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Cited by 218Plant Stress Responses and ToleranceAluminum toxicity and tolerance in plants and animalsRice Cultivation and Yield Improvement

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Root Damage under Alkaline Stress Is Associated with Reactive Oxygen Species Accumulation in Rice (Oryza sativa L.)

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Zhang, Hui, Liu, Xiao-Long, Zhang, Rui-Xue, Yuan, Hai-Yan, Wang, Ming-Ming, Yang, Hao-Yu, Ma, Hong-Yuan, Liu, Duo, Jiang, Chang-Jie, Liang, Zheng-Wei·2017·Frontiers in Plant Science
DOI 10.3389/fpls.2017.01580PMC PMC5596797
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Abstract

Alkaline stress (high pH) severely damages root cells, and consequently, inhibits rice (Oryza sativa L.) seedling growth. In this study, we demonstrate the accumulation of reactive oxygen species (ROS) in root cells under alkaline stress. Seedlings of two rice cultivars with different alkaline tolerances, ‘Dongdao-4’ (moderately alkaline-tolerant) and ‘Jiudao-51’ (alkaline-sensitive), were subjected to alkaline stress simulated by 15 mM sodium carbonate (Na2CO3). Alkaline stress greatly reduced seedling survival rate, shoot and root growth, and root vigor. Moreover, severe root cell damage was observed under alkaline stress, as shown by increased membrane injury, malondialdehyde accumulation, and Evan’s Blue staining. The expression of the cell death-related genes OsKOD1, OsHsr203j, OsCP1, and OsNAC4 was consistently upregulated, while that of a cell death-suppressor gene, OsBI1, was downregulated. Analysis of the ROS contents revealed that alkaline stress induced a marked accumulation of superoxide anions (O2-) and hydrogen peroxide (H2O2) in rice roots. The application of procyanidins (a potent antioxidant) to rice seedlings 24 h prior to alkaline treatment significantly alleviated alkalinity-induced root damage and promoted seedling growth inhibition, which were concomitant with reduced ROS accumulation. These results suggest that root cell damage, and consequently growth inhibition, of rice seedlings under alkaline stress is closely associated with ROS accumulation. The antioxidant activity of superoxide dismutase, catalase, peroxidase, and ascorbate peroxidase increased under alkaline stress in the roots, probably in response to the cellular damage induced by oxidative stress. However, this response mechanism may be overwhelmed by the excess ROS accumulation observed under stress, resulting in oxidative damage to root cells. Our findings provide physiological insights into the molecular mechanisms of alkalinity-induced damage to root cells, and will contribute to the improvement of alkaline stress tolerance in rice plants.

