Growth-limiting drought stress induces time-of-day-dependent transcriptome and physiological responses in hybrid poplar.

Sean M Robertson, Solihu Kayode Sakariyahu, Ayooluwa Bolaji, Mark F Belmonte, Olivia Wilkins
Author Information
  1. Sean M Robertson: Department of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, Canada. ORCID
  2. Solihu Kayode Sakariyahu: Department of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, Canada. ORCID
  3. Ayooluwa Bolaji: Department of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, Canada. ORCID
  4. Mark F Belmonte: Department of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, Canada. ORCID
  5. Olivia Wilkins: Department of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, Canada. ORCID

Abstract

Drought stress negatively impacts the health of long-lived trees. Understanding the genetic mechanisms that underpin response to drought stress is requisite for selecting or enhancing climate change resilience. We aimed to determine how hybrid poplars respond to prolonged and uniform exposure to drought; how responses to moderate and more severe growth-limiting drought stresses differed; and how drought responses change throughout the day. We established hybrid poplar trees ( × 'Okanese') from unrooted stem cutting with abundant soil moisture for 6 weeks. We then withheld water to establish well-watered, moderate and severe growth-limiting drought conditions. These conditions were maintained for 3 weeks during which growth was monitored. We then measured photosynthetic rates and transcriptomes of leaves that had developed during the drought treatments at two times of day. The moderate and severe drought treatments elicited distinct changes in growth and development, photosynthetic rates and global transcriptome profiles. Notably, the time of day of sampling produced the strongest effect in the transcriptome data. The moderate drought treatment elicited global transcriptome changes that were intermediate to the severe and well-watered treatments in the early evening but did not elicit a strong drought response in the morning. Stable drought conditions that are sufficient to limit plant growth elicit distinct transcriptional profiles depending on the degree of water limitation and on the time of day at which they are measured. There appears to be a limited number of genes and functional gene categories that are responsive to all of the tested drought conditions in this study emphasizing the complex nature of drought regulation in long-lived trees.

