Polyphosphate-Induced Changes in Transcriptome and Root-Functional Traits Elucidate Enhanced Phosphorus Acquisition Mechanisms and Growth of Durum Wheat.

Khourchi, Said; Muhovski, Yordan; Blum, Adrien; Jauregui, Ivan; De Clerck, Caroline; Bargaz, Adnane; Delaplace, Pierre

doi:10.1111/pce.15629

Article (Scientific journals)

Polyphosphate-Induced Changes in Transcriptome and Root-Functional Traits Elucidate Enhanced Phosphorus Acquisition Mechanisms and Growth of Durum Wheat.

Khourchi, Said; Muhovski, Yordan; Blum, Adrien et al.

2025 • In Plant, Cell and Environment

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/333166

DOI
10.1111/pce.15629

PubMed
40394953

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Keywords :

gene expression; phosphatases; phosphorus; polyphosphates; rhizosphere processes; transcriptome; Physiology; Plant Science

Abstract :

[en] Phosphate (P) fertilization impacts many rhizosphere processes, driving plant P use efficiency. However, less is known about the induced molecular and physiological root-rhizosphere traits in responses to polyphosphates (PolyP), particularly root transcriptome and belowground functional traits responsible for P acquisition. The present study aims to investigate physiological and transcriptomic belowground mechanisms explaining the enhanced durum wheat P acquisition under PolyP (PolyB and PolyC) supply. Root molecular traits were differentially expressed in response to PolyP, where PolyB induced upregulation of OGDH, MDH, and ENO, PAP21 and downregulation of PFK, and LDH genes. The modulation of gene expression can presumably explain the PolyP-induced changes in rhizosphere (root, rhizosphere soil, soil solution) acidification (pH decreased from 8 to 6.3) and acid phosphatase activities, which were concomitant with enhanced rhizosphere soil P availability and shoot Pi content (145% and 36% compared to OrthoP, respectively) along with changes in morphological and transcriptomic root (particularly, the upregulation of AUX1 and ABA transporter genes) traits. These findings provide novel insights that P acquisition from polyphosphates involves the coordinated regulation of genes governing root-rhizosphere processes and root development, ultimately enhancing wheat P acquisition.

Disciplines :

Agriculture & agronomy

Author, co-author :

Khourchi, Said ; Université de Liège - ULiège > TERRA Research Centre ; Agrobiosciences Program, College of Agriculture and Environmental Sciences, Mohammed VI Polytechnic University (UM6P), Ben Guerir, Morocco ; African Sustainable Agriculture Research Institute, Mohammed VI Polytechnic University, Laâyoune, Morocco ; African Genome Center, Mohammed VI Polytechnic University, Ben Guerir, Morocco

Muhovski, Yordan ; Department of Life Sciences, Walloon Agricultural Research Centre, Gembloux, Belgium

Blum, Adrien ; Université de Liège - ULiège > Département GxABT > Plant Sciences

Jauregui, Ivan ; Université de Liège - ULiège > Département GxABT > Plant Sciences ; Department of Sciences, Public University of Navarre, Campus Arrosadía, Pamplona, Spain

De Clerck, Caroline ; Université de Liège - ULiège > Département GxABT > Plant Sciences

Bargaz, Adnane ; Agrobiosciences Program, College of Agriculture and Environmental Sciences, Mohammed VI Polytechnic University (UM6P), Ben Guerir, Morocco

Delaplace, Pierre ; Université de Liège - ULiège > Département GxABT > Plant Sciences

Language :

English

Title :

Polyphosphate-Induced Changes in Transcriptome and Root-Functional Traits Elucidate Enhanced Phosphorus Acquisition Mechanisms and Growth of Durum Wheat.

Publication date :

20 May 2025

Journal title :

Plant, Cell and Environment

ISSN :

0140-7791

eISSN :

1365-3040

Publisher :

John Wiley and Sons Inc, United States

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://onlinelibrary.wiley.com/doi/pdf/10.1111/pce.15629

Funding text :

The authors thank professors Benjamin Delory, Beno\u00EEt Mercatoris, Gilles Colinet, and the \u201CPlant Sciences\u201D Group staff for their invaluable help in setting up the experiments and conducting the analyses. Iv\u00E1n Jauregui expresses gratitude to the Navarra Government for the Andia contract he has benefiting from. This study was supported by OCP Group and Prayon within the framework of SoilPhorLife Program [SoilPhorLife N\u00B05] carried out jointly between University of Li\u00E8ge and Mohammed VI Polytechnic University.

