A protein binding site in the M mitochondrial genome of Mytilus galloprovincialis may be responsible for its paternal transmission

Gene

Volumn 562, Issue 1, 2015, Pages 83-94

  Kyriakou, Eleni ^a   Kravariti, Lara ^a   Vasilopoulos, Themistoklis ^a   Zouros, Eleftherios ^b   Rodakis, George C ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

Author keywords

doubly uniparental inheritance; Mytilus; Nuclear protein mtDNA binding; Perinuclear mitochondria

Indexed keywords

ADENINE; MITOCHONDRIAL DNA; NUCLEAR PROTEIN; PROTEIN BINDING;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL NUCLEUS; COMPLEX FORMATION; CONTROLLED STUDY; FEMALE; GEL MOBILITY SHIFT ASSAY; GONAD; MALE; MITOCHONDRIAL GENOME; MYTILUS GALLOPROVINCIALIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN INTERACTION; SEQUENCE ANALYSIS; SPERMATOGENESIS; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; INHERITANCE; METABOLISM; MITOCHONDRION; MOLECULAR GENETICS; MYTILUS; NUCLEOTIDE SEQUENCE; OOCYTE; OVARY; REGULATORY SEQUENCE; SPERMATOZOON; TESTIS;

BIVALVIA; MYTILUS; MYTILUS GALLOPROVINCIALIS;

ANIMALS; BASE SEQUENCE; DNA, MITOCHONDRIAL; FEMALE; GENOME, MITOCHONDRIAL; INHERITANCE PATTERNS; MALE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MYTILUS; OVARY; OVUM; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; SPERMATOGENESIS; SPERMATOZOA; TESTIS;

EID: 84925182995     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2015.02.047     Document Type: Article

References (66)

