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Phosphorus solubilizing Bacillus altitudinis WR10 alleviates wheat phosphorus deficiency via remodeling root system architecture, enhancing phosphorus availability, and activating the ASA-GSH cycle

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Abstract

Background and Aims

Phosphorus (P) deficiency is present in 70% of the world's arable land, and severely affects crop growth and productivity. In this study, the ameliorative effects of P-solubilizing Bacillus altitudinis WR10 on P deficiency in wheat were investigated and the underlying mechanisms were explored.

Methods

Wheat was grown in half-strength Hoagland solution with KH2PO4 or Ca3(PO4)2 with or without WR10 inoculation for 14 days. Wheat biomass, root system architecture (RSA), and tissue P content were determined to evaluate the potential for alleviating P deficiency. To elucidate the underlying mechanisms, the ability of WR10 to produce organic acids (OAs), and its effects on root exudates and the ascorbic acid-glutathione (ASA-GSH) cycle in wheat were investigated.

Results

WR10 significantly increased plant biomass and tissue P content, decreased the root/shoot ratio, and remodeled the RSA, predominantly by augmenting root diameter in P-deficient wheat. Under P deficiency, WR10 produced up to 72 OAs, including palmitic, fumaric, methylmalonic, elaidic, benzoic, and nonanoic acids, decreased pH of the culture solution, and increased soluble P content. Our split-root experiment and non-targeted metabolomics revealed that WR10 inoculation reprogrammed root exudated in P-deficient plants, which enhanced the contents of ( −)-threo-isodihomocitric, (R)-2-ethylmalic, 4Z,7Z,10Z,13Z-hexadecatetraenoic, and colnelenic acids. In addition, WR10 significantly upregulated APX, MDHAR, DHAR, GR, and GS gene expression levels and increased the ASA and GSH contents involved in the ASA-GSH cycle, thereby decreasing H2O2 levels.

Conclusion

B. altitudinis WR10 alleviates P deficiency in wheat by remodeling the RSA, improving P availability, and activating the ASA-GSH cycle.

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Data Availability

The non-targeted metabolomics dataset presented in this study has been submitted to MetaboLights database with an accession number: MTBLS8247. The targeted metabolomics data in this study can be found in Supplementary Materials.

Abbreviations

PSB:

Phosphorus solubilizing bacteria

CFU:

Colony forming unit

TRL:

Total root length,

RSFA:

Root surface area

RV:

Root volume

RD:

Root diameter

ASA:

Ascorbic acid

GSH:

Glutathione

H2O2 :

Hydrogen peroxide

APX:

Ascorbate peroxidase

MDHAR:

Monodehydroascorbate reductase

DHAR:

Dehydroascorbate reductase

GR:

Glutathione reductase

GS:

GSH synthetase

OAs:

Organic acids

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 32071478), and the Henan Provincial Department of Science and Technology (No. 222102320365).

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Authors and Affiliations

  1. College of Life Sciences and Agronomy, Zhoukou Normal University, Zhoukou, 466001, China

    Zonghao Yue, Yongchuang Liu, Xiaoman Chen, Chunhong Hu, Manman Zheng, Le He & Keshi Ma

  2. Henan Key Laboratory of Plant Molecular Breeding and Bioreactor, Zhoukou, 466001, China

    Can Chen & Ju Zhang

  3. School of Mechanical and Electrical Engineering, Zhoukou Normal University, Zhoukou, 466001, China

    Yanjuan Chen

  4. College of Biological Engineering, Henan University of Technology, Zhengzhou, 450001, China

    Zhongke Sun

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  1. Zonghao Yue
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  2. Can Chen
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  3. Yongchuang Liu
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  4. Xiaoman Chen
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  10. Keshi Ma
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Contributions

Yue Z, Ma K, and Sun Z conceived the experiments. Yue Z, Chen C, Liu Y, Chen X, and Chen Y conducted the experimental work. Hu C, Zheng M, Zhang J, He L and Ma K analyzed the data. Yue Z prepared the draft manuscript. Ma K provided wheat seeds. Sun Z provided WR10 and edited the final manuscript.

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Correspondence to Keshi Ma or Zhongke Sun.

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Yue, Z., Chen, C., Liu, Y. et al. Phosphorus solubilizing Bacillus altitudinis WR10 alleviates wheat phosphorus deficiency via remodeling root system architecture, enhancing phosphorus availability, and activating the ASA-GSH cycle. Plant Soil 492, 367–379 (2023). https://doi.org/10.1007/s11104-023-06180-7

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