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Bibliography

Aallam, Y., B. E. Maliki, D. Dhiba, et al. 2021. “Multiple Potential Plant Growth Promotion Activities of Endemic Streptomyces Spp. From Moroccan Sugar Beet Fields With Their Inhibitory Activities Against Fusarium Spp.” Microorganisms 9: 1429.
Alonso-Crespo, I. M., E. W. A. Weidlich, V. M. Temperton, and B. M. Delory. 2023. “Assembly History Modulates Vertical Root Distribution in a Grassland Experiment.” Oikos 1: e08886.
Balliu, A., and G. Sallaku. 2017. “Exogenous Auxin Improves Root Morphology and Restores Growth of Grafted Cucumber Seedlings.” Horticultural Science 44: 82–90.
Bargaz, A., G. L. Noyce, R. Fulthorpe, et al. 2017. “Species Interactions Enhance Root Allocation, Microbial Diversity and P Acquisition in Intercropped Wheat and Soybean Under P De Fi Ciency.” Applied Soil Ecology 120: 179–188.
Benmrid, B., A. Bargaz, H. Oukfi, et al. 2024. “Species Interactions and Bacterial Inoculation Enhance Plant Growth and Shape Rhizosphere Bacterial Community Structure in Faba Bean – Wheat Intercropping Under Water and P Limitations.” Environmental and Experimental Botany 225: 105858.
Benmrid, B., C. Ghoulam, Y. Zeroual, L. Kouisni, and A. Bargaz. 2023. “Bioinoculants as a Means of Increasing Crop Tolerance to Drought and Phosphorus Deficiency in Legume-Cereal Intercropping Systems.” Communications Biology 2023 6:1 6: 1016.
Bhadouria, J., A. P. Singh, P. Mehra, et al. 2017. “Identification of Purple Acid Phosphatases in Chickpea and Potential Roles of CaPAP7 in Seed Phytate Accumulation.” Scientific Reports 2017 7:1 7: 11012.
Bourak, K., A. R. Sare, A. Allaoui, M. H. Jijakli, and S. Massart. 2023. “Impact of Two Phosphorus Fertilizer Formulations on Wheat Physiology, Rhizosphere, and Rhizoplane Microbiota.” International Journal of Molecular Sciences 24: 9879.
Chen, L., L. Yang, Z. Lin, and N. Tang. 2013. “Roles of Organic Acid Metabolism in Plant Tolerance to Phosphorus-Deficiency.” Progress in Botany 74: 213–237.
Chtouki, M., F. Laaziz, R. Naciri, S. Garré, F. Nguyen, and A. Oukarroum. 2022. “Interactive Effect of Soil Moisture Content and Phosphorus Fertilizer Form on Chickpea Growth, Photosynthesis, and Nutrient Uptake.” Scientific Reports 2022 12:1 12: 6671.
Chtouki, M., R. Naciri, S. Garré, F. Nguyen, and A. Oukarroum. 2021. “Chickpea Plant Responses to Polyphosphate Fertiliser Forms and Drip Fertigation Frequencies: Effect on Photosynthetic Performance and Phenotypic Traits.” Functional Plant Biology 49: 505–516.
Condori-Apfata, J. A., W. Batista-Silva, D. B. Medeiros, et al. 2021. “Downregulation of the E2 Subunit of 2-Oxoglutarate Dehydrogenase Modulates Plant Growth by Impacting Carbon–Nitrogen Metabolism in Arabidopsis thaliana.” Plant and Cell Physiology 62: 798–814.
Darch, T., M. S. A. Blackwell, D. Chadwick, P. M. Haygarth, J. M. B. Hawkins, and B. L. Turner. 2016. “Assessment of Bioavailable Organic Phosphorus in Tropical Forest Soils by Organic Acid Extraction and Phosphatase Hydrolysis.” Geoderma 284: 93–102.
