{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,22]],"date-time":"2026-05-22T18:06:53Z","timestamp":1779473213331,"version":"3.53.1"},"reference-count":41,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2026,5,22]],"date-time":"2026-05-22T00:00:00Z","timestamp":1779408000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100010236","name":"Tokyo Metropolitan University","doi-asserted-by":"publisher","award":["1D20543"],"award-info":[{"award-number":["1D20543"]}],"id":[{"id":"10.13039\/501100010236","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100010236","name":"Tokyo Metropolitan University","doi-asserted-by":"publisher","award":["1C41104"],"award-info":[{"award-number":["1C41104"]}],"id":[{"id":"10.13039\/501100010236","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>\n                    We present a comparative advantage model of carbon\u2013nitrogen exchange in legume\u2013\n                    <jats:italic>Rhizobium<\/jats:italic>\n                    symbiosis that incorporates ATP budget constraints and the energy\u2013mass balance between the host and symbiont. In this framework, the uptake of carbon and nitrogen is limited by the ATP available to each partner, and any imbalance in trade is compensated by adjustments in symbiont biomass. Using empirical estimates of the ATP costs of carbon and nitrogen uptake, together with data on body C:N ratios, the model generates three key predictions, and we prove that they align with empirical results. (i) The condition for the establishment of symbiosis derived from the model is consistent with measured ATP costs in both host and symbiont. (ii) At equilibrium, the model predicts a relatively low carbon supply from the legume and a relatively high nitrogen supply from\n                    <jats:italic>Rhizobium<\/jats:italic>\n                    , in agreement with reported patterns of exchange. (iii) The model further predicts that the proportion of carbon supplied decreases as the host C:N ratio increases, and that the proportion of nitrogen supplied decreases as the symbiont C:N ratio decreases, which are consistent with the empirically observed decline in nodulation during host aging.\n                  <\/jats:p>","DOI":"10.1371\/journal.pone.0349611","type":"journal-article","created":{"date-parts":[[2026,5,22]],"date-time":"2026-05-22T17:45:20Z","timestamp":1779471920000},"page":"e0349611","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["C\u2013N exchange model of legume\u2013Rhizobium symbiosis incorporating ATP budget constraints and energy\u2013mass balance between the species"],"prefix":"10.1371","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2472-3508","authenticated-orcid":true,"given":"Toshiko","family":"Furukawa","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0299-8890","authenticated-orcid":true,"given":"Takuya","family":"Iimura","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2026,5,22]]},"reference":[{"key":"pone.0349611.ref001","article-title":"On Agriculture.","volume-title":"Complete Works of Cato the Elder","author":"MP. Cato","year":"2016"},{"key":"pone.0349611.ref002","first-page":"1","article-title":"The history of the Leguminosae in agriculture","volume-title":"Root Nodule Bacteria and Leguminous Plants","author":"EB Fred","year":"1932"},{"issue":"13","key":"pone.0349611.ref003","doi-asserted-by":"crossref","first-page":"5230","DOI":"10.1073\/pnas.0600912103","article-title":"Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis","volume":"103","author":"P Mergaert","year":"2006","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"6","key":"pone.0349611.ref004","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1005280","article-title":"A legume genetic framework controls infection of nodules by symbiotic and endophytic bacteria","volume":"11","author":"R Zgadzaj","year":"2015","journal-title":"PLoS Genetics"},{"key":"pone.0349611.ref005","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1007\/978-1-4020-2728-4_4","article-title":"Symbiotic Nitrogen Fixation.","author":"J Ramos","year":"2004","journal-title":"Nitrogen Acquisition and Assimilation in Higher Plants. Dordrecht, Holland: Kluwer Academic Publishers"},{"issue":"4","key":"pone.0349611.ref006","doi-asserted-by":"crossref","first-page":"1237","DOI":"10.1073\/pnas.1315980111","article-title":"Evolution of microbial markets","volume":"111","author":"GDA Werner","year":"2014","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pone.0349611.ref007","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/BF00167053","article-title":"Biological markets: supply and demand determines the effect of partner choice in cooperation, mutualism and mating","volume":"35","author":"R No\u00eb","year":"1994","journal-title":"Behav Ecol