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Phosphorus fertilization affects soybean rhizosphere phosphorus dynamics and the bacterial community in karst soils

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Abstract

Background

Despite the high phosphorus (P)-mobilizing capacity of legumes, little is known about the dynamics of the P fractions and bacterial communities in the rhizosphere of legumes in karst soils.

Methods

A field experiment was established to investigate P uptake, rhizosphere P fractions and bacterial community structure of soybean (Glycine max (L.) Merr.) in response to P fertilization (0 and 90 kg P ha−1) in karst soils.

Results

Significant rhizosphere acidification was observed during soybean cultivation. Phosphorus fertilization further decreased soil pH, HCl-Pi and residual P, but increased NaHCO3-Pi in the rhizosphere of soybean variety YC03–3, which was associated with the simultaneous increase in P uptake and biomass. In addition, the bacterial community composition was significantly altered by P fertilization through its effects on soil pH and Ca. Bacillales and Pseudomonadales were the primary taxa influencing P dynamics, especially in soils without P input. Nevertheless, P fertilization decreased the relative abundance of Bacillales and Pseudomonadales, probably due to the enhanced rhizosphere acidification and improved P status.

Conclusions

In karst soils, recalcitrant P can be depleted directly or transformed into more labile fractions by soybean rhizosphere acidification, even when P fertilizer is applied. As a consequence, P fertilization suppressed the growth of bacteria (Bacillales and Pseudomonadales) that contribute to P mobilization due to the reduced demands on these taxa to release P. Our findings highlight the importance of P fertilization in chemical P mobilization, which may consequently influence biological P turnover in the soybean rhizosphere.

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References

  • Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. P Natl Acad Sci USA 105:11512–11519

    Article  CAS  Google Scholar 

  • Allison VJ, Yermakov Z, Miller RM, Jastrow JD, Matamala R (2007) Using landscape and depth gradients to decouple the impact of correlated environmental variables on soil microbial community composition. Soil Biol Biochem 39:505–516

    Article  CAS  Google Scholar 

  • Chen CR, Condron LM, Davis MR, Sherlock RR (2000) Effects of afforestation on phosphorus dynamics and biological properties in a New Zealand grassland soil. Plant Soil 220:151–163

    Article  CAS  Google Scholar 

  • Chen X, Jiang N, Condron LM, Dunfield KE, Chen Z, Wang J, Chen L (2019) Impact of long-term phosphorus fertilizer inputs on bacterial phoD gene community in a maize field, Northeast China. Sci Total Environ 669:1011–1018

    Article  CAS  PubMed  Google Scholar 

  • Condron LM, Newman S (2011) Revisiting the fundamentals of phosphorus fractionation of sediments and soils. J Soils Sediments 11:830–840

    Article  CAS  Google Scholar 

  • Condron LM, Turner BL, Cade-Menun BJ (2005) Chemistry and dynamics of soil organic phosphorus. In: JT Sims, AN Sharpley (eds) phosphorus: agriculture and the environment. Soil science Society of America, crop science Society of America, and soil science Society of America, Madison, pp 87–121

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • FAO/ISRIC/ISSS (2014) World reference base for soil resources. FAO, Rome

    Google Scholar 

  • Gao P, Liu Y, Wang Y, Liu X, Wang Z, Ma LQ (2019) Spatial and temporal changes of P and Ca distribution and fractionation in soil and sediment in a karst farmland-wetland system. Chemosphere 220:644–650

    Article  CAS  PubMed  Google Scholar 

  • Guo F, Yost RS, Hue NV, Evensen CI, Silva JA (2000) Changes in phosphorus fractions in soils under intensive plant growth. Soil Sci Soc Am J 64:1681–1689

    Article  CAS  Google Scholar 

  • Hassan HM, Marschner P, McNeill A, Tang C (2012) Growth, P uptake in grain legumes and changes in rhizosphere soil P pools. Biol Fert Soils 48:151–159

    Article  CAS  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195

    Article  CAS  Google Scholar 

  • Hu Y, Xia Y, Sun Q, Liu K, Chen X, Ge T, Zhu B, Zhu Z, Zhang Z, Su Y (2018) Effects of long-term fertilization on phoD-harboring bacterial community in karst soils. Sci Total Environ 628-629:53–63

