{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T14:02:57Z","timestamp":1789653777636,"version":"4.0.0"},"reference-count":44,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2026,8,27]],"date-time":"2026-08-27T00:00:00Z","timestamp":1787788800000},"content-version":"vor","delay-in-days":238,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["42207364"],"award-info":[{"award-number":["42207364"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["42230511"],"award-info":[{"award-number":["42230511"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002367","name":"Chinese Academy of Sciences","doi-asserted-by":"publisher","award":["XDA28020202"],"award-info":[{"award-number":["XDA28020202"]}],"id":[{"id":"10.13039\/501100002367","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,7,6]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The rhizosphere metabolic circular economy (RMCE) governs the exchange, reuse, and reconfiguration of metabolites at the root\u2212soil interface. Building on traditional binary plant\u2212microbe models, this perspective advances an expanded RMCE framework by integrating three additional interdependent dimensions that explain how rhizosphere metabolic processes persist over time, organize across space, and recover under environmental stress. First, the live-dead plant\u2212microbe continuum enables metabolic persistence by incorporating microbial necromass and root residues into long-term carbon sequestration and nutrient regeneration. Second, spatial organization across rhizosphere microzones optimizes microscale metabolic interactions through niche heterogeneity. Third, adaptive restoration dynamically re-establishes disrupted metabolic networks through coordinated plant\u2212microbiome stress responses. We further outline scenario-based management strategies to translate the RMCE insights into practical solutions, which necessitates multiple approaches targeting root exudate quality, microbial necromass dynamics, rhizosphere spatial architecture, and cross-kingdom signaling. Together, these advances redefine RMCE as a dynamically regulated, spatially structured, and ecologically complex system, providing a more comprehensive basis for its optimization in sustainable ecosystems.<\/jats:p>","DOI":"10.1093\/sumbio\/qvag037","type":"journal-article","created":{"date-parts":[[2026,8,27]],"date-time":"2026-08-27T14:40:15Z","timestamp":1787841615000},"source":"Crossref","is-referenced-by-count":0,"title":["Optimizing rhizosphere metabolic circular economy toward sustainable ecosystems"],"prefix":"10.1093","volume":"3","author":[{"given":"Kunkun","family":"Fan","sequence":"first","affiliation":[{"name":"State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences , Nanjing 211135 ,","place":["China"]},{"name":"College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences , Beijing 101408 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3987-8836","authenticated-orcid":false,"given":"Zhihui","family":"Xu","sequence":"additional","affiliation":[{"name":"Jiangsu Provincial Key Lab for Organic-based Fertilizers Creation and Soil Health Manipulation, Jiangsu Collaborative Innovation Center for Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University , Nanjing 211800 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2746-4131","authenticated-orcid":false,"given":"Kai","family":"Sun","sequence":"additional","affiliation":[{"name":"Jiangsu Key Laboratory for Pathogens and Ecosystems, Jiangsu Engineering and Technology Research Center for Industrialization of Microbial Resources, College of Life Sciences, Nanjing Normal University , Nanjing 210023 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9004-8750","authenticated-orcid":false,"given":"Haiyan","family":"Chu","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences , Nanjing 211135 ,","place":["China"]},{"name":"College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences , Beijing 101408 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2026,8,27]]},"reference":[{"key":"2026091709120497000_bib1","doi-asserted-by":"publisher","first-page":"1074279","DOI":"10.3389\/fpls.2023.1074279","article-title":"Plant-microbe interactions ameliorate phosphate-mediated responses in the rhizosphere: a review","volume":"14","author":"Abbasi","year":"2023","journal-title":"Front Plant Sci"},{"key":"2026091709120497000_bib2","doi-asserted-by":"publisher","first-page":"109253","DOI":"10.1016\/j.soilbio.2023.109253","article-title":"Emerging sensing, imaging, and computational technologies to scale nano-to macroscale rhizosphere dynamics-review and research perspectives","volume":"189","author":"Ahkami","year":"2024","journal-title":"Soil Biol