UV-B mediated metabolic rearrangements in poplar revealed by non-targeted metabolomics

Plant Cell and Environment

Volumn 38, Issue 5, 2015, Pages 892-904

  Kaling, Moritz ^a   Kanawati, Basem ^a   Ghirardo, Andrea ^a   Albert, Andreas ^a   Winkler, Jana Barbro ^a   Heller, Werner ^a   Barta, Csengele ^b   Loreto, Francesco ^c   Schmitt Kopplin, Philippe ^a   Schnitzler, Jörg Peter ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b MISSOURI WESTERN STATE UNIVERSITY   (United States)

^c CNR   (Italy)

Author keywords

Fourier transform ion cyclotron resonance mass spectrometry; Populus canescens

Indexed keywords

POPULUS; POPULUS ALBA X POPULUS TREMULA;

1,3 BUTADIENE DERIVATIVE; HEMITERPENE; ISOPRENE; PENTANE; PHENOL DERIVATIVE;

CONFOCAL MICROSCOPY; GENETICS; METABOLISM; METABOLOME; METABOLOMICS; PHOTOSYNTHESIS; POPULUS; RADIATION RESPONSE; SECRETION (PROCESS);

BUTADIENES; HEMITERPENES; METABOLOME; METABOLOMICS; MICROSCOPY, CONFOCAL; PENTANES; PHENOLS; PHOTOSYNTHESIS; POPULUS;

EID: 84927715966     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12348     Document Type: Article

References (90)

