mTERF18 and ATAD3 are required for mitochondrial nucleoid structure and their disruption confers heat tolerance in Arabidopsis thaliana

2021 ◽  
Author(s):  
Minsoo Kim ◽  
Vincent Schulz ◽  
Lea Brings ◽  
Theresa Schoeller ◽  
Kristina Kühn ◽  
...  

2020 ◽  
Author(s):  
Minsoo Kim ◽  
Vincent Schulz ◽  
Lea Brings ◽  
Theresa Schoeller ◽  
Kristina Kühn ◽  
...  

AbstractMitochondria play critical roles in eukaryotes in ATP generation through oxidative phosphorylation (OXPHOS) and also produce both damaging and signaling reactive oxygen species (ROS). Originating from endosymbiosis, mitochondria have their own reduced genomes that encode essential subunits of the OXPHOS machinery. MTERF (Mitochondrial Transcription tERmination Factor-related) proteins have been shown to be involved in organelle gene expression by interacting with organellar DNA or RNA in multicellular eukaryotes. We previously identified mutations in Arabidopsis thaliana MTERF18/SHOT1 that enable plants to better tolerate heat and oxidative stresses, presumably due to low ROS and reduced oxidative damage. To understand molecular mechanisms leading to shot1 phenotypes, we investigated mitochondrial defects of shot1 mutants and targets of the SHOT1 protein. shot1 mutants have problems accumulating OXPHOS complexes that contain mitochondria-encoded subunits, with complex I and complex IV most affected. SHOT1 binds specific mitochondrial DNA sequences and localizes to mitochondrial nucleoids, which are diffuse in shot1 mutants. Furthermore, three homologues of mammalian ATAD3A proteins, which are suggested to be involved in mitochondrial nucleoid organization, were identified as SHOT1-interacting proteins (designated SHOT1 BINDING ATPASES (SBA)1, 2 and 3). Importantly, disrupting SBA function also disrupts nucleoids, compromises accumulation of complex I and enhances heat tolerance. We conclude that proper nucleoid organization is critical for correct expression and accumulation of complex I, and propose that nucleoid disruption results in unique changes in mitochondrial metabolism and signaling that lead to heat tolerance.SignificanceIn all eukaryotes, mitochondria are critical organelles that supply chemical energy for life, which is produced by the oxidative phosphorylation (OXPHOS) machinery on the inner mitochondrial membrane. The OXPHOS machinery comprises multiple protein complexes with subunits encoded by both nuclear and mitochondrial genes. Nuclear-encoded mTERF proteins are important for expression of mitochondrial genes, interacting with mitochondrial DNA or RNA. Our study reveals that the Arabidopsis mTERF18/SHOT1 protein interacts with mtDNA and homologs of human ATAD3A proteins, and that both proteins are critical for mitochondrial nucleoid organization and accumulation of OXPHOS Complex I. Further, the data indicate nucleoid disruption leads to unique mitochondrial and cellular responses such that mutant plants have enhanced heat tolerance.



2020 ◽  
Vol 103 (6) ◽  
pp. 2069-2083 ◽  
Author(s):  
Lalit D. Tiwari ◽  
Lisha Khungar ◽  
Anil Grover


1999 ◽  
Vol 145 (2) ◽  
pp. 291-304 ◽  
Author(s):  
Shelly Meeusen ◽  
Quinton Tieu ◽  
Edith Wong ◽  
Eric Weiss ◽  
David Schieltz ◽  
...  

Maintenance of mitochondrial DNA (mtDNA) during cell division is required for progeny to be respiratory competent. Maintenance involves the replication, repair, assembly, segregation, and partitioning of the mitochondrial nucleoid. MGM101 has been identified as a gene essential for mtDNA maintenance in S. cerevisiae, but its role is unknown. Using liquid chromatography coupled with tandem mass spectrometry, we identified Mgm101p as a component of highly enriched nucleoids, suggesting that it plays a nucleoid-specific role in maintenance. Subcellular fractionation, indirect immunofluorescence and GFP tagging show that Mgm101p is exclusively associated with the mitochondrial nucleoid structure in cells. Furthermore, DNA affinity chromatography of nucleoid extracts indicates that Mgm101p binds to DNA, suggesting that its nucleoid localization is in part due to this activity. Phenotypic analysis of cells containing a temperature sensitive mgm101 allele suggests that Mgm101p is not involved in mtDNA packaging, segregation, partitioning or required for ongoing mtDNA replication. We examined Mgm101p's role in mtDNA repair. As compared with wild-type cells, mgm101 cells were more sensitive to mtDNA damage induced by UV irradiation and were hypersensitive to mtDNA damage induced by gamma rays and H2O2 treatment. Thus, we propose that Mgm101p performs an essential function in the repair of oxidatively damaged mtDNA that is required for the maintenance of the mitochondrial genome.



