植物对磷缺乏的适应性塑造了根际细菌群落及酶活性的空间格局

doi:10.1016/j.jia.2025.08.017

Journal of Integrative Agriculture ›› 2026, Vol. 25 ›› Issue (6): 2569-2579.DOI: 10.1016/j.jia.2025.08.017

植物对磷缺乏的适应性塑造了根际细菌群落及酶活性的空间格局

收稿日期:2025-04-08 修回日期:2025-08-21 接受日期:2025-06-25 出版日期:2026-06-20 发布日期:2026-05-06

Adaptability of plants to phosphorus deficiency shapes bacterial community and spatial patterns of enzyme activities in rhizosphere

Xiaomin Ma^1*, Lisha Zeng^1*, Jialin Wang¹, Yan Zhou¹, Yongjian Zhang^{1, 2}, Junhui Chen^1#, Yakov Kuzyakov^{3, 4}

¹Key Laboratory of Soil Remediation and Quality Improvement of Zhejiang Province, Zhejiang A&F University, Hangzhou 311300, China
²College of Optical, Mechanical, and Electrical Engineering, Zhejiang A&F University, Hangzhou 311300, China
³Department of Soil Science of Temperate Ecosystems/Department of Agricultural Soil Science, University of Göttingen, Göttingen 37077, Germany
⁴Peoples Friendship University of Russia (RUDN University), Moscow 117198, Russia

Received:2025-04-08 Revised:2025-08-21 Accepted:2025-06-25 Online:2026-06-20 Published:2026-05-06
About author:Xiaomin Ma, Mobile: +86-15855363948, E-mail: maxiaomin@zafu.edu.cn; #Correspondence Junhui Chen, Mobile: +86-13906814189, E-mail: junhui@zafu.edu.cn * These authors contributed equally to this study.
Supported by:
This study was supported by the National Key R&D Program of China (2023YFD1901800), the National Natural Science Foundation of China (32371726, 42307421 and 42407449), and the Peoples Friendship University of Russia (RUDN University) Strategic Academic Leadership Program, Russia.

摘要/Abstract

摘要：

磷有效性（P）通过影响植物生长和微生物活性，进而调控根际碳（C）循环酶活性的空间分布。玉米（Zea mays L.）和窄叶羽扇豆（Lupinus angustifolius L.）对磷缺乏的适应与获取策略存在显著差异。然而，磷有效性如何影响这两种植物根际碳、磷水解酶活性的空间格局仍不明确。本研究通过酶谱法分析了玉米和羽扇豆根际碳、磷水解酶活性的空间格局，并将其与根际细菌群落结构相关联。结果表明，低磷条件下，玉米生长受到显著抑制，但根系分泌物较高磷条件增加了 2.2-9.6倍。低磷条件下，玉米根系分泌物的增加促进了 r策略细菌（如纤维杆菌门、黄单胞菌目）的增殖，但降低了 K 策略细菌（放线菌门、绿弯菌纲、α-变形菌纲）的相对丰度。玉米根际的酶活性及热点区域面积随 K 策略细菌丰度增加而升高，随 r 策略细菌丰度增加而降低。高磷条件下，玉米生长的较好，具有发达的根系，加上根际微生物群落结构向具有更高酶合成速率的 K 策略细菌转变，因此其碳、磷循环相关酶活性及热点区域比低磷条件高 15%-550%。羽扇豆对磷缺乏表现出更强的适应性，其释放的溶解有机碳（DOC）和有机酸比玉米高 2-19倍，因此其酶活性、热点区域面积及细菌群落组成未随有效磷含量发生显著变化。综上所述，植物对低磷环境的不同方式塑造了根际碳循环酶活性的空间分布和细菌群落结构。

Abstract:

