4.6 Article

Hydroxyl radical scavenging by cerium oxide nanoparticles improves Arabidopsis salinity tolerance by enhancing leaf mesophyll potassium retention

Journal

ENVIRONMENTAL SCIENCE-NANO
Volume 5, Issue 7, Pages 1567-1583

Publisher

ROYAL SOC CHEMISTRY
DOI: 10.1039/c8en00323h

Keywords

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Funding

  1. National Science Foundation [1817363]
  2. University of California, Riverside
  3. USDA National Institute of Food and Agriculture [1009710]
  4. ARC [DPDP150101663]
  5. GRDC [UT00027]
  6. Direct For Biological Sciences
  7. Div Of Molecular and Cellular Bioscience [1817363] Funding Source: National Science Foundation

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Salinity is a widespread environmental stress that severely limits crop yield worldwide. Cerium oxide nanoparticles (nanoceria) have the unique capability of catalytically reducing levels of stress-induced reactive oxygen species (ROS) including hydroxyl radicals (OH) that lack enzymatic scavenging pathways. The underlying mechanisms of how nanoceria ROS scavenging augments plant tolerance to environmental stress are not well understood. Herein, we demonstrate that catalytic OH scavenging by nanoceria in Arabidopsis thaliana leaves significantly improves mesophyll K+ retention, a key trait associated with salinity stress tolerance. Leaves with mesophyll cells interfaced with 50 mg L-1 poly(acrylic acid) coated nanoceria (PNC) have significantly higher (P < 0.05) carbon assimilation rates (85%), quantum efficiency of photosystem II (9%), and chlorophyll content (14%) compared to controls after being exposed to 100 mM NaCl for 3 days. PNC infiltrated leaves (PNC-leaves) under salinity stress exhibit lower ROS levels - including hydroxyl radical (41%) and its precursor hydrogen peroxide (44%) - and one fold higher (P < 0.05) cytosolic K+ dye intensity in leaf mesophyll cells relative to controls. Non-invasive microelectrode ion flux electrophysiological (MIFE) measurements indicated that PNC-leaves have about three-fold lower NaCl-induced K+ efflux from leaf mesophyll cells compared to controls upon exposure to salinity stress. The ROS-activated nonselective cation channels (ROS-NSCC) in the plasma membrane of leaf mesophyll cells were identified as the main OH-inducible K+ efflux channels. Long term catalytic scavenging of OH in leaves by PNC enhances plant photosynthetic performance under salinity stress by enabling plasma membrane channels/transporters to coordinately retain higher levels of K+ in the leaf mesophyll cell cytosol. PNC augmented plant ROS scavenging provides a key tool for understanding and improving plant tolerance against abiotic stresses such as salinity. Environmental significance Environmental stresses, including salinity, lead to the accumulation of reactive oxygen species (ROS) with subsequent damage to plant cellular components, reduced crop growth and yield. Organisms lack enzymatic pathways for catalytically scavenging hydroxyl radicals, one of the most destructive ROS, thus limiting the ability of molecular tools to manipulate this ROS in vivo. Herein, we apply a nanobiotechnology- based approach that improves plant salinity stress tolerance by scavenging hydroxyl radicals and its precursors. We determined the underlying mechanisms of how cerium oxide nanoparticle (nanoceria) reduction of hydroxyl radical levels in Arabidopsis leaves affects potassium fluxes across the plasma membrane. Nanoceria enable higher retention of K+ in leaf mesophyll, thus improving plant photosynthetic performance and biomass against environmental stress e. g. salinity.

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