Imaging Metabolic Flow of Water in Plants with Isotope-Traced Stimulated Raman Scattering Microscopy.

Simin Bi, Jianpeng Ao, Ting Jiang, Xianmiao Zhu, Yimin Zhu, Weibing Yang, Binglian Zheng, Minbiao Ji
Author Information
  1. Simin Bi: State Key Laboratory of Surface Physics and Department of Physics, Academy for Engineering and Technology, Human Phenome Institute, Key Laboratory of Micro and Nano Photonic Structures (Ministry of Education), Shanghai Key Laboratory of Metasurfaces for Light Manipulation, Fudan University, Shanghai, 200433, China.
  2. Jianpeng Ao: State Key Laboratory of Surface Physics and Department of Physics, Academy for Engineering and Technology, Human Phenome Institute, Key Laboratory of Micro and Nano Photonic Structures (Ministry of Education), Shanghai Key Laboratory of Metasurfaces for Light Manipulation, Fudan University, Shanghai, 200433, China.
  3. Ting Jiang: State Key Laboratory of Genetic Engineering, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200438, China.
  4. Xianmiao Zhu: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  5. Yimin Zhu: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  6. Weibing Yang: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  7. Binglian Zheng: State Key Laboratory of Genetic Engineering, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200438, China.
  8. Minbiao Ji: State Key Laboratory of Surface Physics and Department of Physics, Academy for Engineering and Technology, Human Phenome Institute, Key Laboratory of Micro and Nano Photonic Structures (Ministry of Education), Shanghai Key Laboratory of Metasurfaces for Light Manipulation, Fudan University, Shanghai, 200433, China. ORCID

Abstract

Water plays a vital role in the life cycle of plants, participating in various critical biochemical reactions during both non-photosynthetic and photosynthetic processes. Direct visualization of the metabolic activities of water in plants with high spatiotemporal resolution is essential to reveal the functional utilization of water. Here, stimulated Raman scattering (SRS) microscopy is applied to monitor the metabolic processes of deuterated water (DO) in model plant Arabidopsis thaliana (A. thaliana). The work shows that in plants uptaking DO/water solution, proton-transfer from water to organic metabolites results in the formation of C-D bonds in newly synthesized biomolecules (lipid, protein, and polysaccharides, etc.) that allow high-resolution detection with SRS. Reversible metabolic pathways of oil-starch conversion between seed germination and seed development processes are verified. Spatial heterogeneity of metabolic activities along the vertical axis of plants (root, stem, and tip meristem), as well as the radial distributions of secondary growth on the horizontal cross-sections are quantified. Furthermore, metabolic flow of protons from plants to animals is visualized in aphids feeding on A. thaliana. Collectively, SRS microscopy has potential to trace a broad range of matter flows in plants, such as carbon storage and nutrition metabolism.