Phosphorus (P) availability influences the spatial distribution of carbon (C)-cycling enzyme activities in the rhizosphere through its effects on plant growth and microbial activity. However, the influence of P availability on the spatial patterns of C and P hydrolase activities remains unclear in the rhizosphere of Maize (Zea mays L.) and narrow-leaf lupine (Lupinus angustifolius L.), which exhibit contrasting P deficiency adaptation and acquisition strategies. This study analyzed the spatial patterns of C and P hydrolase activities through zymography and correlated them with bacterial community structure in maize and lupine rhizospheres. Under P-deficient conditions, maize exhibited severe growth restriction while demonstrating a 2.2–9.6-fold increase in root exudation compared to P-sufficient conditions. The enhanced exudation under P deficiency promoted r-strategist bacterial proliferation (e.g., Ktedonobacteria and Xanthomonadales) while reducing K-strategist abundance (Actinobacteriota, Chloroflexia, and Alphaproteobacteria). Maize rhizosphere enzyme activities and hotspot areas demonstrated positive correlation with K-strategist abundance and negative correlation with r-strategist abundance. P-sufficient maize exhibited 15–550% higher C- and P-cycle-related enzyme activity and hotspot areas, attributed to its enhanced root system and predominance of K-strategists with superior enzyme synthesis capabilities. Lupine demonstrated superior P deficiency adaptation, producing 2–19 times more DOC and organic acids than maize. Consequently, lupine showed no significant alterations in enzyme activity, hotspot areas, or bacterial community composition in response to P availability. These findings demonstrate that plant-specific P deficiency adaptation mechanisms distinctly influence the spatial distribution of C-cycling enzyme activity and bacterial community structure in the rhizosphere.

Key words: phosphorus acquisition strategy , soil zymography , microbial strategies , root exudate , hotspot areas

Xiaomin Ma, Lisha Zeng, Jialin Wang, Yan Zhou, Yongjian Zhang, Junhui Chen, Yakov Kuzyakov. 植物对磷缺乏的适应性塑造了根际细菌群落及酶活性的空间格局[J]. Journal of Integrative Agriculture, 2026, 25(6): 2569-2579.

Xiaomin Ma, Lisha Zeng, Jialin Wang, Yan Zhou, Yongjian Zhang, Junhui Chen, Yakov Kuzyakov. Adaptability of plants to phosphorus deficiency shapes bacterial community and spatial patterns of enzyme activities in rhizosphere[J]. Journal of Integrative Agriculture, 2026, 25(6): 2569-2579.

参考文献

Bardgett R D, Mommer L, De Vries F T. 2014. Going underground: Root traits as drivers of ecosystem processes. Trends in Ecology & Evolution, 29, 692–699.

Bastian M, Heymann S, Jacomy M. 2009. Gephi: An open source software for exploring and manipulating networks visualization and exploration of large graphs. Proceedings of the International AAAI Conference on Web and Social Media, 3, 361–362.

Bian Q, Wang X, Bao X, Che Z, Sun B, Zhu L, Xie Z. 2022. Exogenous substrate quality determines the dominant keystone taxa linked to carbon mineralization: Evidence from a 30-year experiment. Soil Biology & Biochemistry, 169, 108683.

Chen Q, Zhao Q, Xie B, Lu X, Guo Q, Liu G, Zhou M, Tian J, Lu W, Chen K, Tian J, Liang C. 2024. Soybean (Glycine max) rhizosphere organic phosphorus recycling relies on acid phosphatase activity and specific phosphorus-mineralizing-related bacteria in phosphate deficient acidic soils. Journal of Integrative Agriculture, 23, 1685–1702.

Choreño-Parra E M, Treseder K K. 2024. Mycorrhizal fungi modify decomposition: A meta-analysis. New Phytologist, 242, 2763–2774.

Cong W, Suriyagoda L D B, Lambers H. 2020. Tightening the phosphorus cycle through phosphorus-efficient crop genotypes. Trends in Plant Science, 25, 967–975.

Edgar R C. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996–998.

Fang Y, Nazaries L, Singh B K, Singh B P. 2018. Microbial mechanisms of carbon priming effects revealed during the interaction of crop residue and nutrient inputs in contrasting soils. Global Change Biology, 24, 2775–2790.

Faust K, Raes J. 2012. Microbial interactions: From networks to models. Nature Reviews Microbiology, 10, 538–550.

Frey S D. 2019. Mycorrhizal fungi as mediators of soil organic matter dynamics. Annual Review of Ecology, Evolution, and Systematics, 50, 237–259.

Hammond J P, White P J. 2008. Sucrose transport in the phloem: Integrating root responses to phosphorus starvation. Journal of Experimental Botany, 59, 93–109.

Hao C, Dungait J A J, Wei, X, Ge T, Kuzyakov Y, Cui Z, Tian J, Zhang F. 2022. Maize root exudate composition alters rhizosphere bacterial community to control hotspots of hydrolase activity in response to nitrogen supply. Soil Biology & Biochemistry, 170, 108717.

Hinsinger P. 2001. Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: A review. Plant and Soil, 237, 173–195.

Hocking P J. 2001. Organic acids exuded from roots in phosphorus uptake and aluminum tolerance of plants in acid soils. Agronomy, 74, 63–97.

