Topological Orientation of the Membrane Protein URF13

Korth, Kenneth L.; Struck, Friedhelm; Kaspi, Cyril I.; Siedow, James N.; Levings, Charles S.

doi:10.1007/978-1-4615-3304-7_37

Cited by 12 publications

(8 citation statements)

References 23 publications

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“…URF13 is in a mixed orientation in the E. coli plasma membrane, and the amino and carboxyl termini are located on opposite sides of the membrane, consistent with a postulated three-membrane-spanning helical model (10). cms-T maize mitoplasts and submitochondrial particles (SMPs) were used to examine the membrane topology of URF13 in mitochondria.…”

mentioning

confidence: 69%

URF13, a maize mitochondrial pore-forming protein, is oligomeric and has a mixed orientation in Escherichia coli plasma membranes.

Korth

Kaspi

Siedow

et al. 1991

Proc. Natl. Acad. Sci. U.S.A.

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URF13, an inner mitochondrial membrane protein of the maize Texas male-sterile cytoplasm (cms-T), has one orientation in the inner membrane of maize mitochondria but two topological orientations in the plasma membrane when expressed in Escherichia colt. Antibodies specific for the carboxyl terminus of URF13 and for an amino-terminal tag fused to URF13 in E. colU were used to determine the location of each end of the protein following protease treatments of right-sideout and inside-out vesicles derived from cms-T mitochondria and the E. coli plasma membrane. Cross-linking studies indicate that a portion of the URF13 population in mitochondria and E. coil exists in membranes in an oligomeric state and, in combination with proteolysis studies, show that individual subunits within a given multimer have the same orientation. A three-membrane-spanning helical model for URF13 topology is presented.URF13 is a mitochondrially encoded 13-kDa protein uniquely associated with the inner mitochondrial membrane of maize carrying the Texas male-sterile cytoplasm (cms-T) (1-3). The DNA encoding URF13 (T-urfl3) arose by multiple recombinational events and contains nucleotide sequences derived from four disparate origins (4). The open reading frame is made up of sequences originating from coding and flanking regions of the mitochondrial 26S rRNA gene and a small region ofunknown origin. cms-Tmaize fails to produce viable pollen and is particularly susceptible to two fungal pathogens, Bipolaris maydis race T and Phyllosticta maydis. These pathogens caused widespread disease in the United States maize crop in 1969 and 1970 and effectively stopped the use of cms-T maize for the production of hybrid seed. Maize carrying normal cytoplasm is not seriously affected by these pathogens (reviewed in ref. 5). Isolated cms-T maize mitochondria exposed to specific toxins (T toxins) produced by these fungal pathogens exhibit swelling, inhibition of malatestimulated respiration, uncoupling of oxidative phosphorylation, and leakage of small molecules and ions (NAD+ and Ca2+). Identical effects are seen when cms-T mitochondria are exposed to methomyl, an insecticide structurally unrelated to T toxins (reviewed in ref. 6). The T toxin/URF13 interaction results in pore formation in the cms-T inner mitochondrial membrane (5).Escherichia coli expressing the cloned T-urfl3 gene product respond to T toxin or methomyl like cms-T mitochondria (7,8). This observation provides direct evidence that URF13 is responsible for susceptibility of cms-T maize to the fungal toxins. The analogous responses of cms-T maize mitochondria and E. coli to T toxins or methomyl suggest that URF13 has comparable structural and topographical properties in both membrane systems. P. maydis toxin has been shown to cooperatively bind to URF13 produced in E. coli. The binding is reversible, and T toxins and methomyl compete for the same or overlapping binding sites (9). A possible explanation for the cooperative binding is that URF13 exists in the membrane as a multimeric co...

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mentioning

confidence: 69%

URF13, a maize mitochondrial pore-forming protein, is oligomeric and has a mixed orientation in Escherichia coli plasma membranes.

Korth

Kaspi

Siedow

et al. 1991

Proc. Natl. Acad. Sci. U.S.A.

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“…The cooperativity associated with the binding of toxin to URF13 suggests that URF13 exists in an oligomeric state within the membrane (45). Indeed, cross-linking experiments indicate that a fraction of URF13 in the membrane is present as a dimer or larger species.…”

Section: Susceptibility To Fungal Pathogensmentioning

confidence: 96%

“…Because URF13 binds toxin and permeabilizes membranes in both cms-T maize mitochondria and E. coli, these membranes must have common characteristics relevant to toxin sensitivity and URF13 function during channel formation. Experiments with E. coli have suggested a preliminary model for the orientation of URF13 in the plasma membrane (45). The NH2-terminus of URF13 is located on the cytoplasmic side of the plasma membrane, whereas the COOHterminus is situated on the periplasmic side (Fig.…”

Section: Susceptibility To Fungal Pathogensmentioning

confidence: 99%

The Texas Cytoplasm of Maize: Cytoplasmic Male Sterility and Disease Susceptibility

Levings

1990

Science

250

110

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The Texas cytoplasm of maize carries two cytoplasmically inherited traits, male sterility and disease susceptibility, which have been of great interest both for basic research and plant breeding. The two traits are inseparable and are associated with an unusual mitochondrial gene, T- urf13 , which encodes a 13-kilodalton polypeptide (URF13). An interaction between fungal toxins and URF13, which results in permeabilization of the inner mitochondrial membrane, accounts for the specific susceptibility to the fungal pathogens.

