The Four Subunits of Mitochondrial Respiratory Complex II Are Encoded by Multiple Nuclear Genes and Targeted to Mitochondria in Arabidopsis Thaliana

Overview

Journal Plant Mol Biol

Date 2002 Oct 11

PMID 12374303

Citations 17

Authors

Pablo Figueroa

Gabriel Leon

Alvaro Elorza

Loreto Holuigue

Alejandro Araya

Xavier Jordana

Affiliations

Soon will be listed here.

Abstract

Mitochondrial respiratory complex II contains four subunits: a flavoprotein (SDHI), an iron-sulphur subunit (SDH2) and two membrane anchor subunits (SDH3 and SDH4). We have found that in Arabidopsis thaliana SDH I and SDH3 are encoded by two, and SDH4 by one nuclear genes, respectively. All these encoded polypeptides are found to be imported into isolated plant mitochondria. While both SDHI proteins are highly conserved when compared to their counterparts in other organisms, SDH3 and SDH4 share little similarity with non-plant homologues. Expression of SDH1-1, SDH3 and SDH4 genes was detected in all tissues analysed, with the highest steady-state mRNA levels found in flowers and inflorescences. In contrast, the second SDH1 gene (SDH1-2) is expressed at a low level.

Citing Articles

The biogenesis and regulation of the plant oxidative phosphorylation system.

Ghifari A, Saha S, Murcha M Plant Physiol. 2023; 192(2):728-747.

PMID: 36806687 PMC: 10231475. DOI: 10.1093/plphys/kiad108.

Proteomic and Genomic Studies of Micronutrient Deficiency and Toxicity in Plants.

Prusty S, Sahoo R, Nayak S, Poosapati S, Swain D Plants (Basel). 2022; 11(18).

PMID: 36145825 PMC: 9501179. DOI: 10.3390/plants11182424.

The mitochondrial LYR protein SDHAF1 is required for succinate dehydrogenase activity in Arabidopsis.

Li Y, Belt K, Alqahtani S, Saha S, Fenske R, Van Aken O Plant J. 2022; 110(2):499-512.

PMID: 35080330 PMC: 9306560. DOI: 10.1111/tpj.15684.

The Arabidopsis Proteins AtNHR2A and AtNHR2B Are Multi-Functional Proteins Integrating Plant Immunity With Other Biological Processes.

Singh R, Liyanage R, Gupta C, Lay Jr J, Pereira A, Rojas C Front Plant Sci. 2020; 11:232.

PMID: 32194606 PMC: 7064621. DOI: 10.3389/fpls.2020.00232.

An Assembly Factor Promotes Assembly of Flavinated SDH1 into the Succinate Dehydrogenase Complex.

Belt K, Van Aken O, Murcha M, Millar A, Huang S Plant Physiol. 2018; 177(4):1439-1452.

PMID: 29930107 PMC: 6084658. DOI: 10.1104/pp.18.00320.

References

Figueroa P, Holuigue L, Araya A, Jordana X . The nuclear-encoded SDH2-RPS14 precursor is proteolytically processed between SDH2 and RPS14 to generate maize mitochondrial RPS14. Biochem Biophys Res Commun. 2000; 271(2):380-5. DOI: 10.1006/bbrc.2000.2644. View

Oostveen F, Au H, Meijer P, Scheffler I . A Chinese hamster mutant cell line with a defect in the integral membrane protein CII-3 of complex II of the mitochondrial electron transport chain. J Biol Chem. 1995; 270(44):26104-8. DOI: 10.1074/jbc.270.44.26104. View

Eyal Y, Curie C, McCormick S . Pollen specificity elements reside in 30 bp of the proximal promoters of two pollen-expressed genes. Plant Cell. 1995; 7(3):373-84. PMC: 160789. DOI: 10.1105/tpc.7.3.373. View

Zabaleta E, Heiser V, Grohmann L, Brennicke A . Promoters of nuclear-encoded respiratory chain complex I genes from Arabidopsis thaliana contain a region essential for anther/pollen-specific expression. Plant J. 1998; 15(1):49-59. DOI: 10.1046/j.1365-313x.1998.00177.x. View

