Abstract
In eukaryotes, mitochondrion is an essential organelle which is surrounded by a double membrane system, including the outer membrane, intermembrane space and the inner membrane. The translocase of the outer mitochondrial membrane (TOM) complex has attracted enormous interest for its role in importing the preprotein from the cytoplasm into the mitochondrion. However, little is understood about the potential biological function of the TOM complex in Arabidopsis. The aim of the present study was to investigate how AtTOM40, a gene encoding the core subunit of the TOM complex, works in Arabidopsis. As a result, we found that lack of AtTOM40 disturbed embryo development and its pattern formation after the globular embryo stage, and finally caused albino ovules and seed abortion at the ratio of a quarter in the homozygous tom40 plants. Further investigation demonstrated that AtTOM40 is wildly expressed in different tissues, especially in cotyledons primordium during Arabidopsis embryogenesis. Moreover, we confirmed that the encoded protein AtTOM40 is localized in mitochondrion, and the observation of the ultrastructure revealed that mitochondrion biogenesis was impaired in tom40-1 embryo cells. Quantitative real-time PCR was utilized to determine the expression of genes encoding outer mitochondrial membrane proteins in the homozygous tom40-1 mutant embryos, including the genes known to be involved in import, assembly and transport of mitochondrial proteins, and the results demonstrated that most of the gene expressions were abnormal. Similarly, the expression of genes relevant to embryo development and pattern formation, such as SAM (shoot apical meristem), cotyledon, vascular primordium and hypophysis, was also affected in homozygous tom40-1 mutant embryos. Taken together, we draw the conclusion that the AtTOM40 gene is essential for the normal structure of the mitochondrion, and participates in early embryo development and pattern formation through maintaining the biogenesis of mitochondria. The findings of this study may provide new insight into the biological function of the TOM40 subunit in higher plants.
Highlights
In the past decades, it has been widely studied that the process of embryogenesis in Arabidopsis is highly programmed and controlled by an intricate network of gene expression
The three-dimensional structure of TOM40 was constructed in Arabidopsis thaliana, Saccharomyces cerevisiae and Oryza sativa, the predicted 3D structure demonstrated the similar 19-stranded β-barrel, which forms the characteristic protein-conducting channel (Figures 1B–E)
The results demonstrate that AtTOM40 localizes in mitochondria and the lack of it impedes the proper biogenesis of mitochondria, suggesting the critical role of AtTOM40 in maintaining mitochondrial function in Arabidopsis
Summary
It has been widely studied that the process of embryogenesis in Arabidopsis is highly programmed and controlled by an intricate network of gene expression (ten Hove et al, 2015). TOM40 is a ∼40 kD pore protein that comprises a membrane-inserted, 19-stranded β-barrel domain with three α-helical domains at the N terminus and C terminus (Künkele et al, 1998; Hill et al, 1998; Lackey et al, 2014; Kuszak et al, 2015). These structures form the function area of TOM40 as the major entry gate for the mitochondrial preproteins. To characterize the properties of individual Tom, single molecule tracking technique was utilized to trace individual Tom molecules in yeast, and the results demonstrated that Tom movement in the outer mitochondrial membrane is highly dynamic but confined in nature, suggesting anchoring of the TOM complex as a whole (Kuzmenko et al, 2011)
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