Jiang Z, Vancov T, Fang Y, Tang C, Zhang W, Xiao M, Song X, Zhou J, Ge T, Cai Y, Yu B, White J C, Li Y. 2025. Sustained superiority of biochar over straw for enhancing soil biological-phosphorus via the mediation of phoD-harboring bacteria in subtropical Moso bamboo forest. Forest Ecology and Management, 584, 122606.

Kuzyakov Y, Xu X. 2013. Competition between roots and microorganisms for nitrogen: Mechanisms and ecological relevance. New Phytologist, 198, 656–669.

Lambers H. 2022. Phosphorus acquisition and utilization in plants. Annual Review of Plant Biology, 73, 1–26.

Lambers H, Finnegan P M, Jost R, Plaxton W C, Shane M W, Stitt M. 2015. Phosphorus nutrition in Proteaceae and beyond. Nature Plants, 1, 1–9.

Leff J W, Jones S E, Prober S M, Barberán A, Borer E T, Firn J L, Harpole W S, Hobbie S E, Hofmockel K S, Knops J M H, McCulley R L, La Pierre K, Risch A C, Seabloom E W, Schütz M, Steenbock C, Stevens C J, Fierer N. 2015. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proceedings of the National Academy of Sciences of the United States of America, 112, 10967–10972.

Li Z, Duan X, Guo X, Gao W, Li Y, Zhou P, Zhu Q, O’Donnell A G, Dai K, Wu J. 2024. Microbial metabolic capacity regulates the accrual of mineral-associated organic carbon in subtropical paddy soils. Soil Biology & Biochemistry, 195, 109457.

Ling N, Wang T, Kuzyakov Y. 2022. Rhizosphere bacteriome structure and functions. Nature Communications, 13, 1–13.

Ma X, Geng Q, Zhang H, Bian C, Chen H Y H, Jiang D, Xu X. 2021a. Global negative effects of nutrient enrichment on arbuscular mycorrhizal fungi, plant diversity and ecosystem multifunctionality. New Phytologist, 229, 2957–2969.

Ma X, Li X, Ludewig U. 2021b. Arbuscular mycorrhizal colonization outcompetes root hairs in maize under low phosphorus availability. Annals of Botany, 127, 155–166.

Ma X, Liu Y, Shen W, Kuzyakov Y. 2021c. Phosphatase activity and acidification in lupine and maize rhizosphere depend on phosphorus availability and root properties: Coupling zymography with planar optodes. Applied Soil Ecology, 167, 104029.

Ma X, Liu Y, Zarebanadkouki M, Razavi B S, Blagodatskaya E, Kuzyakov Y. 2018. Spatiotemporal patterns of enzyme activities in the rhizosphere: Effects of plant growth and root morphology. Biology and Fertility of Soils, 54, 819–828.

Ma X, Mason-Jones K, Liu Y, Blagodatskaya E, Kuzyakov Y, Guber A, Dippold M A, Razavi B S. 2019. Coupling zymography with pH mapping reveals a shift in lupine phosphorus acquisition strategy driven by cluster roots. Soil Biology & Biochemistry, 135, 420–428.

Ma X, Zhou Z, Chen J, Xu H, Ma S, Dippold M A, Kuzyakov Y. 2023. Long-term nitrogen and phosphorus fertilization reveals that phosphorus limitation shapes the microbial community composition and functions in tropical montane forest soil. Science of the Total Environment, 854, 158709.

Ma X, Zhu B, Nie Y, Liu Y, Kuzyakov Y. 2021d. Root and mycorrhizal strategies for nutrient acquisition in forests under nitrogen deposition: A meta-analysis. Soil Biology & Biochemistry, 163, 108418.

Mau R L, Liu C M, Aziz M, Schwartz E, Dijkstra P, Marks J C, Price L B, Keim P, Hungate B A. 2015. Linking soil bacterial biodiversity and soil carbon stability. The ISME Journal, 9, 1477–1480.

Neumann G, Martinoia E. 2002. Cluster roots - An underground adaptation for survival in extreme environments. Trends in Plant Science, 7, 162–167.

Pang J, Bansal R, Zhao H, Bohuon E, Lambers H, Ryan M H, Ranathunge K, Siddique K H M. 2018. The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytologist, 219, 518–529.

Parihar M, Rakshit A, Meena V S, Gupta V K, Rana K, Choudhary M, Tiwari G, Mishra P K, Pattanayak A, Bisht J K, Jatav S S, Khati P, Jatav H S. 2020. The potential of arbuscular mycorrhizal fungi in C cycling: A review. Archives of Microbiology, 202, 1581–1596.

