'Cry-for-help' in contaminated soil: a dialogue among plants and soil microbiome to survive in hostile conditions.

Eleonora Rolli, Lorenzo Vergani, Elisa Ghitti, Giovanni Patania, Francesca Mapelli, Sara Borin
Author Information
  1. Eleonora Rolli: Department of Food, Environmental and Nutritional Sciences, DeFENS, University of Milan, Via Celoria 2, Milan, 20133, Italy.
  2. Lorenzo Vergani: Department of Food, Environmental and Nutritional Sciences, DeFENS, University of Milan, Via Celoria 2, Milan, 20133, Italy.
  3. Elisa Ghitti: Department of Food, Environmental and Nutritional Sciences, DeFENS, University of Milan, Via Celoria 2, Milan, 20133, Italy.
  4. Giovanni Patania: Department of Food, Environmental and Nutritional Sciences, DeFENS, University of Milan, Via Celoria 2, Milan, 20133, Italy.
  5. Francesca Mapelli: Department of Food, Environmental and Nutritional Sciences, DeFENS, University of Milan, Via Celoria 2, Milan, 20133, Italy.
  6. Sara Borin: Department of Food, Environmental and Nutritional Sciences, DeFENS, University of Milan, Via Celoria 2, Milan, 20133, Italy. ORCID

Abstract

An open question in environmental ecology regards the mechanisms triggered by root chemistry to drive the assembly and functionality of a beneficial microbiome to rapidly adapt to stress conditions. This phenomenon, originally described in plant defence against pathogens and predators, is encompassed in the 'cry-for-help' hypothesis. Evidence suggests that this mechanism may be part of the adaptation strategy to ensure the holobiont fitness in polluted environments. Polychlorinated biphenyls (PCBs) were considered as model pollutants due to their toxicity, recalcitrance and poor phyto-extraction potential, which lead to a plethora of phytotoxic effects and rise environmental safety concerns. Plants have inefficient detoxification processes to catabolize PCBs, even leading to by-products with a higher toxicity. We propose that the 'cry-for-help' mechanism could drive the exudation-mediated recruitment and sustainment of the microbial services for PCBs removal, exerted by an array of anaerobic and aerobic microbial degrading populations working in a complex metabolic network. Through this synergistic interaction, the holobiont copes with the soil contamination, releasing the plant from the pollutant stress by the ecological services provided by the boosted metabolism of PCBs microbial degraders. Improving knowledge of root chemistry under PCBs stress is, therefore, advocated to design rhizoremediation strategies based on plant microbiome engineering.

