) Brenan) seedlings","volume":"93","author":"Lins","year":"2013","journal-title":"J. Sci. Food Agric."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1176","DOI":"10.1111\/j.1469-8137.2009.02874.x","article-title":"\u201cGlomus intraradices DAOM197198\u201d, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices","volume":"183","author":"Stockinger","year":"2009","journal-title":"New Phytol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"815","DOI":"10.3389\/fpls.2015.00815","article-title":"Soil inoculation with symbiotic microorganisms promotes plant growth and nutrient transporter genes expression in durum wheat","volume":"6","author":"Saia","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1196","DOI":"10.1016\/j.phytochem.2006.05.005","article-title":"Accumulation of apocarotenoids in mycorrhizal roots of Ornithogalum umbellatum","volume":"67","author":"Schliemann","year":"2006","journal-title":"Phytochemistry"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e37093","DOI":"10.7554\/eLife.37093","article-title":"Blumenols as shoot markers of root symbiosis with arbuscular mycorrhizal fungi","volume":"7","author":"Wang","year":"2018","journal-title":"eLife"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1007\/s10886-017-0921-1","article-title":"Arbuscular mycorrhizal fungi and plant chemical defence: Effects of colonisation on above ground and below ground metabolomes","volume":"44","author":"Hill","year":"2018","journal-title":"J. Chem. Ecol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1104\/pp.16.01509","article-title":"Enhanced secondary- and hormone metabolism in leaves of arbuscular mycorrhizal Medicago truncatula","volume":"175","author":"Adolfsson","year":"2017","journal-title":"Plant Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"100314","DOI":"10.1016\/j.rhisph.2021.100314","article-title":"AMF enhance secondary metabolite production in ashwagandha, licorice, and marigold in a fungi-host specific manner","volume":"17","author":"Johny","year":"2021","journal-title":"Rhizosphere"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"899","DOI":"10.1016\/j.indcrop.2017.10.055","article-title":"Plant growth, steviol glycosides and nutrient uptake as affected by arbuscular mycorrhizal fungi and phosphorous fertilization in Stevia rebaudiana Bert","volume":"111","author":"Tavarini","year":"2018","journal-title":"Ind. Crops Prod."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"e12890","DOI":"10.7717\/peerj.12890","article-title":"Arbuscular mycorrhizal fungi improve the growth and performance in the seedlings of Leymus chinensis under alkali and drought stresses","volume":"10","author":"Wang","year":"2022","journal-title":"PeerJ"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"833389","DOI":"10.3389\/fevo.2022.833389","article-title":"Cooperation with arbuscular mycorrhizal fungi increases plant nutrient uptake and improves defenses against insects","volume":"23","author":"Yu","year":"2022","journal-title":"Front. Ecol. Evol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1007\/s00442-011-2037-6","article-title":"Towards a systemic metabolic signature of the arbuscular mycorrhizal interaction","volume":"167","author":"Fester","year":"2011","journal-title":"Oecologia"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Rasouli, F., Amini, T., Asadi, M., Hassanpouraghdam, M.B., Aazami, M.A., Ercisli, S., Skrovankova, S., and Mlcek, J. (2022). Growth and antioxidant responses of lettuce (Lactuca sativa L.) to arbuscular mycorrhiza inoculation and seaweed extract foliar application. Agronomy, 12.","DOI":"10.3390\/agronomy12020401"},{"key":"ref_55","first-page":"1976","article-title":"Impact of arbuscular mycorrhizal inoculation and growth substrate on biomass and content of polyphenols in Eclipta prostrata","volume":"54","author":"Vo","year":"2019","journal-title":"Hortic. Sci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.jare.2019.03.002","article-title":"An arbuscular mycorrhizal fungus and a root pathogen induce different volatiles emitted by Medicago truncatula roots","volume":"19","author":"Dreher","year":"2019","journal-title":"J. Adv. Res."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Tsiokanos, E., Cartabia, A., Tsafantakis, N., Lalaymia, I., Termentzi, A., Miguel, M., Declerck, S., and Fokialakis, N. (2022). The metabolic profile of Anchusa officinalis L. differs according to its associated arbuscular mycorrhizal fungi. Metabolites, 12.","DOI":"10.3390\/metabo12070573"},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Yurkov, A., Kryukov, A., Gorbunova, A., Sherbakov, A., Dobryakova, K., Mikhaylova, Y., Afonin, A., and Shishova, M. (2020). AM-induced alteration in the expression of genes, encoding phosphorus transporters and enzymes of carbohydrate metabolism in Medicago lupulina. Plants, 9.","DOI":"10.3390\/plants9040486"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1713","DOI":"10.1104\/pp.114.244541","article-title":"Root architecture responses: In search of phosphate","volume":"166","author":"Peret","year":"2014","journal-title":"Plant Physiol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1104\/pp.17.01583","article-title":"Reduction in root secondarygrowth as a strategy for phosphorus acquisition","volume":"176","author":"Strock","year":"2018","journal-title":"Plant Physiol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1023\/A:1013324727040","article-title":"Topsoil foraging: An architectural adaptation of plants to low phosphorus availability","volume":"237","author":"Lynch","year":"2001","journal-title":"Plant Soil"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1111\/j.1365-313X.2004.02005.x","article-title":"Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development","volume":"37","author":"Ticconi","year":"2004","journal-title":"Plant J."