Lineage-specific genes are clustered with HET-domain genes and respond to environmental and genetic manipulations regulating reproduction in Neurospora.

Zheng Wang, Yen-Wen Wang, Takao Kasuga, Francesc Lopez-Giraldez, Yang Zhang, Zhang Zhang, Yaning Wang, Caihong Dong, Anita Sil, Frances Trail, Oded Yarden, Jeffrey P Townsend
Author Information
  1. Zheng Wang: Department of Biostatistics, Yale School of Public Health, New Haven, Connecticut, United States of America. ORCID
  2. Yen-Wen Wang: Department of Biostatistics, Yale School of Public Health, New Haven, Connecticut, United States of America.
  3. Takao Kasuga: College of Biological Sciences, University of California, Davis, California, United States of America. ORCID
  4. Francesc Lopez-Giraldez: Yale Center for Genomic Analysis, New Haven, Connecticut, United States of America. ORCID
  5. Yang Zhang: National Genomics Data Center, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  6. Zhang Zhang: National Genomics Data Center, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  7. Yaning Wang: Institute of Microbiology, Chinese Academy of Sciences, Beijing, China.
  8. Caihong Dong: Institute of Microbiology, Chinese Academy of Sciences, Beijing, China. ORCID
  9. Anita Sil: Department of Microbiology and Immunology, University of California, San Francisco, California, United States of America.
  10. Frances Trail: Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, Michigan, United States of America.
  11. Oded Yarden: Department of Plant Pathology and Microbiology, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel. ORCID
  12. Jeffrey P Townsend: Department of Biostatistics, Yale School of Public Health, New Haven, Connecticut, United States of America. ORCID

Abstract

Lineage-specific genes (LSGs) have long been postulated to play roles in the establishment of genetic barriers to intercrossing and speciation. In the genome of Neurospora crassa, most of the 670 Neurospora LSGs that are aggregated adjacent to the telomeres are clustered with 61% of the HET-domain genes, some of which regulate self-recognition and define vegetative incompatibility groups. In contrast, the LSG-encoding proteins possess few to no domains that would help to identify potential functional roles. Possible functional roles of LSGs were further assessed by performing transcriptomic profiling in genetic mutants and in response to environmental alterations, as well as examining gene knockouts for phenotypes. Among the 342 LSGs that are dynamically expressed during both asexual and sexual phases, 64% were detectable on unusual carbon sources such as furfural, a wildfire-produced chemical that is a strong inducer of sexual development, and the structurally-related furan 5-hydroxymethyl furfural (HMF). Expression of a significant portion of the LSGs was sensitive to light and temperature, factors that also regulate the switch from asexual to sexual reproduction. Furthermore, expression of the LSGs was significantly affected in the knockouts of adv-1 and pp-1 that regulate hyphal communication, and expression of more than one quarter of the LSGs was affected by perturbation of the mating locus. These observations encouraged further investigation of the roles of clustered lineage-specific and HET-domain genes in ecology and reproduction regulation in Neurospora, especially the regulation of the switch from the asexual growth to sexual reproduction, in response to dramatic environmental conditions changes.

