Nitric oxide induces rice tolerance to excessive nickel by regulating nickel uptake, reactive oxygen species detoxification and defense-related gene expression

Chemosphere. 2018 Jan:191:23-35. doi: 10.1016/j.chemosphere.2017.09.068. Epub 2017 Sep 30.

Abstract

Soil contamination with nickel (Ni) is a persistent threat to crop production worldwide. The present study examined the putative roles of nitric oxide (NO) in improving Ni-tolerance in rice. Our findings showed that application of exogenous sodium nitroprusside (SNP), a NO donor, significantly improved the growth performance of rice seedlings when grown under excessive Ni. The enhanced Ni-tolerance of rice prompted by SNP could be ascribed to its ability to regulate Ni uptake, decrease Ni-induced oxidative stress as evidenced by reduced levels of hydrogen peroxide, malondialdehyde, and electrolyte leakage in Ni-stressed plants. The positive roles of NO against Ni-toxicity also reflected through its protective effects on photosynthetic pigments, soluble proteins and proline. SNP also boosted antioxidant capacity in Ni-stressed plants by maintaining increased levels of ascorbate, enhanced activities of ROS-detoxifying enzymes, particularly peroxidase (POD) and catalase (CAT) in both roots and shoots compared with Ni-stressed alone plants. Moreover, SNP treatment also upregulated the transcript levels of CAT, POD, ascorbate peroxidase, glutathione reductase and superoxide dismutase genes in shoots under Ni-stress. Using different sulfide compounds and NO scavenger cPTIO, we also provided evidence that NO, rather than other byproducts of SNP, contributed to the improved performance of rice seedlings under Ni-stress. Collectively, our results conclude that exogenous SNP-mediated modulation of endogenous NO enhanced rice tolerance to Ni-stress by restricting Ni accumulation, maintaining photosynthetic performance and reducing oxidative damage through improved antioxidant system, thereby suggesting NO as an effective stress regulator in mitigating Ni-toxicity in economically important rice, and perhaps in other crop plants.

Keywords: Antioxidant system; Gene expression; Nickel stress; Nitric oxide; Oxidative stress; Rice.

MeSH terms

  • Antioxidants / metabolism
  • Ascorbate Peroxidases / metabolism
  • Ascorbic Acid / metabolism
  • Catalase / metabolism
  • Glutathione Reductase / metabolism
  • Hydrogen Peroxide / metabolism
  • Malondialdehyde / metabolism
  • Nickel / metabolism
  • Nickel / toxicity*
  • Nitric Oxide / metabolism*
  • Nitric Oxide Donors
  • Nitroprusside / pharmacology
  • Oryza / genetics
  • Oryza / metabolism
  • Oryza / physiology*
  • Peroxidase / metabolism
  • Photosynthesis / drug effects
  • Plant Roots / metabolism
  • Reactive Oxygen Species / metabolism*
  • Seedlings / drug effects
  • Soil Pollutants / metabolism
  • Soil Pollutants / toxicity*
  • Superoxide Dismutase / metabolism

Substances

  • Antioxidants
  • Nitric Oxide Donors
  • Reactive Oxygen Species
  • Soil Pollutants
  • Nitroprusside
  • Nitric Oxide
  • Malondialdehyde
  • Nickel
  • Hydrogen Peroxide
  • Ascorbate Peroxidases
  • Catalase
  • Peroxidase
  • Superoxide Dismutase
  • Glutathione Reductase
  • Ascorbic Acid