Elsevier

Plant Physiology and Biochemistry

Volume 144, November 2019, Pages 427-435
Plant Physiology and Biochemistry

Research article
Morphological and metabolic responses to salt stress of rice (Oryza sativa L.) cultivars which differ in salinity tolerance

https://doi.org/10.1016/j.plaphy.2019.10.017Get rights and content

Highlights

  • The shoot and root growth were only significantly restrained in sensitive cultivar.

  • Many sugars' levels increased in the tolerant cultivar leaves at early stress time.

  • Malate and sucrose in the leaves are important markers to salt stress.

  • Mannitol in the roots is one of the most distinct markers to salinity.

Abstract

Salinization is one of the most important abiotic stressors for crop growth and productivity. Rice (Oryza sativa L.), as the major food source around the world, is very sensitive to salt, especially at seedling stage. In order to examine how salt stress influences the metabolism of rice, we compared the levels of a range of sugars and organic acids in three rice cultivars with different tolerance under salt stress over time. According to the morphological result, the shoot length and root fresh weight were only affected by salinity in the salt sensitive cultivar (Nipponbare). The responses of metabolites to salinity were time-, tissue- and cultivar-dependent. Shikimate and quinate, involved in the shikimate pathway, were dramatically decreased in the leaves of all three cultivars, which was regarded as a response to salinity. Many sugars in the leaves of the salt tolerant cultivar (Dendang and Fatmawati) showed earlier increases to salt stress compared to Nipponbare leaves. Moreover, only in the leaves of tolerant cultivars (Dendang and Fatimawati), malate was significantly decreased while sucrose was significantly increased. In Dendang roots, mannitol levels were significantly higher than in Nipponbare roots after 14 days of salt treatment, which may be attributed to its higher salt tolerance. It is proposed that these responses in the more tolerant cultivars are involved in their resistance to high salt stress which may lay the foundation for breeding tolerant rice cultivars.

Introduction

Salinity is regarded as a major environmental constraint to crop productivity worldwide (Zhu, 2001). More than 6% of the world land area are either salinity or sodicity affected (FAO, 2008). Due to the human activities and natural causes, soil salinization is increasing. A saline soil is defined to have an electrical conductivity of the saturated paste extract above 4 dS/m (~40 mM NaCl) (Chinnusamy et al., 2005). The high concentration of salt in the soil makes it harder for roots to uptake water and nutrients, therefore inducing ion imbalances and water stress in plants (Hasegawa et al., 2000). Following a consequence of these primary effects, the secondary stresses, such as metabolic damage, growth arrest, and even death, can occur. For example, osmotic stress leads to cell dehydration and a subsequent decrease in shoot and root growth. The high accumulation of Na+ in the leaf blades has been shown to be negatively correlated with plant growth in wheat (Triticum aestivum) (Munns et al., 2000), rice (Oryza sativa L.) (Zhu et al., 2001; Platten et al., 2013) and barley (Hordeum vulgare L.) (Garthwaite et al., 2005).

Metabolite changes are indicators of cellular regulatory processes. The osmotic adjustment in rice can be achieved by synthesis of compatible solutes, such as proline, glycine, GABA and sucrose (Ma et al., 2018; Banerjee et al., 2019; Gayen et al., 2019). Prolonged salt stress in wheat has showed progressive accumulation of sugars to avoid osmotic stress (Guo et al., 2015). Furthermore, cereals with different sensitivity to salt show different metabolite changes. For example, salt stress increased the levels of hexose phosphates and tricarboxylic acid (TCA) cycle intermediates in the salt tolerant barley (Sahara) while these solutes remained unchanged in the sensitive barley (Clipper) (Widodo et al., 2009). The metabolic pathways changes in cereals differing in salinity resistance may provide fundamental information to breed for tolerant cultivars.

Rice is the staple food for nearly half of the world's population. More than 50% of rice is produced and consumed in Asia (GRiSP, 2013). Compared with other crops, such as wheat and barley, rice is the most sensitive crop to salt stress (Munns and Tester, 2008). Rice grain yield can be reduced significantly by the addition of 50 mM NaCl (Yeo and Flowers, 1986), while barley, for instance, can withstand up to 450 mM NaCl (Garthwaite et al., 2005). Among the predominant abiotic stresses, such as drought and cold, salinity tolerance remains the main goal to breed stress-tolerant rice cultivars in order to assure food security (Jini and Joseph, 2017; Reddy et al., 2017).

Nipponbare, a japonica salt sensitive genotype has been used as a model rice cultivar in a variety of abiotic and biotic stress studies (Ahn et al., 2010; Wang et al., 2012). Dendang and Fatmawati are two indica genotypes with relatively high salt tolerance (Barus and Rauf, 2013). In general, indica rice has a higher level of salinity tolerance when compared with japonica (Lee et al., 2003). To our knowledge, there are no reports defining differences in metabolic responses to different salt treatments of these relatively high tolerant rice cultivars (Dendang and Fatmawati).

The growth stages, organ types and cultivars are important factors to select against the sensitivity of rice to salt. Many researchers have shown that salinity influences rice growth throughout its life cycle from germination to maturity, but the most sensitive growth stage is shown to be the seedling stage (Lutts et al., 1995; Khan et al., 1997; Nam, 2018). In this study, we investigated the salt stress response in the leaves and roots of three rice cultivars (Dendang, Fatmawati and Nipponbare) at seedling stage (four-leaf stage) at the metabolic level in order to understand their physiological responses of salt stress. Metabolic profiling may allow an initial functional insight into the metabolic pathways of tolerance acquisition without prior knowledge of genetic variation between these cultivars.