References

  1. Fungal Genet Biol. 2019 May;126:1-11 [PMID: 30731203]
  2. Mol Ecol. 2018 Jan;27(1):216-232 [PMID: 29134709]
  3. Proc Natl Acad Sci U S A. 2012 May 8;109(19):7397-402 [PMID: 22532664]
  4. mBio. 2016 Mar 08;7(2):e02148 [PMID: 26956589]
  5. Nature. 1965 Feb 13;205:680-2 [PMID: 14287408]
  6. Biotechnol Biofuels. 2015 Feb 12;8:21 [PMID: 25691917]
  7. Genetics. 1996 Aug;143(4):1589-600 [PMID: 8844148]
  8. Philos Trans A Math Phys Eng Sci. 2009 Nov 13;367(1906):4255-71 [PMID: 19805444]
  9. J Biosci. 2010 Mar;35(1):119-26 [PMID: 20413916]
  10. Nat Rev Genet. 2002 May;3(5):397-403 [PMID: 11988765]
  11. Mol Biol (Mosk). 2005 Jul-Aug;39(4):602-17 [PMID: 16083009]
  12. Proc Natl Acad Sci U S A. 2012 Apr 17;109(16):6012-7 [PMID: 22474347]
  13. PLoS Biol. 2020 Nov 2;18(11):e3000862 [PMID: 33137085]
  14. G3 (Bethesda). 2014 Jul 21;4(9):1731-45 [PMID: 25053707]
  15. Nat Genet. 2005 Sep;37(9):986-90 [PMID: 16086015]
  16. Cold Spring Harb Perspect Biol. 2013 Oct 01;5(10):a017921 [PMID: 24086046]
  17. Methods Mol Biol. 2018;1775:171-184 [PMID: 29876818]
  18. PLoS Genet. 2017 May 3;13(5):e1006737 [PMID: 28467421]
  19. mBio. 2015 Oct 13;6(5):e01452-15 [PMID: 26463163]
  20. Elife. 2018 Jan 03;7: [PMID: 29297465]
  21. Eukaryot Cell. 2011 Aug;10(8):1100-9 [PMID: 21666072]
  22. Nat Ecol Evol. 2019 Apr;3(4):679-690 [PMID: 30858588]
  23. Plant Physiol. 1983 Aug;72(4):996-1000 [PMID: 16663152]
  24. Nat Rev Genet. 2016 Sep;17(9):567-78 [PMID: 27452112]
  25. Front Fungal Biol. 2021 Apr 16;2:672696 [PMID: 37744127]
  26. Can J Genet Cytol. 1970 Dec;12(4):914-26 [PMID: 5512565]
  27. Genome. 1992 Apr;35(2):347-53 [PMID: 1535606]
  28. Genetics. 2001 Oct;159(2):589-98 [PMID: 11606536]
  29. Elife. 2020 Feb 18;9: [PMID: 32066524]
  30. Bioinformatics. 2005 Sep 1;21 Suppl 2:ii42-6 [PMID: 16204123]
  31. Curr Genet. 1997 Jun;31(6):457-61 [PMID: 9211787]
  32. Mol Microbiol. 2002 Aug;45(3):795-804 [PMID: 12139624]
  33. J Mol Evol. 2022 Aug;90(3-4):244-257 [PMID: 35451603]
  34. PLoS Genet. 2017 Jul 13;13(7):e1006867 [PMID: 28704372]
  35. EMBO J. 2009 Apr 22;28(8):1029-42 [PMID: 19262566]
  36. Eukaryot Cell. 2014 Jan;13(1):154-69 [PMID: 24243796]
  37. PLoS Comput Biol. 2009 Jun;5(6):e1000421 [PMID: 19557160]
  38. PLoS One. 2009 Apr 21;4(4):e5286 [PMID: 19461939]
  39. Bioinformatics. 2010 Aug 1;26(15):1918-9 [PMID: 20538728]
  40. Proc Natl Acad Sci U S A. 2018 Mar 6;115(10):E2292-E2301 [PMID: 29463729]
  41. Syst Biol. 2019 Jan 1;68(1):145-156 [PMID: 29939341]
  42. Nat Rev Genet. 2011 Aug 31;12(10):692-702 [PMID: 21878963]
  43. mBio. 2019 Dec 10;10(6): [PMID: 31822585]
  44. Nucleic Acids Res. 2022 Jan 7;50(D1):D439-D444 [PMID: 34791371]
  45. Trends Genet. 2007 Nov;23(11):533-9 [PMID: 18029048]
  46. Genetics. 1999 Feb;151(2):545-55 [PMID: 9927450]
  47. Nature. 2021 Aug;596(7873):583-589 [PMID: 34265844]