1. Al Rawi S., Louvet-Vallée S., Djeddi A., Sachse M., Culetto E., Hajjar C., Boyd L., Legouis R., Galy V. Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 2011, 334:1144-1147.
2. Bradford M.M. A rapid and sensitive for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
3. Breton S., Doucet-Beaupre H., Stewart D.T., Piontkivska H., Karmakar M., Bogan A.E., Hoeh W.R. Comparative mitochondrial genomics of freshwater mussels (Bivalvia: Unionoids) with doubly uniparental inheritance of mtDNA: gender-specific open reading frames and putative origins of replication. Genetics 2009, 183:1575-1589.
4. Breton S., Ghiselli F., Passamonti M., Milani L., Stewart D.T., Hoeh W.R. Evidence for a fourteenth mtDNA-encoded protein in the female-transmitted mtDNA of marine mussels (Bivalvia: Mytilidae). PLoS One 2011, 6:e19365.
5. Burzyński A. Two events are responsible for an insertion in a paternally inherited mitochondrial genome of the mussel Mytilus galloprovincialis. Genetics 2007, 175:959-962.
6. Burzyński A., Zbawicka M., Skibinski D.O.F., Wenne R. Evidence for recombination in the marine mussel Mytilus trossulus from the Baltic. Mol. Biol. Evol. 2003, 20:388-392.
7. Burzyński A., Zbawicka M., Skibinski D.O.F., Wenne R. Doubly uniparental inheritance is associated with high polymorphism for rearranged and recombinant control region haplotypes in Baltic Mytilus trossulus. Genetics 2006, 174:1081-1094.
8. Cao L., Kenchington E.L., Zouros E. Differential segregation patterns of sperm mitochondria in embryos of the blue mussel (Mytilus edulis). Genetics 2004, 166:883-894.
9. Cao L., Kenchington E., Zouros E., Rodakis G.C. Evidence that the large noncoding sequence is the main control region of maternally and paternally transmitted mitochondrial genomes of the marine mussel (Mytilus spp.). Genetics 2004, 167:835-850.
10. Cao L., Ort S.B., Mizi A., Pogson G., Kenchington E., Zouros E., Rodakis G.C. The control region of maternally and paternally inherited mitochondrial genomes of three species of the sea mussel genus Mytilus. Genetics 2009, 181:1045-1056.
11. Chatzoglou E., Kyriakou E., Zouros E., Rodakis G.C. The mRNAs of maternally and paternally inherited mtDNAs of the mussel Mytilus galloprovincialis: start/end points and polycistronic transcripts. Gene 2013, 520:156-165.
12. Chen X.J., Butow R.A. The organization and inheritance of the mitochondrial genome. Nat. Rev. Genet. 2005, 6:815-825.
13. Chora S., Bebianno M., Romeo M. Analysis of proteins from marine molluscs. Methods Mol. Biol. 2009, 519:197-204.
14. Cogswell A., Kenchington E.L., Zouros E. Segregation of sperm mitochondria in two and four cell embryos of the blue mussel Mytilus edulis: implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA. Genome 2006, 49:799-807.
15. Crothers D.M., Haran T.E., Nadeau J.G. Intrinsically bent DNA. J. Biol. Chem. 1990, 265:7093-7096.
16. Diz A.P., Dudley E., MacDonald B.W., Piña B., Kenchington E.L., Zouros E., Skibinski D.O. Genetic variation underlying protein expression in eggs of the marine mussel Mytilus edulis. Mol. Cell. Proteomics 2009, 8:132-144.
17. Diz A.P., Dudley E., Cogswell A., Macdonald B.W., Kenchington E.L., Zouros E., Skibinski D.O. Proteomic analysis of eggs from Mytilus edulis females differing in mitochondrial DNA transmission mode. Mol. Cell. Proteomics 2013, 12:3068-3080.
18. Douris V., Giokas S., Lecanidou R., Mylonas M., Rodakis G.C. Phylogenetic analysis of mitochondrial DNA and of morphological characters suggests a need for taxonomic re-evaluation within the Alopiinae (Gastropoda: Clausiliidae). J. Molluscan Stud. 1998, 64:81-92.
19. Ghiselli F., Milani L., Chang P.L., Hedgecock D., Davis J.P., Nuzhdin S.V., Passamonti M. De novo assembly of the manila clam Ruditapes philippinarum transcriptome provides new insights into expression bias, mitochondrial doubly uniparental inheritance and sex determination. Mol. Biol. Evol. 2012, 29:771-786.
20. Hajjar C., Sampuda K.M., Boyd L. Dual roles for ubiquitination in the processing of sperm organelles after fertilization. BMC Dev. Biol. 2014, 14:6.