1. Agati G., Matteini P., Goti A. & Tattini M. (2007) Chloroplast-located flavonoids can scavenge singlet oxygen. The New Phytologist 174, 77-89.
2. Agati G., Azzarello E., Pollastri S. & Tattini M. (2012) Flavonoids as antioxidants in plants: location and functional significance. Plant Science 196, 67-76.
3. Aharoni A., Ric de Vos C.H., Verhoeven H.A., Maliepaard C.A., Kruppa G., Bino R. & Goodenowe D. (2002) Nontargeted metabolome analysis by use of Fourier transform ion cyclotron mass spectrometry. Omics: A Journal of Integrative Biology 6, 217-234.
4. von Arnim A.G. & Deng X.-W. (1994) Light inactivation of arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell 79, 1035-1045.
5. Behnke K., Ehlting B., Teuber M., Bauerfeind M., Louis S., Hasch R. & Schnitzler J.P. (2007) Transgenic, non-isoprene emitting poplars don't like it hot. The Plant Journal 51, 485-499.
6. Behnke K., Kaiser A., Zimmer I., Bruggemann N., Janz D., Polle A. & Schnitzler J.P. (2010) RNAi-mediated suppression of isoprene emission in poplar transiently impacts phenolic metabolism under high temperature and high light intensities: a transcriptomic and metabolomic analysis. Plant Molecular Biology 74, 61-75.
7. Behnke K., Grote R., Bruggemann N., Zimmer I., Zhou G.W., Elobeid M. & Schnitzler J.P. (2012) Isoprene emission-free poplars - a chance to reduce the impact from poplar plantations on the atmosphere. New Phytologist 194, 70-82.
8. Behnke K., Ghirardo A., Janz D., Kanawati B., Esperschuetz J., Zimmer I. & Rosenkranz M. (2013) Isoprene function in two contrasting poplars under salt and sunflecks. Tree Physiology 33, 562-578.
9. Brisson L., Vacha W.E.K. & Ibrahim R.K. (1986) Localization of partially methylated flavonol glucosides in Chrysosplenium americanum. II. Immunofluorescence. Plant Science 44, 175-181.
10. Britt A.B. (1995) Repair of DNA damage induced by ultraviolet radiation. Plant Physiology 108, 891-896.
11. Brüggemann N. & Schnitzler J.P. (2002) Comparison of isoprene emission, intercellular isoprene concentration and photosynthetic performance in water-limited oak (Quercus pubescens Willd. and Quercus robur L.) saplings. Plant Biology 4, 456-463.
12. Burchard P., Bilger W. & Weissenböck G. (2000) Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultravioletinduced chlorophyll fluorescence measurements. Plant, Cell & Environment 23, 1373-1380.
13. Caldwell M.M. (1971) Solar UV irradiation and the growth and development of higher plants. In Photophysiology, Vol. 6 (ed. A.C. Giese ), pp. 131-177. Academic Press, New York.
14. Caldwell M.M., Bornman J.F., Ballare C.L., Flint S.D. & Kulandaivelu G. (2007) Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with other climate change factors. Photochemical & Photobiological Sciences 6, 252-266.
15. Carletti P., Masi A., Wonisch A., Grill D., Tausz M. & Ferretti M. (2003) Changes in antioxidant and pigment pool dimensions in UV-B irradiated maize seedlings. Environmental and Experimental Botany 50, 149-157.
16. Chang K.-G., Fechner G.H. & Schroeder H.A. (1989) Notes: anthocyanins in autumn leaves of quaking aspen in colorado. Forest Science 35, 229-236.
17. Charest P.M., Brisson L. & Ibrahim R.K. (1986) Ultrastructural features of flavonoid accumulation in leaf cells of Chrysosplenium americanum. Protoplasma 134, 95-101.
18. Costa H., Gallego S.M. & Tomaro M.L. (2002) Effect of UV-B radiation on antioxidant defense system in sunflower cotyledons. Plant Science 162, 939-945.
19. Dizengremel P., Vaultier M.-N., Le Thiec D., Cabané M., Bagard M., Gérant D. & Jolivet Y. (2012) Phosphoenolpyruvate is at the crossroads of leaf metabolic responses to ozone stress. The New Phytologist 195, 512-517.
20. Dubos C., Stracke R., Grotewold E., Weisshaar B., Martin C. & Lepiniec L. (2010) MYB transcription factors in Arabidopsis. Trends in Plant Science 15, 573-581.
21. Forcisi S., Moritz F., Kanawati B., Tziotis D., Lehmann R. & Schmitt-Kopplin P. (2013) Liquid chromatography-mass spectrometry in metabolomics research: mass analyzers in ultra high pressure liquid chromatography coupling. Journal of Chromatography. A 1292, 51-65.
