Ancient gene duplication provided a key molecular step for anaerobic growth of Baker's yeast.
Mitochondria are essential organelles required for a number of key cellular processes. As most mitochondrial proteins are nuclear encoded, their efficient translocation into the organelle is critical. Transport of proteins across the inner membrane is driven by a multicomponent, matrix-localized "import motor," which is based on the activity of the molecular chaperone Hsp70 and a J-protein cochaperone. In Saccharomyces cerevisiae, two paralogous J-proteins, Pam18 and Mdj2, can form the import motor. Both contain transmembrane and matrix domains, with Pam18 having an additional intermembrane space (IMS) domain. Evolutionary analyses revealed that the origin of the IMS domain of S. cerevisiae Pam18 coincides with a gene duplication event that generated the PAM18/MDJ2 gene pair. The duplication event and origin of the Pam18 IMS domain occurred at the relatively ancient divergence of the fungal subphylum Saccharomycotina. The timing of the duplication event also corresponds with a number of additional functional changes related to mitochondrial function and respiration. Physiological and genetic studies revealed that the IMS domain of Pam18 is required for efficient growth under anaerobic conditions, even though it is dispensable when oxygen is present. Thus, the gene duplication was beneficial for growth capacity under particular environmental conditions as well as diversification of the import motor components.
Department of Biochemistry, University of Wisconsin-Madison, USA.
Masaya
M
Hayashi
Brenda
B
Schilke
Jaroslaw
J
Marszalek
Barry
B
Williams
Elizabeth A
EA
Craig
D000332:Aerobiosis; D000595:Amino Acid Sequence; D000693:Anaerobiosis / Q000235:genetics; D015153:Blotting, Western; D004591:Electrophoresis, Polyacrylamide Gel; D019143:Evolution, Molecular; D020440:Gene Duplication; D008565:Membrane Proteins / Q000235:genetics / Q000378:metabolism; D026901:Membrane Transport Proteins / Q000235:genetics / Q000378:metabolism; D008928:Mitochondria; D000090622:Mitochondrial Precursor Protein Import Complex Proteins; D008969:Molecular Sequence Data; D010802:Phylogeny; D021381:Protein Transport; D012441:Saccharomyces cerevisiae / Q000235:genetics* / Q000254:growth & development* / Q000378:metabolism; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics / Q000378:metabolism; D016415:Sequence Alignment
C108930:MDJ2 protein, S cerevisiae; D008565:Membrane Proteins; D026901:Membrane Transport Proteins; D000090622:Mitochondrial Precursor Protein Import Complex Proteins; C480348:PAM18 J protein, S cerevisiae; D029701:Saccharomyces cerevisiae Proteins
Mol Biol Cell. 2008 Jan;19(1):424-32
18003975
J Mol Evol. 1998 Apr;46(4):409-18
9541535
Science. 2004 Apr 9;304(5668):304-7
15001715
Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14338-43
16176987
J Cell Comp Physiol. 1953 Feb;41(1):23-36
13034889
Bioinformatics. 2003 Aug 12;19(12):1572-4
12912839
J Chem Inf Comput Sci. 2002 May-Jun;42(3):620-32
12086524
J Cell Comp Physiol. 1954 Jun;43(3):271-81
13192151
J Mol Biol. 1998 Oct 23;283(2):489-506
9769220
Proc Natl Acad Sci U S A. 2007 May 15;104(20):8397-402
17494770
