Mutations in the Maize Mitochondrial T-urf13 Gene Eliminate Sensitivity to a Fungal Pathotoxin

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1989 Jun 1

PMID 2660137

Citations 21

Authors

C J Braun

J N Siedow

M E Williams

C S Levings 3rd

Affiliations

Soon will be listed here.

Abstract

URF13, the product of the mitochondrial T-urf13 gene, confers on Texas cytoplasmic male-steril maize (Zea mays L.) a unique susceptibility to a fungal pathogen (Bipolaris maydis race T) and sensitivity to its pathotoxin. Expression of URF13 in Escherichia coli imparts pathotoxin sensitivity to the bacterium. We show by ion uptake studies in E. coli that a pathotoxin-URF13 interaction causes membrane permeability. Similarly, mitochondrial dysfunction caused by membrane permeabilization probably accounts for increased colonization of maize carrying the Texas cytoplasm by toxin-producing pathogens. Site-directed mutagenesis studies show that approximately one-quarter of the amino acids at the carboxyl end of URF13 can be eliminated without affecting toxin sensitivity. We have identified two dicyclohexylcarbodiimide (DCCD) binding sites in the URF13 protein and show that one of the sites is involved in conferring DCCD protection against the pathotoxin. Substitutional mutations at this DCCD binding site also eliminate toxin sensitivity.

Citing Articles

Genetic analysis of nuclear control of T-urf13/orf221 transcription in T cytoplasm maize.

Rocheford T, Kennell J, Pring D Theor Appl Genet. 2013; 84(7-8):891-8.

PMID: 24201491 DOI: 10.1007/BF00227401.

Mapping complementary genes in maize: positioning the rf1 and rf2 nuclear-fertility restorer loci of Texas (T) cytoplasm relative to RFLP and visible markers.

Wise R, Schnable P Theor Appl Genet. 2013; 88(6-7):785-95.

PMID: 24186179 DOI: 10.1007/BF01253987.

Transformation and analysis of tobacco plant var Petit havana with T-urf13 gene under anther-specific TA29 promoter.

Arun V, Kuriakose B, Sridhar V, Thomas G 3 Biotech. 2012; 1(2):73-82.

PMID: 22582148 PMC: 3339608. DOI: 10.1007/s13205-011-0008-6.

Identification of cytoplasmic ancestor gene-pools of Musa acuminata Colla and Musa balbisiana Colla and their hybrids by chloroplast and mitochondrial haplotyping.

Boonruangrod R, Desai D, Fluch S, Berenyi M, Burg K Theor Appl Genet. 2008; 118(1):43-55.

PMID: 18762903 DOI: 10.1007/s00122-008-0875-3.

T-URF 13 Protein from Mitochondria of Texas Male-Sterile Maize (Zea mays L.) : Its Purification and Submitochondrial Localization, and Immunogold Labeling in Anther Tapetum during Microsporogenesis.

Hack E, Lin C, Yang H, Horner H Plant Physiol. 1991; 95(3):861-70.

PMID: 16668065 PMC: 1077617. DOI: 10.1104/pp.95.3.861.

References

Holden M, Sze H . Helminthosporium maydis T Toxin Increased Membrane Permeability to Ca in Susceptible Corn Mitochondria. Plant Physiol. 1984; 75(1):235-7. PMC: 1066870. DOI: 10.1104/pp.75.1.235. View

Fox T, Leaver C . The Zea mays mitochondrial gene coding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell. 1981; 26(3 Pt 1):315-23. DOI: 10.1016/0092-8674(81)90200-2. View

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

Berville A, Ghazi A, Charbonnier M, Bonavent J . Effects of Methomyl and Helminthosporium maydis Toxin on Matrix Volume, Proton Motive Force, and NAD Accumulation in Maize (Zea mays L.) Mitochondria. Plant Physiol. 1984; 76(2):508-17. PMC: 1064318. DOI: 10.1104/pp.76.2.508. View

Dewey R, Timothy D, Levings C . A mitochondrial protein associated with cytoplasmic male sterility in the T cytoplasm of maize. Proc Natl Acad Sci U S A. 1987; 84(15):5374-8. PMC: 298858. DOI: 10.1073/pnas.84.15.5374. View

Sussman M, Strickler J, Hager K, SLAYMAN C . Location of a dicyclohexylcarbodiimide-reactive glutamate residue in the Neurospora crassa plasma membrane H+-ATPase. J Biol Chem. 1987; 262(10):4569-73. View

KYTE J, Doolittle R . A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982; 157(1):105-32. DOI: 10.1016/0022-2836(82)90515-0. View

Remaut E, Stanssens P, Fiers W . Plasmid vectors for high-efficiency expression controlled by the PL promoter of coliphage lambda. Gene. 1981; 15(1):81-93. DOI: 10.1016/0378-1119(81)90106-2. View

Koeppe D, COX J, Malone C . Mitochondrial heredity: a determinant in the toxic response of maize to the insecticide methomyl. Science. 1978; 201(4362):1227-9. DOI: 10.1126/science.201.4362.1227. View

10.

Laughnan J, Gabay-Laughnan S . Cytoplasmic male sterility in maize. Annu Rev Genet. 1983; 17:27-48. DOI: 10.1146/annurev.ge.17.120183.000331. View

11.

Wise R, Pring D, Gengenbach B . Mutation to male fertility and toxin insensitivity in Texas (T)-cytoplasm maize is associated with a frameshift in a mitochondrial open reading frame. Proc Natl Acad Sci U S A. 1987; 84(9):2858-62. PMC: 304759. DOI: 10.1073/pnas.84.9.2858. View

12.

Towbin H, Staehelin T, Gordon J . Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979; 76(9):4350-4. PMC: 411572. DOI: 10.1073/pnas.76.9.4350. View

13.

Kunkel T . Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985; 82(2):488-92. PMC: 397064. DOI: 10.1073/pnas.82.2.488. View

14.

Dewey R, Levings 3rd C, Timothy D . Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell. 1986; 44(3):439-49. DOI: 10.1016/0092-8674(86)90465-4. View

15.

SANGER F, Nicklen S, Coulson A . DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977; 74(12):5463-7. PMC: 431765. DOI: 10.1073/pnas.74.12.5463. View

16.

Holden M, Sze H . Dissipation of the Membrane Potential in Susceptible Corn Mitochondria by the Toxin of Helminthosporium maydis, Race T, and Toxin Analogs. Plant Physiol. 1987; 84(3):670-6. PMC: 1056648. DOI: 10.1104/pp.84.3.670. View

17.

Klein R, Koeppe D . Mode of Methomyl and Bipolaris maydis (race T) Toxin in Uncoupling Texas Male-Sterile Cytoplasm Corn Mitochondria. Plant Physiol. 1985; 77(4):912-6. PMC: 1064630. DOI: 10.1104/pp.77.4.912. View

18.

Schneider E, Altendorf K . Proton-conducting portion (F0) from Escherichia coli ATP synthase: preparation, dissociation into subunits, and reconstitution of an active complex. Methods Enzymol. 1986; 126:569-78. DOI: 10.1016/s0076-6879(86)26059-0. View

19.

Engelman D, Steitz T, Goldman A . Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu Rev Biophys Biophys Chem. 1986; 15:321-53. DOI: 10.1146/annurev.bb.15.060186.001541. View

20.

Dewey R, Siedow J, Timothy D, Levings 3rd C . A 13-kilodalton maize mitochondrial protein in E. coli confers sensitivity to Bipolaris maydis toxin. Science. 1988; 239(4837):293-5. DOI: 10.1126/science.3276005. View