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Expression levels of genes involved in metal homeostasis, physiological adaptation, and growth characteristics of rice (Oryza sativa L.) genotypes under Fe and/or Al toxicity

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Abstract

Acid sulphate soil contains high amounts of iron (Fe) and aluminum (Al), and their contamination has been reported as major problems, especially in rainfed and irrigated lowland paddy fields. Rice is sensitive to Fe and Al grown in acid soil (pH < 5.5), leading to growth inhibition and grain yield loss. The objective of this study was to evaluate Fe and/or Al uptake, translocation, physiological adaptation, metal toxicity, and growth inhibition in rice genotypes grown in acid soil. Fe and Al in the root tissues of all rice genotypes were enriched depending on the exogenous application of either Fe or Al in the soil solution, leading to root growth inhibition, especially in the KDML105 genotype. Expression level of OsYSL1 in KDML105 was increased in relation to metal uptake into root tissues, whereas OsVIT2 was downregulated, leading to Fe (50.3 mg g−1 DW or 13.1 folds over the control) and Al (4.8 mg g−1 DW or 2.2 folds over the control) translocation to leaf tissues. Consequently, leaf greenness (SPAD), net photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (E) in the leaf tissues of genotype KDML105 under Fe + Al toxicity significantly declined by 28.4%, 35.3%, 55.6%, and 51.6% over the control, respectively. In Azucena (AZU; Fe/Al tolerant), there was a rapid uptake of Fe and Al by OsYSL1 expression in the root tissues, but a limited secretion into vacuole organelles by OsVIT2, leading to a maintenance of low level of toxicity driven by an enhanced accumulation of glutathione together with downregulation of OsGR expression level. In addition, Fe and Al restrictions in the root tissues of genotype RD35 were evident; therefore, crop stress index (CSI) of Fe + Al–treated plants was the maximum, leading to an inhibition of gs (53.6% over the control) and E (49.0% over the control). Consequently, free proline, total phenolic compounds, and ascorbic acid in the leaf tissues of rice under Fe + Al toxicity significantly increased by 3.2, 1.2, and 1.5 folds over the control, respectively, indicating their functions in non-enzymatic antioxidant defense. Moreover, physiological parameters including leaf temperature (Tleaf) increment, high level of CSI (>0.6), SPAD reduction, photon yield of PSII (ΦPSII) diminution, Pn, gs, and E inhibition in rice genotype IR64 (Fe/Al-sensitive) under Fe + Al treatment were clearly demonstrated as good indicators of metal-induced toxicity. Our results on Fe- and/or Al-tolerant screening to find out the candidate genotypes will contribute to present screening and breeding efforts, which in turn help increase rice production in the Fe/Al-contaminated acid soil under lowland conditions.

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Acknowledgements

The authors sincerely thank the National Science and Technology Development Agency (NSTDA), Thailand, for funding support (Grant Number P-18-51456).

Funding

This work was supported by the National Science and Technology Development Agency (NSTDA), Thailand (Grant Number P-18-51456).

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Authors and Affiliations

  1. National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), 113 Thailand Science Park, Phahonyothin Road, Khlong Nueng, Khlong Luang, Pathum Thani, 12120, Thailand

    Rujira Tisarum, Sayamon Sithtisarn, Thapanee Sampumphuang, Thanyaporn Sotesaritkul & Suriyan Cha-um

  2. Department of Biology, Faculty of Science, Burapha University, Saen Suk, Chon Buri, 20131, Thailand

    Wasinee Pongprayoon

  3. Agricultural Systems and Engineering, Department of Food, Agriculture and Bioresources, School of Environment, Resources and Development, Asian Institute of Technology, Khlong Luang, Pathum Thani, 12120, Thailand

    Avishek Datta

  4. Department of Environment Studies, Faculty of Science, Panjab University, Chandigarh, 160014, India

    Harminder Pal Singh

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Suriyan Cha-um: project leader, experimental layout, manuscript preparation, and edited version; Wasinee Pongprayoon: plant material preparation, data collection and analysis; Rujira Tisarum and Sayamon Sithtisarn: mRNA expression level and physiological data collection and analysis; Thapanee Sampumphuang and Thanyaporn Sotesaritkul: free proline, non-enzymatic assay and Al and Fe content analysis using ICP-OES and data analysis, measuring of morphological and overall growth characteristics; Harminder Pal Singh and Avishek Datta: manuscript editing, data analysis, and English language proofing.

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Tisarum, R., Pongprayoon, W., Sithtisarn, S. et al. Expression levels of genes involved in metal homeostasis, physiological adaptation, and growth characteristics of rice (Oryza sativa L.) genotypes under Fe and/or Al toxicity. Protoplasma 259, 1013–1028 (2022). https://doi.org/10.1007/s00709-021-01719-w

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