Nitrogen fixation and crop productivity enhancements co‐driven by intercrop root exudates and key rhizosphere bacteria

Crop diversity management is widely used to increase agricultural productivity and sustainability. Recent studies have demonstrated that maize root exudates can drive interspecific facilitation to enhance N2 fixation of bean in intercropping systems. However, the mechanisms of N2 fixation enhancemen...

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Veröffentlicht in:The Journal of applied ecology 2021-10, Vol.58 (10), p.2243-2255
Hauptverfasser: Hu, Heng‐Yu, Li, Hong, Hao, Min‐Min, Ren, Ya‐Nan, Zhang, Meng‐Kun, Liu, Ru‐Yue, Zhang, Yin, Li, Geng, Chen, Jian‐Sheng, Ning, Tang‐Yuan, Kuzyakov, Yakov
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container_title The Journal of applied ecology
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creator Hu, Heng‐Yu
Li, Hong
Hao, Min‐Min
Ren, Ya‐Nan
Zhang, Meng‐Kun
Liu, Ru‐Yue
Zhang, Yin
Li, Geng
Chen, Jian‐Sheng
Ning, Tang‐Yuan
Kuzyakov, Yakov
description Crop diversity management is widely used to increase agricultural productivity and sustainability. Recent studies have demonstrated that maize root exudates can drive interspecific facilitation to enhance N2 fixation of bean in intercropping systems. However, the mechanisms of N2 fixation enhancement stimulated by root exudates in the intercropping systems remain unclear. Four experiments were designed to provide a progressively deeper understanding of how root exudates stimulate microbial‐mediated N2 fixation. First, the effects of faba bean/maize intercropping on yields and soil microbial communities were determined in a field experiment. Second, root‐derived interspecific facilitation was evaluated using a root partitioning approach. Third, the key microbial taxa in the faba bean rhizosphere were traced using 13C‐labelled maize root exudates. Fourth, the co‐driven mechanism of maize root exudates and micro‐organisms in the faba bean rhizosphere were explored. Faba bean/maize intercropping with maize residue return increased the yields of faba bean (26%), maize (27%) and broccoli (9.1%) compared to that under monocropping. Nodulin‐like 4 (NODL4), chalcone‐flavanone isomerase (CFI) and early nodulin‐like (ENODL2) gene expression in faba bean roots intercropped with maize increased by 1.5–2.3‐fold compared to that observed under monoculture. More than half of the N2 fixation of faba bean increase under intercropping was due to interactions with micro‐organisms. Nine key bacterial genera in the faba bean rhizosphere were identified by 13C‐DNA‐based stable isotope probing analysis. Among them Agromyces, Arthrobacter, Bacillus, Lysobacter and Paenibacillus directly fix N2, while Gemmatimonas, Heliobacillus, Natronocella and Sorangium increase the N2 fixation capacity of Azotobacter by providing additional carbon sources. These key bacteria triggered by maize root exudates played an important role in the rhizosphere facilitation of intercropping. Synthesis and applications. We demonstrated a novel root–root facilitation of N2 fixation and increased crop yields co‐driven by root exudates and rhizosphere bacteria under faba bean/maize intercropping, and nine key bacteria associated with this process were identified by 13C‐DNA‐based stable isotope probing. We recommend the adoption and optimization of intercropping systems with residue return to reduce the shortcomings of continuous cropping and to increase the sustainability of crop production. 摘要 作物多样性管理被广泛用于提高
