Glycerol-3-phosphate mediates rhizobia-induced systemic signaling in soybean.

M B Shine, Qing-Ming Gao, R V Chowda-Reddy, Asheesh K Singh, Pradeep Kachroo, Aardra Kachroo
Author Information
  1. M B Shine: Department of Plant Pathology, University of Kentucky, Lexington, KY, 40546, USA.
  2. Qing-Ming Gao: Department of Plant Pathology, University of Kentucky, Lexington, KY, 40546, USA.
  3. R V Chowda-Reddy: Department of Agronomy, Iowa State University, Ames, IA, 50011, USA.
  4. Asheesh K Singh: Department of Agronomy, Iowa State University, Ames, IA, 50011, USA. ORCID
  5. Pradeep Kachroo: Department of Plant Pathology, University of Kentucky, Lexington, KY, 40546, USA. ORCID
  6. Aardra Kachroo: Department of Plant Pathology, University of Kentucky, Lexington, KY, 40546, USA. apkach2@uky.edu.

Abstract

Glycerol-3-phosphate (G3P) is a well-known mobile regulator of systemic acquired resistance (SAR), which provides broad spectrum systemic immunity in response to localized foliar pathogenic infections. We show that G3P-derived foliar immunity is also activated in response to genetically-regulated incompatible interactions with nitrogen-fixing bacteria. Using gene knock-down we show that G3P is essential for strain-specific exclusion of non-desirable root-nodulating bacteria and the associated foliar pathogen immunity in soybean. Grafting studies show that while recognition of rhizobium incompatibility is root driven, bacterial exclusion requires G3P biosynthesis in the shoot. Biochemical analyses support shoot-to-root transport of G3P during incompatible rhizobia interaction. We describe a root-shoot-root signaling mechanism which simultaneously enables the plant to exclude non-desirable nitrogen-fixing rhizobia in the root and pathogenic microbes in the shoot.

