Exploring whole-genome duplicate gene retention with complex genetic interaction analysis.

Elena Kuzmin, Benjamin VanderSluis, Alex N Nguyen Ba, Wen Wang, Elizabeth N Koch, Matej Usaj, Anton Khmelinskii, Mojca Mattiazzi Usaj, Jolanda van Leeuwen, Oren Kraus, Amy Tresenrider, Michael Pryszlak, Ming-Che Hu, Brenda Varriano, Michael Costanzo, Michael Knop, Alan Moses, Chad L Myers, Brenda J Andrews, Charles Boone
Author Information
  1. Elena Kuzmin: Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada. ORCID
  2. Benjamin VanderSluis: Department of Computer Science and Engineering, University of Minnesota, Minneapolis, MN 55455, USA. ORCID
  3. Alex N Nguyen Ba: Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario, Canada. ORCID
  4. Wen Wang: Department of Computer Science and Engineering, University of Minnesota, Minneapolis, MN 55455, USA. ORCID
  5. Elizabeth N Koch: Department of Computer Science and Engineering, University of Minnesota, Minneapolis, MN 55455, USA.
  6. Matej Usaj: Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada. ORCID
  7. Anton Khmelinskii: Zentrum f��r Molekulare Biologie der Universit��t Heidelberg (ZMBH), DKFZ-ZMBH Alliance, 69120 Heidelberg, Germany. ORCID
  8. Mojca Mattiazzi Usaj: Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada. ORCID
  9. Jolanda van Leeuwen: Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada. ORCID
  10. Oren Kraus: Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada.
  11. Amy Tresenrider: Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA. ORCID
  12. Michael Pryszlak: Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada. ORCID
  13. Ming-Che Hu: Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada. ORCID
  14. Brenda Varriano: Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada.
  15. Michael Costanzo: Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada. ORCID
  16. Michael Knop: Zentrum f��r Molekulare Biologie der Universit��t Heidelberg (ZMBH), DKFZ-ZMBH Alliance, 69120 Heidelberg, Germany. ORCID
  17. Alan Moses: Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario, Canada. ORCID
  18. Chad L Myers: Department of Computer Science and Engineering, University of Minnesota, Minneapolis, MN 55455, USA. charlie.boone@utoronto.ca brenda.andrews@utoronto.ca chadm@umn.edu. ORCID
  19. Brenda J Andrews: Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada. charlie.boone@utoronto.ca brenda.andrews@utoronto.ca chadm@umn.edu. ORCID
  20. Charles Boone: Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada. charlie.boone@utoronto.ca brenda.andrews@utoronto.ca chadm@umn.edu. ORCID

Abstract

Whole-genome duplication has played a central role in the genome evolution of many organisms, including the human genome. Most duplicated genes are eliminated, and factors that influence the retention of persisting duplicates remain poorly understood. We describe a systematic complex genetic interaction analysis with yeast paralogs derived from the whole-genome duplication event. Mapping of digenic interactions for a deletion mutant of each paralog, and of trigenic interactions for the double mutant, provides insight into their roles and a quantitative measure of their functional redundancy. Trigenic interaction analysis distinguishes two classes of paralogs: a more functionally divergent subset and another that retained more functional overlap. Gene feature analysis and modeling suggest that evolutionary trajectories of duplicated genes are dictated by combined functional and structural entanglement factors.

