Physiological and transcriptomic analyses reveal that phytohormone pathways and glutathione metabolism are involved in the arsenite toxicity response in tomatoes

Sci Total Environ. 2023 Nov 15:899:165676. doi: 10.1016/j.scitotenv.2023.165676. Epub 2023 Jul 20.

Abstract

The main forms of inorganic arsenic (As) in soil are arsenate [As(V)] and arsenite [As(III)]. Both forms inhibit plant growth. Here, we investigate the effects of As(III) toxicity on the growth of tomatoes by integrating physiological and transcriptomic analyses. As(III) toxicity induces oxidative damage, inhibits photosynthetic efficiency, and reduces soluble sugar levels. As(III) toxicity leads to reductions in auxin, cytokinin and jasmonic acid contents by 29 %, 39 % and 55 %, respectively, but leads to increases in the ethylene precursor 1-amino-cyclopropane carboxylic acid, abscisic acid and salicylic acid contents in roots, by 116 %, 79 % and 39 %, respectively, thereby altering phytohormone signalling pathways. The total glutathione, reduced glutathione (GSH) and oxidized glutathione (GSSG) contents are reduced by 59 %, 49 % and 94 % in roots; moreover, a high GSH/GSSG ratio is maintained through increased glutathione reductase activity (increased by 214 %) and decreased glutathione peroxidase activity (decreased by 40 %) in the roots of As(III)-treated tomato seedlings. In addition, As(III) toxicity affects the expression of genes related to the endoplasmic reticulum stress response. The altered expression of aquaporins and ABCC transporters changes the level of As(III) accumulation in plants. A set of hub genes involved in modulating As(III) toxicity responses in tomatoes was identified via a weighted gene coexpression network analysis. Taken together, these results elucidate the physiological and molecular regulatory mechanism underlying As(III) toxicity and provide a theoretical basis for selecting and breeding tomato varieties with low As(III) accumulation. Therefore, these findings are expected to be helpful in improving food safety and to developing sustainable agricultural.

Keywords: As(III) toxicity; As(III) transporters; Endoplasmic reticulum stress response; Glutathione metabolism; Phytohormone signalling pathways; Solanum lycopersicum.

MeSH terms

  • Antioxidants / metabolism
  • Arsenites* / toxicity
  • Glutathione / metabolism
  • Glutathione Disulfide / pharmacology
  • Oxidative Stress
  • Plant Breeding
  • Plant Growth Regulators / pharmacology
  • Seedlings / metabolism
  • Solanum lycopersicum* / genetics
  • Transcriptome

Substances

  • Plant Growth Regulators
  • Glutathione Disulfide
  • arsenite
  • Arsenites
  • Antioxidants
  • Glutathione