Keywords

References

  1. Annu Rev Plant Biol. 2020 Apr 29;71:217-245 [PMID: 32075407]
  2. Front Plant Sci. 2016 May 26;7:734 [PMID: 27303426]
  3. Plant Physiol. 2002 Sep;130(1):347-61 [PMID: 12226514]
  4. Nat Protoc. 2012 Sep;7(9):1694-708 [PMID: 22918387]
  5. Anal Chem. 2015 Sep 15;87(18):9436-42 [PMID: 26291845]
  6. Cell. 1997 Feb 7;88(3):299-308 [PMID: 9039256]
  7. Plant Cell. 2009 Nov;21(11):3518-34 [PMID: 19915089]
  8. J Agric Food Chem. 2014 Mar 26;62(12):2595-604 [PMID: 24640947]
  9. Curr Biol. 2021 Aug 9;31(15):3365-3373.e7 [PMID: 34129827]
  10. Mol Plant. 2023 Jan 2;16(1):43-63 [PMID: 36114669]
  11. Plant J. 2010 Aug;63(4):680-95 [PMID: 20525007]
  12. J Biol Chem. 1961 Apr;236:988-95 [PMID: 13690532]
  13. Plant Physiol. 2006 Nov;142(3):839-54 [PMID: 16963520]
  14. Nat Biomed Eng. 2019 May;3(5):402-413 [PMID: 31036888]
  15. Annu Rev Plant Biol. 2008;59:115-42 [PMID: 18444898]
  16. ACS Cent Sci. 2020 Apr 22;6(4):478-486 [PMID: 32341997]
  17. Science. 2010 Dec 3;330(6009):1368-70 [PMID: 21127249]
  18. Analyst. 2021 Feb 22;146(4):1234-1238 [PMID: 33355541]
  19. Plant Methods. 2014 May 29;10:14 [PMID: 24917885]
  20. Hortic Res. 2019 Jun 1;6:72 [PMID: 31231530]
  21. Angew Chem Int Ed Engl. 2021 Mar 29;60(14):7637-7642 [PMID: 33491852]
  22. Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1577-82 [PMID: 11171993]
  23. Anal Chem. 2018 Jun 5;90(11):6362-6366 [PMID: 29757615]
  24. Am J Bot. 2013 Jan;100(1):143-52 [PMID: 23002165]
  25. Plant Cell. 2002 Jan;14(1):47-56 [PMID: 11826298]
  26. Proc Natl Acad Sci U S A. 2013 Mar 26;110(13):E1232-41 [PMID: 23476065]
  27. Nat Plants. 2016 Jan 06;2:15206 [PMID: 27250753]
  28. Opt Express. 2013 Jun 3;21(11):13864-74 [PMID: 23736639]
  29. Nat Commun. 2018 Aug 6;9(1):2995 [PMID: 30082908]
  30. Anal Chem. 2013 May 21;85(10):5055-63 [PMID: 23581493]
  31. Adv Sci (Weinh). 2020 Aug 16;7(19):2001452 [PMID: 33042757]
  32. Nat Methods. 2014 Apr;11(4):410-2 [PMID: 24584195]
  33. Plant J. 2022 Feb;109(4):745-763 [PMID: 34997626]
  34. Nat Commun. 2017 Nov 21;8(1):1646 [PMID: 29158483]
  35. Ann Bot. 2020 Sep 14;126(4):511-537 [PMID: 31641747]
  36. Biomed Opt Express. 2019 Jul 10;10(8):3860-3874 [PMID: 31452980]
  37. Adv Sci (Weinh). 2024 Nov;11(42):e2407543 [PMID: 39301930]
  38. Nat Rev Mol Cell Biol. 2014 May;15(5):301-12 [PMID: 24755933]
  39. Anal Chem. 2021 Dec 21;93(50):16796-16803 [PMID: 34870976]
  40. Adv Sci (Weinh). 2022 May;9(15):e2105437 [PMID: 35319171]
  41. Science. 2008 Dec 19;322(5909):1857-61 [PMID: 19095943]
  42. Nature. 2017 Mar 15;543(7645):355-365 [PMID: 28300093]
  43. Plant Cell Environ. 2006 Sep;29(9):1715-29 [PMID: 16913861]
  44. New Phytol. 2020 Aug;227(3):698-713 [PMID: 32242934]
  45. Cells. 2020 Mar 20;9(3): [PMID: 32244921]
  46. J Biol Chem. 2003 Aug 8;278(32):29442-53 [PMID: 12759349]
  47. Science. 2012 Nov 23;338(6110):1055-60 [PMID: 23180856]
  48. Proc Natl Acad Sci U S A. 2008 Apr 22;105(16):6196-201 [PMID: 18408160]
  49. Biotechnol Biofuels. 2016 Nov 22;9:256 [PMID: 27895710]
  50. Plant Cell. 2002 Sep;14(9):2191-213 [PMID: 12215515]
  51. Plant Methods. 2023 Jul 14;19(1):71 [PMID: 37452400]
  52. Aging Cell. 2022 Apr;21(4):e13586 [PMID: 35257470]
  53. J Exp Bot. 2011 Mar;62(6):2179-88 [PMID: 21209027]
  54. Anal Chem. 2013 Jan 2;85(1):98-106 [PMID: 23198914]
  55. Angew Chem Int Ed Engl. 2014 Oct 27;53(44):11787-92 [PMID: 25195517]
  56. Annu Rev Plant Biol. 2016 Apr 29;67:179-206 [PMID: 26845499]
  57. Int J Biol Macromol. 2022 Mar 31;202:256-268 [PMID: 35032493]
  58. Opt Express. 2020 May 11;28(10):15663-15677 [PMID: 32403589]
  59. Nat Commun. 2021 Aug 3;12(1):4682 [PMID: 34344886]
  60. Annu Rev Plant Biol. 2016 Apr 29;67:153-78 [PMID: 26735064]
  61. Plant Cell Environ. 2011 Nov;34(11):1835-48 [PMID: 21707653]
  62. Biochem J. 2007 Jan 1;401(1):13-28 [PMID: 17150041]
  63. J Integr Plant Biol. 2013 Apr;55(4):294-388 [PMID: 23462277]
  64. Trends Plant Sci. 2015 Oct;20(10):676-685 [PMID: 26440436]
  65. Anal Chem. 2022 Jun 28;94(25):8899-8908 [PMID: 35699644]
  66. J Pharm Anal. 2022 Oct;12(5):719-724 [PMID: 36320597]
  67. Tree Physiol. 2014 Aug;34(8):796-818 [PMID: 24907466]
  68. Science. 2014 Aug 8;345(6197):1255215 [PMID: 25104393]
  69. Curr Opin Chem Biol. 2022 Oct;70:102181 [PMID: 35792373]
  70. Plant Cell. 2006 Mar;18(3):665-75 [PMID: 16473965]

Grants

  1. 2021YFF0502900/National Key Research and Development Program of China
  2. 62425501/National Natural Science Foundation of China
  3. 23dz2260100/Municipal Natural Science Foundation of Shanghai
  4. 22Y11907500/Shanghai Municipal Science and Technology Project
  5. 21Y11910500/Shanghai Municipal Science and Technology Project

MeSH Term

Arabidopsis
Water
Nonlinear Optical Microscopy
Animals
Spectrum Analysis, Raman

Chemicals

Water

Word Cloud

Created with Highcharts 10.0.0plantsmetabolicwaterprocessesRamanSRSthalianaWateractivitiesstimulatedscatteringmicroscopyplantseedmetabolismplaysvitalrolelifecycleparticipatingvariouscriticalbiochemicalreactionsnon-photosyntheticphotosyntheticDirectvisualizationhighspatiotemporalresolutionessentialrevealfunctionalutilizationappliedmonitordeuteratedDOmodelArabidopsisworkshowsuptakingDO/watersolutionproton-transferorganicmetabolitesresultsformationC-Dbondsnewlysynthesizedbiomoleculeslipidproteinpolysaccharidesetcallowhigh-resolutiondetectionReversiblepathwaysoil-starchconversiongerminationdevelopmentverifiedSpatialheterogeneityalongverticalaxisrootstemtipmeristemwellradialdistributionssecondarygrowthhorizontalcross-sectionsquantifiedFurthermoreflowprotonsanimalsvisualizedaphidsfeedingCollectivelypotentialtracebroadrangematterflowscarbonstoragenutritionImagingMetabolicFlowPlantsIsotope-TracedStimulatedScatteringMicroscopylabel‐freeimagingscience

Similar Articles

Cited By