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"e0129520","DOI":"10.3389\/fpls.2015.01014","article-title":"Metabolic adaptations of white lupin roots and shoots under phosphorus deficiency","volume":"6","author":"Muller","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Luo, J., Liu, Y., Zhang, H., Wang, J., Chen, Z., Luo, L., Liu, G., and Liu, P. (2020). Metabolic alterations provide insights into Stylosanthes roots responding to phosphorus deficiency. BMC Plant Biol., 20.","DOI":"10.1186\/s12870-020-2283-z"},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Chen, W., Zhou, M., Zhao, M., Chen, R., Tigabu, M., Wu, P., Li, M., and Ma, X. (2021). Transcriptome analysis provides insights into the root response of Chinese firto phosphorus deficiency. BMC Plant Biol., 21.","DOI":"10.1186\/s12870-021-03245-6"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"2093","DOI":"10.1093\/jxb\/erab559","article-title":"Metabolite shift in Medicago truncatula occurs in phosphorus deprivation","volume":"73","author":"Dokwal","year":"2022","journal-title":"J. Exp. Bot."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"e13630","DOI":"10.1111\/ppl.13630","article-title":"Molecular cues of sugar signaling in plants","volume":"174","author":"Choudhary","year":"2022","journal-title":"Physiol. Plant."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1626\/pps.12.9","article-title":"Sucrose metabolism for the development of seminal root in maize seedlings","volume":"12","author":"Ogawa","year":"2009","journal-title":"Plant Prod. Sci."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"519","DOI":"10.17221\/617\/2017-PSE","article-title":"The effect of inoculation with arbuscular mycorrhizal fungus Rhizophagus irregularis on cytokinin content in highly mycotrophic Medicago lupulina line under low phosphorus level in soil","volume":"63","author":"Yurkov","year":"2017","journal-title":"Plant Soil Environ."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"3812","DOI":"10.1105\/tpc.111.089813","article-title":"A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp. is crucial for the symbiotic relationship with plants","volume":"23","author":"Helber","year":"2011","journal-title":"Plant Cell"},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Kapulnik, Y., and Douds, D.D. (2000). Carbon partitioning, cost and metabolism of arbuscular mycorrhizas. Arbuscular Mycorrhizas: Physiology and Function, Kluwer Academic Press.","DOI":"10.1007\/978-94-017-0776-3"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.1093\/treephys\/27.8.1103","article-title":"Variations in organic acid exudation and aluminum resistance among arbuscular mycorrhizal species colonizing Liriodendron tulipifera","volume":"27","author":"Klugh","year":"2007","journal-title":"Tree Physiol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1204","DOI":"10.1016\/j.cub.2011.06.044","article-title":"A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy","volume":"21","author":"Kloppholz","year":"2011","journal-title":"Curr. Biol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1094\/MPMI-10-15-0234-R","article-title":"Strigolactone induced putative secreted protein 1 is required for the establishment of symbiosis by the arbuscular mycorrhizal fungus Rhizophagus irregularis","volume":"29","author":"Tsuzuki","year":"2016","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1111\/tpj.13908","article-title":"Host- and stage-dependent secretome of the arbuscular mycorrhizal fungus Rhizophagus irregularis","volume":"94","author":"Zeng","year":"2018","journal-title":"Plant J."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1111\/tpj.12566","article-title":"Fatty acid synthesis and lipid metabolism in the obligate biotrophic fungus Rhizophagus irregularis during mycorrhization of Lotus japonicus","volume":"79","author":"Wewer","year":"2014","journal-title":"Plant J."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1631","DOI":"10.1111\/nph.14533","article-title":"Arbuscular mycorrhiza-specific enzymes FatM and RAM2 fine-tune lipid biosynthesis to promote development of arbuscular mycorrhiza","volume":"214","author":"Bravo","year":"2017","journal-title":"New Phytol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1046\/j.1469-8137.2003.00810.x","article-title":"Ergosterol and fatty acids for biomass estimation of mycorrhizal fungi","volume":"159","author":"Olsson","year":"2003","journal-title":"New Phytol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"2170","DOI":"10.1111\/j.1365-3040.2012.02547.x","article-title":"Carbon trading for phosphorus gain: The balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition","volume":"35","author":"Ryan","year":"2012","journal-title":"Plant Cell Environ."