  48. Microbiol Mol Biol Rev. 2004 Mar;68(1):1-108 [PMID: 15007097]
  49. Front Fungal Biol. 2023 Jun 30;4:1214537 [PMID: 37746130]
  50. Fungal Genet Biol. 2004 Dec;41(12):1063-76 [PMID: 15531211]
  51. BMC Genomics. 2020 Nov 2;21(1):755 [PMID: 33138786]
  52. Front Microbiol. 2019 Apr 10;10:750 [PMID: 31024511]
  53. Nucleic Acids Res. 2014 Jan;42(Database issue):D222-30 [PMID: 24288371]
  54. Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10352-10357 [PMID: 16801547]
  55. EMBO Rep. 2006 Feb;7(2):199-204 [PMID: 16374510]
  56. Eukaryot Cell. 2008 Sep;7(9):1549-64 [PMID: 18676954]
  57. Nucleic Acids Res. 2014 Jan;42(Database issue):D699-704 [PMID: 24297253]
  58. Genetics. 2009 Mar;181(3):1129-45 [PMID: 19104079]
  59. Commun Integr Biol. 2020 Mar 16;13(1):39-42 [PMID: 32313605]
  60. G3 (Bethesda). 2017 Jan 5;7(1):129-142 [PMID: 27856696]
  61. PLoS One. 2019 Sep 4;14(9):e0215495 [PMID: 31483836]
  62. Mol Biol Evol. 2015 Sep;32(9):2417-32 [PMID: 26025978]
  63. Mol Gen Genet. 2000 Mar;263(2):292-301 [PMID: 10778748]
  64. Genetics. 2007 Jun;176(2):1131-7 [PMID: 17435230]
  65. Nat Ecol Evol. 2022 Jul;6(7):910-923 [PMID: 35551248]
  66. BMC Evol Biol. 2015 May 14;15:86 [PMID: 25968460]
  67. Fungal Genet Biol. 2000 Aug;30(3):197-205 [PMID: 11035941]
  68. Bioinformatics. 2018 Oct 1;34(19):3377-3379 [PMID: 29701747]
  69. PLoS One. 2014 Oct 20;9(10):e110398 [PMID: 25329823]
  70. Front Microbiol. 2021 Nov 26;12:769615 [PMID: 34899653]
  71. Mol Ecol. 2023 Oct 16;: [PMID: 37843462]
  72. J Mol Evol. 2006 Jul;63(1):1-11 [PMID: 16755356]
  73. Genetics. 2006 Mar;172(3):1675-81 [PMID: 16361246]
  74. PLoS One. 2014 Oct 21;9(10):e110603 [PMID: 25333968]
  75. PLoS Genet. 2015 Dec 31;11(12):e1005721 [PMID: 26720152]
  76. Planta. 1970 Dec;94(4):253-64 [PMID: 24496969]
  77. Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4285-8 [PMID: 10200254]
  78. mBio. 2019 Mar 26;10(2): [PMID: 30914504]
  79. Genetics. 2005 Aug;170(4):1589-600 [PMID: 15965256]
  80. G3 (Bethesda). 2022 May 6;12(5): [PMID: 35244156]
  81. J Bacteriol. 1948 Mar;55(3):327-30 [PMID: 16561462]
  82. Genetics. 2018 Jun;209(2):489-506 [PMID: 29678830]
  83. Proc Natl Acad Sci U S A. 2020 Aug 4;117(31):18600-18607 [PMID: 32703806]
  84. Nucleic Acids Res. 2006 Jan 1;34(Database issue):D252-6 [PMID: 16381858]
  85. Microbiologyopen. 2013 Aug;2(4):595-609 [PMID: 23766336]
  86. Genome Biol Evol. 2018 Nov 1;10(11):2906-2918 [PMID: 30346517]
  87. Nature. 2003 Apr 24;422(6934):859-68 [PMID: 12712197]
  88. Methods Mol Biol. 2020;2090:313-336 [PMID: 31975173]
  89. Biotechnol Biofuels. 2019 Sep 04;12:210 [PMID: 31508149]

Grants

  1. R01 AI146584/NIAID NIH HHS
  2. UL1 TR001863/NCATS NIH HHS

MeSH Term

Neurospora
Genes, Fungal
Neurospora crassa
Phenotype
Gene Expression Profiling
Reproduction
Fungal Proteins

Chemicals

Fungal Proteins

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