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Front Microbiol. 2016 Mar 01;7:233. doi: 10.3389/fmicb.2016.00233. eCollection 2016.

A Survey of the Gene Repertoire of Gigaspora rosea Unravels Conserved Features among Glomeromycota for Obligate Biotrophy.

Frontiers in microbiology

Nianwu Tang, Hélène San Clemente, Sébastien Roy, Guillaume Bécard, Bin Zhao, Christophe Roux

Affiliations

  1. State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural UniversityWuhan, China; CNRS, Laboratoire de Recherche en Sciences Végétales, UMR, Université Paul Sabatier - Université de ToulouseCastanet Tolosan, France.
  2. CNRS, Laboratoire de Recherche en Sciences Végétales, UMR, Université Paul Sabatier - Université de Toulouse Castanet Tolosan, France.
  3. AGRONUTRITION Laboratoire de Biotechnologies Toulouse, France.
  4. State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University Wuhan, China.

PMID: 26973612 PMCID: PMC4771724 DOI: 10.3389/fmicb.2016.00233

Abstract

Arbuscular mycorrhizal (AM) fungi are a diverse group of soil fungi (Glomeromycota) that form the most ancient mutualistic association termed AM symbiosis with a majority of land plants, improving their nutrition uptake and resistance to stresses. In contrast to their great ecological implications, the knowledge of the molecular biological mechanisms involved is still scant, partly due to the limited genomic resources available. Here, we describe the gene repertoire of a new AM fungus Gigaspora rosea (Diversisporales). Among the 86332 non-redundant virtual transcripts assembled, 15346 presented similarities with proteins in the Refseq database and 10175 were assigned with GO terms. KOG and Interpro domain annotations clearly showed an enrichment of genes involved in signal transduction in G. rosea. KEGG pathway analysis indicates that most primary metabolic processes are active in G. rosea. However, as for Rhizophagus irregularis, several metabolic genes were not found, including the fatty acid synthase (FAS) gene. This finding supports the hypothesis that AM fungi depend on the lipids produced by their hosts. Furthermore, the presence of a large number of transporters and 100s of secreted proteins, together with the reduced number of plant cell wall degrading enzymes could be interpreted as an evolutionary adaptation to its mutualistic obligate biotrophy. The detection of meiosis-related genes suggests that G. rosea might use a cryptic sexual process. Lastly, a phylogeny of basal fungi clearly shows Glomeromycota as a sister clade to Mucoromycotina, not only to the Mucorales or Mortierellales. The characterization of the gene repertoire from an AM fungal species belonging to the order of Diversisporales and its comparison with the gene sets of R. irregularis (Glomerales) and Gigaspora margarita (Diversisporales), reveal that AM fungi share several features linked to mutualistic obligate biotrophy. This work contributes to lay the foundation for forthcoming studies into the genomics of Diversisporales, and also illuminates the utility of comparing gene repertoires of species from Diversisporales and other clades of Glomeromycota to gain more insights into the genetics and evolution of this fungal group.

Keywords: Glomeromycota; arbuscular mycorrhizal fungi; gene repertoire; mRNA sequencing; obligate biotrophy; phylogenomics