21. 2+ waves in interstitial cells of Cajal-like cells of the rabbit urethra. Br. J. Pharmacol. 2010, 161:680-694.
22. Hoeh W.R., Stewart D.T., Saavedra C., Sutherland B.W., Zouros E. Phylogenetic evidence for role-reversals of gender-associated mitochondrial DNA in Mytilus (Bivalvia: Mytilidae). Mol. Biol. Evol. 1997, 14:959-967.
23. Hoffmann R.J., Boore J.L., Brown W.M. A novel mitochondrial genome organization for the blue mussel., Mytilus edulis. Genetics 1992, 131:397-412.
24. Katayama S., Matsushita O., Jung C.M., Minami J., Okabe A. Promoter upstream bent DNA activates the transcription of the Clostridium perfringens phospholipase C gene in a low temperature-dependent manner. EMBO J. 1999, 18:3442-3450.
25. Kenchington E., MacDonald B., Cao L., Tsagkarakis D., Zouros E. Genetics of mother-dependent sex ratio in blue mussels (Mytilus spp.) and implications for doubly uniparental inheritance of mitochondrial DNA. Genetics 2002, 161:1579-1588.
26. Kenchington E.L., Hamilton L., Cogswell A., Zouros E. Paternal mtDNA and maleness are co-inherited but not causally linked in Mytilid mussels. PLoS One 2009, 4:9.
27. Koo H.S., Wu H.M., Crothers D.M. DNA bending at adenine · thymine tracts. Nature 1986, 320:501-506.
28. Kyriakou E., Zouros E., Rodakis G.C. The atypical presence of the paternal mitochondrial DNA in somatic tissues of male and female individuals of the blue mussel species Mytilus galloprovincialis. BMC Res. Notes 2010, 3:222.
29. Kyriakou E., Chatzoglou E., Zouros E., Rodakis G.C. The rRNA and tRNA transcripts of maternally and paternally inherited mitochondrial DNAs of Mytilus galloprovincialis suggest presence of a "degradosome" in mussel mitochondria and necessitate the re-annotation of the l-rRNA/CR boundary. Gene 2014, 540:78-85.
30. Kyriakou E., Chatzoglou E., Rodakis G.C., Zouros E. Does the ORF in the control region of Mytilus mtDNA code for a protein product?. Gene 2014, 546:448-450.
31. Ladoukakis M.D., Zouros E. Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Mol. Biol. Evol. 2001, 18:1168-1175.
32. Ladoukakis M.D., Zouros E. Recombination in animal mitochondrial DNA: evidence from published sequences. Mol. Biol. Evol. 2001, 18:2127-2131.
33. Ladoukakis L., Saavedra C., Magoulas A., Zouros E. Mitochondrial DNA variation in a species with two mitochondrial genomes: the case of Mytilus galloprovincialis from the Atlantic, the Mediterranean and the Black Sea. Mol. Ecol. 2002, 11:755-769.
34. Lee J., Shin M.K., Ryu D.K., Kim S., Ryu W.S. Insertion and deletion mutagenesis by overlap extension PCR. Methods Mol. Biol. 2010, 634:137-146.
35. Longo F.J., Dornfeld E.J. The fine structure of spermatid differentiation in the mussel., Mytilus edulis. J. Ultrastruct. Res. 1967, 20:462-480.
36. Maxam A.M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980, 65:499-560.
37. Milani L., Ghiselli F., Maurizii M.G., Passamonti M. Doubly uniparental inheritance of mitochondria as a model system for studying germ line formation. PLoS One 2011, 6:11.
38. Milani L., Ghiselli F., Guerra D., Breton S., Rassamonti M. A comparative analysis of mitochondrial ORFans: new clues on their origin and role in species with doubly uniparental inheritance of mitochondria. Genome Biol. Evol. 2013, 5:1408-1434.
39. Milani L., Ghiselli F., Maurizii M.G., Nuzhdin S.V., Passamonti M. Paternally transmitted mitochondria express a new gene of potential viral origin. Genome Biol. Evol. 2014, 6:391-405.
40. Mizi A., Zouros E., Moschonas N., Rodakis G.C. The complete maternal and paternal mitochondrial genomes of the Mediterranean mussel Mytilus galloprovincialis: implications for the doubly uniparental inheritance mode of mtDNA. Mol. Biol. Evol. 2005, 22:952-967.
41. Mizi A., Zouros E., Rodakis G.C. Multiple events are responsible for an insertion in a paternally inherited mitochondrial genome of the mussel Mytilus galloprovincialis. Genetics 2006, 172:2695-2698.
42. Obata M., Komaru A. Specific location of sperm mitochondria in mussel Mytilus galloprovincialis zygotes stained by MitoTracker. Develop. Growth Differ. 2005, 47:255-263.
