Evaluating the hologenome concept by analyzing the root-endosphere microbiota of chimeric plants.

Marine Biget, Tingting Wang, Cendrine Mony, Qicheng Xu, Lucie Lecoq, Véronique Chable, Kevin R Theis, Ning Ling, Philippe Vandenkoornhuyse
Author Information
  1. Marine Biget: Université de Rennes 1, CNRS, UMR 6553 ECOBIO (écosystèmes, biodiversité, évolution), 35000 Rennes, France.
  2. Tingting Wang: Université de Rennes 1, CNRS, UMR 6553 ECOBIO (écosystèmes, biodiversité, évolution), 35000 Rennes, France.
  3. Cendrine Mony: Université de Rennes 1, CNRS, UMR 6553 ECOBIO (écosystèmes, biodiversité, évolution), 35000 Rennes, France.
  4. Qicheng Xu: Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, Nanjing 210095, China.
  5. Lucie Lecoq: Université de Rennes 1, CNRS, UMR 6553 ECOBIO (écosystèmes, biodiversité, évolution), 35000 Rennes, France.
  6. Véronique Chable: UMR BAGAP INRAE, Centre Bretagne-Normandie, Domaine de la Motte, BP35327, 35653 Le Rheu Cedex, France.
  7. Kevin R Theis: Department of Biochemistry, Microbiology and Immunology, Wayne State University School of Medicine, Detroit, MI, USA.
  8. Ning Ling: Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, Nanjing 210095, China.
  9. Philippe Vandenkoornhuyse: Université de Rennes 1, CNRS, UMR 6553 ECOBIO (écosystèmes, biodiversité, évolution), 35000 Rennes, France.

Abstract

The hologenome concept considers the entity formed by a host and its microbiota, the holobiont, as new level of hierarchical organization subject to neutral and selective forces. We used grafted plants to formally evaluate the hologenome concept. We analyzed the root-endosphere microbiota of two independent watermelon and grapevine plant systems, including ungrafted and reciprocal-grafting combinations. Grafted and ungrafted hosts harbor markedly different microbiota compositions. Furthermore, the results indicate a non-random assembly of bacterial communities inhabiting the root endosphere of chimeric plants with interactive effect of both the rootstock and scion on the recruitment of microorganisms. Because chimeric plants did not have a random microbiota, the null hypothesis that holobionts assemble randomly and hologenome concept is an intellectual construction only can be rejected. The study supports the relevance of hologenome as biological level of organization and opens new avenues for a better fundamental understanding of plants as holobionts.