22. 2 emissions after C-13-labeling: online tracing of C translocation dynamics in poplar plants. PLoS ONE 6, e17393.
23. Ghirardo A., Heller W., Fladung M., Schnitzler J.P. & Schroeder H. (2012) Function of defensive volatiles in pedunculate oak (Quercus robur) is tricked by the moth Tortrix viridana. Plant, Cell & Environment 35, 2192-2207.
24. Gil M., Pontin M., Berli F., Bottini R. & Piccoli P. (2012) Metabolism of terpenes in the response of grape (Vitis vinifera L.) leaf tissues to UV-B radiation. Phytochemistry 77, 89-98.
25. Gonzalez A., Zhao M., Leavitt J.M. & Lloyd A.M. (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. The Plant Journal 53, 814-827.
26. Green A.E.S., Sawada T. & Shettle E.P. (1974) The middle ultraviolet reaching the ground. Photochemistry and Photobiology 19, 251-259.
27. Haldimann P., Fracheboud Y. & Stamp P. (1995) Carotenoid composition in Zea mays developed at sub-optimal temperature and different light intensities. Physiologia Plantarum 95, 409-414.
28. Hansel A., Jordan A., Holzinger R., Prazeller P., Vogel W. & Lindinger W. (1995) Proton transfer reaction mass spectrometry: on-line trace gas analysis at the ppb level. International Journal of Mass Spectrometry and Ion Processes 149-150, 609-619.
29. Hanson D.T. & Sharkey T.D. (2001) Rate of acclimation of the capacity for isoprene emission in response to light and temperature. Plant, Cell & Environment, 24, 937-946.
30. Harborne J.B. & Williams C.A. (2000) Advances in flavonoid research since 1992. Phytochemistry 55, 481-504.
31. Harley P., Deem G., Flint S. & Caldwell M. (1996) Effects of growth under elevated UV-B on photosynthesis and isoprene emission in Quercus gambelii and Mucuna pruriens. Global Change Biology 2, 149-154.
32. Heijde M. & Ulm R. (2012) UV-B photoreceptor-mediated signalling in plants. Trends in Plant Science 17, 230-237.
33. Heine G.F., Hernandez J.M. & Grotewold E. (2004) Two cysteines in plant R2R3 MYB domains participate in REDOX-dependent DNA binding. The Journal of Biological Chemistry 279, 37878-37885.
34. Hideg E., Jansen M. & Strid A. (2013) UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends in Plant Science 18, 107-115.
35. Hoch W.A., Singsaas E.L. & McCown B.H. (2003) Resorption protection. Anthocyanins facilitate nutrient recovery in autumn by shielding leaves from potentially damaging light levels. Plant Physiology 133, 1296-1305.
36. Huang T., Tohge T., Lytovchenko A., Fernie A.R. & Jander G. (2010) Pleiotropic physiological consequences of feedback-insensitive phenylalanine biosynthesis in Arabidopsis thaliana. The Plant Journal 63, 823-835.
37. Hutzler P., Fischbach R., Heller W., Jungblut T.P., Reuber S., Schmitz R. & Schnitzler J.P. (1998) Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy. Journal of Experimental Botany 49, 953-965.
38. Ibrahim R.K., De Luca V., Khouri H., Latchinian L., Brisson L. & Charest P.M. (1987) Enzymology and compartmentation of polymethylated flavonol glucosides in chrysosplenium americanum. Phytochemistry 26, 1237-1245.
39. Jansen M.A.K., Gaba V. & Greenberg B. (1998) Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends in Plant Science 3, 131-135.
40. Jenkins G.I. (2009) Signal transduction in responses to UV-B radiation. Annual Review of Plant Biology 60, 407-431.
41. Jiao Y., Lau O.S. & Deng X.W. (2007) Light-regulated transcriptional networks in higher plants. Nature Review Genetics 8, 217-230.
42. Kaspar S., Matros A. & Mock H.P. (2010) Proteome and flavonoid analysis reveals distinct responses of epidermal tissue and whole leaves upon UV-B radiation of barley (Hordeum vulgare L.) seedlings. Journal of Proteome Research 9, 2402-2411.
43. Kim S., Yun E., Hossain M.A., Lee H. & Kim K. (2012) Global profiling of ultraviolet-induced metabolic disruption in Melissa officinalis by using gas chromatography-mass spectrometry. Analytical and Bioanalytical Chemistry 404, 553-562.
