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The class III peroxidase gene OsPrx24 is important for root Iron plaque formation and benefits phosphorus uptake in Rice plants under alternate wetting and drying irrigation

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Abstract

Aims

Alternate wetting and drying irrigation (AWD) benefits root iron plaque (IP) formation and nutrient uptake, but the underlying mechanism is unclear.

Methods

RNA-sequencing, histochemical staining, confocal laser microscopy, and transgenic techniques were used to evaluate the contributions of ionic-bonded cell-wall-located class III peroxidases (iPrxs) and hydrogen peroxide (H2O2) to IP formation in rice (Oryza sativa) under AWD.

Results

AWD significantly enhanced iPrx activity and expression of OsPrx24, a gene encoding iPrx, accompanied by elevated H2O2 accumulation and IP formation. Microscopic analysis indicated that OsPrx24 was mainly expressed in root epidermis, where H2O2 accumulation and IP precipitation also occurred. In an OsPrx24-overexpression line (OsPrx24-OX), the H2O2 concentration was 28.2% lower, and IP formation was 42.6% higher than in the wild type (WT). Treatment with both an iPrx inhibitor and an H2O2 scavenger reduced the IP content, but it was higher in OsPrx24-OX than in the WT under these treatment conditions. Phosphorus concentrations were higher and more IP was found in the roots of OsPrx24-OX than the WT.

Conclusion

The results imply that OsPrx24 participates in IP formation by regulating iPrx activity and H2O2 concentration under AWD. The results enhance our understanding of IP formation and nutrient uptake in rice.

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Abbreviations

AE:

antioxidant enzyme

AsA:

ascorbic acid

AT:

3-amino-1,2,4-triazole

AWD:

alternate wetting and drying irrigation

cPrx:

covalent-bound cell wall-located peroxidase

CW:

continuous waterlogging

DDC:

sodium dimethyldithiocarbamate

DM:

dried mass

DMTU:

dimethylthiourea

FM:

fresh mass

FOX:

ferrous-xylenol orange

H2O2 :

hydrogen peroxide

IP:

iron plaque

iPrx:

ionic-bound cell wall-located peroxidase

O2· :

superoxide anion

·OH:

hydroxyl radical

PBS:

phosphate buffer solution

Prx:

class III peroxidase

PCR:

polymerase chain reaction

ROC:

root oxidising capacity

ROL:

radical oxygen loss

ROS:

reactive oxygen species

Sal:

sodium salicylate

SHAM:

salicylhydroxamic acid

SOD:

superoxide dismutase

sPrx:

soluble peroxidase

WT:

wild-type

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Acknowledgements

We express our thanks to Mr. Xiangxiong Gao from the College of Horticulture, Fujian Agriculture and Forestry University (FAFU) and Ms. Haiyan Zhang from the College of Resources and Environment, FAFU for their kind assistance and guidance in section preparation and confocal laser microscope observation. We also acknowledge the National Natural Science Foundation of China, Ministry of Science and Technology, and Department of Science and Technology, Guangdong for providing funds.

Funding

This study was funded by the National Natural Science Foundation of China (Nos. 31372125, 31872169, 31761130073, and U1701236), the National Key Research and Development Program of China (Nos. 2017YFE0118100 and 2018YFD02003025), and Guangdong Provincial Key Laboratory of Eco-Circular Agriculture/Science and Technology Program of Guangdong (2019B030301007).

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Authors and Affiliations

Authors

Contributions

Xu-Jian Yang, Weifeng Xu and Hong Shen planned and designed the research and wrote the manuscript. Xu-Jian Yang, You-Qiang Fu and Shuo Ma performed the experiments. Xu-Jian Yang and Haihua Gan analysed data.

Corresponding authors

Correspondence to Weifeng Xu or Hong Shen.

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All authors declare that they have no conflicts of interest.

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Responsible Editor: Philip John White.

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Yang, XJ., Fu, YQ., Ma, S. et al. The class III peroxidase gene OsPrx24 is important for root Iron plaque formation and benefits phosphorus uptake in Rice plants under alternate wetting and drying irrigation. Plant Soil 448, 621–646 (2020). https://doi.org/10.1007/s11104-020-04455-x

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  • DOI: https://doi.org/10.1007/s11104-020-04455-x

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