Keywords

References

  1. Environ Sci Pollut Res Int. 2016 Sep;23(17):17647-55 [PMID: 27236444]
  2. Plant Mol Biol. 2019 Sep;101(1-2):1-19 [PMID: 31062216]
  3. Nat Biotechnol. 2019 Aug;37(8):907-915 [PMID: 31375807]
  4. J Environ Manage. 2007 Nov;85(3):672-9 [PMID: 17110018]
  5. PLoS One. 2011;6(6):e16907 [PMID: 21694767]
  6. Tree Physiol. 2003 Nov;23(16):1125-36 [PMID: 14522718]
  7. Plant Cell Physiol. 2021 Oct 11;62(6):1012-1029 [PMID: 34059891]
  8. J Exp Bot. 2015 Jul;66(14):4373-81 [PMID: 25954045]
  9. Bioinformatics. 2009 Aug 15;25(16):2078-9 [PMID: 19505943]
  10. Sci Rep. 2019 Mar 18;9(1):4814 [PMID: 30886204]
  11. Plant Cell. 2021 Aug 13;33(7):2164-2182 [PMID: 33871647]
  12. Sci Rep. 2015 Jun 10;5:11108 [PMID: 26059057]
  13. Plant J. 2019 Jan;97(1):40-55 [PMID: 30444573]
  14. Bioinformatics. 2014 Apr 1;30(7):923-30 [PMID: 24227677]
  15. Plant Physiol. 2016 Oct;172(2):734-748 [PMID: 27246097]
  16. Proc Natl Acad Sci U S A. 2011 Jul 26;108(30):12521-6 [PMID: 21746919]
  17. Tree Physiol. 2016 Jul;36(7):909-28 [PMID: 27174702]
  18. Plant J. 2010 Sep;63(5):715-27 [PMID: 20553421]
  19. Mol Plant. 2013 Mar;6(2):311-22 [PMID: 23015761]
  20. Nucleic Acids Res. 2002 Jan 1;30(1):207-10 [PMID: 11752295]
  21. Plant Cell Environ. 2009 Dec;32(12):1724-36 [PMID: 19671097]
  22. Elife. 2020 Sep 30;9: [PMID: 32996462]
  23. J Exp Bot. 2012 Aug;63(13):4959-71 [PMID: 22760471]
  24. Bioinformatics. 2014 Aug 1;30(15):2114-20 [PMID: 24695404]
  25. Nat Plants. 2021 May;7(5):579-586 [PMID: 33723429]
  26. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  27. Nature. 2020 Feb;578(7796):572-576 [PMID: 32051590]
  28. Genome Biol. 2008;9(8):R130 [PMID: 18710561]
  29. Physiol Plant. 2014 Aug;151(4):480-94 [PMID: 24320774]
  30. PeerJ. 2017 Dec 1;5:e4088 [PMID: 29209576]
  31. Plant Cell Environ. 2017 Feb;40(2):180-189 [PMID: 27479938]
  32. Plant Cell. 2016 Oct;28(10):2365-2384 [PMID: 27655842]
  33. J Exp Bot. 2020 Jun 26;71(13):3765-3779 [PMID: 31768543]
  34. Tree Physiol. 2014 Nov;34(11):1203-19 [PMID: 24178982]
  35. Elife. 2015 Nov 26;4: [PMID: 26609814]
  36. EMBO J. 2013 Feb 20;32(4):511-23 [PMID: 23241948]
  37. Mol Ecol. 2014 Dec;23(23):5771-90 [PMID: 25319679]
  38. Bioinformatics. 2010 Jan 1;26(1):139-40 [PMID: 19910308]
  39. Physiol Plant. 2009 Jun;136(2):150-68 [PMID: 19453505]
  40. Plant Biol (Stuttg). 2012 Jul;14(4):612-20 [PMID: 22188382]
  41. Plant Physiol. 2011 Jun;156(2):803-15 [PMID: 21474437]
  42. Plant Cell. 2005 Dec;17(12):3257-81 [PMID: 16299223]
  43. New Phytol. 2019 Jun;222(4):1789-1802 [PMID: 30681725]
  44. Bioinformatics. 2008 Mar 1;24(5):719-20 [PMID: 18024473]
  45. EMBO J. 2009 Dec 2;28(23):3745-57 [PMID: 19816401]
  46. Plant Cell Environ. 2010 Oct;33(10):1742-55 [PMID: 20525001]
  47. Science. 2006 Sep 15;313(5793):1596-604 [PMID: 16973872]
  48. Plant Cell. 2016 Feb;28(2):345-66 [PMID: 26842464]
  49. AoB Plants. 2017 Dec 01;10(1):plx067 [PMID: 29354257]
  50. Plant J. 2009 Nov;60(4):703-15 [PMID: 19682285]
  51. PLoS One. 2014 Jan 27;9(1):e86402 [PMID: 24475115]
  52. Tree Physiol. 2019 Dec 16;39(11):1855-1866 [PMID: 31595965]
  53. Plant Sci. 2012 Oct;195:24-35 [PMID: 22920996]
  54. Plant Cell Environ. 2019 Jul;42(7):2259-2273 [PMID: 29981147]
  55. Nucleic Acids Res. 2012 Jan;40(Database issue):D1178-86 [PMID: 22110026]
  56. Proc Natl Acad Sci U S A. 2021 Jun 22;118(25): [PMID: 34155145]
  57. Trends Plant Sci. 2006 Jan;11(1):15-9 [PMID: 16359910]
  58. G3 (Bethesda). 2021 Dec 8;11(12): [PMID: 34570202]
  59. BMC Syst Biol. 2013 Mar 19;7:23 [PMID: 23506153]
  60. New Phytol. 2020 Jan;225(2):679-692 [PMID: 31276231]
  61. Science. 2019 Sep 20;365(6459):1291-1295 [PMID: 31604238]
  62. Nat Rev Genet. 2015 Oct;16(10):598-610 [PMID: 26370901]
  63. Nucleic Acids Res. 2017 Jul 3;45(W1):W122-W129 [PMID: 28472432]
  64. Science. 2020 Apr 17;368(6488):261-266 [PMID: 32299945]

Word Cloud

Created with Highcharts 10.0.0droughttranscriptomehybridmoderateseveredayconditionsstresstreeschangeresponsespoplargrowthtreatmentslong-livedresponsegrowth-limitingweekswaterwell-wateredmeasuredphotosyntheticrateseliciteddistinctchangesglobalprofilestimeelicitDroughtnegativelyimpactshealthUnderstandinggeneticmechanismsunderpinrequisiteselectingenhancingclimateresilienceaimeddeterminepoplarsrespondprolongeduniformexposurestressesdifferedthroughoutestablished×'Okanese'unrootedstemcuttingabundantsoilmoisture6withheldestablishmaintained3monitoredtranscriptomesleavesdevelopedtwotimesdevelopmentNotablysamplingproducedstrongesteffectdatatreatmentintermediateearlyeveningstrongmorningStablesufficientlimitplanttranscriptionaldependingdegreelimitationappearslimitednumbergenesfunctionalgenecategoriesresponsivetestedstudyemphasizingcomplexnatureregulationGrowth-limitinginducestime-of-day-dependentphysiologicalClimatehigh-throughputsequencing

Similar Articles

Cited By