References

  1. Curr Opin Plant Biol. 2012 Aug;15(4):454-61 - PubMed
  2. BMC Genomics. 2014 Mar 20;15:214 - PubMed
  3. Mol Plant Microbe Interact. 2000 Jun;13(6):693-8 - PubMed
  4. Nat Rev Microbiol. 2008 Oct;6(10):763-75 - PubMed
  5. Mol Biol Evol. 2000 Apr;17(4):540-52 - PubMed
  6. Fungal Genet Biol. 2006 Feb;43(2):102-10 - PubMed
  7. Front Plant Sci. 2014 May 06;5:178 - PubMed
  8. Mol Plant Microbe Interact. 2001 Oct;14(10):1140-8 - PubMed
  9. J Evol Biol. 2010 Jul;23(7):1519-27 - PubMed
  10. Nature. 2005 Apr 21;434(7036):980-6 - PubMed
  11. Mycorrhiza. 2007 Jul;17(5):375-93 - PubMed
  12. New Phytol. 2015 Mar;205(4):1394-8 - PubMed
  13. Science. 1996 Oct 25;274(5287):546, 563-7 - PubMed
  14. PLoS Genet. 2014 May 08;10(5):e1004281 - PubMed
  15. FEMS Microbiol Lett. 2005 Oct 15;251(2):185-92 - PubMed
  16. ISME J. 2016 Jan;10 (1):130-44 - PubMed
  17. Mol Plant. 2013 Jan;6(1):100-12 - PubMed
  18. Nature. 2004 Feb 19;427(6976):733-7 - PubMed
  19. Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W116-20 - PubMed
  20. Nucleic Acids Res. 2012 Jul;40(Web Server issue):W445-51 - PubMed
  21. Mol Biol Evol. 2009 Jan;26(1):27-34 - PubMed
  22. Genome Biol Evol. 2011;3:950-8 - PubMed
  23. Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):20117-22 - PubMed
  24. Curr Biol. 2012 Dec 4;22(23):2242-6 - PubMed
  25. Plant Physiol. 2010 Jul;153(3):1175-87 - PubMed
  26. New Phytol. 2015 Mar;205(4):1464-72 - PubMed
  27. Bioinformatics. 2015 Oct 1;31(19):3210-2 - PubMed
  28. Nat Protoc. 2007;2(4):953-71 - PubMed
  29. PLoS Genet. 2011 Aug;7(8):e1002230 - PubMed
  30. Bioinformatics. 2003 Aug 12;19(12):1572-4 - PubMed
  31. New Phytol. 2009;183(1):200-11 - PubMed
  32. Nature. 2001 Dec 13;414(6865):745-8 - PubMed
  33. Bioinformatics. 2006 Jul 1;22(13):1658-9 - PubMed
  34. Bioinformatics. 2008 Apr 1;24(7):1024-5 - PubMed
  35. Genome Biol Evol. 2014 Jul 24;6(8):1938-48 - PubMed
  36. Proc Natl Acad Sci U S A. 2004 May 11;101(19):7329-34 - PubMed
  37. J Exp Bot. 2006;57(15):4015-23 - PubMed
  38. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11841-3 - PubMed
  39. Mol Biol Evol. 2013 Dec;30(12):2725-9 - PubMed
  40. BMC Evol Biol. 2009 Jan 15;9:13 - PubMed
  41. Annu Rev Genet. 2010;44:271-92 - PubMed
  42. Science. 2011 Aug 12;333(6044):880-2 - PubMed
  43. Genome Biol Evol. 2012;4(1):13-23 - PubMed
  44. Nucleic Acids Res. 2012 Jan;40(Database issue):D653-9 - PubMed
  45. New Phytol. 2012 Feb;193(3):755-69 - PubMed
  46. Nature. 2005 Dec 22;438(7071):1105-15 - PubMed
  47. Fungal Genet Biol. 2008 Jun;45(6):812-7 - PubMed
  48. New Phytol. 2012 Mar;193(4):970-84 - PubMed
  49. Nature. 2015 Nov 26;527(7579):521-4 - PubMed
  50. Nucleic Acids Res. 2002 Jul 15;30(14):3059-66 - PubMed
  51. Nucleic Acids Res. 2009 Jan;37(1):289-97 - PubMed
  52. Eukaryot Cell. 2013 Nov;12(11):1554-62 - PubMed
  53. Nucleic Acids Res. 2014 Jan;42(Database issue):D26-31 - PubMed
  54. New Phytol. 2011 Dec;192(4):794-7 - PubMed
  55. Phytochemistry. 2010 Oct;71(14-15):1615-24 - PubMed
  56. Curr Biol. 2011 Jul 26;21(14):1204-9 - PubMed
  57. Nat Genet. 2015 Apr;47(4):410-5 - PubMed
  58. Plant Physiol. 2008 Sep;148(1):402-13 - PubMed
  59. Plant Physiol. 2005 Apr;137(4):1319-30 - PubMed
  60. Appl Environ Microbiol. 2005 Sep;71(9):5341-7 - PubMed
  61. PLoS Genet. 2014 Jan;10(1):e1004078 - PubMed
  62. Nat Rev Mol Cell Biol. 2009 Mar;10(3):218-27 - PubMed
  63. Biol Lett. 2011 Aug 23;7(4):574-7 - PubMed
  64. New Phytol. 2013 Jan;197(2):617-30 - PubMed
