Mitochondrial Aldehyde Dehydrogenase Activity Is Required for Male Fertility in Maize

Abstract

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;...

A survey of the plant mitochondrial proteome in relation to development

“…2) that have a very high degree of similarity with the maize RF2 nuclear restorer protein which is required to restore male fertility in the Texas cytoplasm maize [29]. Very recently, Liu et al [30] demonstrated that RF2 is a mitochondrial aldehyde dehydrogenase. A second ALDH (called ALDH 5 in Fig.…”

Inheritance and molecular mapping of two fertility-restoring loci for Honglian gametophytic cytoplasmic male sterility in rice (Oryza sativa L.)

“…All of the CMS systems so far characterized are attributable to defects in the mitochondrial genome (Mackenzie et al 1994;Schnable and Wise 1998;Sta¨dler and Delph 2002). Fertility can be restored in CMS lines by nuclear restorer genes, termed Rf s (Budar and Pelletier 2001;Liu et al 2001). Up to now, four restorer genes have been cloned.…”

“…Up to now, four restorer genes have been cloned. The maize Rf2 gene encodes an aldehyde dehydrogenase (Cui et al 1996;Liu et al 2001) which compensates for the metabolic defect produced by the chimeric mitochondrial gene URF13 in maize T-cytoplasm. The other three Rf genes, cloned from Petunia (Bentolila et al 2002), radish (Brown et al 2003;Koizuka et al 2003) and rice (Kazama and Toriyama 2003;Komori et al 2004), all encode pentatricopeptide repeat (PPR)-containing proteins, which are targeted to mitochondria, and play a role in regulating the expression of the abnormal, CMS-associated genes at the transcriptional and/or translational level.…”

Arabidopsis thaliana chromosome III restores fertility in a cytoplasmic male-sterile Brassica napus line with A. thaliana mitochondrial DNA

“…These nuclear genes, termed restorer of fertility (Rf) genes, have been found to alter the expression of specific regions in the mitochondrial genome that are associated with CMS (Schnable and Wise 1998). The action of restorer genes have been found to involve several different mechanisms, such as copy number abundance of the CMS gene (Janska et al 1998), transcript initiation (Edqvist and Bergman 2002), maturation of transcripts (Dill et al 1997;Singh et al 1996), post-transcriptional expression of the CMS gene product (Bellaoui et al 1999) or compensatory metabolic effects (Cui et al 1996;Liu et al 2001). However, the exact mode of action of the restorer genes remains to be elucidated.…”