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“…The genomes of T cytoplasm mitochondria contain a unique mitochondrial gene, urf13 , which encodes the URF13 protein. URF13 accumulates in the inner membrane of the mitochondria (Forde and Leaver, 1980; Dewey et al, 1986;Wise et al, 1987a;Hack et al, 1991;Korth et al, 1991;Levings and Siedow, 1992) and is believed to be responsible for both the sensitivity to T toxin and the male sterility of cms-T maize (reviewed in Levings, 1990Levings, , 1993Wise et al, 1999). The URF13 protein accumulates in many tissues of cms-T maize plants.…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial Aldehyde Dehydrogenase Activity Is Required for Male Fertility in Maize

et al. 2001

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Some plant cytoplasms express novel mitochondrial genes that cause male sterility. Nuclear genes that disrupt the accumulation of the corresponding mitochondrial gene products can restore fertility to such plants. The Texas (T) cytoplasm mitochondrial genome of maize expresses a novel protein, URF13, which is necessary for T cytoplasm-induced male sterility. Working in concert, functional alleles of two nuclear genes, rf1 and rf2 , can restore fertility to T cytoplasm plants. Rf1 alleles, but not Rf2 alleles, reduce the accumulation of URF13. Hence, Rf2 differs from typical nuclear restorers in that it does not alter the accumulation of the mitochondrial protein necessary for T cytoplasm-induced male sterility. This study established that the rf2 gene encodes a soluble protein that accumulates in the mitochondrial matrix. Three independent lines of evidence establish that the RF2 protein is an aldehyde dehydrogenase (ALDH). The finding that T cytoplasm plants that are homozygous for the rf2-R213 allele are male sterile but accumulate normal amounts of RF2 protein that lacks normal mitochondrial (mt) ALDH activity provides strong evidence that rf2 -encoded mtALDH activity is required to restore male fertility to T cytoplasm maize. Detailed genetic analyses have established that the rf2 gene also is required for anther development in normal cytoplasm maize. Hence, it appears that the rf2 gene was recruited recently to function as a nuclear restorer. ALDHs typically have very broad substrate specificities. Indeed, the RF2 protein is capable of oxidizing at least three aldehydes. Hence, the specific metabolic pathway(s) within which the rf2 -encoded mtALDH acts remains to be discovered. INTRODUCTIONMaternally inherited cytoplasmic male sterility (CMS) occurs in many plant species and is widely used to facilitate the production of hybrid seed because it eliminates the need for emasculation by hand. Mitochondrial defects account for all instances in which the nature of the lesion responsible for CMS has been identified (reviewed in Mackenzie et al., 1994;Schnable and Wise, 1998). In many species, the deleterious effects of these mitochondrial defects can be avoided or overcome by the action of nuclear genes, termed nuclear restorers. However, the specific mechanisms by which restoration can occur are only poorly understood.The male-sterile Texas (T) cytoplasm (cms-T) was used to produce ‫ف‬ 85% of U.S. hybrid maize seed until the 1970 epidemic of southern corn leaf blight (Ullstrup, 1972;Pring and Lonsdale, 1989). cms-T maize is highly sensitive to a hostselective toxin (T toxin) produced by race T of Cochliobolus heterostrophus , the causal organism of southern corn leaf blight (Hooker et al., 1970; Comstock and Scheffer, 1973; Yoder, 1973). The genomes of T cytoplasm mitochondria contain a unique mitochondrial gene, urf13 , which encodes the URF13 protein. URF13 accumulates in the inner membrane of the mitochondria (Forde and Leaver, 1980; Dewey et al., 1986;Wise et al., 1987a;Hack et al., 1991;Korth et al., 1991;...

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Topological Orientation of the Membrane Protein URF13

Cited by 12 publications

References 23 publications

URF13, a maize mitochondrial pore-forming protein, is oligomeric and has a mixed orientation in Escherichia coli plasma membranes.

URF13, a maize mitochondrial pore-forming protein, is oligomeric and has a mixed orientation in Escherichia coli plasma membranes.

The Texas Cytoplasm of Maize: Cytoplasmic Male Sterility and Disease Susceptibility

Mitochondrial Aldehyde Dehydrogenase Activity Is Required for Male Fertility in Maize

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