Deng, S., L. Lu, J. Li, et al. 2020. “Purple Acid Phosphatase 10c Encodes a Major Acid Phosphatase That Regulates Plant Growth Under Phosphate-Deficient Conditions in Rice.” Journal of Experimental Botany 71: 4321–4332.
Dick, R. P. 1985. Hydrolysis and Availability to Plants of Polyphosphates Added to Soils. Iowa State University.
Dick, R. P., and M. A. Tabatabai. 1986. “Hydrolysis of Polyphosphates in Soils.” Soil Science 142: 132–140.
Ding, Y., P. Kalo, C. Yendrek, et al. 2008. “Abscisic Acid Coordinates Nod Factor and Cytokinin Signaling During the Regulation of Nodulation in Medicago truncatula.” Plant Cell 20: 2681–2695.
Dionisio, G., C. K. Madsen, P. B. Holm, et al. 2011. “Cloning and Characterization of Purple Acid Phosphatase Phytases From Wheat, Barley, Maize, and Rice.” Plant Physiology 156: 1087–1100.
El-Mejjaouy, Y., M. Lahrir, R. Naciri, et al. 2022. “How Far Can Chlorophyll a Fluorescence Detect Phosphorus Status In Wheat Leaves (Triticum durum L.).” Environmental and Experimental Botany 194: 104762.
Gao, Y., X. Wang, J. A. Shah, and G. Chu. 2020. “Polyphosphate Fertilizers Increased Maize (Zea mays L.) P, Fe, Zn, and Mn Uptake by Decreasing P Fixation and Mobilizing Microelements in Calcareous Soil.” Journal of Soils and Sediments 20: 1–11.
Giri, J., R. Bhosale, G. Huang, et al. 2018. “Rice Auxin Influx Carrier OsAUX1 Facilitates Root Hair Elongation in Response to Low External Phosphate.” Nature Communications 2018 9:1 9: 1–7.
Gruber, B. D., R. F. H. Giehl, S. Friedel, and N. von Wirén. 2013. “Plasticity of the Arabidopsis Root System under Nutrient Deficiencies.” Plant Physiology 163: 161–179.
Guo, Q., S. Zhu, T. Lai, et al. 2025. “A Phosphate-Starvation Enhanced Purple Acid Phosphatase, GmPAP23 Mediates Intracellular Phosphorus Recycling and Yield in Soybean.” Plant, Cell & Environment, ahead of print, January 22, 2025. https://doi.org/10.1111/pce.15400.
Hernández, G., M. Ramírez, O. Valdés-López, et al. 2007. “Phosphorus Stress in Common Bean: Root Transcript and Metabolic Responses.” Plant Physiology 144: 752–767.
Hou, L., D. Zhang, Q. Wu, X. Gao, and J. Wang. 2025. “Analysis and Profiling of the Purple Acid Phosphatase Gene Family in Wheat (Triticum aestivum L.).” Protoplasma 262: 73–86.
Huang, R., B. Wan, M. Hultz, J. M. Diaz, and Y. Tang. 2018. “Phosphatase-Mediated Hydrolysis of Linear Polyphosphates.” Environmental Science & Technology 52: 1183–1190.
Janati, W., B. Benmrid, W. Elhaissoufi, Y. Zeroual, J. Nasielski, and A. Bargaz. 2021. “Will Phosphate Bio-Solubilization Stimulate Biological Nitrogen Fixation in Grain Legumes?” Frontiers in Agronomy 3: 637196.
Jensen, C. N. G., J. K. Y. Pang, C. M. Hahn, et al. 2024. “Differential Influence of Bacillus Subtilis Strains on Arabidopsis Root Architecture Through Common and Distinct Plant Hormonal Pathways.” Plant Science 339: 111936.
Kaida, R., Y. Satoh, V. Bulone, et al. 2009. “Activation of β-Glucan Synthases by Wall-Bound Purple Acid Phosphatase in Tobacco Cells.” Plant Physiology 150: 1822–1830.
Khourchi, S., P. Delaplace, and A. Bargaz. 2023a. “Polyphosphate Fertilizer Use Efficiency Strongly Relies on Soil Physicochemical Properties and Root-Microbial Activities.” Geoderma 429: 116281.
