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Arabidopsis AtMPV17, a homolog of mice MPV17, enhances osmotic stress tolerance

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Abstract

Mutation in the human MPV17 gene or the functional yeast orthologue SYM1 result in mitochondrial DNA depletion. MPV17 homologs are also found in plants including Arabidopsis, but the function of these genes remain unclear. Arabidopsis genome contains 10 MPV17 homologs. Among these, the AtMPV17 protein was localized in mitochondria as MPV17 and SYM1. The yeast sym1 knock out mutant cannot grow on ethanol-containing medium at 37 °C. AtMPV17 complements the ethanol growth defection of sym1 yeast MPV17 ortholog cells at 37 °C, suggesting that AtMPV17 is a functional ortholog of SYM1. AtMPV17 knock out mutant, atmpv17 show similar growth and seed development to those of the wild-type plant on normal growth condition. However, atmpv17 mutant is more sensitive to ABA and mannitol during germination and seedling growth than wild type plants. Growth retardation of the atmpv17 knock out mutant on medium containing ABA and mannitol is complemented by AtMPV17 overexpression. These results suggest that the AtMPV17 contributes to osmotic stress tolerance in plants.

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References

  • Alonzo JR, Venkataraman CV, Field MS, Stover PJ (2018) The mitochondrial inner membrane protein MPV17 prevents uracil accumulation in mitochondrial DNA. J Biol Chem. https://doi.org/10.1074/jbc.RA118.004788

    Article  PubMed  PubMed Central  Google Scholar 

  • Antonenkov V, Isomursu A, Mennerich D, Vapola MH, Weiher H, Kietzmann T, Hiltunen JK (2015) The human mitochondria DNA depletion syndrome gene MPV17 encodes a non-selective channel that modulates membrane potential. J Biol Chem 290:13840–13861

    Article  CAS  Google Scholar 

  • Binder CJ, Weiher H, Exner M, Kerjaschki D (1999) Glomerular overproduction of oxgen radicals in MPV17 gene-inactivated mice causes podocyte foot process flattening and proteinuria. Am J Pathol 154:1067–1075

    Article  CAS  Google Scholar 

  • Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867

    Article  CAS  Google Scholar 

  • Dallabona C, Marsano RM, Arzuffi P, Ghezzi D, Mancini P, Zeviani M, Ferrero I, Donnini C (2010) SYM1, the yeast ortholog of the MPV17 human disease protein, is a stress induced bioenergetic and morphogenetic mitochondrial modulator. Hum Mol Genet 19:1098–1107

    Article  CAS  Google Scholar 

  • Ha YI, Lim JM, Ko SM, Liu JR, Choi DW (2007) A ginseng-specific abundant protein (GSAP) located on the cell wall is involved in abiotic stress tolerance. Gene 386:115–122

    Article  CAS  Google Scholar 

  • Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438

    Article  CAS  Google Scholar 

  • Im S, Lee HN, Jung HS, Yang S, Park EJ, Hwang MS, Jeong WJ, Choi DW (2017) Transcriptome based identification of the desiccation response genes in marine red algae Pyropia tenera (Rhodophyta) and enhancement of abiotic stress tolerance by PtDRG2 in Chlamydomonas. Mar Biotechnol 19:232–245

    Article  CAS  Google Scholar 

  • Karasawa M, Zwacka RM, Reuter A, Fink T, Hsieh CL, Lichter P, Francke U, Weiher H (1993) The human homolog of the glomerulosclerosis gene MPV17: structure and genomic organization. Hum Mol Genet 2:1829–1834

    Article  CAS  Google Scholar 

  • Krauss J, Astrinides P, Frohnhofer HG, Walderich B, Nusslein-Volhard C (2013) Transparent, a gene affecting stripe formation in Zebrafish, encodes the mitochondrial protein MPV17 that is required for iridophore survival. Biol Open 2:703–710

    Article  Google Scholar 

  • Lee YJ, Kim DH, Kim YW, Hwang I (2001) Identification of a signal that distinguishes between the chloroplast outer envelope membrane and the endomembrane system in vivo. Plant Cell 13:2175–2190

    Article  CAS  Google Scholar 

  • Lollgene S, Weiher H (2015) The role of the MPV17 protein mutations of which cause mitochondrial DNA depletion syndrome (MDDS): lessons from homologs in different species. Biol Chem 396:13–25

    Article  Google Scholar 

  • Manivasakam P, Schiest RH (1993) High efficiency transformation of Saccharomyces cerevisiae by electroporation. Nucleic Acids Res 21:4414–4415