PLoS Genet. 2010 Jul 22;6(7):e1001030
20661438
FEMS Yeast Res. 2003 Jun;3(4):417-32
12748053
Antonie Van Leeuwenhoek. 2004 Jan;85(1):9-21
15031659
Mol Cell Biol. 2008 Jul;28(13):4424-33
18426906
J Cell Biol. 2008 Dec 29;183(7):1213-21
19114592
FEBS Lett. 2010 Jan 21;584(2):334-41
19941859
EMBO J. 1992 Oct;11(10):3619-28
1396562
Genome Res. 2005 Oct;15(10):1456-61
16169922
Fungal Genet Biol. 2008 Sep;45(9):1248-56
18647654
Cell. 2005 Mar 25;120(6):817-29
15797382
J Biol Chem. 1982 Nov 10;257(21):13062-7
6215406
Nature. 1970 Aug 15;227(5259):680-5
5432063
Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):13839-44
14605210
Nucleic Acids Res. 2000 Jan 1;28(1):292
10592250
Biochemistry. 1969 Jan;8(1):335-9
4304987
BMC Evol Biol. 2006 Nov 22;6:99
17121679
Nat Rev Genet. 2009 Oct;10(10):715-24
19763154
Arch Biochem Biophys. 1976 May;174(1):45-51
7207
Science. 1997 Jan 17;275(5298):387-9
8994035
Bioinformatics. 2001 Sep;17(9):849-50
11590105
Genome Res. 2007 Dec;17(12):1809-22
17984228
Mol Gen Genet. 1984;197(2):345-6
6394957
Gene. 1995 Apr 14;156(1):119-22
7737504
Nat Protoc. 2006;1(1):16-22
17406207
J Mol Biol. 1996 Jul 19;260(3):289-98
8757792
Nature. 2004 Apr 8;428(6983):617-24
15004568
Mol Biol Evol. 2007 Aug;24(8):1586-91
17483113
Funct Integr Genomics. 2009 May;9(2):145-51
18795352
Cell. 2009 Aug 21;138(4):628-44
19703392
BMC Genomics. 2007 Sep 17;8:325
17868481
Nature. 2004 Jul 1;430(6995):35-44
15229592
Biochim Biophys Acta. 2010 Jun;1803(6):732-9
20100523
J Biol Chem. 2007 Jun 22;282(25):18037-18045
17452317
Nature. 1997 Jun 12;387(6634):708-13
9192896
EMBO J. 2008 May 21;27(10):1469-80
18418384
Science. 2003 Apr 4;300(5616):139-41
12677068
Annu Rev Biochem. 2008;77:669-700
18366324
Nat Struct Mol Biol. 2004 Nov;11(11):1084-91
15489862
J Mol Biol. 1997 Oct 3;272(4):477-83
9325105
Syst Biol. 2004 Feb;53(1):47-67
14965900
J Cell Biol. 2007 Dec 17;179(6):1115-22
18070913
Mol Biol Evol. 1998 May;15(5):568-73
9580986
Methods Enzymol. 2002;350:87-96
12073338
Cell. 1998 Nov 25;95(5):717-28
9845373
J Biol Chem. 2005 Sep 9;280(36):31608-14
16027163
J Biol Chem. 2001 Mar 2;276(9):6112-8
11096111
Algorithms Mol Biol. 2008 May 27;3:6
18505568
EMBO J. 2003 Oct 1;22(19):4945-56
14517234
Mol Biol Evol. 2007 Aug;24(8):1596-9
17488738
Yeast. 1991 Oct;7(7):657-78
1776357
Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
9254694
J Cell Biol. 2003 Nov 24;163(4):707-13
14638855
J Cell Biol. 1993 Oct;123(1):109-17
8408191
Proc Natl Acad Sci U S A. 1971 Feb;68(2):308-11
5277075
Biochim Biophys Acta. 2009 Jan;1793(1):33-41
18672008
J Biol Chem. 2000 Jul 21;275(29):22387-94
10777514
J Mol Biol. 1997 Feb 7;265(5):541-52
9048947
Yeast. 1999 Oct;15(14):1541-53
10514571
Genetics. 1989 May;122(1):19-27
2659436
Mol Biol Cell. 2008 Jun;19(6):2642-9
18400944
Cell Mol Life Sci. 2007 Mar;64(5):542-54
17192808
J Cell Biol. 2009 Jun 15;185(6):1029-45
19506038
Nucleic Acids Res. 1994 Nov 11;22(22):4673-80
7984417
Mol Cell Biol. 2005 Sep;25(17):7449-58
16107694
J Mol Biol. 1990 Oct 5;215(3):403-10
2231712
J Biol Chem. 2003 Dec 26;278(52):52873-80
14561769
Cell. 1999 May 28;97(5):565-74
10367886
Yeast. 2000 Jun 30;16(9):857-60
10861908
Curr Biol. 2006 Nov 21;16(22):2271-6
17113393