Biochem"},{"key":"2026091709120497000_bib3","doi-asserted-by":"publisher","first-page":"2041","DOI":"10.1007\/s11104-025-07972-9","article-title":"Arbuscular mycorrhizal fungi mediated hormonal interplay under drought stress conditions: current insights and future directions","volume":"517","author":"Chandrasekaran","year":"2025","journal-title":"Plant Soil"},{"key":"2026091709120497000_bib4","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1016\/j.pedsph.2022.10.001","article-title":"Molecular mechanisms of plant adaptation to acid soils: a review","volume":"33","author":"Che","year":"2023","journal-title":"Pedosphere"},{"key":"2026091709120497000_bib5","doi-asserted-by":"publisher","first-page":"1106033","DOI":"10.3389\/fpls.2023.1106033","article-title":"Autotoxins in continuous tobacco cropping soils and their management","volume":"14","author":"Chen","year":"2023","journal-title":"Front Plant Sci"},{"key":"2026091709120497000_bib6","doi-asserted-by":"publisher","first-page":"773","DOI":"10.1038\/s41579-024-01073-7","article-title":"Cross-kingdom nutrient exchange in the plant-arbuscular mycorrhizal fungus-bacterium continuum","volume":"22","author":"Duan","year":"2024","journal-title":"Nat Rev Micro"},{"key":"2026091709120497000_bib7","doi-asserted-by":"publisher","first-page":"wraf040","DOI":"10.1093\/ismejo\/wraf040","article-title":"Plant growth-promotion triggered by extracellular polymer is associated with facilitation of bacterial cross-feeding networks of the rhizosphere","volume":"19","author":"Gu","year":"2025","journal-title":"ISMEJ"},{"key":"2026091709120497000_bib8","doi-asserted-by":"publisher","first-page":"2738","DOI":"10.1038\/s41467-018-05122-7","article-title":"Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota","volume":"9","author":"Hu","year":"2018","journal-title":"Nat Commun"},{"key":"2026091709120497000_bib9","doi-asserted-by":"publisher","first-page":"21186","DOI":"10.1021\/acs.est.4c07264","article-title":"Lithological controls on soil aggregates and minerals regulate microbial carbon use efficiency and necromass stability","volume":"58","author":"Hu","year":"2024","journal-title":"Environ Sci Technol"},{"key":"2026091709120497000_bib10","doi-asserted-by":"publisher","first-page":"3476","DOI":"10.1111\/gcb.16685","article-title":"Plant growth strategy determines the magnitude and direction of drought-induced changes in root exudates in subtropical forests","volume":"29","author":"Jiang","year":"2023","journal-title":"Global Change Biol"},{"key":"2026091709120497000_bib11","doi-asserted-by":"publisher","first-page":"104503","DOI":"10.1016\/j.apsoil.2022.104503","article-title":"Consortia-based microbial inoculants for sustaining agricultural activities","volume":"176","author":"Khan","year":"2022","journal-title":"Appl Soil Ecol"},{"key":"2026091709120497000_bib12","doi-asserted-by":"publisher","first-page":"3168","DOI":"10.1093\/plcell\/koac163","article-title":"Plant-microbe interactions in the rhizosphere via a circular metabolic economy","volume":"34","author":"Korenblum","year":"2022","journal-title":"Plant Cell"},{"key":"2026091709120497000_bib13","doi-asserted-by":"publisher","first-page":"109457","DOI":"10.1016\/j.soilbio.2024.109457","article-title":"Microbial metabolic capacity regulates the accrual of mineral-associated organic carbon in subtropical paddy soils","volume":"195","author":"Li","year":"2024","journal-title":"Soil Biol Biochem"},{"key":"2026091709120497000_bib14","doi-asserted-by":"publisher","first-page":"1410","DOI":"10.3390\/f14071410","article-title":"Physiology, transcriptome and root exudates analysis of response to aluminum stress in pinus massoniana","volume":"14","author":"Ling","year":"2023","journal-title":"Forests"},{"key":"2026091709120497000_bib15","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.soilbio.2015.09.020","article-title":"Substrate quality affects kinetics and catalytic efficiency of exo-enzymes in rhizosphere and detritusphere","volume":"92","author":"Loeppmann","year":"2016","journal-title":"Soil Biol Biochem"},{"key":"2026091709120497000_bib16","doi-asserted-by":"publisher","first-page":"989","DOI":"10.1007\/s00374-023-01768-8","article-title":"Halophyte functional groups influence seasonal variations in rhizosphere microbial necromass and enzyme activities in an inland saline ecosystem","volume":"59","author":"Lu","year":"2023","journal-title":"Biol Fertil Soils"},{"key":"2026091709120497000_bib17","doi-asserted-by":"publisher","first-page":"477","DOI":"10.3390\/stresses2040033","article-title":"Involvement of nitric oxide in methyl jasmonate-mediated regulation of water metabolism in wheat plants under drought stress","volume":"2","author":"Lubyanova","year":"2022","journal-title":"Stresses"},{"key":"2026091709120497000_bib18","doi-asserted-by":"publisher","first-page":"10148","DOI":"10.1038\/s41467-024-54616-0","article-title":"Quinolone-mediated