Integrated multi-omics analysis unravels the floral scent characteristics and regulation in "Hutou" multi-petal jasmine.

Jingping Fang, Linwei Zhou, Qinchang Chen, Jinbin Wang, Ying Zhuang, Shaoqing Lin, Hansong Yan, Kai Zhao, Jisen Zhang, Robert J Henry
Author Information
  1. Jingping Fang: College of Life Science, Fujian Normal University, Fuzhou, China. jinphia@fjnu.edu.cn. ORCID
  2. Linwei Zhou: College of Life Science, Fujian Normal University, Fuzhou, China.
  3. Qinchang Chen: College of Life Science, Fujian Normal University, Fuzhou, China. cqc2511@163.com. ORCID
  4. Jinbin Wang: College of Life Science, Fujian Normal University, Fuzhou, China.
  5. Ying Zhuang: College of Life Science, Fujian Normal University, Fuzhou, China.
  6. Shaoqing Lin: College of Life Science, Fujian Normal University, Fuzhou, China.
  7. Hansong Yan: Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, China.
  8. Kai Zhao: College of Life Science, Fujian Normal University, Fuzhou, China.
  9. Jisen Zhang: Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, China. ORCID
  10. Robert J Henry: Queensland Alliance for Agriculture and Food Innovation, University of Queensland, Brisbane, QLD, Australia.

Abstract

The multi-petal "Hutou" jasmine (Jasminum sambac var. Trifoliatum) is highly valued for bonsai cultivation and landscape design, however, the aroma profile and mechanisms underlying floral scent formation remain elusive. In this study, we generate a nearly complete telomere-to-telomere (T2T) genome assembly of "Hutou" jasmine (487.45���Mb with contig N50 of 38.93���Mb). Metabolomic profiling unveils that 16 significantly differential volatiles (SDVs) may play a crucial role in the formation of flower aroma. Among them, five scented SDVs, particularly ��-farnesene and pentanoic acid 1-ethenyl-1,5-dimethyl-4-hexenyl ester, contribute to the characteristic aroma profile of "Hutou" jasmine flowers. Weighted gene co-expression network analysis (WGCNA) identifies HTWRKY41, HTWRKY53, and HTHSP90 as the hub genes potentially regulating the production of these 16 metabolites. The expression of selected genes and duplication events drive the increased relative content of major sesquiterpenoids in terpenoid biosynthetic pathway. Four structural genes (BEAT3, BSMT1, BPBT2, and BPBT3) are potentially implicated in the emission of downstream key volatile esters (benzyl acetate, methyl benzoate, and benzyl benzoate) in the phenylpropanoids synthesis. Our integrated dataset of genomics, transcriptomics, and metabolomics present here provides a theoretical basis for the practical utilization of fragrance and genetic improvement in horticultural applications of "Hutou" jasmine.

