Functional Specialization of Maize Mitochondrial Aldehyde Dehydrogenases

Abstract

The maize (Zea mays) rf2a and rf2b genes both encode homotetrameric aldehyde dehydrogenases (ALDHs). The RF2A protein was shown previously to accumulate in the mitochondria. In vitro import experiments and ALDH assays on mitochondrial extracts from rf2a mutant plants established that the RF2B protein also accumulates in the mitochondria. RNA gel-blot analyses and immunohistolocation experiments revealed that these two proteins have only partially redundant expression patterns in organs and cell types. For example, RF2A, but not RF2B, accumulates to high levels in the tapetal cells of anthers. Kinetic analyses established that RF2A and RF2B have quite different substrate specificities; although RF2A can oxidize a broad range of aldehydes, including aliphatic aldehydes and aromatic aldehydes, RF2B can oxidize only short-chain aliphatic aldehydes. These two enzymes also have different pH optima and responses to changes in substrate concentration. In addition, RF2A, but not RF2B or any other natural ALDHs, exhibits positive cooperativity. These functional specializations may explain why many species have two mitochondrial ALDHs. This study provides data that serve as a basis for identifying the physiological pathway by which the rf2a gene participates in normal anther development and the restoration of Texas cytoplasm-based male sterility. For example, the observations that Texas cytoplasm anthers do not accumulate elevated levels of reactive oxygen species or lipid peroxidation and the kinetic features of RF2A make it unlikely that rf2a restores fertility by preventing premature programmed cell death.Aldehyde dehydrogenases (ALDHs) oxidize aldehydes to the corresponding carboxylic acid and simultaneously reduce NAD ϩ and/or NADP ϩ . Over 300 ALDH genes have been identified from mammals, insects, bacteria, yeast, and plants (Sophos et al., 2001). The nomenclature of the ALDH super gene family was recently revised taking into account the evolutionary distances among the proteins encoded by these genes (Sophos et al., 2001). Family 1 ALDHs include the original Class 1 ALDHs, which are targeted to the cytosol. Family 2 consists of the Class 2 ALDHs, which are targeted to the mitochondria. In mammals and yeast, at least one role of Family 1 and 2 ALDHs is the detoxification of ethanol-derived acetaldehyde (Wang et al., 1998). Family 3 ALDHs of mammals are involved in the detoxification of aldehydes that form during lipid peroxidation (Lindahl and Petersen, 1991). Some of the Family 3 ALDHs are, in addition, expressed in tumors (Satomichi et al., 2000), where they are thought to be involved in antitumor drug resistance (Sladek, 1988). Other roles of ALDHs include vitamin A biosynthesis (Hind et al., 2002) and amino acid metabolism (Davies, 1959; Styrvold et al., 1986; Ferrandez et al., 1997). In bacteria, ALDHs are, in addition, involved in the metabolism of rare sugars (Boronat et al., 1983). In insects, ALDHs are involved in both the detoxification of aldehydes and the biosynthesis of pheromones (Morse and Meigh...

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