Associated Data

Dryad | 10.5061/dryad.g79cnp5m9

References

  1. Mol Biosyst. 2010 Nov;6(11):2305-15 [PMID: 20820472]
  2. Mol Cell Biol. 1991 Mar;11(3):1295-305 [PMID: 1996092]
  3. Nat Genet. 2008 May;40(5):676-81 [PMID: 18408719]
  4. Science. 2008 Oct 3;322(5898):104-10 [PMID: 18719252]
  5. Science. 2016 Sep 23;353(6306): [PMID: 27708008]
  6. Nature. 2007 Sep 6;449(7158):54-61 [PMID: 17805289]
  7. Genome Biol. 2008;9(3):R54 [PMID: 18336717]
  8. Nat Biotechnol. 2011 Apr;29(4):361-7 [PMID: 21441928]
  9. Bioinformatics. 2006 Dec 1;22(23):2890-7 [PMID: 17005538]
  10. Science. 2016 Nov 4;354(6312): [PMID: 27811238]
  11. Science. 2010 Jan 22;327(5964):425-31 [PMID: 20093466]
  12. Cell. 1985 Feb;40(2):405-16 [PMID: 3967297]
  13. J Theor Biol. 2006 Mar 21;239(2):141-51 [PMID: 16242725]
  14. Proc Natl Acad Sci U S A. 2005 Apr 12;102(15):5454-9 [PMID: 15800040]
  15. Nature. 2003 Jan 2;421(6918):63-6 [PMID: 12511954]
  16. Elife. 2019 Aug 27;8: [PMID: 31454312]
  17. PLoS Biol. 2006 Apr;4(4):e109 [PMID: 16555924]
  18. Genome Res. 2005 Oct;15(10):1456-61 [PMID: 16169922]
  19. Genome Biol. 2006;7(5):R39 [PMID: 16684370]
  20. Genetics. 2007 Feb;175(2):933-43 [PMID: 17151249]
  21. Sci Signal. 2012 Mar 13;5(215):rs1 [PMID: 22416277]
  22. Science. 2008 Jun 13;320(5882):1465-70 [PMID: 18467557]
  23. Science. 2002 Mar 22;295(5563):2262-4 [PMID: 11910110]
  24. Genetics. 2005 Dec;171(4):1455-61 [PMID: 15965245]
  25. Genome Biol. 2007;8(4):R50 [PMID: 17411427]
  26. Science. 2017 Feb 10;355(6325):630-634 [PMID: 28183979]
  27. Proteins. 2018 Sep;86(9):945-955 [PMID: 29790597]
  28. Nature. 2006 Mar 23;440(7083):561-4 [PMID: 16554824]
  29. Science. 2012 Sep 14;337(6100):1353-6 [PMID: 22984072]
  30. Genome Res. 2008 Jul;18(7):1092-9 [PMID: 18463300]
  31. Proc Natl Acad Sci U S A. 2008 Mar 4;105(9):3461-6 [PMID: 18305163]
  32. Biochim Biophys Acta. 2000 Jul 31;1467(1):207-18 [PMID: 10930523]
  33. Nat Methods. 2010 Dec;7(12):1017-24 [PMID: 21076421]
  34. PLoS Biol. 2005 Oct;3(10):e314 [PMID: 16128622]
  35. Trends Genet. 2008 Oct;24(10):485-8 [PMID: 18786741]
  36. Nature. 2004 Jun 10;429(6992):661-4 [PMID: 15190353]
  37. Nat Genet. 2005 Mar;37(3):295-9 [PMID: 15723064]
  38. PLoS Genet. 2010 Nov 04;6(11):e1001187 [PMID: 21079672]
  39. Genome Biol Evol. 2009 Jul 22;1:198-204 [PMID: 20333190]
  40. Nature. 2004 Apr 8;428(6983):617-24 [PMID: 15004568]
  41. Mol Biol Evol. 2007 Aug;24(8):1586-91 [PMID: 17483113]
  42. Cold Spring Harb Protoc. 2016 Apr 01;2016(4):pdb.prot088807 [PMID: 27037072]
  43. Plant J. 2011 Apr;66(1):161-81 [PMID: 21443630]
  44. Mol Syst Biol. 2007;3:86 [PMID: 17389874]
  45. FEBS Lett. 2004 Apr 30;564(3):239-44 [PMID: 15111103]
  46. PLoS One. 2011;6(8):e23794 [PMID: 21915245]
  47. Science. 2001 Dec 14;294(5550):2364-8 [PMID: 11743205]
  48. Nature. 2006 Mar 2;440(7080):96-100 [PMID: 16511496]
  49. Genetics. 1999 Apr;151(4):1531-45 [PMID: 10101175]
  50. Science. 1991 May 24;252(5009):1078-9 [PMID: 2031181]