References

  1. Front Microbiol. 2017 Dec 18;8:2529 [PMID: 29326674]
  2. Appl Microbiol Biotechnol. 2013 Oct;97(20):9245-56 [PMID: 23250224]
  3. Chemosphere. 2008 Nov;73(10):1608-16 [PMID: 18793792]
  4. Plant Cell. 2002;14 Suppl:S239-49 [PMID: 12045280]
  5. Appl Environ Microbiol. 2006 Oct;72(10):6607-14 [PMID: 17021212]
  6. Annu Rev Phytopathol. 2019 Aug 25;57:505-529 [PMID: 31470772]
  7. Chemosphere. 2001 Sep;44(7):1547-55 [PMID: 11545520]
  8. Plant Biol (Stuttg). 2020 Jul;22(4):701-708 [PMID: 32174006]
  9. Environ Microbiol. 2017 Aug;19(8):2992-3011 [PMID: 28401633]
  10. Microb Biotechnol. 2010 Jul;3(4):389-402 [PMID: 21255338]
  11. Proc Natl Acad Sci U S A. 2019 Jun 18;116(25):12558-12565 [PMID: 31152139]
  12. Proc Natl Acad Sci U S A. 2014 Aug 19;111(33):11919-20 [PMID: 25099356]
  13. Chemosphere. 2009 Aug;76(6):740-6 [PMID: 19541345]
  14. Environ Sci Technol. 2014 Feb 18;48(4):2436-44 [PMID: 24467194]
  15. Phytochem Anal. 2017 Jul;28(4):267-276 [PMID: 28146307]
  16. Environ Sci Technol. 2013 Sep 17;47(18):10526-34 [PMID: 23964900]
  17. Appl Microbiol Biotechnol. 2012 Sep;95(6):1589-603 [PMID: 22202970]
  18. Environ Microbiol Rep. 2019 Aug;11(4):479-486 [PMID: 31054200]
  19. Ecotoxicol Environ Saf. 2021 Jan 15;208:111703 [PMID: 33396034]
  20. Microb Cell. 2014 Apr 23;1(5):145-149 [PMID: 28357236]
  21. Sci Total Environ. 2008 Nov 1;405(1-3):14-25 [PMID: 18786697]
  22. Plant Physiol. 2003 May;132(1):146-53 [PMID: 12746520]
  23. Biotechnol Adv. 2000 Mar;18(1):23-34 [PMID: 14538117]
  24. Ecotoxicol Environ Saf. 2018 Aug 15;157:40-60 [PMID: 29605643]
  25. J Hazard Mater. 2017 Feb 15;324(Pt B):701-710 [PMID: 27894756]
  26. Front Microbiol. 2020 Jan 28;11:34 [PMID: 32047489]
  27. Plant Cell Environ. 2015 Aug;38(8):1673-82 [PMID: 25736839]
  28. Front Microbiol. 2017 Jul 25;8:1385 [PMID: 28790991]
  29. Environ Res. 2020 Dec;191:110211 [PMID: 32937175]
  30. Int J Phytoremediation. 2017 Aug 3;19(8):732-738 [PMID: 28121460]
  31. Biotechnol Adv. 2006 May-Jun;24(3):309-20 [PMID: 16413162]
  32. Sci Total Environ. 2017 Jan 1;575:1395-1406 [PMID: 27717569]
  33. Chemosphere. 2012 Sep;88(11):1317-23 [PMID: 22546633]
  34. New Phytol. 2015 Jun;206(4):1196-206 [PMID: 25655016]
  35. Int J Biol Macromol. 2021 Apr 15;176:217-225 [PMID: 33581208]
  36. Curr Opin Biotechnol. 2018 Feb;49:1-9 [PMID: 28732264]
  37. Appl Environ Microbiol. 2007 Oct;73(19):6224-32 [PMID: 17693557]
  38. Environ Sci Pollut Res Int. 2005;12(1):34-48 [PMID: 15768739]
  39. Environ Sci Pollut Res Int. 2002;9(1):73-85 [PMID: 11885420]
  40. Microb Genom. 2020 Apr;6(4): [PMID: 32238227]
  41. Proc Natl Acad Sci U S A. 2020 Feb 18;117(7):3874-3883 [PMID: 32015118]
  42. Mol Plant Microbe Interact. 2017 Jan;30(1):53-62 [PMID: 27937752]
  43. Stand Genomic Sci. 2018 Feb 1;13:3 [PMID: 29435100]
  44. Plant Cell Physiol. 2019 Jul 1;60(7):1405-1419 [PMID: 31076771]
  45. World J Microbiol Biotechnol. 2020 Aug 30;36(10):145 [PMID: 32862310]
  46. Nat Rev Microbiol. 2011 Oct 03;9(11):803-16 [PMID: 21963803]
