Dual RNA-seq reveals large-scale non-conserved genotype × genotype-specific genetic reprograming and molecular crosstalk in the mycorrhizal symbiosis.

Ivan D Mateus, Frédéric G Masclaux, Consolée Aletti, Edward C Rojas, Romain Savary, Cindy Dupuis, Ian R Sanders
Author Information
  1. Ivan D Mateus: Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015, Lausanne, Switzerland.
  2. Frédéric G Masclaux: Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015, Lausanne, Switzerland.
  3. Consolée Aletti: Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015, Lausanne, Switzerland.
  4. Edward C Rojas: Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015, Lausanne, Switzerland.
  5. Romain Savary: Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015, Lausanne, Switzerland.
  6. Cindy Dupuis: Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015, Lausanne, Switzerland.
  7. Ian R Sanders: Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015, Lausanne, Switzerland. ian.sanders@unil.ch. ORCID

Abstract

Arbuscular mycorrhizal fungi (AMF) impact plant growth and are a major driver of plant diversity and productivity. We quantified the contribution of intra-specific genetic variability in cassava (Manihot esculenta) and Rhizophagus irregularis to gene reprogramming in symbioses using dual RNA-sequencing. A large number of cassava genes exhibited altered transcriptional responses to the fungus but transcription of most of these plant genes (72%) responded in a different direction or magnitude depending on the plant genotype. Two AMF isolates displayed large differences in their transcription, but the direction and magnitude of the transcriptional responses for a large number of these genes was also strongly influenced by the genotype of the plant host. This indicates that unlike the highly conserved plant genes necessary for the symbiosis establishment, most of the plant and fungal gene transcriptional responses are not conserved and are greatly influenced by plant and fungal genetic differences, even at the within-species level. The transcriptional variability detected allowed us to identify an extensive gene network showing the interplay in plant-fungal reprogramming in the symbiosis. Key genes illustrated that the two organisms jointly program their cytoskeleton organization during growth of the fungus inside roots. Our study reveals that plant and fungal genetic variation has a strong role in shaping the genetic reprograming in response to symbiosis, indicating considerable genotype × genotype interactions in the mycorrhizal symbiosis. Such variation needs to be considered in order to understand the molecular mechanisms between AMF and their plant hosts in natural communities.

References

  1. New Phytol. 2017 May;214(3):1330-1337 [PMID: 28186629]
  2. Curr Opin Plant Biol. 2007 Aug;10(4):393-8 [PMID: 17658291]
  3. Nat Biotechnol. 2016 May;34(5):562-70 [PMID: 27088722]
  4. ISME J. 2016 Dec;10(12):2780-2786 [PMID: 27128992]
  5. Ann Bot. 2009 Dec;104(7):1263-80 [PMID: 19815570]
  6. PLoS Negl Trop Dis. 2014 May 22;8(5):e2905 [PMID: 24853112]
  7. Eur J Histochem. 1999;43(2):105-11 [PMID: 10439213]
  8. Ecol Lett. 2006 Feb;9(2):103-10 [PMID: 16958874]
  9. PLoS Genet. 2014 Jul 17;10(7):e1004487 [PMID: 25032823]
  10. BMC Genomics. 2013 May 07;14:306 [PMID: 23647797]
  11. Mycorrhiza. 2015 Oct;25(7):533-46 [PMID: 25708401]
  12. Plant Physiol. 2005 Apr;137(4):1283-301 [PMID: 15778460]
  13. Curr Opin Plant Biol. 2009 Aug;12(4):421-6 [PMID: 19608449]
  14. Plant J. 2018 May;94(3):411-425 [PMID: 29570877]
  15. New Phytol. 2009 Oct;184(2):412-423 [PMID: 19674324]
  16. New Phytol. 2009 Oct;184(2):424-437 [PMID: 19558424]
  17. Plant Physiol. 2014 Sep;166(1):281-92 [PMID: 25096975]
  18. New Phytol. 2012 Apr;194(2):536-547 [PMID: 22269207]
  19. Nat Microbiol. 2016 Mar 21;1(6):16033 [PMID: 27572831]
  20. Mol Plant Microbe Interact. 2010 Jan;23(1):67-81 [PMID: 19958140]
  21. Brief Funct Genomics. 2018 Jul 1;17(4):240-245 [PMID: 29236955]
  22. Trends Plant Sci. 2013 Jun;18(6):298-304 [PMID: 23462549]
  23. J Plant Physiol. 2005 Jun;162(6):634-49 [PMID: 16008086]
  24. PLoS One. 2015 Mar 02;10(3):e0118731 [PMID: 25730421]
  25. Oecologia. 1993 May;94(2):229-234 [PMID: 28314036]
  26. Plant Signal Behav. 2008 Oct;3(10):831-3 [PMID: 19704513]
  27. Nat Rev Microbiol. 2012 Sep;10(9):618-30 [PMID: 22890146]
  28. PLoS One. 2015 Nov 24;10(11):e0143128 [PMID: 26599013]
  29. Protoplasma. 2001;217(4):154-65 [PMID: 11732307]
  30. New Phytol. 2010 Feb;185(3):716-33 [PMID: 20003073]
  31. New Phytol. 2012 Feb;193(3):755-769 [PMID: 22092242]
  32. ISME J. 2016 Oct;10(10):2514-26 [PMID: 26953600]
  33. Front Microbiol. 2017 Jul 21;8:1403 [PMID: 28785256]
  34. Curr Biol. 2010 Jul 13;20(13):1216-21 [PMID: 20541408]
  35. Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):20117-22 [PMID: 24277808]
  36. Annu Rev Cell Dev Biol. 2013;29:593-617 [PMID: 24099088]
  37. Plant Physiol. 1995 May;108(1):7-15 [PMID: 12228450]
  38. New Phytol. 2004 Nov;164(2):357-364 [PMID: 33873553]
  39. Planta. 2009 Apr;229(5):1023-34 [PMID: 19169704]
  40. BMC Bioinformatics. 2008 Dec 29;9:559 [PMID: 19114008]
  41. ISME J. 2014 Feb;8(2):284-94 [PMID: 24030596]
  42. PLoS One. 2013 Aug 07;8(8):e70633 [PMID: 23950975]
  43. Science. 2015 Aug 28;349(6251):970-3 [PMID: 26315436]

MeSH Term

Genotype
Glomeromycota
Manihot
Mycorrhizae
Sequence Analysis, RNA
Symbiosis
Transcription, Genetic

Word Cloud

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