43. Obata M., Sano N., Komaru A. Different transcriptional ratios of male and female transmitted mitochondrial DNA and tissue-specific expression patterns in the blue mussel, Mytilus galloprovincialis. Develop. Growth Differ. 2011, 53:878-886.
44. Park M.K., Ashby M.C., Erdemli G., Petersen O.H., Tepikin A.V. Perinuclear, perigranular and sub-plasmalemmal mitochondria have distinct functions in the regulation of cellular calcium transport. EMBO J. 2001, 20:1863-1874.
45. Pérez-Martín J., Rojo F., de Lorenzo V. Promoters responsive to DNA bending: a common theme in prokaryotic gene expression. Microbiol. Rev. 1994, 58:268-290.
46. Quesada H., Wenne R., Skibinsi D.O.F. Interspecies transfer of female mitochondrial DNA is coupled with role-reversals and departure from neutrality in the mussel Mytilus trossulus. Mol. Biol. Evol. 1999, 16:655-665.
47. Saavedra C., Reyero M.I., Zouros E. Male-dependent doubly uniparental inheritance of mitochondrial DNA and female-dependent sex-ratio in the mussel Mytilus galloprovincialis. Genetics 1997, 145:1073-1082.
48. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: a Laboratory Manual 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
49. Sato M., Sato K. Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 2011, 334:1141-1144.
50. Skibinski D.O., Gallagher C., Beynon C.M. Mitochondrial DNA inheritance. Nature 1994, 368:817-818.
51. Skibinski D.O.F., Gallagher C., Beynon C.M. Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics 1994, 138:801-809.
52. Soltys B.J., Gupta R.S. Interrelationships of endoplasmic reticulum, mitochondria, intermediate filaments and microtubules - a quadruple fluorescence labeling study. Biochem. Cell Biol. 1992, 70:1174-1186.
53. Stewart D.T., Kenchington E.R., Singh R.K., Zouros E. Degree of selective constraint as an explanation of the different rates of evolution of gender-specific mitochondrial DNA lineages in the mussel Mytilus. Genetics 1996, 143:1349-1357.
54. Sutovsky P., Moreno R.D., Ramalho-Santos J., Dominko T., Simerly C., Schatten G. Ubiquitin tag for sperm mitochondria. Nature 1999, 402:371-372.
55. Sutovsky P., Moreno R.D., Ramalho-Santos J., Dominko T., Simerly C., Schatten G. Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol. Reprod. 2000, 63:582-590.
56. Tang H.L., Lung H.L., Wu K.C., Le A.P., Tang H.M., Fung M.C. Vimentin supports mitochondrial morphology and organization. Biochem. J. 2007, 410:141-146.
57. Theologidis I., Saavedra C., Zouros E. No evidence for absence of paternal mtDNA in male progeny from pair matings of the mussel Mytilus galloprovincialis. Genetics 2007, 176:1367-1369.
58. Venetis C., Theologidis I., Zouros E., Rodakis G.C. No evidence for presence of maternal mitochondrial DNA in the sperm of Mytilus galloprovincialis males. Proc. R. Soc. B 2006, 273:2483-2489.
59. Venetis C., Theologidis I., Zouros E., Rodakis G.C. A mitochondrial genome with a reversed transmission route in the Mediterranean mussel Mytilus galloprovincialis. Gene 2007, 406:79-90.
60. Verdonk N.H., Van Den Biggelaar J.A.M. Early development and the formation of germ layers. Development 1983, vol. 3:91-134. Academic Press, New York. N.H. Verdonk, J.A.M. van den Biggelaar, A.S. Tompa (Eds.).
61. Wenne R., Skibinski D.O.F. Mitochondrial DNA heteroplasmy in European populations of the mussel Mytilus edulis. Mar. Biol. 1995, 122:619-624.
62. White D.J., Wolff J.N., Pierson M., Gemmell N.J. Revealing the hidden complexities of mtDNA inheritance. Mol. Ecol. 2008, 17:4925-4942.
63. Zhou Q., Li H., Xue D. Elimination of paternal mitochondria through the lysosomal degradation pathway in C. elegans. Cell Res. 2011, 21:1662-1669.
64. Zouros E. Biparental inheritance through uniparental transmission: the doubly uniparental inheritance (DUI) of mitochondrial DNA. Evol. Biol. 2013, 40:1-31.
65. Zouros E., Ball A.O., Saavedra C., Freeman K.R. Mitochondrial DNA inheritance. Nature 1994, 368:818.
66. Zouros E., Oberhouser Ball A., Saavedra C., Freeman K.R. An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:7463-7467.