  47. Int J Mol Sci. 2016 Jul 29;17(8): [PMID: 27483244]
  48. Clin Breast Cancer. 2020 Feb;20(1):12-18 [PMID: 31521536]
  49. Environ Sci Technol. 2016 Apr 5;50(7):3668-75 [PMID: 26928534]
  50. Sci Rep. 2020 Jul 1;10(1):10691 [PMID: 32612150]
  51. Appl Environ Microbiol. 2012 Apr;78(8):2706-15 [PMID: 22327590]
  52. Sci Total Environ. 2019 May 20;666:368-376 [PMID: 30798243]
  53. Sci Total Environ. 2021 Jan 1;750:141411 [PMID: 32841806]
  54. PLoS One. 2013 Nov 13;8(11):e79428 [PMID: 24236133]
  55. ISME J. 2019 Jul;13(7):1647-1658 [PMID: 30796337]
  56. New Phytol. 2021 Mar;229(5):2873-2885 [PMID: 33131088]
  57. Nature. 2005 Apr 7;434(7034):732-7 [PMID: 15815622]
  58. Environ Pollut. 2005 Nov;138(2):290-8 [PMID: 15950342]
  59. Environ Int. 2020 Jun;139:105695 [PMID: 32272295]
  60. Environ Sci Technol. 2019 Sep 17;53(18):10601-10611 [PMID: 31412202]
  61. Sci Total Environ. 2019 Oct 10;686:484-496 [PMID: 31185397]
  62. Sci Total Environ. 2017 Aug 15;592:68-77 [PMID: 28314132]
  63. New Phytol. 2020 Mar;225(5):1899-1905 [PMID: 31571220]
  64. Sci Rep. 2016 Jun 29;6:28958 [PMID: 27353292]
  65. Front Microbiol. 2019 Jun 07;10:1258 [PMID: 31231342]
  66. Curr Opin Microbiol. 2019 Jun;49:73-82 [PMID: 31731229]
  67. Environ Sci Pollut Res Int. 2020 Mar;27(9):8872-8884 [PMID: 31686332]
  68. Proc Natl Acad Sci U S A. 2014 Aug 19;111(33):12103-8 [PMID: 25028492]
  69. Curr Probl Pediatr Adolesc Health Care. 2019 Jun;49(6):133-159 [PMID: 31147261]
  70. Biol Direct. 2018 Oct 26;13(1):24 [PMID: 30621755]
  71. Appl Microbiol Biotechnol. 2019 Feb;103(3):1155-1166 [PMID: 30570692]
  72. Fungal Biol. 2013 Apr;117(4):268-74 [PMID: 23622721]
  73. J Hazard Mater. 2014 Aug 15;278:189-202 [PMID: 24976127]
  74. Nat Microbiol. 2018 Apr;3(4):470-480 [PMID: 29556109]
  75. ISME J. 2010 Feb;4(2):279-85 [PMID: 19776767]
  76. Biotechnol Adv. 2007 Sep-Oct;25(5):442-51 [PMID: 17553651]
  77. Environ Sci Pollut Res Int. 2018 Jan;25(1):12-17 [PMID: 27699658]
  78. Environ Sci Technol. 2018 Aug 7;52(15):8558-8567 [PMID: 29733586]
  79. mSystems. 2018 Jan 23;3(1): [PMID: 29404422]
  80. J Plant Physiol. 2020 Feb;245:153094 [PMID: 31862647]
  81. Sci Total Environ. 2010 Jul 15;408(16):3469-76 [PMID: 20483449]
  82. FEMS Microbiol Ecol. 2010 Jun;72(3):313-27 [PMID: 20370828]
  83. Int J Phytoremediation. 2006;8(3):199-221 [PMID: 17120525]
  84. Chemosphere. 2013 Mar;90(11):2645-53 [PMID: 23290946]
  85. Genes (Basel). 2019 May 27;10(5): [PMID: 31137913]
  86. Trends Plant Sci. 2012 Aug;17(8):478-86 [PMID: 22564542]
  87. Int J Mol Sci. 2021 Mar 24;22(7): [PMID: 33805032]
  88. Plant Cell Rep. 2020 Jan;39(1):3-17 [PMID: 31346716]
  89. Pharmacogenetics. 1994 Oct;4(5):225-41 [PMID: 7894495]
  90. Microb Cell Fact. 2009 Jan 12;8:5 [PMID: 19138404]
  91. J Bacteriol. 2007 Aug;189(15):5705-15 [PMID: 17526697]
  92. J Agric Food Chem. 2020 Sep 30;68(39):10542-10549 [PMID: 32916050]
  93. Proc Natl Acad Sci U S A. 2018 May 29;115(22):E5213-E5222 [PMID: 29686086]