Khourchi, S., W. Elhaissoufi, A. Ibnyasser, et al. 2023b. “Integrated Use of Polyphosphate and P-Solubilizing Bacteria Enhanced P Use Efficiency and Growth Performance of Durum Wheat.” Frontiers in Microbiology 14: 1211397.
Khourchi, S., W. Elhaissoufi, M. Loum, et al. 2022a. “Phosphate Solubilizing Bacteria Can Significantly Contribute to Enhance P Availability From Polyphosphates and Their Use Efficiency in Wheat.” Microbiological Research 262: 127094.
Khourchi, S., A. Oukarroum, A. Tika, P. Delaplace, and A. Bargaz. 2022b. “Polyphosphate Application Influences Morpho-Physiological Root Traits Involved in P Acquisition and Durum Wheat Growth Performance.” BMC Plant Biology 22: 1–15.
Kim, D., B. Langmead, and S. L. Salzberg. 2015. “HISAT: A Fast Spliced Aligner With Low Memory Requirements.” Nature Methods 12: 357–360.
Laskowski, M., V. A. Grieneisen, H. Hofhuis, et al. 2008. “Root System Architecture From Coupling Cell Shape to Auxin Transport.” PLoS Biology 6: e307.
Li, C., S. Gui, T. Yang, T. Walk, X. Wang, and H. Liao. 2012. “Identification of Soybean Purple Acid Phosphatase Genes and Their Expression Responses to Phosphorus Availability and Symbiosis.” Annals of Botany 109: 275–285.
Li, C., C. Li, H. Zhang, H. Liao, and X. Wang. 2017. “The Purple Acid Phosphatase GmPAP21 Enhances Internal Phosphorus Utilization and Possibly Plays a Role in Symbiosis With Rhizobia in Soybean.” Physiologia Plantarum 159: 215–227.
Li, M., J. Zhou, Q. Liu, et al. 2023. “Dynamic Variation of Nutrient Absorption, Metabolomic and Transcriptomic Indexes of Soybean (Glycine max) Seedlings Under Phosphorus Deficiency.” AoB Plants 15: 1–12.
Liang, C., J. Tian, H. M. Lam, B. L. Lim, X. Yan, and H. Liao. 2010. “Biochemical and Molecular Characterization of PvPAP3, a Novel Purple Acid Phosphatase Isolated From Common Bean Enhancing Extracellular ATP Utilization.” Plant Physiology 152: 854–865.
López-Bucio, J., A. Cruz-Ramı́rez, and L. Herrera-Estrella. 2003. “The Role of Nutrient Availability in Regulating Root Architecture.” Current Opinion in Plant Biology 6: 280–287.
Loudari, A., A. Mayane, R. Naciri, Y. Zeroual, G. Colinet, and A. Oukarroum. 2022. “Root Morphological and Anatomical Responses to Increasing Phosphorus Concentration of Wheat Plants Grown Under Salinity.” Plant Stress 6: 100121.
Lu, L., W. Qiu, W. Gao, S. D. Tyerman, H. Shou, and C. Wang. 2016. “OsPAP10c, a Novel Secreted Acid Phosphatase in Rice, Plays an Important Role in the Utilization of External Organic Phosphorus.” Plant, Cell & Environment 39: 2247–2259.
Maccaferri, M., N. S. Harris, S. O. Twardziok, et al. 2019. “Durum Wheat Genome Highlights Past Domestication Signatures and Future Improvement Targets.” Nature Genetics 51: 885–895.
Martin, J. A., and Z. Wang. 2011. “Next-Generation Transcriptome Assembly.” Nature Reviews Genetics 12: 671–682.
McBeath, T. M., E. Lombi, M. J. McLaughlin, and E. K. Bünemann. 2007. “Polyphosphate-Fertilizer Solution Stability With Time, Temperature, and pH.” Journal of Plant Nutrition and Soil Science 170: 387–391.
Mehra, P., B. K. Pandey, and J. Giri. 2017. “Improvement in Phosphate Acquisition and Utilization by a Secretory Purple Acid Phosphatase (OsPAP21b) in Rice.” Plant Biotechnology Journal 15: 1054–1067.