References

  1. Nucleic Acids Res. 2018 Nov 30;46(21):e126 [PMID: 30107434]
  2. Bioinformatics. 2009 May 15;25(10):1329-30 [PMID: 19349283]
  3. Bioinformatics. 2009 Jul 15;25(14):1754-60 [PMID: 19451168]
  4. Plant Physiol. 2018 Feb;176(2):1410-1422 [PMID: 29233850]
  5. Plant Physiol. 2004 Aug;135(4):1993-2011 [PMID: 15286288]
  6. Planta. 2016 Apr;243(4):909-23 [PMID: 26721646]
  7. BMC Plant Biol. 2024 Apr 1;24(1):232 [PMID: 38561659]
  8. Bioinformatics. 2014 Apr 1;30(7):923-30 [PMID: 24227677]
  9. Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:47-65 [PMID: 15012203]
  10. J Agric Food Chem. 2023 Nov 6;: [PMID: 37930796]
  11. J Exp Bot. 2011 Nov;62(15):5497-508 [PMID: 21868399]
  12. Plant Cell Environ. 2014 Aug;37(8):1936-49 [PMID: 24588567]
  13. Nat Plants. 2019 Aug;5(8):833-845 [PMID: 31383970]
  14. Nucleic Acids Res. 2012 Apr;40(7):e49 [PMID: 22217600]
  15. Plant Sci. 2021 Sep;310:110960 [PMID: 34315585]
  16. Natl Sci Rev. 2021 Sep 27;9(1):nwab180 [PMID: 35079411]
  17. Front Plant Sci. 2022 Mar 10;13:860157 [PMID: 35360336]
  18. Phytochemistry. 2016 Feb;122:230-237 [PMID: 26675361]
  19. Cell Syst. 2016 Jul;3(1):95-8 [PMID: 27467249]
  20. Hortic Res. 2022 Jan 18;: [PMID: 35039835]
  21. Plant Physiol Biochem. 2012 Jun;55:93-102 [PMID: 22562019]
  22. Curr Biol. 2010 May 11;20(9):R392-7 [PMID: 20462477]
  23. Curr Biol. 2024 Aug 5;34(15):3550-3563.e8 [PMID: 39043188]
  24. Molecules. 2017 Mar 29;22(4): [PMID: 28353656]
  25. Bioinformatics. 2013 Oct 1;29(19):2487-9 [PMID: 23842809]
  26. OMICS. 2012 May;16(5):284-7 [PMID: 22455463]
  27. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  28. Bioinformatics. 2014 May 1;30(9):1312-3 [PMID: 24451623]
  29. Nat Prod Res. 2015;29(14):1328-35 [PMID: 25583067]
  30. Trends Genet. 2023 Oct;39(10):787-801 [PMID: 37633768]
  31. BMC Plant Biol. 2024 Sep 14;24(1):861 [PMID: 39272034]
  32. Ecol Lett. 2010 May;13(5):643-56 [PMID: 20337694]
  33. Genomics Proteomics Bioinformatics. 2023 Feb;21(1):127-149 [PMID: 36587654]
  34. Genome Biol. 2020 Sep 14;21(1):245 [PMID: 32928274]
  35. Mol Plant. 2020 Aug 3;13(8):1194-1202 [PMID: 32585190]
  36. Front Plant Sci. 2017 Apr 12;8:565 [PMID: 28446918]
  37. Curr Opin Plant Biol. 2015 Jun;25:17-22 [PMID: 25909859]
  38. Bioinformatics. 2018 Sep 1;34(17):i884-i890 [PMID: 30423086]
  39. Trends Plant Sci. 2002 Jul;7(7):301-8 [PMID: 12119167]
  40. Trends Plant Sci. 2008 Dec;13(12):619-23 [PMID: 18948055]
  41. Biochimie. 2013 Jan;95(1):79-85 [PMID: 22705387]
  42. Plant Methods. 2005 Dec 18;1:13 [PMID: 16359558]
  43. Nucleic Acids Res. 1999 Jan 15;27(2):573-80 [PMID: 9862982]
  44. Food Chem. 2019 Jul 15;286:170-178 [PMID: 30827592]
  45. Bioinformatics. 2015 Oct 1;31(19):3210-2 [PMID: 26059717]
  46. Nat Plants. 2018 Sep;4(9):721-729 [PMID: 30127411]
  47. Plants (Basel). 2020 Jun 23;9(6): [PMID: 32585874]
  48. Annu Rev Plant Biol. 2013;64:665-700 [PMID: 23451776]
  49. Int J Mol Sci. 2019 Aug 16;20(16): [PMID: 31426432]
  50. Nat Commun. 2019 Jan 3;10(1):15 [PMID: 30604768]
  51. Proc Natl Acad Sci U S A. 2020 Apr 28;117(17):9451-9457 [PMID: 32300014]
  52. Plants (Basel). 2021 Dec 21;11(1): [PMID: 35009018]
  53. Nucleic Acids Res. 2021 Jul 2;49(W1):W293-W296 [PMID: 33885785]
  54. Bot Stud. 2017 Nov 15;58(1):50 [PMID: 29143225]
  55. Genome Res. 2009 Sep;19(9):1639-45 [PMID: 19541911]
  56. BMC Bioinformatics. 2008 Jan 14;9:18 [PMID: 18194517]
  57. New Phytol. 2020 Jul;227(1):24-37 [PMID: 32297991]
  58. J Agric Food Chem. 2002 Aug 14;50(17):4878-84 [PMID: 12166975]
  59. Ann Bot. 2006 Dec;98(6):1253-9 [PMID: 17060364]
  60. J Exp Bot. 2014 Sep;65(17):5077-92 [PMID: 25013119]
  61. Nat Commun. 2020 Mar 18;11(1):1432 [PMID: 32188846]
  62. J Exp Bot. 2008;59(3):609-18 [PMID: 18256048]
  63. Nat Plants. 2024 Aug;10(8):1184-1200 [PMID: 39103456]
  64. Nat Prod Commun. 2010 Jan;5(1):157-62 [PMID: 20184043]
  65. Plant Cell. 2012 Dec;24(12):4948-60 [PMID: 23263767]
  66. Curr Protoc Bioinformatics. 2009 Mar;Chapter 4:4.10.1-4.10.14 [PMID: 19274634]
  67. PLoS One. 2017 Apr 18;12(4):e0176026 [PMID: 28419158]
  68. Nat Methods. 2021 Feb;18(2):170-175 [PMID: 33526886]
  69. Nat Commun. 2024 Apr 8;15(1):3041 [PMID: 38589412]
  70. Plant Physiol. 2011 Dec;157(4):2081-93 [PMID: 21988879]
  71. Plant J. 2011 Apr;66(1):212-29 [PMID: 21443633]
  72. Food Chem. 2021 Apr 2;357:129654 [PMID: 33866239]
  73. Plant Biol (Stuttg). 2011 Nov;13(6):918-24 [PMID: 21972888]
  74. Biochemistry. 2011 Apr 12;50(14):2919-30 [PMID: 21361343]
  75. Nat Rev Mol Cell Biol. 2019 Nov;20(11):665-680 [PMID: 31253954]
  76. Bioinformatics. 2020 May 1;36(9):2896-2898 [PMID: 31971576]
  77. Hortic Res. 2019 Sep 7;6:106 [PMID: 31645961]
  78. J Exp Bot. 2023 Feb 13;74(4):1275-1290 [PMID: 36433929]
  79. Methods. 2001 Dec;25(4):402-8 [PMID: 11846609]
  80. BMC Bioinformatics. 2008 Dec 29;9:559 [PMID: 19114008]
  81. Nat Methods. 2015 Apr;12(4):357-60 [PMID: 25751142]
  82. Nucleic Acids Res. 2012 Jan;40(Database issue):D1178-86 [PMID: 22110026]
  83. Genomics. 2021 Jan;113(1 Pt 2):1071-1086 [PMID: 33181247]
  84. Phytochemistry. 2005 Jun;66(11):1211-30 [PMID: 15946712]
  85. Cell. 2020 Nov 12;183(4):875-889.e17 [PMID: 33035453]
  86. Bioinformatics. 2011 Mar 15;27(6):764-70 [PMID: 21217122]
  87. Mol Plant. 2016 Dec 5;9(12):1667-1670 [PMID: 27717919]
  88. Nucleic Acids Res. 2007 Jul;35(Web Server issue):W265-8 [PMID: 17485477]
  89. Plant Biotechnol J. 2022 Jul;20(7):1232-1234 [PMID: 35373460]
  90. Nucleic Acids Res. 2021 Sep 20;49(16):9077-9096 [PMID: 34417604]
  91. Genome Biol. 2020 Aug 10;21(1):200 [PMID: 32778152]
  92. Bioinformatics. 2009 Aug 15;25(16):2078-9 [PMID: 19505943]
  93. PLoS One. 2024 Mar 25;19(3):e0300895 [PMID: 38527035]
  94. Genome Biol. 2015 Dec 01;16:259 [PMID: 26619908]
  95. Bioinformatics. 2018 Sep 15;34(18):3094-3100 [PMID: 29750242]
  96. Plant Sci. 2017 Mar;256:25-38 [PMID: 28167035]
  97. Plant J. 2021 May;106(3):616-629 [PMID: 33547688]
  98. Mol Ecol Resour. 2022 Feb;22(2):724-739 [PMID: 34460989]
  99. Heliyon. 2024 Mar 16;10(6):e27817 [PMID: 38545150]
  100. Dermatitis. 2017 Jan/Feb;28(1):14-21 [PMID: 28002230]
  101. Bioinformatics. 2013 Nov 15;29(22):2933-5 [PMID: 24008419]
  102. J Mol Biol. 1990 Oct 5;215(3):403-10 [PMID: 2231712]
  103. Nucleic Acids Res. 2004 Mar 19;32(5):1792-7 [PMID: 15034147]
  104. Nucleic Acids Res. 2007;35(9):3100-8 [PMID: 17452365]

