Progress in NMR-based metabolomics of Catharanthus roseus
Qifang PAN,Jingya ZHAO,Yuliang WANG,Kexuan TANG()
Joint International Research Laboratory of Metabolic & Developmental Sciences, Key Laboratory of Urban Agriculture (South), Ministry of Agriculture, Plant Biotechnology Research Center, Fudan-SJTU-Nottingham Plant Biotechnology R&D Center, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China
Metabolomics has been rapidly developed as an important field in plant sciences and natural products chemistry. As the only natural source for a diversity of monoterpenoid indole alkaloids (MIAs), especially the low-abundance antitumor agents vinblastine and vincristine, Catharanthus roseus is highly valued and has been studied extensively as a model for medicinal plants improvement. Due to multistep enzymatic biosynthesis and complex regulation, genetic modification in the MIA pathway has resulted in complicated changes of both secondary and primary metabolism in C. roseus, affecting not only the MIA pathway but also other pathways. Research at the metabolic level is necessary to increase knowledge on the genetic regulation of the whole metabolic network connected to MIA biosynthesis. Nuclear magnetic resonance (NMR) is a very suitable and powerful complementary technique for the identification and quantification of metabolites in the plant matrix. NMR-based metabolomics has been used in studies of C. roseus for pathway elucidation, understanding stress responses, classification among different cultivars, safety and quality controls of transgenic plants, cross talk between pathways, and diversion of carbon fluxes, with the aim of fully unravelling MIA biosynthesis, its regulation and the function of the alkaloids in the plant from a systems biology point of view.
Miettinen K, Dong L, Navrot N, Schneider T, Burlat V, Pollier J, Woittiez L, van der Krol S, Lugan R, Ilc T, Verpoorte R, Oksman-Caldentey K M, Martinoia E, Bouwmeester H, Goossens A, Memelink J, Werck-Reichhart D. The seco-iridoid pathway from Catharanthus roseus. Nature Communications, 2014, 5: 3606
https://doi.org/10.1038/ncomms4606
pmid: 24710322
4
De Luca V, Salim V, Thamm A, Masada S A, Yu F. Making iridoids/secoiridoids and monoterpenoid indole alkaloids: progress on pathway elucidation. Current Opinion in Plant Biology, 2014, 19: 35–42
https://doi.org/10.1016/j.pbi.2014.03.006
pmid: 24709280
Choi Y H, Tapias E C, Kim H K, Lefeber A W M, Erkelens C, Verhoeven J T J, Brzin J, Zel J, Verpoorte R. Metabolic discrimination of Catharanthus roseus leaves infected by phytoplasma using 1H-NMR spectroscopy and multivariate data analysis. Plant Physiology, 2004, 135(4): 2398–2410
https://doi.org/10.1104/pp.104.041012
pmid: 15286294
8
Sriram G, Fulton D B, Shanks J V. Flux quantification in central carbon metabolism of Catharanthus roseus hairy roots by 13C labeling and comprehensive bondomer balancing. Phytochemistry, 2007, 68(16−18): 2243–2257
https://doi.org/10.1016/j.phytochem.2007.04.009
pmid: 17532015
9
Toki K, Saito N, Irie Y, Tatsuzawa F, Shigihara A, Honda T. 7-O-Methylated anthocyanidin glycosides from Catharanthus roseus. Phytochemistry, 2008, 69(5): 1215–1219
https://doi.org/10.1016/j.phytochem.2007.11.005
pmid: 18164044
10
Chung I M, Ahmad A, Ali M, Lee O K, Kim M Y, Kim J H, Yoon D Y, Peebles C A M, San K Y. Flavonoid glucosides from the hairy roots of Catharanthus roseus. Journal of Natural Products, 2009, 72(4): 613–620
https://doi.org/10.1021/np800378q
pmid: 19271765
11
Yang S O, Kim S H, Kim Y, Kim H S, Chun Y J, Choi H K. Metabolic discrimination of Catharanthus roseus calli according to their relative locations using 1H-NMR and principal component analysis. Bioscience, Biotechnology, and Biochemistry, 2009, 73(9): 2032–2036
https://doi.org/10.1271/bbb.90240
pmid: 19734668
12
