The Arabidopsis thaliana Gulono-1,4 γ-lactone oxidase 2 (GULLO2) facilitates iron transport from endosperm into developing embryos and affects seed coat suberization

Plants synthesize ascorbate (ASC) via the D-mannose/L-galactose pathway whereas animals produce ASC and H2O2via the UDP-glucose pathway, with Gulono-1,4 γ-lactone oxidases (GULLO) as the last step. A. thaliana has seven isoforms, GULLO1-7; previous in silico analysis suggested that GULLO2, mostly ex...

Full description

Saved in:
Bibliographic Details
Published in:Plant physiology and biochemistry 2023-03, Vol.196, p.712-723
Main Authors: Murgia, Irene, Midali, Alessia, Cimini, Sara, De Gara, Laura, Manasherova, Ekaterina, Cohen, Hagai, Paucelle, Alexis, Morandini, Piero
Format: Article
Language:English
Subjects:
Animals
Arabidopsis - metabolism
Arabidopsis Proteins - metabolism
Ascorbate
Ascorbic Acid - metabolism
Embryos
Endosperm - metabolism
Ferric Compounds - metabolism
Gulono-1,4 γ-lactone oxidase
Hydrogen Peroxide - metabolism
Iron
Iron - metabolism
Life Sciences
Oxidoreductases - metabolism
Seeds
Seeds - metabolism
Suberin
Vitamin C
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
Description
Summary:Plants synthesize ascorbate (ASC) via the D-mannose/L-galactose pathway whereas animals produce ASC and H2O2via the UDP-glucose pathway, with Gulono-1,4 γ-lactone oxidases (GULLO) as the last step. A. thaliana has seven isoforms, GULLO1-7; previous in silico analysis suggested that GULLO2, mostly expressed in developing seeds, might be involved in iron (Fe) nutrition. We isolated atgullo2-1 and atgullo2-2 mutants, quantified ASC and H2O2 in developing siliques, Fe(III) reduction in immature embryos and seed coats. Surfaces of mature seed coats were analysed via atomic force and electron microscopies; suberin monomer and elemental compositions of mature seeds, including Fe, were profiled via chromatography and inductively coupled plasma-mass spectrometry. Lower levels of ASC and H2O2 in atgullo2 immature siliques are accompanied by an impaired Fe(III) reduction in seed coats and lower Fe content in embryos and seeds; atgullo2 seeds displayed reduced permeability and higher levels of C18:2 and C18:3 ω-hydroxyacids, the two predominant suberin monomers in A. thaliana seeds. We propose that GULLO2 contributes to ASC synthesis, for Fe(III) reduction into Fe(II). This step is critical for Fe transport from endosperm into developing embryos. We also show that alterations in GULLO2 activity affect suberin biosynthesis and accumulation in the seed coat. •Gulono-1,4 γ-lactone oxidases (GULLO) are enzymes devoted to biosynthesis of ascorbic acid (vitamin C) in animal cells.•GULLO enzymes are also present in plant cells.•Our results suggest that Arabidopsis thaliana GULLO2 isoform catalyzes the in vivo production of ascorbic acid.•GULLO2 contributes to Fe transport from endosperm into the developing embryo and to suberin biosynthesis in the seed coat.
ISSN:0981-9428
1873-2690
0981-9428
DOI:10.1016/j.plaphy.2023.01.064