    Article  CAS  PubMed  Google Scholar 

  • Jarvie HP, Sharpley AN, Brahana V, Simmons T, Price A, Neal C, Lawlor AJ, Sleep D, Thacker S, Haggard BE (2014) Phosphorus retention and remobilization along hydrological pathways in karst terrain. Environ Sci Technol 48:4860–4868

    Article  CAS  PubMed  Google Scholar 

  • Jones JB, Case VW (1990) Sampling, handling, and analyzing plant tissue samples. In: RL Westerman (ed) soil testing and plant analysis. Soil science Society of America, crop science Society of America, and soil science Society of America, Madison

  • Kuo S (1996) Phosphorus. In: Sparks DL, Page AL, Helmke PA, Loeppert RH (eds) Methods of soil analysis part 3—chemical methods. Soil Science Society of America, American Society of Agronomy, Madison, WI, pp 389–427

    Google Scholar 

  • Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H, Shen J, Zhang F, Clairotte M, Drevon JJ, Le Cadre E, Hinsinger P (2008) Dynamics of phosphorus fractions in the rhizosphere of common bean (Phaseolus vulgaris L.) and durum wheat (Triticum turgidum durum L.) grown in monocropping and intercropping systems. Plant Soil 312:139–150

    Article  CAS  Google Scholar 

  • Lin Z (2016) Functional analysis of a root specific phosphate transporter, GmPT4, in soybean. Master thesis. South China Agricultural University, China (In Chinese)

  • Long X-E, Yao H, Wang J, Huang Y, Singh BK, Zhu Y-G (2015) Community structure and soil pH determine chemoautotrophic carbon dioxide fixation in drained paddy soils. Environ Sci Technol 49:7152–7160

    Article  CAS  PubMed  Google Scholar 

  • Long X-E, Yao H, Huang Y, Wei W, Zhu Y-G (2018) Phosphate levels influence the utilisation of rice rhizodeposition carbon and the phosphate-solubilising microbial community in a paddy soil. Soil Biol Biochem 118:103–114

    Article  CAS  Google Scholar 

  • Mander C, Wakelin S, Young S, Condron L, O’Callaghan M (2012) Incidence and diversity of phosphate-solubilising bacteria are linked to phosphorus status in grassland soils. Soil Biol Biochem 44:93–101

    Article  CAS  Google Scholar 

  • Mulvaney RL (1996) Nitrogen-inorganic forms. In: Sparks DL, Page AL, Helmke PA, Loeppert RH (eds) Methods of soil analysis part 3-chemical methods. Soil Science Society of America, American Society of Agronomy, Madison, WI, pp 1123–1184

    Google Scholar 

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action. Springer, Berlin Heidelberg, pp 215–243

    Chapter  Google Scholar 

  • Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2006) Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil 281:109–120

    Article  CAS  Google Scholar 

  • Ogut M, Er F, Kandemir N (2010) Phosphate solubilization potentials of soil Acinetobacter strains. Biol Fertil Soils 46:707–715

    Article  CAS  Google Scholar 

  • Olde Venterink H (2011) Legumes have a higher root phosphatase activity than other forbs, particularly under low inorganic P and N supply. Plant Soil 347:137–146

    Article  CAS  Google Scholar 

  • Peng W, Wu W, Peng J, Li J, Lin Y, Wang Y, Tian J, Sun L, Liang C, Liao H (2018) Characterization of the soybean GmALMT family genes and the function of GmALMT5 in response to phosphate starvation. J Integrative Plant Biol 60:216–231

    Article  CAS  Google Scholar 

  • Pistocchi C, Meszaros E, Tamburini F, Frossard E, Bunemann EK (2018) Biological processes dominate phosphorus dynamics under low phosphorus availability in organic horizons of temperate forest soils. Soil Biol Biochem 126:64–75

    Article  CAS  Google Scholar 

  • Ragot SA, Huguenin-Elie O, Kertesz MA, Frossard E, Bunemann EK (2016) Total and active microbial communities and phoD as affected by phosphate depletion and pH in soil. Plant Soil 408:15–30