Section snippets

Chemicals and reagents

Sugars and organic acids standards, internal standards (ISTD) and the derivatization reagent, methoxyamine hydrochloride (Meox), used for Gas chromatography-mass spectrometry (GC-MS) were acquired from Sigma Aldrich (Castle Hill, NSW, Australis). N,O-Bis (trimethylsilyl) trifluoroacetamide with 1% trimethylsilyl chloride (BSTFA + 1% TMCS) was from Thermo Scientific (Bellefonte, USA). All solvents used were High performance liquid chromatography (HPLC)-grade purchased from Merck (Australia).

Plant materials and stress treatment

The

Morphological responses to salt stress

The three rice cultivars with different tolerance to salt (Dendang, Fatmawati, and Nipponbare) were evaluated for growth parameters after the time-series salt treatment. There were no obvious symptoms at the beginning of salt stress, but the reduction in shoot and root growth, and faster senescence of leaves occurred as exposure time increased. Rice plants began to develop leaf symptoms such as yellowing and necrotic lesions of old leaf tips after 3–4 days of exposure. After 2 weeks of stress,

Shoot length and root fresh weight in Nipponbare were affected by salt stress

Under salinity, the three cultivars performed differently during the 14 days of treatment. Compared with Nipponbare, Dendang and Fatmawati were less affected as indicated by a smaller reduction in shoot length, root length and root fresh weight. As morphological parameters are used for screening salt tolerant cultivars (Munns, 2002; Shahzad et al., 2012; Yildirim et al., 2015), our results demonstrate that Dendang and Fatmawati showed higher salt tolerance than Nipponbare.

The shoot and root

Declaration of interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Author contributions

Ute Roessner and Jing Chang developed the experiment. Siria Natera and Ute Roessner provided assistance with metabolite analysis. Jing Chang and Ute Roessner analysed data. Jing Chang drafted the manuscript which has been revised and reviewed by all other authors. Bo Eng Cheong provided advice and suggestions on plant growth and data analysis.

Acknowledgment

Jing Chang thanks for the support of the University of Chinese Academy of Sciences (UCAS, UCAS[2015]37) Joint PhD Training Program and the University of Melbourne Study Abroad Scholarship Program. Metabolite analysis was carried out at Metabolomics Australia (School of BioSciences, University of Melbourne, Australia), which is a National Collaborative Research Infrastructure Strategy initiative under Bioplatforms Australia Pty Ltd (http://www.bioplatforms.com/). The work was funded through an

References (47)

  • J.K. Zhu

    Plant salt tolerance

    Trends Plant Sci.

    (2001)
  • J.C. Ahn et al.

    Classification of rice (Oryza sativa L. Japonica nipponbare) immunophilins (fkbps, cyps) and expression patterns under water stress

    BMC Plant Biol.

    (2010)
  • A. Banerjee et al.

    Salt acclimation differentially regulates the metabolites commonly involved in stress tolerance and aroma synthesis in indica rice cultivars

    Plant Growth Regul.

    (2019)
  • W.A. Barus et al.

    Screening and adaptation in some varieties of rice under salinity stress (case study at Paluh Merbau, Deli Serdang district, North Sumatera, Indonesia)

    J. Rice Res.

    (2013)
  • V. Chinnusamy et al.

    Understanding and improving salt tolerance in plants

    Crop Sci.

    (2005)
  • A. Conde et al.

    Mannitol transport and mannitol dehydrogenase activities are coordinated in Olea europaea under salt and osmotic stresses

    Plant Cell Physiol.

    (2011)
  • FAO

    FAO land and plant nutrition management service

  • A.J. Garthwaite et al.

    Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl- into the shoots

    J. Exp. Bot.

    (2005)
  • GRiSP

    Rice Almanac

    (2013)
  • R. Guo et al.

    Comparative metabolic responses and adaptive strategies of wheat (Triticum aestivum) to salt and alkali stress

    BMC Plant Biol.

    (2015)
  • A.K. Gupta et al.

    Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants

    J. Biosci.

    (2005)
  • M.A. Hannah et al.

    Transport and metabolism of raffinose family oligosaccharides in transgenic potato

    J. Exp. Bot.

    (2006)
  • P.M. Hasegawa et al.

    Plant cellular and molecular responses to high salinity

    Annu. Rev. Plant Physiol. Plant Mol. Biol.

    (2000)
  • Cited by (56)

    • An α/β hydrolase family member negatively regulates salt tolerance but promotes flowering through three distinct functions in rice

      2022, Molecular Plant
      Citation Excerpt :

      Metabolites in plants are widely involved in the process of dealing with biotic and abiotic stresses. To date, a number of metabolites have been implicated in the acclimation to salinity, including sugars, amino acids, and lipids (Wingler, 2002; Ge et al., 2008; Hou et al., 2016; Chang et al., 2019). Fatty acids, a basic category of lipids, have been reported to be bound up in response to chilling injury and thermal damage (Yang et al., 2013; Tovuu et al., 2016; Chen et al., 2021a).

    • Getting to the roots of Cicer arietinum L. (chickpea) to study the effect of salinity on morpho-physiological, biochemical and molecular traits

      2022, Saudi Journal of Biological Sciences
      Citation Excerpt :

      The results obtained in the present study revealed that both fresh and dry weight of root reduced, and this reduction was due to a lesser number of secondary roots that decreased that root volume. Hindrance in the water uptake leads to a loss in turgor under salinity that might affect the fresh and dry weight of the root (Chang et al., 2019; Mann et al., 2019). The initial phase of salinity i.e., the osmotic phase reduces the efficiency of the root to uptake water and the traits related to water are affected.

    • Plant Metabolomics: Current Initiatives and Future Prospects

      2023, Current Issues in Molecular Biology
    View all citing articles on Scopus
    View full text