  94. Chemosphere. 2021 Jan;262:128351 [PMID: 33182113]
  95. Environ Microbiol. 2018 Mar;20(3):934-948 [PMID: 29215190]
  96. Environ Sci Pollut Res Int. 2010 Aug;17(7):1355-61 [PMID: 20336492]
  97. Environ Sci Technol. 2020 Aug 18;54(16):10000-10011 [PMID: 32687327]
  98. J Microbiol Methods. 2013 Jul;94(1):30-6 [PMID: 23611840]
  99. Pest Manag Sci. 2019 Sep;75(9):2368-2377 [PMID: 30884099]
  100. Environ Sci Technol. 2010 Apr 15;44(8):2767-76 [PMID: 20384372]
  101. Front Microbiol. 2016 Jun 16;7:933 [PMID: 27379063]
  102. J Biosci Bioeng. 2008 May;105(5):433-49 [PMID: 18558332]
  103. Science. 2019 Nov 1;366(6465):606-612 [PMID: 31672892]
  104. Environ Pollut. 2017 Apr;223:367-375 [PMID: 28118998]
  105. ISME J. 2016 Jan;10(1):265-8 [PMID: 26023875]
  106. Plant J. 2017 Oct;92(1):147-162 [PMID: 28742258]
  107. Chemosphere. 2011 Jun;84(2):199-206 [PMID: 21596420]
  108. PLoS One. 2015 May 13;10(5):e0126033 [PMID: 25970559]
  109. Trends Plant Sci. 2020 Aug;25(8):733-743 [PMID: 32345569]
  110. Plant Methods. 2018 Dec 20;14:114 [PMID: 30598690]
  111. Sci Rep. 2016 Feb 26;6:22145 [PMID: 26915282]
  112. Environ Pollut. 2002;120(3):509-11 [PMID: 12442774]
  113. J Protein Chem. 2003 May;22(4):377-86 [PMID: 13678302]
  114. Environ Pollut. 2008 Sep;155(1):1-12 [PMID: 18035460]
  115. Environ Int. 2004 Aug;30(6):799-804 [PMID: 15120198]
  116. Curr Opin Microbiol. 2002 Jun;5(3):246-53 [PMID: 12057677]
  117. Glob Chang Biol. 2018 Jan;24(1):1-12 [PMID: 28752603]
  118. Front Plant Sci. 2020 Aug 27;11:1179 [PMID: 32983187]
  119. Chemosphere. 2019 Nov;235:969-975 [PMID: 31561313]
  120. Sci Total Environ. 2007 Mar 1;374(1):1-12 [PMID: 17258285]
  121. Curr Opin Plant Biol. 2016 Aug;32:62-68 [PMID: 27393937]
  122. Plants (Basel). 2018 Apr 03;7(2): [PMID: 29614017]
  123. Curr Opin Plant Biol. 2006 Aug;9(4):436-42 [PMID: 16759898]
  124. Appl Environ Microbiol. 2006 Apr;72(4):2331-42 [PMID: 16597927]
  125. Environ Microbiol Rep. 2017 Oct;9(5):589-598 [PMID: 28631340]
  126. Chemosphere. 2007 Oct;69(8):1221-7 [PMID: 17640705]
  127. Sci Total Environ. 2021 Jun 10;772:144825 [PMID: 33581524]
  128. Environ Microbiol. 2004 Aug;6(8):842-50 [PMID: 15250886]
  129. Chemosphere. 2021 Mar;267:129152 [PMID: 33316619]
  130. Front Microbiol. 2018 Feb 15;9:232 [PMID: 29497412]
  131. J Appl Toxicol. 2020 Dec;40(12):1592-1601 [PMID: 32648282]
  132. ISME J. 2012 Feb;6(2):410-21 [PMID: 21881617]
  133. Environ Sci Technol. 2011 Aug 1;45(15):6511-6 [PMID: 21696136]
  134. Environ Sci Technol. 2017 Jun 20;51(12):7263-7270 [PMID: 28541669]
  135. J Exp Bot. 2012 Jun;63(11):3999-4014 [PMID: 22493519]
  136. Nat Commun. 2018 Jul 16;9(1):2738 [PMID: 30013066]
  137. Toxics. 2017 Dec 21;6(1): [PMID: 29267240]

MeSH Term

Biodegradation, Environmental
Environmental Pollution
Microbiota
Polychlorinated Biphenyls
Soil
Soil Microbiology
Soil Pollutants

Chemicals

Soil
Soil Pollutants
Polychlorinated Biphenyls

Word Cloud

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