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Journal of Integrative Agriculture  2026, Vol. 25 Issue (5): 2077-2092    DOI: 10.1016/j.jia.2025.08.015
Agro-ecosystem & Environment Advanced Online Publication | Current Issue | Archive | Adv Search |
Low-phosphorus stress induces GmSTOP1-3-mediated organic acid exudation to recruit phosphate-solubilizing bacteria for organic phosphorus mineralization in soybean rhizosphere

Qianqian Chen1, 2, 3, 5, Xing Lu1, 3, Guoxuan Liu1, 3, Tianqi Wang1, 3, Huiying Zhou1, 3, Jihui Tian4, Qing Yao5, Jinming He2, Jiang Tian1, 3#, Cuiyue Liang1, 3#

1 Root Biology Center, State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China

2 Guangdong Provincial Key Laboratory of Utilization and Conservation of Food and Medicinal Resources in Northern Region, School of Biology and Agriculture, Shaoguan University, Shaoguan 512005, China

3 Guangdong Engineering Technology Research Center of Low Carbon Agricultural Green Inputs, South China Agricultural University, Guangzhou 510642, China

4 College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China

5 Guangdong Province Key Laboratory of Microbial Signals and Disease Control/Guangdong Engineering Research Center for Litchi, College of Horticulture, South China Agricultural University, Guangzhou 510642, China

 Highlights 
● Expression of GmSTOP1-3 is up-regulated by phosphate starvation in soybean roots.
GmSTOP1-3 regulates root organic acid exudation and facilitates soil P utilization.
GmSTOP1-3-mediated organic acid exudation recruits phosphate-solubilizing bacteria.
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摘要  

植物根系分泌物在招募有益溶磷细菌(Phosphate-solubilizing bacteriaPSB)中发挥着关键作用。C2H2型锌指蛋白转录因子STOP1Sensitive to Proton Rhizotoxicity1)能够调控植物根系有机酸的分泌,但STOP1调控的根系有机酸分泌对根际微生物组成的影响尚不清楚。本研究发现在缺磷条件下,大豆根际土壤的有机酸含量更高,且富集了三种特定的PSB,包括Gammaproteobacteria_Incertae_SedisKF_JG30_C25Solirubrobacterales。这些PSB的相对丰度与大豆根际土壤草酸和柠檬酸浓度呈显著正相关。值得注意的是,即便在磷充足条件下,超量表达GmSTOP1-3也促进了大豆根系草酸和柠檬酸的分泌以及上述三种特定的PSB在大豆根际的富集。这些PSB的相对丰度与参与土壤磷循环的基因丰度呈显著正相关,尤其是编码酸性/碱性磷酸酶的关键基因。结合大豆根系GmSTOP1-3的表达受低磷胁迫上调这一现象,本研究的结果表明GmSTOP1-3介导的大豆根系草酸和柠檬酸分泌招募了特定的PSB,进而促进了其根际有机磷的矿化。本研究结果明确了GmSTOP1-3是酸性土壤中微生物组重塑和磷获取效率的关键调控因子。



Abstract  

Root exudates serve a vital function in recruiting beneficial phosphate-solubilizing bacteria (PSB), thereby enhancing plant adaptation to phosphorus (P) deficiency.  The C2H2-type zinc finger transcription factor STOP1 (sensitive to proton rhizotoxicity 1) regulates root organic acid (OA) exudation in plants.  However, the impact of STOP1-regulated root OA exudation on rhizosphere microbial composition remains unexplored.  This study revealed enhanced vegetation properties of soybean with higher P content in P-rich soils, while rhizosphere organic acid concentrations were elevated in P-poor soils.  The soybean genotype YC03-3 in P-deficient soils specifically recruited three PSB in acid soils: Gammaproteobacteria_Incertae_Sedis, KF_JG30_C25, and Solirubrobacterales.  These PSB abundances correlated positively with rhizosphere oxalate and citrate concentrations.  Under P-sufficient conditions, GmSTOP1-3 overexpression in soybean plants increased oxalate and citrate exudation compared to YCO3-3 wild type (WT), leading to preferential colonization by the same three PSB species naturally present in P-deficient WT rhizosphere.  The population dynamics of these PSB demonstrated strong positive correlations with the abundance of key genes involved in P cycling, particularly those governing acid/alkaline phosphatase activities and organic-P mineralization.  Given the phosphate starvation-enhanced expression pattern of GmSTOP1-3, the findings indicate that specific PSB recruitment for organic-P remobilization in soybean rhizosphere depends on GmSTOP1-3-mediated oxalate and citrate exudation in P-deficient acid soils.  This research establishes GmSTOP1-3 as a crucial regulator of rhizosphere microbiome assembly and P-acquisition efficiency in acid soils.

Keywords:  organic acid       phosphorus-cycling genes        phosphorus fractions        transcription factor        phosphatase activity  
Received: 01 April 2025   Accepted: 01 June 2025 Online: 21 August 2025  
Fund: 

This work was supported by National Key Research and Development Program of China (2021YFF1000500), the National Science and Technology Innovation 2030 Major Program, China (2023ZD04072), the Guangdong Basic and Applied Basic Research Foundation, China (2025A1515012159).  

About author:  Qianqian Chen, Mobile: +86-15915704184, E-mail: chenqq@scau.edu.cn; #Correspondence Jiang Tian, E-mail: jtian@scau.edu.cn; Cuiyue Liang, Mobile: +86-13570467247, E-mail: liangcy@scau.edu.cn

Cite this article: 

Qianqian Chen, Xing Lu, Guoxuan Liu, Tianqi Wang, Huiying Zhou, Jihui Tian, Qing Yao, Jinming He, Jiang Tian, Cuiyue Liang. 2026. Low-phosphorus stress induces GmSTOP1-3-mediated organic acid exudation to recruit phosphate-solubilizing bacteria for organic phosphorus mineralization in soybean rhizosphere. Journal of Integrative Agriculture, 25(5): 2077-2092.

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