Philippot L, Raaijmakers J M, Lemanceau P, Van Der Putten W H. 2013. Going back to the roots: The microbial ecology of the rhizosphere. Nature Reviews Microbiology, 11, 789–799.

Postma J A, Dathe A, Lynch J P. 2014. The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability. Plant Physiology, 166, 590–602.

Roller B R K, Schmidt T M. 2015. The physiology and ecological implications of efficient growth. The ISME Journal, 9, 1481–1487.

Sasse J, Martinoia E, Northen T. 2018. Feed your friends: Do plant exudates shape the root microbiome? Trends in Plant Science, 23, 25–41.

Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett W S, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biology, 12, R60.

Shang W, Razavi B.S, Yao S, Hao C, Kuzyakov Y, Blagodatskaya E, Tian J. 2023. Contrasting mechanisms of nutrient mobilization in rhizosphere hotspots driven by straw and biochar amendment. Soil Biology & Biochemistry, 187, 109212.

Soong J L, Marañon-jimenez S, Cotrufo M F, Boeckx P, Bodé S, Guenet B, Peñuelas J, Richter A, Stahl C, Verbruggen E, Janssens I A. 2018. Soil microbial CNP and respiration responses to organic matter and nutrient additions : Evidence from a tropical soil incubation. Soil Biology & Biochemistry, 122, 141–149.

Trivedi P, Delgado-Baquerizo M, Trivedi C, Hu H, Anderson I C, Jeffries T C, Zhou J, Singh B K. 2016. Microbial regulation of the soil carbon cycle: Evidence from gene-enzyme relationships. The ISME Journal, 10, 2593–2604.

Trouvelot A, Kough J L, Gianinazzi-Pearson V. 1986. Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Pearson G, Gianinazzi S, eds., Physiological and Genetical Aspects of Mycorrhizae. Proceedings of the 1st European Symposiurn on Mycorrhizae. Institut Na tional de la Recherche Agronomiqu, Paris. pp. 217–221. (in French)

Vierheilig H, Coughlan A P, Wyss U, Piché Y. 1998. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology, 64, 5004–5007.

Walker T S, Bais H P, Grotewold E, Vivanco J M. 2003. Root exudation and rhizosphere biology Plant Physiology, 132, 44–51.

Wang C, Kuzyakov Y. 2024. Rhizosphere engineering for soil carbon sequestration. Trends in Plant Science, 29, 447–468.

Wang L, Li X, Mang M, Ludewig U, Shen J. 2021. Heterogeneous nutrient supply promotes maize growth and phosphorus acquisition : Additive and compensatory effects of lateral roots and root hairs. Annals of Botany, 128, 431–440.

Wang X, Zhang W, Liu Y, Jia Z, Li H, Yang Y, Wang D, He H, Zhang X. 2021. Identification of microbial strategies for labile substrate utilization at phylogenetic classification using a microcosm approach. Soil Biology & Biochemistry, 153, 107970.

Wen Z, Li H, Shen Q, Tang X, Xiong C, Li H, Pang J, Ryan M H, Lambers H, Shen J. 2019. Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytologist, 223, 882–895.

WRB (World Reference Base for Soil Resources). 2006. A Framework for International Classification, Correlation and Communication. Food and Agriculture Organization of the United Nations, Rome.

Zhang D, Zhang C, Tang X, Li H, Zhang F, Rengel Z, Whalley W R, Davies W J, Shen J. 2016. Increased soil phosphorus availability induced by faba bean root exudation stimulates root growth and phosphorus uptake in neighbouring maize. New Phytologist, 209, 823–831.

Zhang T, Liu Y, Ge S, Peng P, Tang H, Wang J. 2024. Sugarcane/soybean intercropping with reduced nitrogen addition enhances residue-derived labile soil organic carbon and microbial network complexity in the soil during straw decomposition. Journal of Integrative Agriculture, 23, 4216–4236.

Zhang X, Myrold D D, Shi L, Kuzyakov Y, Dai H, Thu Hoang D T, Dippold M A, Meng X, Song X, Li Z, Zhou J, Razavi B S. 2021. Resistance of microbial community and its functional sensitivity in the rhizosphere hotspots to drought. Soil Biology & Biochemistry, 161, 108360.

植物对磷缺乏的适应性塑造了根际细菌群落及酶活性的空间格局

Adaptability of plants to phosphorus deficiency shapes bacterial community and spatial patterns of enzyme activities in rhizosphere

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