Research Article: Regulation of reactive oxygen and nitrogen species by salicylic acid in rice plants under salinity stress conditions

Date Published: March 20, 2018

Publisher: Public Library of Science

Author(s): Yoonha Kim, Bong-Gyu Mun, Abdul Latif Khan, Muhammad Waqas, Hyun-Ho Kim, Raheem Shahzad, Muhammad Imran, Byung-Wook Yun, In-Jung Lee, Keqiang Wu.


This study investigated the regulatory role of exogenous salicylic acid (SA) in rice and its effects on toxic reactive oxygen and nitrogen species during short-term salinity stress. SA application (0.5 and 1.0 mM) during salinity-induced stress (100 mM NaCl) resulted in significantly longer shoot length and higher chlorophyll and biomass accumulation than with salinity stress alone. NaCl-induced reactive oxygen species production led to increased levels of lipid peroxidation in rice plants, which were significantly reduced following SA application. A similar finding was observed for superoxide dismutase; however, catalase (CAT) and ascorbate peroxidase (APX) were significantly reduced in rice plants treated with SA and NaCl alone and in combination. The relative mRNA expression of OsCATA and OsAPX1 was lower in rice plants during SA stress. Regarding nitrogenous species, S-nitrosothiol (SNO) was significantly reduced initially (one day after treatment [DAT]) but then increased in plants subjected to single or combined stress conditions. Genes related to SNO biosynthesis, S-nitrosoglutathione reductase (GSNOR1), NO synthase-like activity (NOA), and nitrite reductase (NIR) were also assessed. The mRNA expression of GSNOR1 was increased relative to that of the control, whereas OsNOA was expressed at higher levels in plants treated with SA and NaCl alone relative to the control. The mRNA expression of OsNR was decreased in plants subjected to single or combination treatment, except at 2 DAT, compared to the control. In conclusion, the current findings suggest that SA can regulate the generation of NaCl-induced oxygen and nitrogen reactive species in rice plants.

Partial Text

High salinity is caused by improper irrigation and drainage and affects over half of the productive irrigated land globally at an average rate of up to one-half million hectares per year [1]. Rice paddy fields also experience increased salinity due to water evaporation during the summer season, which reduces crop growth and yield [2]. Rice plants—which provide food for over 70% of the human population—are exposed to salinity stress, and the concurrent generation of reactive oxygen species (ROS) also accelerates cell damage. During abiotic stress, plant cells are exposed to an array of ROS, such as superoxide radicals (O2−), hydrogen peroxide (H2O2), hydroxyl radicals (OH−), and singlet oxygen (1O2), during the photosynthetic processes of photosystems I and II [3–5]. ROS generation maintains stable growth during non-stress conditions; however, under abiotic stresses, internal ROS activity increases rapidly, subsequently attacking biomolecules such as lipids, proteins, and nucleic acids [6–8]. Thus, to protect cellular components, plants must recruit antioxidant enzymes such as ascorbate peroxidase (APX), catalase (CAT), glutathione (GSH), and superoxide dismutase (SOD) [8, 9], which act to eliminate oxygenated radicals [10]. The stress signaling molecule nitric oxide (NO) is a highly reactive free radical, which may substantially participate in plant development and immunity [11]. NO is highly toxic to plants in the presence of ROS due to its chemical properties; thus, it must be converted by the plants into a non-toxic form, such as S-nitrosoglutathione (GSNO) [12, 13]. Furthermore, NO can covalently bind to cysteine residues through S-nitrosylation, and, thus, NO can be converted to nitrosylated proteins (SNOs). Although the importance of NO in plants has been recognized in various studies, the exact NO signaling pathway remains unknown [12–15].

With the current changes in global climatic conditions, the occurrence of multiple stress conditions (biotic and abiotic) can be detrimental to crop growth and production [44]. Over the past few decades, SA (endogenous or exogenous) has been identified as a key regulator of physiological, biochemical, and genetic mechanisms against various stress conditions, such as pathogen or insect attacks and abiotic stresses in plants [45, 46]. However, high concentrations of exogenously applied SA can induce artificial biotic stress in plants and can inhibit the ROS scavenging pathway in plants; elevated levels of SA inhibit the activity of APX and CAT [30]. Furthermore, elevated levels of SA in plants markedly enhance plant cell death due to increased production of H2O2 and lipid peroxidation [47, 48]. Conventionally, exogenous application of NaCl has been used to induce artificial salinity stress in many studies; since NaCl application induces osmotic imbalance in the cell, we applied NaCl to induce abiotic stress (salinity stress) [2, 49]. The results of the current study support the negative effects of SA on rice plant growth. The combination of biotic (SA, 0.5 and 1.0 mM) and abiotic (NaCl) stress led to changes in plant plasticity by significantly affecting the leaf length and biomass. In addition, the sodium ion content differed between plants treated with NaCl and SA.

Studies on the physiological responses of plants exposed to multiple stress conditions are limited; thus, our study involved the application of SA and NaCl to rice plants to induce artificial abiotic and biotic stress. Our results showed that cell death was induced in rice plants treated with combined SA and NaCl through the downregulation of antioxidant activity of CAT as well as APX. The activity of these enzymes was regulated at the genetic level. Finally, artificial abiotic and biotic stress conditions induced the downregulation of OsCATA and OsAPX1, resulting in reduced enzyme activity (CAT and APX). Under stress conditions (single and multiple stress conditions), rice growth characteristics were significantly correlated with CAT and its mRNA expression level; therefore, we assume that CAT activity was most sensitive to stress. Both stress conditions could induce the upregulation of OsGSNOR and, thus, increase SNO contents.




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