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FIGURE 1 Images of growth (A) and survival rates (B) of rice seedlings under alkaline conditions. Two-week-old rice seedlings (0 days) were grown for 3 days under unstressed control (CK) or alkaline (Na2CO3)-stressed conditions.
FIGURE 1 Images of growth (A) and survival rates (B) of rice seedlings under alkaline conditions. Two-week-old rice seedlings (0 days) were grown for 3 days under unstressed control (CK) or alkaline (Na2CO3)-stressed conditions.CC BY · PubMed Central
FIGURE 2 Fresh weight (FW) of shoots (A) and roots (B), dry weight (DW) of shoots (C) and roots (D), and relative water content (RWC) of shoots (E) of rice seedlings grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Values are means ± SD, n = 3. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).
FIGURE 2 Fresh weight (FW) of shoots (A) and roots (B), dry weight (DW) of shoots (C) and roots (D), and relative water content (RWC) of shoots (E) of rice seedlings grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Values are means ± SD, n = 3. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).CC BY · PubMed Central
FIGURE 3 Shoot length (A), total root length (B), root surface area (C), root diameter (D), root volume (E), and root number (F) of rice seedlings grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Values are means ± SD, n = 3. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).
FIGURE 3 Shoot length (A), total root length (B), root surface area (C), root diameter (D), root volume (E), and root number (F) of rice seedlings grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Values are means ± SD, n = 3. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).CC BY · PubMed Central
FIGURE 4 Membrane injury (MI) (A) and malondialdehyde (MDA) content (B) of rice roots grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Values are means ± SD, n = 3. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).
FIGURE 4 Membrane injury (MI) (A) and malondialdehyde (MDA) content (B) of rice roots grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Values are means ± SD, n = 3. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).CC BY · PubMed Central
FIGURE 5 Root vigor (A) and cell viability (B,C) of rice roots grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Cell viability was visualized by Evan’s Blue staining as described in the “Materials and Methods” section. Values are means ± SD, n = 3. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).
FIGURE 5 Root vigor (A) and cell viability (B,C) of rice roots grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Cell viability was visualized by Evan’s Blue staining as described in the “Materials and Methods” section. Values are means ± SD, n = 3. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).CC BY · PubMed Central
FIGURE 6 (A–E) Transcriptional induction of cell death-related genes under alkaline stress in rice roots. Two-week-old rice seedlings were grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. A quantitative real-time polymerase chain reaction was performed using OsACT1 as an internal standard. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).
FIGURE 6 (A–E) Transcriptional induction of cell death-related genes under alkaline stress in rice roots. Two-week-old rice seedlings were grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. A quantitative real-time polymerase chain reaction was performed using OsACT1 as an internal standard. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).CC BY · PubMed Central
FIGURE 7 Increases in O2^(•-) (A) and H2O2 (B) levels in rice roots under alkaline stress. Two-week-old rice seedlings were grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Values are means ± SD, n = 3. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).
FIGURE 7 Increases in O2^(•-) (A) and H2O2 (B) levels in rice roots under alkaline stress. Two-week-old rice seedlings were grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Values are means ± SD, n = 3. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).CC BY · PubMed Central
FIGURE 8 Activation of antioxidant enzymes in response to alkaline stress in rice roots. (A) Superoxide (SOD), (B) peroxidase (POD), (C) catalase (CAT), and (D) ascorbate peroxidase (APX). Two-week-old rice seedlings were grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).
FIGURE 8 Activation of antioxidant enzymes in response to alkaline stress in rice roots. (A) Superoxide (SOD), (B) peroxidase (POD), (C) catalase (CAT), and (D) ascorbate peroxidase (APX). Two-week-old rice seedlings were grown under unstressed control (open columns) or alkaline-stressed (filled columns) conditions for 3 days. Asterisks denote a significant difference to the control plants (∗P < 0.05, ∗∗P < 0.01).CC BY · PubMed Central
FIGURE 9 Mitigation of cellular damage by the exogenous antioxidant procyanidins under alkaline stress. Two-week-old rice seedlings were pretreated with or without 0.98% procyanidins for 24 h, then subjected to unstressed control (CK and procyanidins) or alkaline-stressed conditions (Na2CO3 and procyanidins+Na2CO3) for 3 days. (A) Images of seedling growth under different treatments, (B) chlorophyll content, (C) membrane injury (MI), (D) Evan’s Blue staining (cell viability), (E) H2O2, and (F) O2^(•-) content. The bars represent means ± SE, n = 3. The data were analyzed by conducting an analysis of variance, and different letters on the column denote a statistically significant difference (P < 0.05).
FIGURE 9 Mitigation of cellular damage by the exogenous antioxidant procyanidins under alkaline stress. Two-week-old rice seedlings were pretreated with or without 0.98% procyanidins for 24 h, then subjected to unstressed control (CK and procyanidins) or alkaline-stressed conditions (Na2CO3 and procyanidins+Na2CO3) for 3 days. (A) Images of seedling growth under different treatments, (B) chlorophyll content, (C) membrane injury (MI), (D) Evan’s Blue staining (cell viability), (E) H2O2, and (F) O2^(•-) content. The bars represent means ± SE, n = 3. The data were analyzed by conducting an analysis of variance, and different letters on the column denote a statistically significant difference (P < 0.05).CC BY · PubMed Central

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Citations

Cites

Research works printed but not linked: 5

  1. Amini, 2016, Salt-affected soils, reclamation, carbon dynamics, and biochar: a review., J. Soils Sediments, 16, 939, 10.1007/s11368-015-1293-1 · DOI
  2. Chen, 2012, Comparative effects of neutral salt and alkaline salt stress on seed germination, early seedling growth and physiological response of a halophyte species Chenopodium glaucum., Afr. J. Biotechnol., 11, 9572
  3. Feng, 2016, Comprehensive evaluation of rice (Oryza sativa japonica) germplasm for alkaline and saline tolerance at germination stage from Jilin province, China., Soils Crops, 5, 120, 10.11689/j.issn.2095-2961.02.009 · DOI
  4. Islam, 2011, Comparative studies on growth and physiological responses to saline and alkaline stresses of Foxtail millet (Setaria italica L.) and Proso millet (Panicum miliaceum L.)., Aust. J. Crop Sci., 5, 1269
  5. Yang, 2011, Breeding and cultivation techniques of new rice variety of Dongdao 4., Crops, 2, 10.16035/j.issn.1001-7283.2011.02.027 · DOI

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Metadata

Authors
Zhang, H., Liu, X.-L., Zhang, R.-X., Yuan, H.-Y., Wang, M.-M., Yang, H.-Y., Ma, H.-Y., Liu, D., Jiang, C.-J., & Liang, Z.-W.
Affiliations
  • Chinese Academy of Sciences (CN)
  • National Agriculture and Food Research Organization (JP)
Corresponding author
Jiang, Chang-Jie
ORCID
Venue
Frontiers in Plant Science
Publisher
Frontiers Media SA
Published
2017-09-08
Volume
8
Pages
1580-1580
ISSN
1664-462X (ISSN-L)
DOI
10.3389/fpls.2017.01580
PMC
PMC5596797
OpenAlex
W2751550853
Cited by
218
References
66
Citations by year
2026: 29 · 2025: 37 · 2024: 36 · 2023: 39 · 2022: 33 · 2021: 19 · 2020: 7 · 2019: 12 · 2018: 5 · 2017: 1
FWCI
6.73
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Plant Science (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Aluminum toxicity and tolerance in plants and animals
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Rice Cultivation and Yield Improvement
Keywords
alkaline stress, rice, reactive oxygen species, seedling growth inhibition, superoxide, hydrogen peroxide, oxidative stress, cell death genes, procyanidins, antioxidant enzymes, alkaline tolerance, sodium carbonate, malondialdehyde, membrane damage

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