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Evolution of phosphate metabolism in Tibetan wild barley to adapt to aluminum stress

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Abstract

Aims

Aluminum (Al) toxicity in acid soil significantly reduces plant growth, agricultural productivity and ecosystem health. The Al-tolerant barley cultivars were reported to mainly rely on the Al-activated efflux of citrate from root apices, but the key mechanisms for Al tolerance may differ for wild relatives of barley adapted to acid soil.

Methods

Here, we investigated plant Al tolerance from evolutionary physiological, molecular, and ecological perspectives.

Results

Phylogenetic analysis of Al tolerance-associated gene families showed that most of these genes were conserved from streptophyte algae to angiosperms, indicating land plants have evolved gradually in adaption to Al-rich acid soil during plant terrestrialization. Vacuolar phosphate transporter SPX-major facility superfamily (SPX-MFS) and inorganic phosphate transporter 1 family (PHT1s) of streptophyte algae showed high genetic similarity to land plants. PHT1s exhibited a significant expand during the evolution from streptophyte algae to liverworts and then eudicots. Al-tolerant Tibetan wild barley accession, XZ29 showed high levels of P-containing glycolytic intermediates including Glu-6-P, Fru-6-P, 3-PGA, 2-PGA and PEP under Al stress. Some primary metabolites were evolutionarily conserved in liverwort, gymnosperm and three tested angiosperms. Furthermore, we found that Al-induced Pi efflux from root elongation zone to chelate rhizosphere Al3+, and immobilization of Al with P at the inner epidermal layer of root mature zone to reduce Al accumulation in the cortical layer in barley.

Conclusions

These results indicated that Tibetan wild barley has evolved unique P transport and metabolism for the adaptation to harsh conditions in eastern and southeastern Tibet where acid soils contain high P.

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Acknowledgements

This work is supported by National Natural Science Foundation of China (31771687) and China Agriculture Research System (CARS-05). S.C is supported by Kuayue Project in College of Agriculture and Biotechnology, Zhejiang University. Z.H.C is supported by the Australian Research Council (FT210100366, DE1401011143). We thank Prof. Dongfa Sun of Huazhong Agricultural University for providing Tibetan wild barley accessions. We thank Western Sydney University for the SIMS and Confocal Bio-imaging facility. We thank Lijuan Mao and Zhiwei Ge (985-Institute of Agrobiology and Environmental Sciences, Zhejiang University) and Linda Westmoreland, Dr Sumedha Dharmaratne, Dr Anya Sali, and David Randall (Western Sydney University) for technical assistance.

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Authors and Affiliations

  1. Agronomy Department, Key Laboratory of Crop Germplasm Resource of Zhejiang Province, Zhejiang University, Hangzhou, 310058, China

    Shengguan Cai, Yuqing Huang, Yang Liu, Liyuan Wu, Dezhi Wu & Guoping Zhang

  2. Shandong (Linyi) Institute of Modern Agriculture, Zhejiang University, Linyi, 276000, China

    Shengguan Cai & Guoping Zhang

  3. School of Science, Western Sydney University, Penrith, NSW, 2751, Australia

    Shengguan Cai, Yuqing Huang & Zhong-Hua Chen

  4. Office of the DVC R&D, Western Sydney University, 2751, Penrith, NSW, Australia

    Rong Liu

  5. CAMECA SAS, 29, quai des Gresillons, 92230, Gennevilliers Cedex, France

    Rong Liu

  6. CSIRO Plant Industry, Canberra, Australia

    Peter R. Ryan

  7. School of Land and Food, Tasmanian Institute for Agriculture, University of Tasmania, P.O. Box 46, 7249, Kings Meadows, TAS, Australia

    Meixue Zhou

  8. Hawkesbury Institute for the Environment, Western Sydney University, 2751, Penrith, NSW, Australia

    Zhong-Hua Chen

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  1. Shengguan Cai
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Contributions

S.C., G.Z. and Z.H.C. designed and supervised this study. S.C. and Y.H. performed bioinformatic analysis and metabolome analysis. Y.L. and L.W. conducted the physiological experiments. R.L. guided SIMS analysis. S.C., G.Z. and Z.H.C. wrote and revised the manuscript with inputs from D.W., P.R.R. and M.Z.

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Correspondence to Shengguan Cai or Zhong-Hua Chen.

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Evolution and regulation of cellular phosphorus transport and metabolism facilitates Tibetan wild barley to adapt to low pH and high P soils on the Tibetan plateau.

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Cai, S., Huang, Y., Liu, Y. et al. Evolution of phosphate metabolism in Tibetan wild barley to adapt to aluminum stress. Plant Soil (2022). https://doi.org/10.1007/s11104-022-05444-y

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