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Recent studies have demonstrated that maize root exudates can drive interspecific facilitation to enhance N2 fixation of bean in intercropping systems. However, the mechanisms of N2 fixation enhancement stimulated by root exudates in the intercropping systems remain unclear. Four experiments were designed to provide a progressively deeper understanding of how root exudates stimulate microbial‐mediated N2 fixation. First, the effects of faba bean/maize intercropping on yields and soil microbial communities were determined in a field experiment. Second, root‐derived interspecific facilitation was evaluated using a root partitioning approach. Third, the key microbial taxa in the faba bean rhizosphere were traced using 13C‐labelled maize root exudates. Fourth, the co‐driven mechanism of maize root exudates and micro‐organisms in the faba bean rhizosphere were explored. Faba bean/maize intercropping with maize residue return increased the yields of faba bean (26%), maize (27%) and broccoli (9.1%) compared to that under monocropping. Nodulin‐like 4 (NODL4), chalcone‐flavanone isomerase (CFI) and early nodulin‐like (ENODL2) gene expression in faba bean roots intercropped with maize increased by 1.5–2.3‐fold compared to that observed under monoculture. More than half of the N2 fixation of faba bean increase under intercropping was due to interactions with micro‐organisms. Nine key bacterial genera in the faba bean rhizosphere were identified by 13C‐DNA‐based stable isotope probing analysis. Among them Agromyces, Arthrobacter, Bacillus, Lysobacter and Paenibacillus directly fix N2, while Gemmatimonas, Heliobacillus, Natronocella and Sorangium increase the N2 fixation capacity of Azotobacter by providing additional carbon sources. These key bacteria triggered by maize root exudates played an important role in the rhizosphere facilitation of intercropping. Synthesis and applications. We demonstrated a novel root–root facilitation of N2 fixation and increased crop yields co‐driven by root exudates and rhizosphere bacteria under faba bean/maize intercropping, and nine key bacteria associated with this process were identified by 13C‐DNA‐based stable isotope probing. We recommend the adoption and optimization of intercropping systems with residue return to reduce the shortcomings of continuous cropping and to increase the sustainability of crop production. 摘要 作物多样性管理被广泛用于提高农业生产力与可持续性。最近的研究表明, 玉米根系分泌物可以促进种间互惠作用, 从而提高间作系统中豆科作物的固氮能力。然而, 套作系统中根系分泌物引起的豆科作物固氮量增加的机制尚不清楚。 我们设计了四个逐步加深试验来研究根系分泌物如何富集微生物并提高豆科作物固氮能力的机制。首先, 通过田间试验确定了蚕豆/玉米间作对作物产量和土壤微生物群落的影响。其次, 采用根系隔离方法验证根际种间互惠作用是否存在。利用13C标记的玉米根系分泌物对蚕豆根际关键微生物类群进行了示踪。第四, 探讨了玉米根系分泌物和蚕豆根际微生物对种间互惠作用的协同驱动机制。 蚕豆/玉米间作结合玉米秸秆还田蚕豆、玉米和西兰花分别比对应单作增产26%、27%和9.1%。玉米间作蚕豆根部关键结瘤基因NODL4、ENODL2和查尔酮‐黄酮异构酶CFI的表达量比单作增加1.5 ~ 2.3倍。间作条件下, 蚕豆固氮量增加的一半以上来源于微生物的作用。采用13C‐DNA稳定同位素探针方法, 鉴定出了9个利用玉米根系分泌物的蚕豆根际关键细菌。其中Agromyces、Arthrobacter、Bacillus、Lysobacter和Paenibacillus直接固氮, 而Gemmatimonas、Heliobacillus、Natronocella和Sorangium则通过提供额外的碳源增加固氮菌的固氮能力。这些由玉米根系分泌物招集的关键细菌在间作根际互惠效应中起着重要作用。 理论与应用。我们揭示了蚕豆/玉米间作根系分泌物和根际微生物细菌共同驱动的根系固氮促进和作物产量增加的新机制, 并通过13C‐DNA‐稳定同位素探针鉴定出与此过程密切相关的9种关键细菌。建议采用并优化间作模式, 结合秸秆还田技术, 以减少连作障碍, 提高粮食生产的可持续性。 We demonstrated a novel root–root facilitation of N2 fixation and increased crop yields co‐driven by root exudates and rhizosphere bacteria under faba bean/maize intercropping, and nine key bacteria associated with this process were identified by 13C‐DNA‐based stable isotope probing. We recommend the adoption and optimization of intercropping systems with residue return to reduce the shortcomings of continuous cropping and to increase the sustainability of crop production.