Loss of function of Arabidopsis NADP-malic enzyme 1 results in enhanced tolerance to aluminum stress

Plant J. 2020 Feb;101(3):653-665. doi: 10.1111/tpj.14571. Epub 2019 Nov 20.


In acidic soils, aluminum (Al) toxicity is a significant limitation to crop production worldwide. Given its Al-binding capacity, malate allows internal as well as external detoxification strategies to cope with Al stress, but little is known about the metabolic processes involved in this response. Here, we analyzed the relevance of NADP-dependent malic enzyme (NADP-ME), which catalyzes the oxidative decarboxylation of malate, in Al tolerance. Plants lacking NADP-ME1 (nadp-me1) display reduced inhibition of root elongation along Al treatment compared with the wild type (wt). Moreover, wt roots exposed to Al show a drastic decrease in NADP-ME1 transcript levels. Although malate levels in seedlings and root exudates are similar in nadp-me1 and wt, a significant increase in intracellular malate is observed in roots of nadp-me1 after long exposure to Al. The nadp-me1 plants also show a lower H2 O2 content in root apices treated with Al and no inhibition of root elongation when exposed to glutamate, an amino acid implicated in Al signaling. Proteomic studies showed several differentially expressed proteins involved in signal transduction, primary metabolism and protection against biotic and other abiotic stimuli and redox processes in nadp-me1, which may participate directly or indirectly in Al tolerance. The results indicate that NADP-ME1 is involved in adjusting the malate levels in the root apex, and its loss results in an increased content of this organic acid. Furthermore, the results suggest that NADP-ME1 affects signaling processes, such as the generation of reactive oxygen species and those that involve glutamate, which could lead to inhibition of root growth.

Keywords: Arabidopsis thaliana; aluminum toxicity; malate; roots; stress signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aluminum / toxicity*
  • Arabidopsis / enzymology*
  • Arabidopsis / genetics
  • Arabidopsis / physiology
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Loss of Function Mutation
  • Malate Dehydrogenase (NADP+) / genetics
  • Malate Dehydrogenase (NADP+) / metabolism*
  • Malates / metabolism*
  • Plant Roots / enzymology
  • Plant Roots / genetics
  • Plant Roots / physiology
  • Proteomics
  • Stress, Physiological


  • Arabidopsis Proteins
  • Malates
  • malic acid
  • Aluminum
  • AT2G19900 protein, Arabidopsis
  • Malate Dehydrogenase (NADP+)