},{"key":"ref_80","first-page":"16","article-title":"Effect of phosphorus fertilizers, lime materials, and biopreparations in barley and clover plants in a mixed plantation","volume":"11","author":"Kirpichnikov","year":"2012","journal-title":"Agrohimia"},{"key":"ref_81","first-page":"73","article-title":"New methods of agroecology for improving the quality of apple planting material","volume":"4","author":"Efimova","year":"2015","journal-title":"Proc. Kuban State Univ."},{"key":"ref_82","first-page":"18","article-title":"Productivity of spring and winter wheat in drought conditions dependent on the application of arbuscular mycorrhizal fungus Glomus intraradices","volume":"12","author":"Yurkov","year":"2012","journal-title":"Fodd. Prod."},{"key":"ref_83","first-page":"38","article-title":"Optimization procedures for molecular-genetic identification of arbuscular mycorrhizal fungi in symbiotic phase on the example of two closely kindred strains","volume":"52","author":"Kryukov","year":"2018","journal-title":"Mikol. Fitopatol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/S0007-1536(70)80110-3","article-title":"Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection","volume":"55","author":"Phillips","year":"1970","journal-title":"Trans. Br. Mycol. Soc."},{"key":"ref_85","unstructured":"Gianinazzi-Pearson, V., and Gianinazzi, S. (1986). Mesure du taux de mycorhization VA d\u2019un syst\u00e8me radiculaire. Recherche de m\u00e9thodes ayant une signification fonctionnelle. Physiological and Genetical Aspects of Mycorrhizae, INRA-Press."},{"key":"ref_86","unstructured":"Vorobyev, N.I., Yurkov, A.P., and Provorov, N.A. (2016). Certificate N2010612112 about the Registration of the Computer Program \u201cProgram for Calculating the Mycorrhization Indices of Plant Roots\u201d (Dated 2 December 2016), The Federal Service for Intellectual Property."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.chroma.2017.04.052","article-title":"Gas chromatography\u2014Mass spectrometry data processing made easy","volume":"1503","author":"Johnsen","year":"2017","journal-title":"J. Chromatogr. A"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/4735_2007_0229","article-title":"The Golm Metabolome Database: A database for GC-MS based metabolite profiling","volume":"Volume 18","author":"Nielsen","year":"2007","journal-title":"Topics in Current Genetics"},{"key":"ref_89","unstructured":"R Core Team (2020). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing. Available online: https:\/\/www.R-project.org\/."},{"key":"ref_90","unstructured":"Komsta, L. (2022, July 19). Outliers: Tests for Outliers. Available online: https:\/\/CRAN.R-project.org\/package=outliers."},{"key":"ref_91","unstructured":"Hastie, T., Tibshirani, R., Narasimhan, B., and Chu, G. (2022, July 19). Impute: Imputation for Microarray Data. Available online: https:\/\/bioconductor.org\/packages\/release\/bioc\/html\/impute.html."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1164","DOI":"10.1093\/bioinformatics\/btm069","article-title":"pcaMethods-a bioconductor package providing PCA methods for incomplete data","volume":"23","author":"Stacklies","year":"2007","journal-title":"Bioinformatics"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"3322","DOI":"10.1021\/acs.jproteome.5b00354","article-title":"Analysis of the human adult urinary metabolome variations with age, body mass index, and gender by implementing a comprehensive workflow for univariate and OPLS statistical analyses","volume":"14","author":"Roux","year":"2015","journal-title":"J. Proteome Res."},{"key":"ref_94","unstructured":"Korotkevich, G., Sukhov, V., and Sergushichev, A. (2021). Fast gene set enrichment analysis. bioRxiv, 060012."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"1947","DOI":"10.1002\/pro.3715","article-title":"Toward understanding the origin and evolution of cellular organisms","volume":"28","author":"Kanehisa","year":"2019","journal-title":"Protein Sci."},{"key":"ref_96","unstructured":"Tenenbaum, D., and Maintainer, B. (2022, July 19). KEGGREST: Client-Side REST Access to the Kyoto Encyclopedia of Genes and Genomes (KEGG). Available online: https:\/\/bioconductor.org\/packages\/release\/bioc\/html\/KEGGREST.html."},{"key":"ref_97","unstructured":"Csardi, G., and Nepusz, T. (2022, July 19). The Igraph Software Package for Complex Network Research. Available online: https:\/\/igraph.org."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1101\/gr.1239303","article-title":"Cytoscape: A software environment for integrated models of biomolecular interaction networks","volume":"13","author":"Shannon","year":"2003","journal-title":"Genome Res."}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/11\/18\/2338\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:25:12Z","timestamp":1760142312000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/11\/18\/2338"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,7]]},"references-count":98,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2022,9]]}},"alternative-id":["plants11182338"],"URL":"https:\/\/doi.org\/10.3390\/plants11182338","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,7]]}}}