Miao, J., J. Sun, D. Liu, et al. 2009. “Characterization of the Promoter of Phosphate Transporter TaPHT1.2 Differentially Expressed in Wheat Varieties.” Journal of Genetics and Genomics 36: 455–466.
Nilsson, L., R. Müller, and T. H. Nielsen. 2010. “Dissecting the Plant Transcriptome and the Regulatory Responses to Phosphate Deprivation.” Physiologia Plantarum 139: 129–143.
Plaxton, W. C., and H. T. Tran. 2011. “Metabolic Adaptations of Phosphate-Starved Plants.” Plant Physiology 156: 1006–1015.
Roussis, A., E. Flemetakis, M. Dimou, et al. 2003. “Nodulin PvNOD33, a Putative Phosphatase Whose Expression Is Induced During Phaseolus vulgaris Nodule Development.” Plant Physiology and Biochemistry 41: 719–725.
Seeberg-Elverfeldt, J., M. Schlüter, T. Feseker, and M. Kölling. 2005. “Rhizon Sampling of Porewaters Near the Sediment-Water Interface of Aquatic Systems.” Limnology and Oceanography: Methods 3: 361–371.
Seethepalli, A., K. Dhakal, M. Griffiths, H. Guo, G. T. Freschet, and L. M. York. 2021. “Rhizovision Explorer: Open-Source Software for Root Image Analysis and Measurement Standardization.” AoB Plants 13: plab056.
Severin, A. J., J. L. Woody, Y. T. Bolon, et al. 2010. “RNA-Seq Atlas of Glycine max: A Guide to the Soybean Transcriptome.” BMC Plant Biology 10: 160.
Shen, J., C. Li, G. Mi, et al. 2013. “Maximizing Root/Rhizosphere Efficiency to Improve Crop Productivity and Nutrient Use Efficiency in Intensive Agriculture of China.” Journal of Experimental Botany 64: 1181–1192.
Smith, A. G., E. Han, J. Petersen, et al. 2022. “Rootpainter: Deep Learning Segmentation of Biological Images With Corrective Annotation.” New Phytologist 236: 774–791.
Sun, Y., C. Mu, and X. Liu. 2018. “Key Factors Identified by Proteomic Analysis in Maize (Zea mays L.) Seedlings' Response to Long-Term Exposure to Different Phosphate Levels.” Proteome Science 16: 19.
Tiessen, H. 2008. “Phosphorus in the Global Environment.” In The Ecophysiology of Plant-Phosphorus Interactions (7, 1. Springer.
Tran, H. T., W. Qian, B. A. Hurley, Y. M. She, D. Wang, and W. C. Plaxton. 2010. “Biochemical and Molecular Characterization of AtPAP12 and AtPAP26: The Predominant Purple Acid Phosphatase Isozymes Secreted by Phosphate-Starved Arabidopsis thaliana.” Plant, Cell & Environment 33: 1789–1803.
Wan, B., R. Huang, J. M. Diaz, and Y. Tang. 2019. “Polyphosphate Adsorption and Hydrolysis on Aluminum Oxides.” Environmental Science & Technology 53: 9542–9552.
Wang, X., Y. Gao, B. Hu, and G. Chu. 2019. “Comparison of the Hydrolysis Characteristics of Three Polyphosphates and Their Effects on Soil Phosphorus and Micronutrient Availability.” Soil Use and Management 35: 664–674.
Wu, P., L. Ma, X. Hou, et al. 2003. “Phosphate Starvation Triggers Distinct Alterations of Genome Expression in Arabidopsis Roots and Leaves.” Plant Physiology 132: 1260–1271.
Zhang, F., J. Shen, J. Zhang, Y. Zuo, L. Li, and X. Chen. 2010. “Rhizosphere Processes and Management for Improving Nutrient Use Efficiency and Crop Productivity: Implications for China.” Advances in Agronomy 107: 1–32.