metabolic cross-feeding develops aluminium tolerance in soil microbial consortia","volume":"15","author":"Ma","year":"2024","journal-title":"Nat Commun"},{"key":"2026091709120497000_bib19","doi-asserted-by":"publisher","first-page":"100553","DOI":"10.1016\/j.rhisph.2022.100553","article-title":"High content and distinct spectroscopic characteristics of water-extractable organic matter in rhizosheath soils in a semiarid grassland","volume":"23","author":"Mo","year":"2022","journal-title":"Rhizosphere"},{"key":"2026091709120497000_bib20","doi-asserted-by":"publisher","first-page":"877","DOI":"10.1007\/s00253-022-11772-x","article-title":"Possible mechanisms for the equilibrium of acc and role of acc deaminase-producing bacteria","volume":"106","author":"Moon","year":"2022","journal-title":"Appl Microbiol Biotechnol"},{"key":"2026091709120497000_bib21","doi-asserted-by":"publisher","first-page":"1623","DOI":"10.1007\/s11104-025-07944-z","article-title":"Early inoculation with arbuscular mycorrhizal fungi shifts metabolic functions of rhizosphere bacteria in field-grown tomato plants","volume":"517","author":"Moreno","year":"2025","journal-title":"Plant Soil"},{"key":"2026091709120497000_bib22","doi-asserted-by":"publisher","first-page":"109396","DOI":"10.1016\/j.soilbio.2024.109396","article-title":"From rhizosphere to detritusphere-soil structure formation driven by plant roots and the interactions with soil biota","volume":"193","author":"Mueller","year":"2024","journal-title":"Soil Biol Biochem"},{"key":"2026091709120497000_bib23","doi-asserted-by":"publisher","first-page":"7253","DOI":"10.1073\/pnas.1006740108","article-title":"Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants","volume":"108","author":"Ortiz-Castro","year":"2011","journal-title":"Proc Natl Acad Sci USA"},{"key":"2026091709120497000_bib24","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1016\/j.plantsci.2019.04.010","article-title":"Review: phytostimulation and root architectural responses to quorum-sensing signals and related molecules from rhizobacteria","volume":"284","author":"Ortiz-Castro","year":"2019","journal-title":"Plant Sci"},{"key":"2026091709120497000_bib25","doi-asserted-by":"publisher","first-page":"1046","DOI":"10.1016\/j.tplants.2025.04.007","article-title":"Hub metabolites at the root-microbiome interface: unlocking plant drought resilience","volume":"30","author":"Pantigoso","year":"2025","journal-title":"Trends Plant Sci"},{"key":"2026091709120497000_bib26","doi-asserted-by":"publisher","first-page":"172116","DOI":"10.1016\/j.scitotenv.2024.172116","article-title":"Mechanistic and future prospects in rhizospheric engineering for agricultural contaminants removal, soil health restoration, and management of climate change stress","volume":"927","author":"Pathak","year":"2024","journal-title":"Sci Total Environ"},{"key":"2026091709120497000_bib27","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1038\/s41579-023-00980-5","article-title":"The interplay between microbial communities and soil properties","volume":"22","author":"Philippot","year":"2024","journal-title":"Nat Rev Micro"},{"key":"2026091709120497000_bib28","doi-asserted-by":"publisher","first-page":"632","DOI":"10.1111\/tpj.15490","article-title":"Fungal social influencers: secondary metabolites as a platform for shaping the plant-associated community","volume":"108","author":"Rangel","year":"2021","journal-title":"Plant J"},{"key":"2026091709120497000_bib29","doi-asserted-by":"publisher","first-page":"167463","DOI":"10.1016\/j.scitotenv.2023.167463","article-title":"Reevaluation and novel insights into amino sugar and neutral sugar necromass biomarkers in archaea, bacteria, fungi, and plants","volume":"906","author":"Salas","year":"2024","journal-title":"Sci Total Environ"},{"key":"2026091709120497000_bib30","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1038\/nature07088","article-title":"A new class of homoserine lactone quorum-sensing signals","volume":"454","author":"Schaefer","year":"2008","journal-title":"Nature"},{"key":"2026091709120497000_bib31","doi-asserted-by":"publisher","first-page":"109212","DOI":"10.1016\/j.soilbio.2023.109212","article-title":"Contrasting mechanisms of nutrient mobilization in rhizosphere hotspots driven by straw and biochar amendment","volume":"187","author":"Shang","year":"2023","journal-title":"Soil Biol Biochem"},{"key":"2026091709120497000_bib32","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1186\/s12915-022-01464-3","article-title":"Ahl-priming protein 1 mediates n-3-oxo-tetradecanoyl-homoserine lactone priming in arabidopsis","volume":"20","author":"Shrestha","year":"2022","journal-title":"BMC