2020 ◽  
Vol 20 (1) ◽  
Author(s):  
Yuliang Liu ◽  
Xinye Liu ◽  
Xue Wang ◽  
Kang Gao ◽  
Weiwei Qi ◽  
...  

Abstract Background As global warming becomes increasingly severe, it is urgent that we enhance the heat tolerance of crops. We previously reported that Arabidopsis thaliana PHOSPHOINOSITIDE-SPECIFIC PHOSPHOLIPASE C9 (AtPLC9) promotes heat tolerance. Results In this study, we ectopically expressed AtPLC9 in rice to examine its potential to improve heat tolerance in this important crop. Whereas AtPLC9 did not improve rice tolerance to salt, drought or cold, transgenic rice did exhibit greater heat tolerance than the wild type. High-throughput RNA-seq revealed extensive and dynamic transcriptome reprofiling in transgenic plants after heat stress. Moreover, the expression of some transcription factors and calcium ion-related genes showed specific upregulation in transgenic rice after heat stress, which might contribute to the enhanced heat tolerance. Conclusions This study provides preliminary guidance for using AtPLC9 to improve heat tolerance in cereal crops and, more broadly, highlights that heterologous transformation can assist with molecular breeding.



2015 ◽  
Vol 59 (2) ◽  
pp. 305-315 ◽  
Author(s):  
C. M. Chiang ◽  
H. L. Chien ◽  
L. F. O. Chen ◽  
T. C. Hsiung ◽  
M. C. Chiang ◽  
...  


2014 ◽  
Vol 36 (6) ◽  
pp. 1555-1564 ◽  
Author(s):  
Lu Zhang ◽  
Qixiang Zhang ◽  
Yike Gao ◽  
Huitang Pan ◽  
Shaochuan Shi ◽  
...  


Biology Open ◽  
2021 ◽  
Vol 10 (6) ◽  
Author(s):  
Li-jie Wang ◽  
Tian Hsu ◽  
Hsiang-ling Lin ◽  
Chi-yu Fu

ABSTRACT Mitochondrial DNA (mtDNA) encodes gene products that are essential for oxidative phosphorylation. They organize as higher order nucleoid structures (mtNucleoids) that were shown to be critical for the maintenance of mtDNA stability and integrity. While mtNucleoid structures are associated with cellular health, how they change in situ under physiological maturation and aging requires further investigation. In this study, we investigated the mtNucleoid assembly at an ultrastructural level in situ using the TFAM-Apex2 Drosophila model. We found that smaller and more compact TFAM-nucleoids are populated in the mitochondria of indirect flight muscle of aged flies. Furthermore, mtDNA transcription and replication were cross-regulated in the mtTFB2-knockdown flies as in the mtRNAPol-knockdown flies that resulted in reductions in mtDNA copy numbers and nucleoid-associated TFAM. Overall, our study reveals that the modulation of TFAM-nucleoid structure under physiological aging, which is critically regulated by mtDNA content.



2012 ◽  
Vol 18 (S2) ◽  
pp. 674-675
Author(s):  
B.G. Kopek ◽  
G. Shtengel ◽  
C. Xu ◽  
T. Brown ◽  
A. Tkachuk ◽  
...  

Extended abstract of a paper presented at Microscopy and Microanalysis 2012 in Phoenix, Arizona, USA, July 29 – August 2, 2012.



2021 ◽  
Vol 534 ◽  
pp. 747-751
Author(s):  
Masaaki Ono ◽  
Kazuho Isono ◽  
Yoichi Sakata ◽  
Teruaki Taji


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