Grants

  1. 2023J01508/Natural Science Foundation of Fujian Province (Fujian Provincial Natural Science Foundation)
  2. 201908350014/China Scholarship Council (CSC)

MeSH Term

Flowers
Odorants
Gene Expression Regulation, Plant
Jasminum
Volatile Organic Compounds
Metabolomics
Transcriptome
Multiomics

Chemicals

Volatile Organic Compounds

Word Cloud

Created with Highcharts 10.0.0"Hutou"jasminearomagenesmulti-petalprofilefloralscentformation16SDVsanalysispotentiallybenzylbenzoateJasminumsambacvarTrifoliatumhighlyvaluedbonsaicultivationlandscapedesignhowevermechanismsunderlyingremainelusivestudygeneratenearlycompletetelomere-to-telomereT2Tgenomeassembly48745���MbcontigN503893���MbMetabolomicprofilingunveilssignificantlydifferentialvolatilesmayplaycrucialroleflowerAmongfivescentedparticularly��-farnesenepentanoicacid1-ethenyl-15-dimethyl-4-hexenylestercontributecharacteristicflowersWeightedgeneco-expressionnetworkWGCNAidentifiesHTWRKY41HTWRKY53HTHSP90hubregulatingproductionmetabolitesexpressionselectedduplicationeventsdriveincreasedrelativecontentmajorsesquiterpenoidsterpenoidbiosyntheticpathwayFourstructuralBEAT3BSMT1BPBT2BPBT3implicatedemissiondownstreamkeyvolatileestersacetatemethylphenylpropanoidssynthesisintegrateddatasetgenomicstranscriptomicsmetabolomicspresentprovidestheoreticalbasispracticalutilizationfragrancegeneticimprovementhorticulturalapplicationsIntegratedmulti-omicsunravelscharacteristicsregulation

Similar Articles

Cited By