Roos M, Tielens A . Differential expression of two succinate dehydrogenase subunit-B genes and a transition in energy metabolism during the development of the parasitic nematode Haemonchus contortus. Mol Biochem Parasitol. 1994; 66(2):273-81. DOI: 10.1016/0166-6851(94)90154-6. View

Burger G, Lang B, Reith M, Gray M . Genes encoding the same three subunits of respiratory complex II are present in the mitochondrial DNA of two phylogenetically distant eukaryotes. Proc Natl Acad Sci U S A. 1996; 93(6):2328-32. PMC: 39795. DOI: 10.1073/pnas.93.6.2328. View

Logemann J, Schell J, Willmitzer L . Improved method for the isolation of RNA from plant tissues. Anal Biochem. 1987; 163(1):16-20. DOI: 10.1016/0003-2697(87)90086-8. View

Au H, Mascarello J, Ream-Robinson D, Scheffler I . Characterization of the human SDHC gene encoding of the integral membrane proteins of succinate-quinone oxidoreductase in mitochondria. Gene. 1998; 213(1-2):133-40. DOI: 10.1016/s0378-1119(98)00186-3. View

Claros M, Vincens P . Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem. 1996; 241(3):779-86. DOI: 10.1111/j.1432-1033.1996.00779.x. View

10.

Giege P, Knoop V, Brennicke A . Complex II subunit 4 (sdh4) homologous sequences in plant mitochondrial genomes. Curr Genet. 1998; 34(4):313-7. DOI: 10.1007/s002940050401. View

11.

Stupar R, Lilly J, Town C, Cheng Z, Kaul S, Buell C . Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats. Proc Natl Acad Sci U S A. 2001; 98(9):5099-103. PMC: 33170. DOI: 10.1073/pnas.091110398. View

12.

Ackrell B . Progress in understanding structure-function relationships in respiratory chain complex II. FEBS Lett. 2000; 466(1):1-5. DOI: 10.1016/s0014-5793(99)01749-4. View

13.

Unseld M, Marienfeld J, Brandt P, Brennicke A . The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet. 1997; 15(1):57-61. DOI: 10.1038/ng0197-57. View

14.

Figueroa P, Gomez I, Holuigue L, Araya A, Jordana X . Transfer of rps14 from the mitochondrion to the nucleus in maize implied integration within a gene encoding the iron-sulphur subunit of succinate dehydrogenase and expression by alternative splicing. Plant J. 1999; 18(6):601-9. DOI: 10.1046/j.1365-313x.1999.00485.x. View

15.

Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D . The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1998; 25(24):4876-82. PMC: 147148. DOI: 10.1093/nar/25.24.4876. View

16.

Twell D, Yamaguchi J, Wing R, Ushiba J, McCormick S . Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev. 1991; 5(3):496-507. DOI: 10.1101/gad.5.3.496. View

17.

Scheffler I . Molecular genetics of succinate:quinone oxidoreductase in eukaryotes. Prog Nucleic Acid Res Mol Biol. 1998; 60:267-315. DOI: 10.1016/s0079-6603(08)60895-8. View

18.

Oyedotun K, Lemire B . The Saccharomyces cerevisiae succinate-ubiquinone oxidoreductase. Identification of Sdh3p amino acid residues involved in ubiquinone binding. J Biol Chem. 1999; 274(34):23956-62. DOI: 10.1074/jbc.274.34.23956. View

19.

Valens M, Lemire B, Bolotin-Fukuhara M . Structure and regulation of SDH3, the yeast gene encoding the cytochrome b560 subunit of respiratory complex II. J Biol Chem. 1994; 269(22):15469-72. View

20.

Figueroa P, Leon G, Elorza A, Holuigue L, Jordana X . Three different genes encode the iron-sulfur subunit of succinate dehydrogenase in Arabidopsis thaliana. Plant Mol Biol. 2001; 46(2):241-50. DOI: 10.1023/a:1010612506070. View