    Article  CAS  Google Scholar 

  • Randall K, Brennan F, Clipson N, Creamer R, Griffiths B, Storey S, Doyle E (2019) Soil bacterial community structure and functional responses across a long-term mineral phosphorus (pi) fertilisation gradient differ in grazed and cut grasslands. Appl Soil Ecol 138:134–143

    Article  Google Scholar 

  • Richardson AE, Barea J-M, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    Article  CAS  Google Scholar 

  • Rose TJ, Hardiputra B, Rengel Z (2010) Wheat, canola and grain legume access to soil phosphorus fractions differs in soils with contrasting phosphorus dynamics. Plant Soil 326:159–170

    Article  CAS  Google Scholar 

  • Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    Article  PubMed  Google Scholar 

  • Santachiara G, Salvagiotti F, Rotundo JL (2019) Nutritional and environmental effects on biological nitrogen fixation in soybean: a meta-analysis. Field Crop Res 240:106–115

    Article  Google Scholar 

  • Sharpe RR, Boswell FC, Hargrove WL (1986) Phosphorus fertilization and tillage effect on dinitrogen fixation in soybeans. Plant Soil 96:31–44

    Article  CAS  Google Scholar 

  • Shen J, Rengel Z, Tang C, Zhang F (2003) Role of phosphorus nutrition in development of cluster roots and release of carboxylates in soil-grown Lupinus albus. Plant Soil 248:199–206

    Article  CAS  Google Scholar 

  • Shi Y, Ziadi N, Hamel C, Belanger G, Abdi D, Lajeunesse J, Lafond J, Lalande R, Shang J (2020) Soil microbial biomass, activity and community structure as affected by mineral phosphorus fertilization in grasslands. Appl Soil Ecol 146:1–11

    Article  Google Scholar 

  • Tan H, Barret M, Mooij MJ, Rice O, Morrissey JP, Dobson A, Griffiths B, O'Gara F (2013) Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol Fert Soils 49:661–672

    Article  CAS  Google Scholar 

  • Tang C, McLay CDA, Barton L (1997) A comparison of proton excretion of twelve pasture legumes grown in nutrient solution. Aust J Exp Agr 37:563–570

    Article  Google Scholar 

  • Tang C, Fang RY, Raphael C (1998) Factors affecting soil acidification under legumes. II. Effect of phosphorus supply. Aust J Agric Res 49:657–664

    Article  CAS  Google Scholar 

  • Tang C, Qiao YF, Han XZ, Zheng SJ (2007) Genotypic variation in phosphorus utilisation of soybean Glycine max (L.) Murr. Grown in various sparingly soluble P sources. Aust J Agric Res 58:443–451

    Article  CAS  Google Scholar 

  • Tang J, Tang X, Qin Y, He Q, Yi Y, Ji Z (2019) Karst rocky desertification progress: soil calcium as a possible driving force. Sci Total Environ 649:1250–1259

    Article  CAS  PubMed  Google Scholar 

  • Teng Z, Zhu Y, Li M, Whelan MJ (2018) Microbial community composition and activity controls phosphorus transformation in rhizosphere soils of the Yeyahu wetland in Beijing, China. Sci Total Environ 628-629:1266–1277

    Article  CAS  PubMed  Google Scholar 

  • Tian J, Boitt G, Black A, Wakelin S, Condron LM, Chen L (2017) Accumulation and distribution of phosphorus in the soil profile under fertilized grazed pasture. Agric Ecosyst Environ 239:228–235

    Article  CAS  Google Scholar 

  • Aguilar S. A, van Diest A (1981) Rock-phosphate mobilization induced by the alkaline uptake pattern of legumes utilizing symbiotically fixed nitrogen. Plant Soil 61: 27–42

  • Vu DT, Tang C, Armstrong RD (2008) Changes and availability of P fractions following 65 years of P application to a calcareous soil in a Mediterranean climate. Plant Soil 304:21–33

