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How the Nucleus and Mitochondria Communicate in Energy Production During Stress: Nuclear MtATP6, an Early-Stress Responsive Gene, Regulates the Mitochondrial F1F0-ATP Synthase Complex

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Abstract

A small number of stress-responsive genes, such as those of the mitochondrial F1F0-ATP synthase complex, are encoded by both the nucleus and mitochondria. The regulatory mechanism of these joint products is mysterious. The expression of 6-kDa subunit (MtATP6), a relatively uncharacterized nucleus-encoded subunit of F0 part, was measured during salinity stress in salt-tolerant and salt-sensitive cultivated wheat genotypes, as well as in the wild wheat genotypes, Triticum and Aegilops using qRT-PCR. The MtATP6 expression was suddenly induced 3 h after NaCl treatment in all genotypes, indicating an early inducible stress-responsive behavior. Promoter analysis showed that the MtATP6 promoter includes cis-acting elements such as ABRE, MYC, MYB, GTLs, and W-boxes, suggesting a role for this gene in abscisic acid-mediated signaling, energy metabolism, and stress response. It seems that 6-kDa subunit, as an early response gene and nuclear regulatory factor, translocates to mitochondria and completes the F1F0-ATP synthase complex to enhance ATP production and maintain ion homeostasis under stress conditions. These communications between nucleus and mitochondria are required for inducing mitochondrial responses to stress pathways. Dual targeting of 6-kDa subunit may comprise as a mean of inter-organelle communication and save energy for the cell. Interestingly, MtATP6 showed higher and longer expression in the salt-tolerant wheat and the wild genotypes compared to the salt-sensitive genotype. Apparently, salt-sensitive genotypes have lower ATP production efficiency and weaker energy management than wild genotypes; a stress tolerance mechanism that has not been transferred to cultivated genotypes.

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Abbreviations

MtATP6:

Mitochondrial F1F0-ATP synthase 6-kDa subunit

qRT-PCR:

Quantitative reverse transcriptase polymerase chain reaction

ABA:

Abscisic acid

AREB/ABF:

ABA-responsive element binding/ABA-responsive element binding factor

ABRE:

Abscisic acid response element

MYC:

Myelocytomatosis oncogene cellular homolog

MYB:

Myeloblastosis viral oncogene homolog

W-boxes:

WRKY-binding sites

CT :

Cycle threshold

HKT:

High affinity potassium transporter

SOS:

Salt overly sensitive

DRE:

Dehydration-responsive element

GTLs:

GT-element-binding proteins

CBF/DREB:

C-repeat binding factor/Dehydration-responsive element binding protein

AP2:

Apetala 2

ROS:

Reactive oxygen species

AOX:

Alternative oxidase

ABI4:

Abscisic acid insensitive 4

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Acknowledgments

The authors would like to thank the Institute of Biotechnology for supporting this research and the Bioinformatics Research Group in the College of Agriculture (Shiraz University). We thank Dr. Mehrabi (Ilam University) for kindly supplying seeds of wild genotypes for this study. We thank Dr. Manijeh Mohammadi Dehcheshmah for his help in performing the qRT-PCR experiments.

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Authors and Affiliations

  1. Biotechnology Institute, Shiraz University, Bajgah, 71441-65186, Shiraz, Iran

    Ali Asghar Moghadam, Ali Niazi, Mahbobeh Zamani Babgohari & Tahereh Deihimi

  2. Department of Plant Breeding, Shiraz University, Bajgah, 71441-65186, Shiraz, Iran

    Eemaeil Ebrahimie

  3. School of Molecular and Biomedical Science, The University of Adelaide, Adelaide, Australia

    Eemaeil Ebrahimie

  4. Department of Plant Protection, College of Agriculture, Shiraz University, Shiraz, Iran

    Seyed Mohsen Taghavi & Mohammad Djavaheri

  5. Department of Medical Biotechnology, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences, Shiraz, Iran

    Amin Ramezani

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  1. Ali Asghar Moghadam
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Correspondence to Eemaeil Ebrahimie.

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Moghadam, A.A., Ebrahimie, E., Taghavi, S.M. et al. How the Nucleus and Mitochondria Communicate in Energy Production During Stress: Nuclear MtATP6, an Early-Stress Responsive Gene, Regulates the Mitochondrial F1F0-ATP Synthase Complex. Mol Biotechnol 54, 756–769 (2013). https://doi.org/10.1007/s12033-012-9624-6

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