  51. Nature. 2006 Mar 30;440(7084):637-43 [PMID: 16554755]
  52. Proc Natl Acad Sci U S A. 2005 Jan 18;102(3):707-12 [PMID: 15647348]
  53. Nature. 2003 Mar 27;422(6930):433-8 [PMID: 12660784]
  54. PLoS Comput Biol. 2014 Dec 04;10(12):e1003977 [PMID: 25474245]
  55. Yeast. 1999 Jul;15(10B):963-72 [PMID: 10407276]
  56. PLoS Genet. 2013;9(3):e1003376 [PMID: 23516382]
  57. Methods Mol Biol. 2014;1205:143-68 [PMID: 25213244]
  58. Nature. 1997 Jun 12;387(6634):708-13 [PMID: 9192896]
  59. Nature. 2006 Mar 30;440(7084):631-6 [PMID: 16429126]
  60. Mol Cell. 2005 Jan 21;17(2):277-90 [PMID: 15664196]
  61. Genetics. 2000 Mar;154(3):1389-401 [PMID: 10757778]
  62. PLoS Comput Biol. 2009 Jan;5(1):e1000270 [PMID: 19180179]
  63. Cell. 2018 Feb 22;172(5):910-923.e16 [PMID: 29474919]
  64. Science. 2018 Apr 20;360(6386): [PMID: 29674565]
  65. G3 (Bethesda). 2017 May 5;7(5):1539-1549 [PMID: 28325812]
  66. Nature. 2002 Jul 25;418(6896):387-91 [PMID: 12140549]
  67. Nucleic Acids Res. 2019 Jan 8;47(D1):D529-D541 [PMID: 30476227]
  68. Science. 2004 Feb 6;303(5659):808-13 [PMID: 14764870]
  69. Yeast. 2008 Apr;25(4):301-11 [PMID: 18350525]
  70. Biochim Biophys Acta. 2008 Jul;1783(7):1354-68 [PMID: 18298957]
  71. Nature. 2003 Jul 10;424(6945):194-7 [PMID: 12853957]
  72. Open Biol. 2016 Jan;6(1):150223 [PMID: 26763345]
  73. Nature. 2012 Sep 27;489(7417):585-9 [PMID: 22940862]
  74. Trends Genet. 2001 Nov;17(11):661-9 [PMID: 11672867]
  75. Cell Syst. 2016 Jun 22;2(6):412-21 [PMID: 27237738]
  76. PLoS Genet. 2008 Jul 04;4(7):e1000113 [PMID: 18604285]
  77. Genome Biol. 2007;8(10):R209 [PMID: 17916239]
  78. Nature. 1997 Jul 10;388(6638):167-71 [PMID: 9217155]
  79. Cell. 2015 Jun 4;161(6):1413-24 [PMID: 26046442]
  80. Curr Opin Microbiol. 1999 Oct;2(5):548-54 [PMID: 10508730]
  81. Cold Spring Harb Protoc. 2016 Apr 01;2016(4):pdb.top086652 [PMID: 27037078]
  82. Mol Syst Biol. 2010 Nov 16;6:429 [PMID: 21081923]
  83. Biochim Biophys Acta. 2009 May;1788(5):1044-50 [PMID: 19285482]
  84. Cell. 1991 Aug 9;66(3):519-31 [PMID: 1651172]
  85. Nat Methods. 2012 Jul;9(7):671-5 [PMID: 22930834]
  86. Mol Biol Cell. 2000 Feb;11(2):435-52 [PMID: 10679005]
  87. Mol Biol Cell. 2009 Jul;20(14):3239-50 [PMID: 19458192]
  88. PLoS Biol. 2015 Aug 07;13(8):e1002220 [PMID: 26252497]
  89. Genome Biol. 2004;5(10):R76 [PMID: 15461795]
  90. Genome Biol. 2006;7(10):R100 [PMID: 17076895]
  91. PLoS Biol. 2010 Mar 30;8(3):e1000347 [PMID: 20361019]

Grants

  1. R01 GM104975/NIGMS NIH HHS
  2. R01 HG005084/NHGRI NIH HHS
  3. R01 HG005853/NHGRI NIH HHS

MeSH Term

Gene Deletion
Gene Duplication
Gene Regulatory Networks
Genes, Duplicate
Genetic Techniques
Genome, Fungal
Membrane Proteins
Peroxins
Protein Interaction Maps
Saccharomyces cerevisiae
Saccharomyces cerevisiae Proteins

Chemicals

Membrane Proteins
PEX25 protein, S cerevisiae
Peroxins
Pex27 protein, S cerevisiae
Saccharomyces cerevisiae Proteins

Word Cloud

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