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The adaptability of plants to phosphorus deficiency shapes the bacterial community and the spatial patterns of enzyme activities in the rhizosphere

Xiaomin Ma1*, Lisha Zeng1*, Jialin Wang1, Yan Zhou1, Yongjian Zhang1, 2, Junhui Chen1#, Yakov Kuzyakov3, 4

1 Key Laboratory of Soil Remediation and Quality Improvement of Zhejiang Province, Zhejiang A&F University, Hangzhou 311300, China

2 College of Optical, Mechanical, and Electrical Engineering, Zhejiang A&F University, Hangzhou 311300, China

3 Department of Soil Science of Temperate Ecosystems, Department of Agricultural Soil Science, University of Göttingen, Göttingen 37077, Germany

4 Peoples Friendship University of Russia (RUDN University), Moscow 117198, Russia

 Highlights 

• Lupine exhibited enhanced P deficiency adaptation through increased root exudation compared to maize

• Low P conditions inhibited maize growth but enhanced root exudation efficiency compared to high P conditions

• Enhanced root exudation promoted r-strategists while reducing K-strategists

• Maize demonstrated increased enzyme activities and hotspot areas correlating with K-strategist abundance

• Both plant and microbial factors influenced enzyme activity and hotspot area distribution

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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,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.

Keywords:  phosphorus acquisition strategy       soil zymography        microbial strategies        root exudate        hotspot areas  
Online: 21 August 2025  
Fund: 

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

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.

Cite this article: 

Xiaomin Ma, Lisha Zeng, Jialin Wang, Yan Zhou, Yongjian Zhang, Junhui Chen, Yakov Kuzyakov. 2025. The adaptability of plants to phosphorus deficiency shapes the bacterial community and the spatial patterns of enzyme activities in the rhizosphere. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.08.017

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