</description><identifier>ISSN: 0021-8901</identifier><identifier>EISSN: 1365-2664</identifier><identifier>DOI: 10.1111/1365-2664.13964</identifier><language>eng</language><publisher>HOBOKEN: Wiley</publisher><subject>Agricultural practices ; Agricultural production ; Arthrobacter ; Azotobacter ; Bacillus ; Bacteria ; Beans ; Biodiversity &amp; Conservation ; Broad beans ; Broccoli ; Carbon sources ; Continuous cropping ; Corn ; crop biodiversity ; Crop diversification ; Crop production ; Crop residues ; Crop yield ; Crops ; Deoxyribonucleic acid ; DNA ; Ecology ; Environmental Sciences &amp; Ecology ; Exudates ; Exudation ; Gene expression ; Intercropping ; Interspecific ; Life Sciences &amp; Biomedicine ; Microbial activity ; Microorganisms ; Monoculture ; Nitrogen fixation ; Nitrogenation ; Optimization ; Productivity ; residue retention ; Residues ; Rhizosphere ; rhizosphere facilitation ; root exudates ; Science &amp; Technology ; soil bacteria ; stable isotope probing ; Stable isotopes ; Sustainability ; Vegetables</subject><ispartof>The Journal of applied ecology, 2021-10, Vol.58 (10), p.2243-2255</ispartof><rights>2021 British Ecological Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>40</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000678635800001</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c3154-a8e9d44e1891779eba26139e8f27fe07c962225bbeee3a7f6d829076963a0cf13</citedby><cites>FETCH-LOGICAL-c3154-a8e9d44e1891779eba26139e8f27fe07c962225bbeee3a7f6d829076963a0cf13</cites><orcidid>0000-0002-7356-5294 ; 0000-0002-9863-8461</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1365-2664.13964$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1365-2664.13964$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,781,785,1418,1434,27928,27929,39262,45578,45579,46413,46837</link.rule.ids></links><search><creatorcontrib>Hu, Heng‐Yu</creatorcontrib><creatorcontrib>Li, Hong</creatorcontrib><creatorcontrib>Hao, Min‐Min</creatorcontrib><creatorcontrib>Ren, Ya‐Nan</creatorcontrib><creatorcontrib>Zhang, Meng‐Kun</creatorcontrib><creatorcontrib>Liu, Ru‐Yue</creatorcontrib><creatorcontrib>Zhang, Yin</creatorcontrib><creatorcontrib>Li, Geng</creatorcontrib><creatorcontrib>Chen, Jian‐Sheng</creatorcontrib><creatorcontrib>Ning, Tang‐Yuan</creatorcontrib><creatorcontrib>Kuzyakov, Yakov</creatorcontrib><title>Nitrogen fixation and crop productivity enhancements co‐driven by intercrop root exudates and key rhizosphere bacteria</title><title>The Journal of applied ecology</title><addtitle>J APPL ECOL</addtitle><description>Crop diversity management is widely used to increase agricultural productivity and sustainability. Recent studies have demonstrated that maize root exudates can drive interspecific facilitation to enhance N2 fixation of bean in intercropping systems. However, the mechanisms of N2 fixation enhancement stimulated by root exudates in the intercropping systems remain unclear. Four experiments were designed to provide a progressively deeper understanding of how root exudates stimulate microbial‐mediated N2 fixation. First, the effects of faba bean/maize intercropping on yields and soil microbial communities were determined in a field experiment. Second, root‐derived interspecific facilitation was evaluated using a root partitioning approach. Third, the key microbial taxa in