44. Koes R., Verweij W. & Quattrocchio F. (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends in Plant Science 10, 236-242.
45. Kusano M., Tohge T., Fukushima A., Kobayashi M., Hayashi N., Otsuki H. & Fernie A.R. (2011) Metabolomics reveals comprehensive reprogramming involving two independent metabolic responses of Arabidopsis to UV-B light. The Plant Journal 67, 354-369.
46. Lake J.A., Field K.J., Davey M.P., Beerling D.J. & Lomax B.H. (2009) Metabolomic and physiological responses reveal multi-phasic acclimation of Arabidopsis thaliana to chronic UV radiation. Plant, Cell & Environment 32, 1377-1389.
47. Landry L.G., Chapple C.C.S. & Last R.L. (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiology 109, 1159-1166.
48. Lau O.S. & Deng X.W. (2012) The photomorphogenic repressors COP1 and DET1: 20years later. Trends in Plant Science 17, 584-593.
49. Lavola A. (1998) Accumulation of flavonoids and related compounds in birch induced by UV-B irradiance. Tree Physiology 18, 53-58.
50. Li J., Oulee T.M., Raba R., Amundson R.G. & Last R.L. (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. The Plant Cell 5, 171-179.
51. Li Z. & Sharkey T.D. (2013) Metabolic profiling of the methylerythritol phosphate pathway reveals the source of post-illumination isoprene burst from leaves. Plant, Cell & Environment 36, 429-437.
52. Lidon F.J.C., Teixeira M. & Ramalho J.C. (2012) Decay of the chloroplast pool of ascorbate switches on the oxidative burst in UV-B-irradiated rice. Journal of Agronomy and Crop Science 198, 130-144.
53. Loreto F. & Schnitzler J.P. (2010) Abiotic stresses and induced BVOCs. Trends in Plant Science 15, 154-166.
54. Lucio M., Fekete A., Frommberger M. & Schmitt-Kopplin P. (2011) Metabolomics: high-resolution tools offer to follow bacterial growth on a molecular level. In: Handbook of Molecular Microbial Ecology I, pp. 683-695. John Wiley & Sons, Inc.
55. Maeda H. & Dudareva N. (2012) The shikimate pathway and aromatic amino acid biosynthesis in plants. Annual Review of Plant Biology 63, 73-105.
56. Martens H. & Martens M. (2000) Modified Jack-knife estimation of parameter uncertainty in bilinear modelling by partial least squares regression (PLSR). Food Quality and Preference 11, 5-16.
57. Monson R.K., Jones R.T., Rosenstiel T.N. & Schnitzler J.-P. (2013) Why only some plants emit isoprene. Plant, Cell & Environment 36, 503-516.
58. Oikawa A., Nakamura Y., Ogura T., Kimura A., Suzuki H., Sakurai N., ... Ohta D. (2006) Clarification of pathway-specific inhibition by fourier transform ion cyclotron resonance/mass spectrometry-based metabolic phenotyping studies. Plant Physiology, 142, 398-413.
59. Pietta P.-G. (2000) Flavonoids as antioxidants. Journal of Natural Products 63, 1035-1042.
60. Quideau S., Deffieux D., Douat-Casassus C. & Pouységu L. (2011) Plant polyphenols: chemical properties, biological activities, and synthesis. Angewandte Chemie International Edition 50, 586-621.
61. Razal R.A., Ellis S., Singh S., Lewis N.G. & Towers G.H.N. (1996) Nitrogen recycling in phenylpropanoid metabolism. Phytochemistry 41, 31-35.
62. Riederer M. & Schreiber L. (2001) Protecting against water loss: analysis of the barrier properties of plant cuticles. Journal of Experimental Botany 52, 2023-2032.
63. Ries G., Heller W., Puchta H., Sandermann H., Seidlitz H.K. & Hohn B. (2000) Elevated UV-B radiation reduces genome stability in plants. Nature 406, 98-101.
64. Rizzini L., Favory J.J., Cloix C., Faggionato D., O'Hara A., Kaiserli E. & Ulm R. (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332, 103-106.
65. Schmelzer E., Jahnen W. & Hahlbrock K. (1988) In situ localization of light-induced chalcone synthase mRNA, chalcone synthase, and flavonoid end products in epidermal cells of parsley leaves. Proceedings of the National Academy of Sciences 85, 2989-2993.
66. Schnitzler J.P., Jungblut T.P., Heller W., Kofferlein M., Hutzler P., Heinzmann U. & Sandermann H. (1996) Tissue localization of UV-B-screening pigments and of chalcone synthase mRNA in needles of Scots pine seedlings. The New Phytologist 132, 247-258.
