AtOMA1 Affects the OXPHOS System and Plant Growth in Contrast to Other Newly Identified ATP-Independent Proteases in Arabidopsis Mitochondria

Abstract

Compared with yeast, our knowledge on members of the ATP-independent plant mitochondrial proteolytic machinery is rather poor. In the present study, using confocal microscopy and immunoblotting, we proved that homologs of yeast Oma1, Atp23, Imp1, Imp2, and Oct1 proteases are localized in Arabidopsis mitochondria. We characterized these components of the ATP-independent proteolytic system as well as the earlier identified protease, AtICP55, with an emphasis on their significance in plant growth and functionality in the OXPHOS system. A functional complementation assay demonstrated that out of all the analyzed proteases, only AtOMA1 and AtICP55 could substitute for a lack of their yeast counterparts. We did not observe any significant developmental or morphological changes in plants lacking the studied proteases, either under optimal growth conditions or after exposure to stress, with the only exception being retarded root growth in oma1-1, thus implying that the absence of a single mitochondrial ATP-independent protease is not critical for Arabidopsis growth and development. We did not find any evidence indicating a clear functional complementation of the missing protease by any other protease at the transcript or protein level. Studies on the impact of the analyzed proteases on mitochondrial bioenergetic function revealed that out of all the studied mutants, only oma1-1 showed differences in activities and amounts of OXPHOS proteins. Among all the OXPHOS disorders found in oma1-1, the complex V deficiency is distinctive because it is mainly associated with decreased catalytic activity and not correlated with complex abundance, which has been observed in the case of supercomplex I + III2 and complex I deficiencies. Altogether, our study indicates that despite the presence of highly conservative homologs, the mitochondrial ATP-independent proteolytic system is not functionally conserved in plants as compared with yeast. Our findings also highlight the importance of AtOMA1 in maintenance of proper function of the OXPHOS system as well as in growth and development of Arabidopsis thaliana.

What Does the Molecular Genetics of Different Types of Restorer-of-Fertility Genes Imply?

“…The occurrence of multiple Oma1 homologues in the sugar beet genome contrasts with Arabidopsis and rice, both of which have a single Oma1 copy as is also the case for yeast and humans [41]. An Arabidopsis plant with a defect in atOma1 is viable but has malfunctioning oxidative phosphorylation [75]. A comparison of the proteins' ability to bind with preSATP6 and the expression pattern among RF1-Oma1, bvOma1 and atOma1 is summarized in Table 2; neither bvOma1 nor atOma1 had binding activity with preSATP6 protein [56].…”

Molecular Biomarkers of the Mitochondrial Quality Control Are Differently Affected by Hypoxia-Reoxygenation Stress in Marine Bivalves Crassostrea gigas and Mytilus edulis

“…Furthermore, OMA1 mediates an ATP-independent proteolytic breakdown of misfolded inner membrane proteins and is complementary to the action of m-AAA proteases (Käser et al, 2003). OMA1 activity is strongly upregulated in response to various stresses in metazoans, plants and yeast (Bohovych et al, 2014;Rainbolt et al, 2015;Migdal et al, 2017) and is required for stabilization of the mitochondrial respiratory supercomplexes and maintenance of the mitochondrial respiration (Bohovych et al, 2015;Richter et al, 2015). Therefore, transcriptional upregulation of oma1 during H/R stress in the mussels might assist in the degradation of the damaged mitochondrial proteins and protection of the mitochondrial integrity and function.…”

How did a duplicated gene copy evolve into arestorer-of-fertilitygene in a plant? The case ofOma1

“…The expression patterns of bvOma1 , RF1-Oma1 and atOma1 were compared. We considered atOma1 to be an outgroup Oma1 for the beet Oma1 -like genes, because atOma1 is the only Oma1 homologue in Arabidopsis, and it can complement the deficiency of yeast Oma1 [23]. Web-retrieved microarray-based expression data of atOma1 indicated the detection of atOma1 mRNA from almost all organ/tissues, whereas increased expression was seen in young stamens, mature pollen, immature seeds and dry seeds (expression levels 2–9 times that of root) (electronic supplementary material, figure S5).…”

“…The Oma1 -like genes form a small gene family in beets, unlike in the model plants Arabidopsis and rice [15,23]. Gene duplication is the most likely mechanism to explain the generation of this gene family.…”