Inactivation of cytosolic FUMARASE2 enhances growth and photosynthesis under simultaneous copper and iron deprivation in Arabidopsis

Abstract

Copper (Cu) and iron (Fe) are essential for plant growth and are often in short supply under natural conditions. Molecular responses to simultaneous lack of both metals (-Cu-Fe) differ from those seen in the absence of either alone. Metabolome profiling of plant leaves previously revealed that fumarate levels fall under -Cu-Fe conditions. We employed lines lacking cytosolic FUMARASE2 (FUM2) activity to study the impact of constitutive suppression of cytosolic fumarate synthesis on plant growth under Cu and/or Fe deficiency. In fum2 mutants, photosynthesis and growth were less impaired under -Cu-Fe conditions than in wild-type (WT) seedlings. In particular, levels of photosynthetic proteins, chloroplast ultrastructure, amino acid profiles and redox state were less perturbed by simultaneous Cu-Fe deficiency in lines that cannot produce fumarate in the cytosol. Although cytosolic fumarate has been reported to promote acclimation of photosynthesis to low temperatures when metal supplies are adequate, the photosynthetic efficiency of fum2 lines grown under Cu-Fe deficiency in the cold was higher than in WT. Uptake and contents of Cu and Fe are similar in WT and fum2 plants under control and -Cu-Fe conditions, and lack of FUM2 does not alter the ability to sense metal deficiency, as indicated by marker gene expression. Collectively, we propose that reduced levels of cytosolic fumarate synthesis ultimately increase the availability of Fe for incorporation into metalloproteins.

Analysis of Alternative Splicing During the Combinatorial Response to Simultaneous Copper and Iron Deficiency in Arabidopsis Reveals Differential Events in Genes Involved in Amino Acid Metabolism

“…Further analysis of metabolome profiles explained such trends by significant drops in the concentration of phenylalanine (Phe), asparagine (Asn), tryptophan (Trp), and the organic acid fumarate. Moreover, loss-of-function lines of the cytosolic fumarase FUMARASE2 displayed improved growth and photosynthesis performance in seedlings cultivated under Cu and Fe deficient conditions, which was accompanied by balanced levels of amino acids (Garcia-Molina et al, 2021). This finding confirmed the existence of specific mechanisms exclusively operating in plants under simultaneous Cu and Fe deficiency and posed fumaric acid as a central modulator of the combinatorial response.…”

“…Metabolome profiling of Arabidopsis seedlings under double Cu and Fe deficiency uncovered a significant 2-fold increase in the amino acid fraction as a result of growth impairments and chloroplast misfunction. However, abrogation of Arabidopsis cytosolic fumarase FUMARASE2 (FUM2) conferred improved growth and photosynthesis rates under simultaneous Cu and Fe deficiency, and led to a barely unaltered amino acid composition in comparison with standard conditions (Garcia-Molina et al, 2021). Considering the interplay of Cu and Fe in sustaining antioxidant activities mediated by superoxide dismutases and electron transport chains in chloroplast and mitochondrion (Kliebenstein et al, 1998;Abdel-Ghany et al, 2005;Yamasaki et al, 2009;Bernal et al, 2012), the detrimental consequences of the simultaneous limitation of Cu and Fe would prevent the proper function of photosynthesis and respiration to obtain energy based on carbon skeletons.…”

Involvement of Arabidopsis Multi-Copper Oxidase-Encoding LACCASE12 in Root-to-Shoot Iron Partitioning: A Novel Example of Copper-Iron Crosstalk

“…This was proposed to be associated with a swap from autotrophic to heterotrophic growth, and also includes organic acids like fumaric acid in the response to both deficiencies that may help plants to acclimate to simultaneous -Cu -Fe deficiency (Garcia-Molina et al, 2020). A more recent publication reports that the availability of cytosolic Fe is increased when the synthesis of cytosolic fumarate is decreased (Garcia-Molina et al, 2021).…”

Assessing the Suitability of Sediment Soil to Be Reused by Different Soil Treatments for Forest Agriculture

“…All experiments were repeated three times per treatment. The measured image was defined as an area of interest using ImagingWin v2.41 software, where we computed the maximum quantum yield of PS II photochemistry measured in the dark-adapted state (Fv/Fm), the PS II actual photochemical quantum yield (Y(II)), the quantum yield of regulated energy dissipation in PS II (Y(NPQ)), and the quantum yield of nonregulated energy dissipation in PS II (Y(NO)) [30][31][32].…”