67. Schnitzler J.P., Louis S., Behnke K. & Loivamaki M. (2010) Poplar volatiles - biosynthesis, regulation and (eco)physiology of isoprene and stress-induced isoprenoids. Plant Biology 12, 302-316.
68. Seckmeyer G., Pissulla D., Glandorf M., Henriques D., Johnsen B., Webb A. & Carvalho F. (2008) Variability of UV irradiance in Europe. Photochemistry and Photobiology 84, 172-179.
69. Sharkey T. & Loreto F. (1993) Water stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves. Oecologia 95, 328-333.
70. Sharkey T.D. & Yeh S.S. (2001) Isoprene emission from plants. Annual Review of Plant Physiology and Plant Molecular Biology 52, 407-436.
71. Shin D.H., Choi M., Kim K., Bang G., Cho M., Choi S.-B. & Park Y.-I. (2013) HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis. FEBS Letters 587, 1543-1547.
72. Shinbo Y., Nakamura Y., Altaf-Ul-Amin M., Asahi H., Kurokawa K., Arita M., ... Kanaya S. (2006) KNApSAcK: a comprehensive species-metabolite relationship database. In: Plant Metabolomics (eds K. Saito, R. Dixon, & L. Willmitzer ), pp. 165-181. Springer Berlin Heidelberg.
73. Sims D.A. & Gamon J.A. (2002) Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sensing of Environment 81, 337-354.
74. Smith C., O'Maille G., Want E., Qin C., Trauger S., Brandon T., ... Siuzdak G. (2005) METLIN - A metabolite mass spectral database. Therapeutic Drug Monitoring, 27, 747-751.
75. Strid A., Chow W.S. & Anderson J.M. (1994) UV-B damage and protection at the molecular level in plants. Photosynthesis Research 39, 475-489.
76. Suhre K. & Schmitt-Kopplin P. (2008) MassTRIX: mass translator into pathways. Nucleic Acids Research, 36, 481-484.
77. Tanaka Y., Sasaki N. & Ohmiya A. (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. The Plant Journal 54, 733-749.
78. Thayer S. & Björkman O. (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynthesis Research 23, 331-343.
79. Thiel S., Döhring T., Köfferlein M., Kosak A., Martin P. & Seidlitz H. (1996) A phytotron for plant stress research: how far can artificial lighting compare to natural sunlight? Journal of Plant Physiology 148, 456-463.
80. Tiiva P., Rinnan R., Faubert P., Räsänen J., Holopainen T., Kyrö E. & Holopainen J.K. (2007) Isoprene emission from a subarctic peatland under enhanced UV-B radiation. The New Phytologist 176, 346-355.
81. Tossi V., Amenta M., Lamattina L. & Cassia R. (2011) Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway. Plant, Cell & Environment 34, 909-921.
82. Vanderauwera S., Zimmermann P., Rombauts S., Vandenabeele S., Langebartels C., Gruissem W. & Van Breusegem F. (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiology 139, 806-821.
83. Warren J., Bassman J., Fellman J., Mattinson D. & Eigenbrode S. (2003) Ultraviolet-B radiation alters phenoloc salicylate and flavonoid composition of Populus trichocarpa leaves. Tree Physiology 23, 527-535.
84. 2 reduces metabolic and physiological differences between isoprene- and non-isoprene-emitting poplars. The New Phytologist 200, 534-546.
85. Winkel-Shirley B. (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology 126, 485-493.
86. Woodall G.S. & Stewart G.R. (1998) Do anthocyanins play a role in UV protection of the red juvenile leaves of Syzygium? Journal of Experimental Botany 49, 1447-1450.
87. 2. Plant Physiology 115, 1405-1412.
88. Zhang P., Dreher K., Karthikeyan A., Chi A., Pujar A., Caspi R., ... Rhee S.Y. (2010) Creation of a genome-wide metabolic pathway database for populus trichocarpa using a new approach for reconstruction and curation of metabolic pathways for plants. Plant Physiology, 153, 1479-1491.
89. Zhou B., Miao Q., Yang L. & Liu Z.-L. (2005) Antioxidative effects of flavonols and their glycosides against the free-radical-induced peroxidation of linoleic acid in solution and in micelles. Chemistry - A European Journal 11, 680-691.
90. Zhou J.-M., Gold N.D., Martin V.J.J., Wollenweber E. & Ibrahim R.K. (2006) Sequential O-methylation of tricetin by a single gene product in wheat. Biochimica et Biophysica Acta (BBA) - General Subjects 1760, 1115-1124.