Exogenous proanthocyanidins improve tolerance of Cu-toxicity by amelioration of oxidative damage and re-programming of gene expression in Medicago sativa

PLoS One. 2021 Oct 26;16(10):e0259100. doi: 10.1371/journal.pone.0259100. eCollection 2021.

Abstract

Excess copper (Cu) in soil due to industrial and agricultural practices can result in reduced plant growth. Excess Cu resulted in severely retarded root growth with severe discoloration of Alfalfa (Medicago sativa) and Medicago truncatula. Growth in the presence of hydrogen peroxide resulted in similar symptoms that could be partially recovered by the addition of the reductant ascorbic acid revealing damage was likely due to oxidative stress. The addition of proanthocyanidins (PAs) in the presence of Cu prevented much of the damage, including plant growth and restoration of lignin synthesis which was inhibited in the presence of excess Cu. Transcriptome analyses of the impact of excess Cu and the amelioration after PAs treatment revealed that changes were enriched in functions associated with the cell wall and extracellular processes, indicating that inhibition of cell wall synthesis was likely the reason for retarded growth. Excess Cu appeared to induce a strong defense response, along with alterations in the expression of a number of genes encoding transcription factors, notably related to ethylene signaling. The addition of PAs greatly reduced this response, and also induced novel genes that likely help ameliorate the effects of excess Cu. These included induction of genes involved in the last step of ascorbic acid biosynthesis and of enzymes involved in cell wall synthesis. Combined, these results show that excess Cu causes severe oxidative stress damage and inhibition of cell wall synthesis, which can be relieved by the addition of PAs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Copper / toxicity*
  • Gene Expression Regulation, Plant / drug effects*
  • Medicago sativa / drug effects
  • Medicago sativa / genetics*
  • Medicago sativa / metabolism
  • Oxidative Stress / drug effects*
  • Plant Leaves / metabolism
  • Plant Roots / metabolism
  • Proanthocyanidins / pharmacology*
  • Transcriptome / drug effects

Substances

  • Proanthocyanidins
  • Copper

Grants and funding

This work was supported by grants from the Agricultural Variety Improvement Project of Shandong Province [2019LZGC010]; the Major Program of Shandong Province Natural Science Foundation [No. ZR2018ZB0213]; Special Funds for the Construction of Innovative Provinces in Hunan [No. 2019NK3028]; the National Natural Science Foundation of China [No. 32071877]; and the National Key P & D Program of China [2018YFE0108100]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.