Sociobiol"},{"issue":"8","key":"pone.0349611.ref008","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1016\/S0169-5347(00)89123-5","article-title":"Biological markets","volume":"10","author":"R No\u00eb","year":"1995","journal-title":"Trends Ecol Evol"},{"issue":"3","key":"pone.0349611.ref009","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1890\/0012-9658(1998)079[1029:SARTBM]2.0.CO;2","article-title":"Specialization and resource trade: biological markets as a model of mutualisms","volume":"79","author":"MW Schwartz","year":"1998","journal-title":"Ecology"},{"issue":"1518","key":"pone.0349611.ref010","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1098\/rspb.2002.2312","article-title":"Expanding comparative-advantage biological market models: contingency of mutualism on partners\u2019 resource requirements and acquisition trade-offs","volume":"270","author":"JD Hoeksema","year":"2003","journal-title":"Proc Biol Sci"},{"key":"pone.0349611.ref011","volume-title":"On the Principles of Political Economy and Taxation","author":"D Ricardo","year":"1817"},{"issue":"4","key":"pone.0349611.ref012","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1890\/0012-9658(2006)87[892:TEOMOU]2.0.CO;2","article-title":"The economics of mutualisms: optimal utilization of mycorrhizal mutualistic partners by plants","volume":"87","author":"M Kummel","year":"2006","journal-title":"Ecology"},{"key":"pone.0349611.ref013","doi-asserted-by":"crossref","first-page":"1522","DOI":"10.1016\/j.ecolmodel.2009.03.028","article-title":"A multi-mutualist simulation: applying biological market models to diverse mycorrhizal communities","volume":"220","author":"CC Cowden","year":"2009","journal-title":"Ecol Model"},{"issue":"1687","key":"pone.0349611.ref014","doi-asserted-by":"crossref","first-page":"20150101","DOI":"10.1098\/rstb.2015.0101","article-title":"Biological trade and markets","volume":"371","author":"P Hammerstein","year":"2016","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"issue":"1","key":"pone.0349611.ref015","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/07352688809382257","article-title":"Inhibition of legume nodule formation and N2fixation by nitrate","volume":"7","author":"J Streeter","year":"1988","journal-title":"Crit Rev Plant Sci"},{"issue":"5","key":"pone.0349611.ref016","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1080\/00380768.2017.1370960","article-title":"Effects of nitrogen concentrations on nodulation and nitrogenase activity in dual root systems of soybean plants","volume":"63","author":"X Xia","year":"2017","journal-title":"Soil Sci Plant Nutr"},{"key":"pone.0349611.ref017","volume-title":"Die Chemie in irher Anwendung auf Agricultur und Physiologie","author":"J von Liebig","year":"1862","edition":"7"},{"issue":"3","key":"pone.0349611.ref018","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/j.1461-0248.2009.01431.x","article-title":"A resource ratio theory of cooperation","volume":"13","author":"C de Mazancourt","year":"2010","journal-title":"Ecol Lett"},{"issue":"5","key":"pone.0349611.ref019","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1086\/665006","article-title":"Ecological specialization and trade affect the outcome of negotiations in mutualism","volume":"179","author":"E Grman","year":"2012","journal-title":"Am Nat"},{"key":"pone.0349611.ref020","doi-asserted-by":"crossref","first-page":"762510","DOI":"10.3389\/fsoil.2021.762510","article-title":"High maintenance of rhizosphere soil C and N equilibrium regardless of plant species or species traits","volume":"1","author":"SA Wakelin","year":"2021","journal-title":"Front. Soil Sci"},{"key":"pone.0349611.ref021","volume-title":"Microeconomic Analysis","author":"HR Varian","year":"1992","edition":"3"},{"key":"pone.0349611.ref022","volume-title":"Biochemistry and Molecular Biology of Plants","author":"BB Buchanan","year":"2017","edition":"2"},{"key":"pone.0349611.ref023","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1007\/BF00750503","article-title":"Nitrogen assimilation by legumes: processes and ecological limitations","volume":"42","author":"S Schubert","year":"1995","journal-title":"Fert Res"},{"key":"pone.0349611.ref024","first-page":"517","article-title":"Anaerobic growth and denitrification by Rhizobium japonicum and other Rhizobia","volume":"120","author":"RM Daniel","year":"1980","journal-title":"J Gen Microbiol"},{"key":"pone.0349611.ref025","volume-title":"The use of nutrients in crop plants","author":"NK Fageria","year":"2009"},{"key":"pone.0349611.ref026","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/978-1-4020-2728-4_1","article-title":"Nitrate uptake by roots: transporters and root development.","volume-title":"Nitrogen Acquisition and Assimilation in Higher