    Article  CAS  Google Scholar 

  • Moss CF, Rosa ID, Hunt LE, Yasukawa T, Young R, Jones AWE, Reddy K, Desai R, Virtue S, Elgar G, Voshol P, Yaylor MS, Holt IJ, Reijns MAM, Spinazzola A (2017) Aberrant ribonucelotide incorporation and multiple deletions in mitochondrial DNA of the murine MPV17 disease model. Nucleic Acids Res 45:12808–12815

    Article  CAS  Google Scholar 

  • Murphy MA, Phillipson A, Baker A, Mullen RT (2003) Characterization of the targeting signal of the Arabidopsis 22-kD integral peroxisomal membrane protein. Plant Physiol 133:813–828

    Article  CAS  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32:959–970

    Article  CAS  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:25–31

    Article  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Cristmann A, Grill E (2010) ABA reception and signaling. Trends Plant Sci 15:395–401

    Article  CAS  Google Scholar 

  • Reinhold R, Kruger V, Meinecke M, Schulz C, Schmidt B, Grunau SD, Guiard B, Wiedemann N, van der Laan M, Wagner R, Rehling R, Dudek J (2012) The channel-forming SYM1 protein is transported by the TIM23 complex in a presequence-independent manner. Mol Cell Biol 32:5009–5021

    Article  CAS  Google Scholar 

  • Rosa ID, Camara Y, Durigon R, Moss CF, Vidoni S, Akman G, Hunt L, Johnson MA, Grocott S, Wang L, Thorburn DR, Hirano M, Poulton J, Taylor RW, Elgar G, Marti R, Voshol P, Holt IJ, Spinazzola A (2016) MPV17 loss causes deoxynucleotide insufficiency and slow DNA replication in mitochondria. PLoS Genet 10:10. https://doi.org/10.1371/journal.pgen.1005779

    Article  CAS  Google Scholar 

  • Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–72

    Article  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  CAS  Google Scholar 

  • Shinozaki K, Uemura M, Baily-Serres J, Bray EA, Bailey-Serres J, Weretilnyk E (2015) Responses to abiotic stresses. In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Biologist, Rockville, pp 1051–1100

    Google Scholar 

  • Spinazzola A, Viscomi C, Fernandez-Vizarra E, Carrara F, D’Adamo P, Calvo S, Marsano RM, Donnini C, Weiher H, Strisciuglio P, Parini R, Sarzi E, Chan A, DiMauro S, Rotig A, Gasparini P, Ferrero I, Mootha VK, Tiranti V, Zeviani M (2006) MPV17 encodes an inner mitochondrial membrane protein and is mutated in infantile hepatic mitochondrial DNA depletion. Nat Genet 38:570–575

    Article  CAS  Google Scholar 

  • Trott A, Morano KA (2004) SYM1 is the stress-induced Saccharomyces cerevisiae ortholog of the mammalian kidney disease gene MPV17 and is required for ethanol metabolism and tolerance during heat shock. Eukaryot Cell 3:620–631

    Article  CAS  Google Scholar 

  • Tugal HB, Pool M, Baker A (1999) Arabidopsis 22-kilodalton peroxisomal membrane protein, Nucleotide sequence analysis and biochemical characterization. Plant Physiol 120:309–320

    Article  CAS  Google Scholar 

  • Weiher H, Noda T, Gray DA, Sharpe AH, Jaenisch R (1990) Transgenic mouse model of kidney disease: insertional inactivation of ubiquitously expressed gene leads to nephritic syndrome. Cell 62:425–434

    Article  CAS  Google Scholar 

  • Wi J, Park EJ, Hwang MS, Jeong WJ, Choi DW (2020) PyMPV17, a homolog of MPV17 from Pyropia yezoensis (Rhodophyta) enhances osmotic stress tolerance in Chamydomonas. Plant Mol Biol Rep 38:39–47

    Article  CAS  Google Scholar 

  • Wiese J (2014) Propionate metabolism in yeast and plants. Ph.D. thesis. Institute for Biochemistry of Plants. Heirich-Heine University, Dusseldorf. Germen

  • Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Korean Institute of Planning and Evaluation for Technology, Agriculture, Forestry and Fisheries (IPET) as a Golden Seed Project (project number 213008-05-3-SB830) and the Ministry of Oceans and Fisheries (MOF), Republic of Korea, and by Chonnam National University (Grant Number: 2017-2657).

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Correspondence to Dong-Woog Choi.

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Wi, J., Na, Y., Yang, E. et al. Arabidopsis AtMPV17, a homolog of mice MPV17, enhances osmotic stress tolerance. Physiol Mol Biol Plants 26, 1341–1348 (2020). https://doi.org/10.1007/s12298-020-00834-x

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