the faba bean rhizosphere were traced using 13C‐labelled maize root exudates. Fourth, the co‐driven mechanism of maize root exudates and micro‐organisms in the faba bean rhizosphere were explored. Faba bean/maize intercropping with maize residue return increased the yields of faba bean (26%), maize (27%) and broccoli (9.1%) compared to that under monocropping. Nodulin‐like 4 (NODL4), chalcone‐flavanone isomerase (CFI) and early nodulin‐like (ENODL2) gene expression in faba bean roots intercropped with maize increased by 1.5–2.3‐fold compared to that observed under monoculture. More than half of the N2 fixation of faba bean increase under intercropping was due to interactions with micro‐organisms. Nine key bacterial genera in the faba bean rhizosphere were identified by 13C‐DNA‐based stable isotope probing analysis. Among them Agromyces, Arthrobacter, Bacillus, Lysobacter and Paenibacillus directly fix N2, while Gemmatimonas, Heliobacillus, Natronocella and Sorangium increase the N2 fixation capacity of Azotobacter by providing additional carbon sources. These key bacteria triggered by maize root exudates played an important role in the rhizosphere facilitation of intercropping. Synthesis and applications. We demonstrated a novel root–root facilitation of N2 fixation and increased crop yields co‐driven by root exudates and rhizosphere bacteria under faba bean/maize intercropping, and nine key bacteria associated with this process were identified by 13C‐DNA‐based stable isotope probing. We recommend the adoption and optimization of intercropping systems with residue return to reduce the shortcomings of continuous cropping and to increase the sustainability of crop production. 摘要 作物多样性管理被广泛用于提高农业生产力与可持续性。最近的研究表明, 玉米根系分泌物可以促进种间互惠作用, 从而提高间作系统中豆科作物的固氮能力。然而, 套作系统中根系分泌物引起的豆科作物固氮量增加的机制尚不清楚。 我们设计了四个逐步加深试验来研究根系分泌物如何富集微生物并提高豆科作物固氮能力的机制。首先, 通过田间试验确定了蚕豆/玉米间作对作物产量和土壤微生物群落的影响。其次, 采用根系隔离方法验证根际种间互惠作用是否存在。利用13C标记的玉米根系分泌物对蚕豆根际关键微生物类群进行了示踪。第四, 探讨了玉米根系分泌物和蚕豆根际微生物对种间互惠作用的协同驱动机制。 蚕豆/玉米间作结合玉米秸秆还田蚕豆、玉米和西兰花分别比对应单作增产26%、27%和9.1%。玉米间作蚕豆根部关键结瘤基因NODL4、ENODL2和查尔酮‐黄酮异构酶CFI的表达量比单作增加1.5 ~ 2.3倍。间作条件下, 蚕豆固氮量增加的一半以上来源于微生物的作用。采用13C‐DNA稳定同位素探针方法, 鉴定出了9个利用玉米根系分泌物的蚕豆根际关键细菌。其中Agromyces、Arthrobacter、Bacillus、Lysobacter和Paenibacillus直接固氮, 而Gemmatimonas、Heliobacillus、Natronocella和Sorangium则通过提供额外的碳源增加固氮菌的固氮能力。这些由玉米根系分泌物招集的关键细菌在间作根际互惠效应中起着重要作用。 理论与应用。我们揭示了蚕豆/玉米间作根系分泌物和根际微生物细菌共同驱动的根系固氮促进和作物产量增加的新机制, 并通过13C‐DNA‐稳定同位素探针鉴定出与此过程密切相关的9种关键细菌。建议采用并优化间作模式, 结合秸秆还田技术, 以减少连作障碍, 提高粮食生产的可持续性。 We demonstrated a novel root–root facilitation of N2 fixation and increased crop yields co‐driven by root exudates and rhizosphere bacteria under faba bean/maize intercropping, and nine key bacteria associated with this process were identified by 13C‐DNA‐based stable isotope probing. We recommend the adoption and optimization of intercropping systems with residue return to reduce the shortcomings of continuous cropping and to increase the sustainability of crop production.</description><subject>Agricultural practices</subject><subject>Agricultural production</subject><subject>Arthrobacter</subject><subject>Azotobacter</subject><subject>Bacillus</subject><subject>Bacteria</subject><subject>Beans</subject><subject>Biodiversity &amp; Conservation</subject><subject>Broad beans</subject><subject>Broccoli</subject><subject>Carbon sources</subject><subject>Continuous cropping</subject><subject>Corn</subject><subject>crop biodiversity</subject><subject>Crop diversification</subject><subject>Crop production</subject><subject>Crop residues</subject><subject>Crop