Plants","author":"B. Touraine","year":"2004"},{"issue":"394","key":"pone.0349611.ref027","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1093\/jxb\/erh010","article-title":"Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake","volume":"55","author":"S Mantelin","year":"2004","journal-title":"J Exp Bot"},{"issue":"11","key":"pone.0349611.ref028","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1016\/j.tplants.2006.09.011","article-title":"Futile cycling at the plasma membrane: a hallmark of low-affinity nutrient transport","volume":"11","author":"DT Britto","year":"2006","journal-title":"Trends Plant Sci"},{"key":"pone.0349611.ref029","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1146\/annurev.mi.39.100185.000513","article-title":"Carbon metabolism in Rhizobium species","volume":"39","author":"MD Stowers","year":"1985","journal-title":"Annu Rev Microbiol"},{"issue":"5","key":"pone.0349611.ref030","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0064682","article-title":"ABC transport is inactivated by the PTS(Ntr) under potassium limitation in Rhizobium leguminosarum 3841","volume":"8","author":"V Untiet","year":"2013","journal-title":"PLoS One"},{"key":"pone.0349611.ref031","first-page":"1","article-title":"Energetics and biological costs of nitrogen assimilation.","volume-title":"The Biochemistry of Plants","author":"JS Pate","year":"1990"},{"key":"pone.0349611.ref032","unstructured":"USDA. 2011 Carbon to nitrogen ratios in cropping systems. USDA Natural Resources Conservation Service. https:\/\/www.nrcs.usda.gov\/Internet\/FSE_DOCUMENTS\/nrcseprd331820.pdf"},{"key":"pone.0349611.ref033","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1017\/S0021859600011163","article-title":"On the influence of the carbon:nitrogen ratios of organic material on the mineralization of nitrogen","volume":"19","author":"HL Jensen","year":"1929","journal-title":"J Agr Sci"},{"key":"pone.0349611.ref034","first-page":"73","article-title":"Cultural and biochemical characteristics of the root nodule bacteria","volume-title":"Root Nodule Bacteria and Leguminous Plants","author":"EB Fred","year":"1932"},{"issue":"3","key":"pone.0349611.ref035","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1007\/BF02184267","article-title":"Efficiencies and inefficiencies in the legume\/Rhizobium symbiosis\u2014a review","volume":"82","author":"CA Atkins","year":"1984","journal-title":"Plant Soil"},{"issue":"6","key":"pone.0349611.ref036","doi-asserted-by":"crossref","first-page":"888","DOI":"10.1080\/00380768.2013.838742","article-title":"Quantitative analysis of the initial transport of fixed nitrogen in nodulated soybean plants using15N as a tracer","volume":"59","author":"N Van Phi Hung","year":"2013","journal-title":"Soil Sci Plant Nutr"},{"key":"pone.0349611.ref037","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.3389\/fpls.2015.01062","article-title":"Stoichiometric Characteristics of Carbon, Nitrogen, and Phosphorus in Leaves of Differently Aged Lucerne (Medicago sativa) Stands","volume":"6","author":"Z Wang","year":"2015","journal-title":"Front Plant Sci"},{"key":"pone.0349611.ref038","unstructured":"USDA. 2014 Plant\u2013microbe interaction\u2014C:N ratio. Agronomy Tech Note 76. 2014. Available from: http:\/\/www.nrcs.usda.gov\/wps\/portal\/nrcs\/detail\/nm\/technical\/?cid=nrcs144p2_068965"},{"issue":"9","key":"pone.0349611.ref039","first-page":"333","article-title":"Regulation of symbiotic nitrogen fixation in legume root nodules","volume":"8","author":"AR Schwember","year":"2019","journal-title":"Plants (Basel)"},{"key":"pone.0349611.ref040","doi-asserted-by":"crossref","first-page":"507946","DOI":"10.1155\/2014\/507946","article-title":"The carbon-nitrogen balance of the nodule and its regulation under elevated carbon dioxide concentration","volume":"2014","author":"M Libault","year":"2014","journal-title":"Biomed Res Int"},{"key":"pone.0349611.ref041","doi-asserted-by":"crossref","first-page":"1860","DOI":"10.3389\/fpls.2018.01860","article-title":"Interaction and regulation of carbon, nitrogen, and phosphorus metabolisms in root nodules of legumes","volume":"9","author":"A Liu","year":"2018","journal-title":"Front Plant Sci"}],"container-title":["PLOS One"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0349611","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,22]],"date-time":"2026-05-22T17:45:28Z","timestamp":1779471928000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0349611"}},"subtitle":[],"editor":[{"given":"Nabin","family":"Rawal","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026,5,22]]},"references-count":41,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2026,5,22]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0349611","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,5,22]]}}}