The Arabidopsis electron‐transfer flavoprotein:ubiquinone oxidoreductase is required during normal seed development and germination

• Published in: The Plant journal : for cell and molecular biology 2022-01, Vol.109 (1), p.196-214
• Main Authors: da Fonseca‐Pereira, Paula, Pham, Phuong Anh, Cavalcanti, João Henrique F., Omena‐Garcia, Rebeca P., Barros, Jessica A. S., Rosado‐Souza, Laise, Vallarino, José G., Mutwil, Marek, Avin‐Wittenberg, Tamar, Nunes‐Nesi, Adriano, Fernie, Alisdair R., Araújo, Wagner L.
• Format: Article
• Language: English
• Subjects: Alternative energy sources; Alternative pathway; amino acid metabolism; Amino acids; Amino Acids - metabolism; Arabidopsis; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Carbon - metabolism; carbon partition; Carbon sequestration; Carbon sources; Dehydrogenase; Dehydrogenases; Electron-Transferring Flavoproteins - genetics; Electron-Transferring Flavoproteins - metabolism; Electrons; Energy metabolism; ETF/electron‐transfer flavoprotein:ubiquinone oxidoreductase pathway; Fatty acid composition; Fatty acids; Gene expression; Germination; Iron-Sulfur Proteins - genetics; Iron-Sulfur Proteins - metabolism; Life cycles; Mutants; Mutation; Oxidoreductases Acting on CH-NH Group Donors - genetics; Oxidoreductases Acting on CH-NH Group Donors - metabolism; primary metabolism; Proteins; Respiration; seed development; Seed germination; Seeds; Seeds - enzymology; Seeds - genetics; Seeds - growth & development; Sucrose; Transcriptomes; Transcriptomics; Ubiquinol; Ubiquinone - analogs & derivatives; Ubiquinone - metabolism; Ubiquinone oxidoreductase
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.15566

SUMMARY The importance of the alternative donation of electrons to the ubiquinol pool via the electron‐transfer flavoprotein/electron‐transfer flavoprotein:ubiquinone oxidoreductase (ETF/ETFQO) complex has been demonstrated. However, the functional significance of this pathway during seed development and germination remains to be elucidated. To assess the function of this pathway, we performed a detailed metabolic and transcriptomic analysis of Arabidopsis mutants to test the molecular consequences of a dysfunctional ETF/ETFQO pathway. We demonstrate that the disruption of this pathway compromises seed germination in the absence of an external carbon source and also impacts seed size and yield. Total protein and storage protein content is reduced in dry seeds, whilst sucrose levels remain invariant. Seeds of ETFQO and related mutants were also characterized by an altered fatty acid composition. During seed development, lower levels of fatty acids and proteins accumulated in the etfqo‐1 mutant as well as in mutants in the alternative electron donors isovaleryl‐CoA dehydrogenase (ivdh‐1) and d‐2‐hydroxyglutarate dehydrogenase (d2hgdh1‐2). Furthermore, the content of several amino acids was increased in etfqo‐1 mutants during seed development, indicating that these mutants are not using such amino acids as alternative energy source for respiration. Transcriptome analysis revealed alterations in the expression levels of several genes involved in energy and hormonal metabolism. Our findings demonstrated that the alternative pathway of respiration mediated by the ETF/ETFQO complex affects seed germination and development by directly adjusting carbon storage during seed filling. These results indicate a role for the pathway in the normal plant life cycle to complement its previously defined roles in the response to abiotic stress. Significance Statement The importance of the alternative donation of electrons to the ubiquinol pool via the electron‐transfer flavoprotein/electron‐transfer flavoprotein:ubiquinone oxidoreductase (ETF/ETFQO) complex during normal seed development and germination is presented. Our results provide compelling evidence for a pivotal role of the alternative ETF/ETFQO respiration pathway in the normal life cycle of a plant in addition to its previously defined roles in response the to abiotic stress.