    Article  CAS  Google Scholar 

  • Wan W, Tan J, Wang Y, Qin Y, He H, Wu H, Zuo W, He D (2020) Responses of the rhizosphere bacterial community in acidic crop soil to pH: changes in diversity, composition, interaction, and function. Sci Total Environ 700:1–10

    Article  CAS  Google Scholar 

  • Wang H, Teng C, Li H, Sun X, Jiang C, Lou L, Yue C, Zhang Z (2018a) Microbial community shifts trigger loss of orthophosphate in wetland soils subjected to experimental warming. Plant Soil 424:351–365

    Article  CAS  Google Scholar 

  • Wang K, Zhang C, Chen H, Yue Y, Zhang W, Zhang M, Qi X, Fu Z (2019) Karst landscapes of China: patterns, ecosystem processes and services. Landsc Ecol 34:2743–2763

    Article  Google Scholar 

  • Wang Q, Jiang X, Guan D, Wei D, Zhao B, Ma M, Chen S, Li L, Cao F, Li J (2018b) Long-term fertilization changes bacterial diversity and bacterial communities in the maize rhizosphere of Chinese Mollisols. Appl Soil Ecol 125:88–96

    Article  Google Scholar 

  • Wang Y, Zhao X, Guo Z, Jia Z, Wang S, Ding K (2018c) Response of soil microbes to a reduction in phosphorus fertilizer in rice-wheat rotation paddy soils with varying soil P levels. Soil Till Res 181:127–135

    Article  Google Scholar 

  • Zhang W, Zhao J, Pan F, Li D, Chen H, Wang K (2015) Changes in nitrogen and phosphorus limitation during secondary succession in a karst region in Southwest China. Plant Soil 391:77–91

    Article  CAS  Google Scholar 

  • Zheng B-X, Zhang D-P, Wang Y, Hao X-L, Wadaan MAM, Hozzein WN, Penuelas J, Zhu Y-G, Yang X-R (2019) Responses to soil pH gradients of inorganic phosphate solubilizing bacteria community. Sci Rep 9:25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu X, Chen J, Tan C, Yang C, Tan C, Li Z, Chen D, Lou L (2019) Breeding of high-yield widespread new soybean variety Qiandou 12. Soybean Sci 38:330–332 (In Chinese)

    Google Scholar 

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Acknowledgements

This study was financially supported by the Integrated Demonstration of Key Techniques for the Industrial Development of Featured Crops in Rocky Desertification Areas of Yunnan–Guangxi–Guizhou Provinces (SMH2019-2021), the National Natural Science Foundation of China (41807084, 31601830), the Natural Science Foundation of Guangdong Province, China (2018A030310214) and the Science and Technology Project of Guangdong Province, China (2019B030301007). We thank Dr. Xiaodong Chen from Zhejiang Academy of Agricultural Sciences for reviewing the manuscript, we thank Baoxing Xie, Guoxuan Liu, Guangfen Peng and Panmin He for their assistance with soil sampling in 2019. Special thanks are also due to Mr. Dafang Song for his assistance with managing the field trial.

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Author notes

  1. Jihui Tian and Xing Lu contributed equally to this work.

Authors and Affiliations

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

    Jihui Tian, Xing Lu, Qianqian Chen, Xizhi Kuang, Cuiyue Liang, Lansheng Deng, Dongjiao Lin, Kunzheng Cai & Jiang Tian

  2. Guangdong Provincial Key Laboratory of Eco-Circular Agriculture, South China Agricultural University, Guangzhou, 510642, China

    Jihui Tian & Kunzheng Cai

  3. Guangdong Laboratory of Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, 510642, China

    Jihui Tian, Xing Lu, Cuiyue Liang, Lansheng Deng, Dongjiao Lin, Kunzheng Cai & Jiang Tian

  4. State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Root Biology Center, South China Agricultural University, Guangzhou, 510642, China

    Xing Lu, Cuiyue Liang & Jiang Tian

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  1. Jihui Tian
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Tian, J., Lu, X., Chen, Q. et al. Phosphorus fertilization affects soybean rhizosphere phosphorus dynamics and the bacterial community in karst soils. Plant Soil 475, 137–152 (2022). https://doi.org/10.1007/s11104-020-04662-6

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