yield</subject><subject>Crops</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Ecology</subject><subject>Environmental Sciences &amp; Ecology</subject><subject>Exudates</subject><subject>Exudation</subject><subject>Gene expression</subject><subject>Intercropping</subject><subject>Interspecific</subject><subject>Life Sciences &amp; Biomedicine</subject><subject>Microbial activity</subject><subject>Microorganisms</subject><subject>Monoculture</subject><subject>Nitrogen fixation</subject><subject>Nitrogenation</subject><subject>Optimization</subject><subject>Productivity</subject><subject>residue retention</subject><subject>Residues</subject><subject>Rhizosphere</subject><subject>rhizosphere facilitation</subject><subject>root exudates</subject><subject>Science &amp; Technology</subject><subject>soil bacteria</subject><subject>stable isotope probing</subject><subject>Stable isotopes</subject><subject>Sustainability</subject><subject>Vegetables</subject><issn>0021-8901</issn><issn>1365-2664</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>HGBXW</sourceid><recordid>eNqNkLtuFDEUhi0UJDYhdVpLlGgSX2Z8KdEqgaAIKKC2PJ4zWediL7Yn7FDlEXhGngTvbpSWuLFl_d-5fAidUHJK6zmjXHQNE6I9pVyL9hVaPP8coAUhjDZKE_oGHeZ8QwjRHecLtPniS4rXEPDoN7b4GLANA3YprvE6xWFyxT_4MmMIKxsc3EMoGbv49_HPkPxD5foZ-1Ag7ZAUY8GwmQZbIO8q3cKM08r_jnm9ggS4t66GvX2LXo_2LsPx032Eflycf19-aq6-frxcfrhqHKdd21gFemhboEpTKTX0lom6H6iRyRGIdFowxrq-BwBu5SgGxTSRQgtuiRspP0Lv9nXrNj8nyMXcxCmF2tKwTirNqdS6ps72qbpFzglGs07-3qbZUGK2es1WptnKNDu9lVB74hf0cczOQ7XzTFW_QirBO1VfhC592bldximUir5_OVrT3VPa38H8v7nM52_n-wH_Af25oFk</recordid><startdate>202110</startdate><enddate>202110</enddate><creator>Hu, Heng‐Yu</creator><creator>Li, Hong</creator><creator>Hao, Min‐Min</creator><creator>Ren, Ya‐Nan</creator><creator>Zhang, Meng‐Kun</creator><creator>Liu, Ru‐Yue</creator><creator>Zhang, Yin</creator><creator>Li, Geng</creator><creator>Chen, Jian‐Sheng</creator><creator>Ning, Tang‐Yuan</creator><creator>Kuzyakov, Yakov</creator><general>Wiley</general><general>Blackwell Publishing Ltd</general><scope>BLEPL</scope><scope>DTL</scope><scope>HGBXW</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7SS</scope><scope>7T7</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><orcidid>https://orcid.org/0000-0002-7356-5294</orcidid><orcidid>https://orcid.org/0000-0002-9863-8461</orcidid></search><sort><creationdate>202110</creationdate><title>Nitrogen fixation and crop productivity enhancements co‐driven by intercrop root exudates and key rhizosphere bacteria</title><author>Hu, Heng‐Yu ; Li, Hong ; Hao, Min‐Min ; Ren, Ya‐Nan ; Zhang, Meng‐Kun ; Liu, Ru‐Yue ; Zhang, Yin ; Li, Geng ; Chen, Jian‐Sheng ; Ning, Tang‐Yuan ; Kuzyakov, Yakov</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3154-a8e9d44e1891779eba26139e8f27fe07c962225bbeee3a7f6d829076963a0cf13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Agricultural practices</topic><topic>Agricultural production</topic><topic>Arthrobacter</topic><topic>Azotobacter</topic><topic>Bacillus</topic><topic>Bacteria</topic><topic>Beans</topic><topic>Biodiversity &amp; Conservation</topic><topic>Broad beans</topic><topic>Broccoli</topic><topic>Carbon sources</topic><topic>Continuous cropping</topic><topic>Corn</topic><topic>crop biodiversity</topic><topic>Crop diversification</topic><topic>Crop production</topic><topic>Crop residues</topic><topic>Crop yield</topic><topic>Crops</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Ecology</topic><topic>Environmental Sciences &amp; Ecology</topic><topic>Exudates</topic><topic>Exudation</topic><topic>Gene expression</topic><topic>Intercropping</topic><topic>Interspecific</topic><topic>Life Sciences &amp; Biomedicine</topic><topic>Microbial activity</topic><topic>Microorganisms</topic><topic>Monoculture</topic><topic>Nitrogen fixation</topic><topic>Nitrogenation</topic><topic>Optimization</topic><topic>Productivity</topic><topic>residue retention</topic><topic>Residues</topic><topic>Rhizosphere</topic><topic>rhizosphere facilitation</topic><topic>root exudates</topic><topic>Science &amp; Technology</topic><topic>soil bacteria</topic><topic>stable isotope probing</topic><topic>Stable isotopes</topic><topic>Sustainability</topic><topic>Vegetables</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hu, Heng‐Yu</creatorcontrib><creatorcontrib>Li, Hong</creatorcontrib><creatorcontrib>Hao, Min‐Min</creatorcontrib><creatorcontrib>Ren, Ya‐Nan</creatorcontrib><creatorcontrib>Zhang, Meng‐Kun</creatorcontrib><creatorcontrib>Liu, Ru‐Yue</creatorcontrib><creatorcontrib>Zhang, Yin</creatorcontrib><creatorcontrib>Li, Geng</creatorcontrib><creatorcontrib>Chen, Jian‐Sheng</creatorcontrib><creatorcontrib>Ning, Tang‐Yuan</creatorcontrib><creatorcontrib>Kuzyakov, Yakov</creatorcontrib><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>Web of Science - Science Citation Index Expanded - 2021</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>The Journal of applied ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hu, Heng‐Yu</au><au>Li, Hong</au><au>Hao, Min‐Min</au><au>Ren, Ya‐Nan</au><au>Zhang, Meng‐Kun</au><au>Liu, Ru‐Yue</au><au>Zhang, Yin</au><au>Li, Geng</au><au>Chen, Jian‐Sheng</au><au>Ning, Tang‐Yuan</au><au>Kuzyakov, Yakov</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Nitrogen fixation and crop productivity enhancements co‐driven by intercrop root exudates and key rhizosphere bacteria</atitle><jtitle>The Journal of applied ecology</jtitle><stitle>J APPL ECOL</stitle><date>2021-10</date><risdate>2021</risdate><volume>58</volume><issue>10</issue><spage>2243</spage><epage>2255</epage><pages>2243-2255</pages><issn>0021-8901</issn><eissn>1365-2664</eissn><abstract>Crop diversity management is widely used to increase agricultural productivity and sustainability. Recent studies have demonstrated that maize root exudates can drive interspecific facilitation to enhance N2 fixation of bean in intercropping systems. However, the mechanisms of N2 fixation enhancement stimulated by root exudates in the intercropping systems remain unclear. Four experiments were designed to provide a progressively deeper understanding of how root exudates stimulate microbial‐mediated N2 fixation. First, the effects of faba bean/maize intercropping on yields and soil microbial communities were determined in a field experiment. Second, root‐derived interspecific facilitation was evaluated using a root partitioning approach. Third, the key microbial taxa in the faba bean rhizosphere were traced using 13C‐labelled maize root exudates. Fourth, the co‐driven mechanism of maize root exudates and micro‐organisms in the faba bean rhizosphere were explored. Faba bean/maize intercropping with maize residue return increased the yields of faba bean (26%), maize (27%) and broccoli (9.1%) compared to that under monocropping. Nodulin‐like 4 (NODL4), chalcone‐flavanone isomerase (CFI) and early nodulin‐like (ENODL2) gene expression in faba bean roots intercropped with maize increased by 1.5–2.3‐fold compared to that observed under monoculture. More than half