  65. PLoS Pathog. 2011 Oct;7(10):e1002290 - PubMed
  66. BMC Evol Biol. 2006 Mar 10;6:21 - PubMed
  67. Bioinformatics. 2009 Jan 1;25(1):126-7 - PubMed
  68. Commun Integr Biol. 2012 Mar 1;5(2):187-9 - PubMed
  69. Trends Plant Sci. 2003 Apr;8(4):143-5 - PubMed
  70. New Phytol. 2015 Jan;205(2):743-56 - PubMed
  71. BMC Evol Biol. 2006 Sep 29;6:74 - PubMed
  72. Int J Plant Genomics. 2008;2008:412696 - PubMed
  73. Proc Natl Acad Sci U S A. 2011 May 31;108(22):9166-71 - PubMed
  74. Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11889-94 - PubMed
  75. Nat Rev Genet. 2014 Dec;15(12):797-813 - PubMed
  76. Mol Plant Microbe Interact. 2009 Sep;22(9):1169-78 - PubMed
  77. New Phytol. 2009;181(3):693-707 - PubMed
  78. New Phytol. 2008;178(3):672-87 - PubMed
  79. Plant J. 2014 Aug;79(3):398-412 - PubMed
  80. Nat Commun. 2010 Nov 02;1:103 - PubMed
  81. Nucleic Acids Res. 2007 Jul;35(Web Server issue):W182-5 - PubMed
  82. Front Plant Sci. 2014 Jun 23;5:293 - PubMed
  83. Nucleic Acids Res. 2012 Jan;40(Database issue):D695-9 - PubMed
  84. PLoS Genet. 2009 Jul;5(7):e1000549 - PubMed
  85. BMC Genomics. 2011 Sep 07;12:444 - PubMed
  86. Plant Cell. 2011 Oct;23(10):3812-23 - PubMed
  87. Mycorrhiza. 2005 Nov;15(8):620-7 - PubMed
  88. FEMS Microbiol Lett. 2008 Sep;286(2):145-51 - PubMed
  89. BMC Evol Biol. 2009 Jun 30;9:148 - PubMed
  90. Nature. 2002 Feb 21;415(6874):871-80 - PubMed
  91. Nature. 2010 Apr 15;464(7291):1033-8 - PubMed
  92. New Phytol. 2014 Jan;201(1):254-68 - PubMed
  93. Nature. 2005 Jun 9;435(7043):824-7 - PubMed
  94. New Phytol. 2006;172(1):22-34 - PubMed
  95. Plant Physiol. 1999 Jun;120(2):587-98 - PubMed
  96. PLoS Genet. 2014 Apr 17;10(4):e1004261 - PubMed
  97. Bioinformatics. 2013 Oct 15;29(20):2641-2 - PubMed
  98. Annu Rev Cell Dev Biol. 2013;29:593-617 - PubMed
  99. Science. 2007 Jun 22;316(5832):1746-8 - PubMed
  100. BMC Genomics. 2015 Jan 27;16:28 - PubMed
  101. Proc Natl Acad Sci U S A. 2012 Feb 14;109(7):2666-71 - PubMed
  102. Trends Plant Sci. 2008 Feb;13(2):93-7 - PubMed
  103. Curr Opin Plant Biol. 2012 Dec;15(6):691-8 - PubMed
  104. Nat Commun. 2010 Jul 27;1:48 - PubMed
  105. Nature. 2008 Mar 6;452(7183):88-92 - PubMed
  106. BMC Evol Biol. 2015 Dec 28;15:249 - PubMed
  107. Nature. 1995 Dec 7;378(6557):626-9 - PubMed
  108. Fungal Genet Biol. 2011 Nov;48(11):1044-55 - PubMed
  109. Nucleic Acids Res. 2006 Jan 1;34(Database issue):D459-64 - PubMed
  110. PLoS Genet. 2005 Jul;1(1):36-57 - PubMed
  111. Trends Cell Biol. 2001 Sep;11(9):366-71 - PubMed
  112. Nature. 2003 Apr 24;422(6934):859-68 - PubMed
  113. Mol Ecol. 2005 Mar;14(3):743-52 - PubMed
  114. New Phytol. 2010 Oct;188(1):223-41 - PubMed
  115. Plant Physiol. 2007 Apr;143(4):1827-40 - PubMed
  116. Eukaryot Cell. 2012 Nov;11(11):1413-4 - PubMed
  117. Nature. 2006 Dec 14;444(7121):933-6 - PubMed
  118. Syst Biol. 2010 May;59(3):307-21 - PubMed
  119. Plant J. 2007 Aug;51(3):390-405 - PubMed
  120. Science. 2010 Dec 10;330(6010):1543-6 - PubMed
  121. Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W677-80 - PubMed
  122. PLoS Biol. 2006 Jul;4(7):e226 - PubMed
  123. Microbiol Mol Biol Rev. 1998 Mar;62(1):1-34 - PubMed
  124. Nature. 2006 Nov 2;444(7115):97-101 - PubMed
  125. Nature. 2006 Oct 19;443(7113):818-22 - PubMed
  126. Mol Biol Evol. 2012 Sep;29(9):2199-210 - PubMed
  127. Nature. 2005 Jan 13;433(7022):160-3 - PubMed
  128. Genome Biol Evol. 2015 Jan 07;7(2):505-21 - PubMed

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