Biol"},{"key":"2026091709120497000_bib33","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1038\/s41561-018-0258-6","article-title":"Microbial formation of stable soil carbon is more efficient from belowground than aboveground input","volume":"12","author":"Sokol","year":"2019","journal-title":"Nat Geosci"},{"key":"2026091709120497000_bib34","doi-asserted-by":"publisher","first-page":"100907","DOI":"10.1016\/j.stress.2025.100907","article-title":"Plant root exudates: advances in belowground signaling networks, resilience, and ecosystem functioning for sustainable agriculture","volume":"17","author":"Sorty","year":"2025","journal-title":"Plant Stress"},{"key":"2026091709120497000_bib35","doi-asserted-by":"publisher","first-page":"270","DOI":"10.56557\/pcbmb\/2025\/v26i9-109828","article-title":"Biochemical interactions in the rhizosphere: roles of root exudates, flavonoids and phytoalexins in plant-microbe communication","volume":"26","author":"Suresh","year":"2025","journal-title":"Plant Cell Biotech Mol Biol"},{"key":"2026091709120497000_bib36","doi-asserted-by":"publisher","first-page":"917","DOI":"10.1007\/s00374-025-01975-5","article-title":"The rhizosphere exhibits higher microbial carbon use efficiency compared to bulk soil","volume":"62","author":"Tan","year":"2026","journal-title":"Biol Fertil Soils"},{"key":"2026091709120497000_bib37","doi-asserted-by":"publisher","first-page":"eadu4235","DOI":"10.1126\/science.adu4235","article-title":"Localized glutamine leakage drives the spatial structure of root microbial colonization","volume":"390","author":"Tsai","year":"2025","journal-title":"Science"},{"key":"2026091709120497000_bib38","doi-asserted-by":"publisher","first-page":"108422","DOI":"10.1016\/j.soilbio.2021.108422","article-title":"Microbial necromass as the source of soil organic carbon in global ecosystems","volume":"162","author":"Wang","year":"2021","journal-title":"Soil Biol Biochem"},{"key":"2026091709120497000_bib39","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1016\/j.tplants.2023.09.015","article-title":"Rhizosphere engineering for soil carbon sequestration","volume":"29","author":"Wang","year":"2023","journal-title":"Trends Plant Sci"},{"key":"2026091709120497000_bib40","doi-asserted-by":"publisher","first-page":"109529","DOI":"10.1016\/j.soilbio.2024.109529","article-title":"Microbial metabolic traits drive the differential contribution of microbial necromass to soil organic carbon between the rhizosphere of absorptive roots and transport roots","volume":"197","author":"Wang","year":"2024","journal-title":"Soil Biol Biochem"},{"key":"2026091709120497000_bib41","doi-asserted-by":"publisher","first-page":"1194","DOI":"10.1016\/j.tplants.2020.07.006","article-title":"Sustainable cropping requires adaptation to a heterogeneous rhizosphere","volume":"25","author":"Wang","year":"2020","journal-title":"Trends Plant Sci"},{"key":"2026091709120497000_bib42","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1186\/s40168-018-0537-x","article-title":"Root exudates drive the soil-borne legacy of aboveground pathogen infection","volume":"6","author":"Yuan","year":"2018","journal-title":"Microbiome"},{"key":"2026091709120497000_bib43","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1038\/s41564-018-0129-3","article-title":"Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly","volume":"3","author":"Zhalnina","year":"2018","journal-title":"Nat Microbiol"},{"key":"2026091709120497000_bib44","doi-asserted-by":"publisher","first-page":"108880","DOI":"10.1016\/j.agee.2023.108880","article-title":"Intercropping regulates plant- and microbe-derived carbon accumulation by influencing soil physicochemical and microbial physiological properties","volume":"364","author":"Zhu","year":"2024","journal-title":"Agricult Ecosyst Environ"}],"container-title":["Sustainable Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/sumbio\/advance-article-pdf\/doi\/10.1093\/sumbio\/qvag037\/70819668\/qvag037.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/sumbio\/article-pdf\/3\/3\/qvag037\/70819668\/qvag037.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/sumbio\/article-pdf\/3\/3\/qvag037\/70819668\/qvag037.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T13:12:08Z","timestamp":1789650728000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/sumbio\/article\/doi\/10.1093\/sumbio\/qvag037\/8771870"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026]]},"references-count":44,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2026,7,6]]}},"URL":"https:\/\/doi.org\/10.1093\/sumbio\/qvag037","relation":{},"ISSN":["2755-1970"],"issn-type":[{"value":"2755-1970","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2026]]},"published":{"date-parts":[[2026]]},"article-number":"qvag037"}}