Differential Expression of Alternative Oxidase Genes in Maize Mitochondrial Mutants

Abstract

We have examined the expression of three alternative oxidase ( aox ) genes in two types of maize mitochondrial mutants. Nonchromosomal stripe (NCS) mutants carry mitochondrial DNA deletions that affect subunits of respiratory complexes and show constitutively defective growth. Cytoplasmic male-sterile (CMS) mutants have mitochondrial DNA rearrangements, but they are impaired for mitochondrial function only during anther development. In contrast to normal plants, which have very low levels of AOX, NCS mutants exhibit high expression of aox genes in all nonphotosynthetic tissues tested. The expression pattern is specific for each type of mitochondrial lesion: the NADH dehydrogenase-defective NCS2 mutant has high expression of aox2 , whereas the cytochrome oxidase-defective NCS6 mutant predominantly expresses aox3 . Similarly, aox2 and aox3 can be induced differentially in normal maize seedlings by specific inhibitors of these two respiratory complexes. Translation-defective NCS4 plants show induction of both aox2 and aox3 . AOX2 and AOX3 proteins differ in their ability to be regulated by reversible dimerization. CMS mutants show relatively high levels of aox2 mRNAs in young tassels but none in ear shoots. Significant expression of aox1 is detected only in NCS and CMS tassels. The induction pattern of maize aox genes could serve as a selective marker for diverse mitochondrial defects.

The Pentatricopeptide Repeat GeneOTP43Is Required fortrans-Splicing of the Mitochondrialnad1Intron 1 inArabidopsis thaliana

“…The mutant sectors have no Complex I activity but a partially assembled Complex I (Karpova and Newton, 1999). As observed in the CMSII mutant, the amount of AOX is increased in NCS2 sectors (Karpova et al, 2002). Both of these mutants resemble otp43 in that they lack a mitochondrially encoded subunit of Complex I, leading to a partial or complete loss of the complex and a complete loss of activity.…”

“…The previously described Nicotiana and maize mutants lacking Complex I had elevated levels of alternative oxidase (AOX) (Karpova et al, 2002;Dutilleul et al, 2003b). To check whether this Arabidopsis mutant has the same phenotype, we performed quantitative RT-PCR assays for transcripts coding for alternative respiratory pathway proteins, namely, the alternative external (NDB1-4) and internal (NDA1-2 and NDC1) NAD(P)H dehydrogenases and the AOX isoforms AOX1a-c and AOX2 ( Figure 5A).…”

Mitochondrial Reactive Oxygen Species. Contribution to Oxidative Stress and Interorganellar Signaling

“…In addition to sharing downstream, PCD-related mitochondrial events, inhibition of the mtETC by chemicals or by mutation and inhibition by pathogen challenge share similar gene induction profiles, evidence of similar MRR signaling occurring in each of these cases. Nuclear genes induced by harpin overlap with nuclear genes induced by disruption of the mtETC by mitochondrial mutants (Karpova et al, 2002;Krause and Durner, 2004;Kuzmin et al, 2004). In addition, the profile of the whole transcriptome response to AA is most similar to the transcriptome responses to pathogen attack (Yu et al, 2001 (Subbaiah et al, 1998, and refs.…”

“…Although not directly demonstrated in these examples, there is evidence for the importance of mtROS in plant MRR. Inhibition of the cytochrome pathway by AA results in production of mtROS (Maxwell et al, 1999;Yao et al, 2002) and altered nuclear gene expression (Saisho et al, 1997;Yu et al, 2001;Karpova et al, 2002;Maxwell et al, 2002). The direct involvement of mtROS in MRR in plants is strongly suggested by the dramatic reduction of AAinitiated gene induction observed when antioxidants are added prior to AA (Maxwell et al, 1999).…”

“…Altered nuclear gene expression is part of this new homeostasis. Mutants exhibit altered expression of genes encoding AOXs, heat shock proteins, and antioxidant enzymes (Karpova et al, 2002;Dutilleul et al, 2003;Kuzmin et al, 2004). Thus, permanent alteration of mtETC function results in constitutively altered nuclear gene expression.…”