Keywords

References

  1. Microbiome. 2018 Apr 26;6(1):79 [PMID: 29695286]
  2. Nat Protoc. 2021 May;16(5):2450-2470 [PMID: 33911260]
  3. ISME J. 2016 Mar;10(3):655-64 [PMID: 26296066]
  4. Science. 2019 May 10;364(6440): [PMID: 31073042]
  5. Appl Environ Microbiol. 2019 Jan 9;85(2): [PMID: 30413478]
  6. Trends Ecol Evol. 2011 Jul;26(7):340-8 [PMID: 21561679]
  7. Microbiome. 2018 Jan 3;6(1):3 [PMID: 29298729]
  8. Environ Microbiol. 2022 Aug;24(8):3791-3808 [PMID: 35581159]
  9. Proc Natl Acad Sci U S A. 2007 Oct 23;104(43):16970-5 [PMID: 17939995]
  10. Proc Natl Acad Sci U S A. 2019 Jun 18;116(25):12558-12565 [PMID: 31152139]
  11. Trends Plant Sci. 2021 Feb;26(2):132-141 [PMID: 33036916]
  12. Front Microbiol. 2017 May 16;8:849 [PMID: 28559882]
  13. Environ Microbiol. 2021 Apr;23(4):1812-1829 [PMID: 32955144]
  14. New Phytol. 2021 Jun;230(5):2047-2060 [PMID: 33626176]
  15. Hortic Res. 2022 Feb 19;: [PMID: 35184168]
  16. FEMS Microbiol Rev. 2013 Sep;37(5):634-63 [PMID: 23790204]
  17. Front Microbiol. 2016 Oct 21;7:1647 [PMID: 27818648]
  18. Environ Microbiol Rep. 2010 Aug;2(4):500-6 [PMID: 23766221]
  19. New Phytol. 2015 Jun;206(4):1196-206 [PMID: 25655016]
  20. Science. 2016 Feb 19;351(6275): [PMID: 26912898]
  21. Bioinformatics. 2010 Oct 1;26(19):2460-1 [PMID: 20709691]
  22. ISME J. 2019 Jul;13(7):1647-1658 [PMID: 30796337]
  23. Environ Microbiol. 2009 Dec;11(12):2959-62 [PMID: 19573132]
  24. Nucleic Acids Res. 2021 Jul 2;49(W1):W293-W296 [PMID: 33885785]
  25. BMC Plant Biol. 2021 Apr 5;21(1):165 [PMID: 33820543]
  26. Curr Opin Plant Biol. 2017 Aug;38:109-116 [PMID: 28545003]
  27. Nat Plants. 2021 Aug;7(8):1078-1092 [PMID: 34226690]
  28. Front Physiol. 2018 Dec 20;9:1836 [PMID: 30618841]
  29. FEMS Microbiol Rev. 2008 Aug;32(5):723-35 [PMID: 18549407]
  30. Nature. 2020 Nov;587(7832):103-108 [PMID: 32999461]
  31. Nature. 2012 Aug 2;488(7409):91-5 [PMID: 22859207]
  32. New Phytol. 2021 Jan;229(2):1091-1104 [PMID: 32852792]
  33. J Adv Res. 2019 Mar 20;19:29-37 [PMID: 31341667]
  34. Int J Mol Sci. 2021 Jun 25;22(13): [PMID: 34202205]
  35. Front Plant Sci. 2015 Dec 23;6:1159 [PMID: 26779191]
  36. Microorganisms. 2017 Nov 10;5(4): [PMID: 29125552]
  37. Science. 2016 Sep 16;353(6305):1272-7 [PMID: 27634532]
  38. FEMS Microbiol Rev. 2021 Nov 23;45(6): [PMID: 33930136]
  39. Microbiome. 2017 Feb 23;5(1):25 [PMID: 28231859]
  40. Nat Methods. 2011 Jul 17;8(9):761-3 [PMID: 21765408]
  41. New Phytol. 2015 Aug;207(3):841-57 [PMID: 25919406]
  42. Front Microbiol. 2021 Dec 20;12:780469 [PMID: 34987488]
  43. Plants (Basel). 2020 Jul 16;9(7): [PMID: 32708770]
  44. F1000Res. 2020 Feb 26;9: [PMID: 32148778]
  45. PeerJ. 2017 Jun 8;5:e3454 [PMID: 28607843]
  46. Annu Rev Genet. 2016 Nov 23;50:211-234 [PMID: 27648643]
  47. PLoS Biol. 2015 Aug 18;13(8):e1002226 [PMID: 26284777]
  48. Nat Rev Microbiol. 2020 Nov;18(11):607-621 [PMID: 32788714]
  49. Metabolites. 2020 Aug 18;10(8): [PMID: 32824704]
  50. mSystems. 2016 Mar 29;1(2): [PMID: 27822520]
  51. Environ Microbiol. 2006 Apr;8(4):732-40 [PMID: 16584484]
  52. Nature. 2012 Aug 2;488(7409):86-90 [PMID: 22859206]
  53. Nat Microbiol. 2021 Sep;6(9):1150-1162 [PMID: 34312531]
  54. F1000Res. 2018 Oct 19;7: [PMID: 30410727]
  55. Microbiome. 2018 Jan 27;6(1):18 [PMID: 29374490]
  56. Hortic Res. 2022 Jan 5;9: [PMID: 35043188]

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