of the N2 fixation of faba bean increase under intercropping was due to interactions with micro‐organisms. Nine key bacterial genera in the faba bean rhizosphere were identified by 13C‐DNA‐based stable isotope probing analysis. Among them Agromyces, Arthrobacter, Bacillus, Lysobacter and Paenibacillus directly fix N2, while Gemmatimonas, Heliobacillus, Natronocella and Sorangium increase the N2 fixation capacity of Azotobacter by providing additional carbon sources. These key bacteria triggered by maize root exudates played an important role in the rhizosphere facilitation of intercropping. Synthesis and applications. We demonstrated a novel root–root facilitation of N2 fixation and increased crop yields co‐driven by root exudates and rhizosphere bacteria under faba bean/maize intercropping, and nine key bacteria associated with this process were identified by 13C‐DNA‐based stable isotope probing. We recommend the adoption and optimization of intercropping systems with residue return to reduce the shortcomings of continuous cropping and to increase the sustainability of crop production. 摘要 作物多样性管理被广泛用于提高农业生产力与可持续性。最近的研究表明, 玉米根系分泌物可以促进种间互惠作用, 从而提高间作系统中豆科作物的固氮能力。然而, 套作系统中根系分泌物引起的豆科作物固氮量增加的机制尚不清楚。 我们设计了四个逐步加深试验来研究根系分泌物如何富集微生物并提高豆科作物固氮能力的机制。首先, 通过田间试验确定了蚕豆/玉米间作对作物产量和土壤微生物群落的影响。其次, 采用根系隔离方法验证根际种间互惠作用是否存在。利用13C标记的玉米根系分泌物对蚕豆根际关键微生物类群进行了示踪。第四, 探讨了玉米根系分泌物和蚕豆根际微生物对种间互惠作用的协同驱动机制。 蚕豆/玉米间作结合玉米秸秆还田蚕豆、玉米和西兰花分别比对应单作增产26%、27%和9.1%。玉米间作蚕豆根部关键结瘤基因NODL4、ENODL2和查尔酮‐黄酮异构酶CFI的表达量比单作增加1.5 ~ 2.3倍。间作条件下, 蚕豆固氮量增加的一半以上来源于微生物的作用。采用13C‐DNA稳定同位素探针方法, 鉴定出了9个利用玉米根系分泌物的蚕豆根际关键细菌。其中Agromyces、Arthrobacter、Bacillus、Lysobacter和Paenibacillus直接固氮, 而Gemmatimonas、Heliobacillus、Natronocella和Sorangium则通过提供额外的碳源增加固氮菌的固氮能力。这些由玉米根系分泌物招集的关键细菌在间作根际互惠效应中起着重要作用。 理论与应用。我们揭示了蚕豆/玉米间作根系分泌物和根际微生物细菌共同驱动的根系固氮促进和作物产量增加的新机制, 并通过13C‐DNA‐稳定同位素探针鉴定出与此过程密切相关的9种关键细菌。建议采用并优化间作模式, 结合秸秆还田技术, 以减少连作障碍, 提高粮食生产的可持续性。 We demonstrated a novel root–root facilitation of N2 fixation and increased crop yields co‐driven by root exudates and rhizosphere bacteria under faba bean/maize intercropping, and nine key bacteria associated with this process were identified by 13C‐DNA‐based stable isotope probing. We recommend the adoption and optimization of intercropping systems with residue return to reduce the shortcomings of continuous cropping and to increase the sustainability of crop production.</abstract><cop>HOBOKEN</cop><pub>Wiley</pub><doi>10.1111/1365-2664.13964</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-7356-5294</orcidid><orcidid>https://orcid.org/0000-0002-9863-8461</orcidid></addata></record>
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subjects Agricultural practices
Agricultural production
Arthrobacter
Azotobacter
Bacillus
Bacteria
Beans
Biodiversity & Conservation
Broad beans
Broccoli
Carbon sources
Continuous cropping
Corn
crop biodiversity
Crop diversification
Crop production
Crop residues
Crop yield
Crops
Deoxyribonucleic acid
DNA
Ecology
Environmental Sciences & Ecology
Exudates
Exudation
Gene expression
Intercropping
Interspecific
Life Sciences & Biomedicine
Microbial activity
Microorganisms
Monoculture
Nitrogen fixation
Nitrogenation
Optimization
Productivity
residue retention
Residues
Rhizosphere
rhizosphere facilitation
root exudates
Science & Technology
soil bacteria
stable isotope probing
Stable isotopes
Sustainability
Vegetables
title Nitrogen fixation and crop productivity enhancements co‐driven by intercrop root exudates and key rhizosphere bacteria
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