References

  1. Cell Microbiol. 2012 Mar;14(3):334-42 [PMID: 22168434]
  2. Cell Microbiol. 2003 Mar;5(3):143-53 [PMID: 12614458]
  3. Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):1075-80 [PMID: 17215350]
  4. Curr Opin Plant Biol. 2013 Aug;16(4):527-33 [PMID: 23870750]
  5. Plant Cell. 2012 Dec;24(12):5123-41 [PMID: 23221596]
  6. Nature. 2003 Oct 9;425(6958):637-40 [PMID: 14534591]
  7. Plant Physiol. 2014 May 28;165(3):1269-1284 [PMID: 24872380]
  8. Nat Rev Microbiol. 2007 Aug;5(8):619-33 [PMID: 17632573]
  9. Bioinformatics. 2014 Apr 1;30(7):923-30 [PMID: 24227677]
  10. Science. 2003 Oct 24;302(5645):630-3 [PMID: 12947035]
  11. Proc Natl Acad Sci U S A. 2013 Oct 15;110(42):17131-6 [PMID: 24082124]
  12. FEMS Microbiol Lett. 2008 Aug;285(1):1-9 [PMID: 18616593]
  13. Plant Physiol. 2012 Dec;160(4):2155-72 [PMID: 23077241]
  14. Nat Genet. 2011 May;43(5):421-7 [PMID: 21441932]
  15. Curr Opin Plant Biol. 2014 Aug;20:127-34 [PMID: 24929297]
  16. Nucleic Acids Res. 2012 May;40(10):4288-97 [PMID: 22287627]
  17. Nature. 2010 Jan 14;463(7278):178-83 [PMID: 20075913]
  18. Annu Rev Phytopathol. 2014;52:347-75 [PMID: 24906124]
  19. Curr Opin Plant Biol. 2005 Aug;8(4):383-9 [PMID: 15939664]
  20. Plant Cell. 2016 Jan;28(1):102-29 [PMID: 26672068]
  21. Trends Biochem Sci. 2010 Apr;35(4):199-207 [PMID: 20096590]
  22. Plant Sci. 2019 Feb;279:81-86 [PMID: 30709496]
  23. Plant Cell. 2002 May;14(5):1005-15 [PMID: 12034893]
  24. Nat Rev Microbiol. 2009 Apr;7(4):312-20 [PMID: 19270720]
  25. Mol Plant Microbe Interact. 2012 Feb;25(2):139-50 [PMID: 21995763]
  26. Nat Commun. 2014 Sep 19;5:4983 [PMID: 25236855]
  27. Nature. 2017 Mar 15;543(7645):328-336 [PMID: 28300100]
  28. Nat Commun. 2018 Aug 7;9(1):3139 [PMID: 30087346]
  29. Nature. 2015 Jul 16;523(7560):308-12 [PMID: 26153863]
  30. Proc Natl Acad Sci U S A. 2010 Oct 26;107(43):18735-40 [PMID: 20937853]
  31. New Phytol. 2016 Nov;212(3):627-636 [PMID: 27411159]
  32. J Bacteriol. 1988 Oct;170(10):4846-54 [PMID: 3049552]
  33. Mol Cell Biol. 1994 Jun;14(6):4135-44 [PMID: 8196651]
  34. Science. 2018 Oct 12;362(6411):233-236 [PMID: 30166437]
  35. Science. 2005 Jun 17;308(5729):1786-9 [PMID: 15961668]
  36. Annu Rev Genet. 2011;45:119-44 [PMID: 21838550]
  37. Plant Physiol. 2007 May;144(1):324-35 [PMID: 17369436]
  38. Microbiol Rev. 1995 Mar;59(1):124-42 [PMID: 7708010]
  39. Cell Host Microbe. 2016 Apr 13;19(4):541-9 [PMID: 27078071]
  40. New Phytol. 2014 Apr;202(2):485-498 [PMID: 24372490]
  41. Front Plant Sci. 2018 Mar 09;9:313 [PMID: 29593768]
  42. Mol Plant Microbe Interact. 2005 Nov;18(11):1161-74 [PMID: 16353551]
  43. J Bacteriol. 1981 Mar;145(3):1129-36 [PMID: 7009569]
  44. Bioinformatics. 2013 Jan 1;29(1):15-21 [PMID: 23104886]
  45. Science. 2009 Apr 3;324(5923):89-91 [PMID: 19342588]
  46. Plant Cell Environ. 2019 Jan;42(1):41-51 [PMID: 29808564]
  47. Breed Sci. 2012 Jan;61(5):544-53 [PMID: 23136493]
  48. Science. 2005 Jun 17;308(5729):1789-91 [PMID: 15961669]
  49. Methods. 2001 Dec;25(4):402-8 [PMID: 11846609]
  50. Mol Plant Microbe Interact. 2009 Jan;22(1):86-95 [PMID: 19061405]
  51. Virology. 2006 Jan 20;344(2):401-11 [PMID: 16226780]
  52. Nucleic Acids Res. 2012 Jan;40(Database issue):D1178-86 [PMID: 22110026]
  53. Curr Opin Plant Biol. 1998 Aug;1(4):299-304 [PMID: 10066602]
  54. Nature. 2006 Nov 16;444(7117):323-9 [PMID: 17108957]
  55. Sci Adv. 2018 May 30;4(5):eaar4509 [PMID: 29854946]
  56. Cell Rep. 2014 Apr 24;7(2):348-355 [PMID: 24726369]
  57. New Phytol. 2004 Sep;163(3):661-668 [PMID: 33873748]

MeSH Term

Gene Knockdown Techniques
Glycerophosphates
Plant Immunity
Plant Proteins
Plant Roots
Plant Shoots
Rhizobium
Signal Transduction
Glycine max
Symbiosis

Chemicals

Glycerophosphates
Plant Proteins
alpha-glycerophosphoric acid