Mustafa N R, Kim H K, Choi Y H, Verpoorte R. Metabolic changes of salicylic acid-elicited Catharanthus roseus cell suspension cultures monitored by NMR-based metabolomics. Biotechnology Letters, 2009, 31(12): 1967–1974
https://doi.org/10.1007/s10529-009-0107-1
pmid: 19701606
13
Mustafa N R, Kim H K, Choi Y H, Erkelens C, Lefeber A W M, Spijksma G, van der Heijden R, Verpoorte R. Biosynthesis of salicylic acid in fungus elicited Catharanthus roseus cells. Phytochemistry, 2009, 70(4): 532–539
https://doi.org/10.1016/j.phytochem.2009.01.009
pmid: 19251288
14
Pan Q, Dai Y, Nuringtyas T R, Mustafa N R, Schulte A E, Verpoorte R, Choi Y H. Investigation of the chemomarkers correlated with flower colour in different organs of Catharanthus roseus using NMR-based metabolomics. Phytochemical Analysis, 2014, 25(1): 66–74
https://doi.org/10.1002/pca.2464
pmid: 24151112
15
Pan Q, Wang Q, Yuan F, Xing S, Zhao J, Choi Y H, Verpoorte R, Tian Y, Wang G, Tang K. Overexpression of ORCA3 and G10H in Catharanthus roseus plants regulated alkaloid biosynthesis and metabolism revealed by NMR-metabolomics. PLoS ONE, 2012, 7(8): e43038
https://doi.org/10.1371/journal.pone.0043038
pmid: 22916202
16
Pan Q, Mustafa N R, Tang K, Choi Y H, Verpoorte R. Monoterpenoid indole alkaloids biosynthesis and its regulation in Catharanthus roseus: a literature review from genes to metabolites. Phytochemistry Reviews, 2015, DOI: 10.1007/s11101–015–9406–4 (first published online)
17
Mahrous E A, Farag M A. Two dimensional NMR spectroscopic approaches for exploring plant metabolome: a review. Journal of Advanced Research, 2015, 6(1): 3–15
https://doi.org/10.1016/j.jare.2014.10.003
pmid: 25685540
18
van der Kooy F, Maltese F, Choi Y H, Kim H K, Verpoorte R. Quality control of herbal material and phytopharmaceuticals with MS and NMR based metabolic fingerprinting. Planta Medica, 2009, 75(7): 763–775
https://doi.org/10.1055/s-0029-1185450
pmid: 19288400
19
Murata J, Luca V D. Localization of tabersonine 16-hydroxylase and 16-OH tabersonine-16-O-methyltransferase to leaf epidermal cells defines them as a major site of precursor biosynthesis in the vindoline pathway in Catharanthus roseus. Plant Journal, 2005, 44(4): 581–594
https://doi.org/10.1111/j.1365-313X.2005.02557.x
pmid: 16262708
20
Murata J, Roepke J, Gordon H, De Luca V. The leaf epidermome of Catharanthus roseus reveals its biochemical specialization. Plant Cell, 2008, 20(3): 524–542
https://doi.org/10.1105/tpc.107.056630
pmid: 18326827
21
Ratcliffe R G, Shachar-Hill Y. Revealing metabolic phenotypes in plants: inputs from NMR analysis. Biological Reviews of the Cambridge Philosophical Society, 2005, 80(1): 27–43
https://doi.org/10.1017/S1464793104006530
pmid: 15727037
22
Stephanopoulos G, Stafford D E. Metabolic engineering: a new frontier of chemical reaction engineering. Chemical Engineering Science, 2002, 57(14): 2595–2602
https://doi.org/10.1016/S0009-2509(02)00088-X
Kim S W, Ban S H, Jeong S C, Chung H J, Ko S M, Yoo O J, Liu J R. Genetic discrimination between Catharanthus roseus cultivars by metabolic fingerprinting using1H NMR spectra of aromatic compounds. Biotechnology and Bioprocess Engineering, 2007, 12(6): 646–652
https://doi.org/10.1007/BF02931081
25
Hoekenga O A. Using metabolomics to estimate unintended effects in transgenic crop plants: problems, promises, and opportunities. Journal of Biomolecular Techniques, 2008, 19(3): 159–166
pmid: 19137102
26
Contin A, van der Heijden R, Lefeber A W M, Verpoorte R. The iridoid glucoside secologanin is derived from the novel triose phosphate/pyruvate pathway in a Catharanthus roseus cell culture. FEBS Letters, 1998, 434(3): 413–416
https://doi.org/10.1016/S0014-5793(98)01022-9
pmid: 9742965
27
Muljono R A B, Scheffer J J C, Verpoorte R. Isochorismate is an intermediate in 2, 3-dihydroxybenzoic acid biosynthesis in Catharanthus roseus cell cultures. Plant Physiology and Biochemistry, 2002, 40(3): 231–234
https://doi.org/10.1016/S0981-9428(02)01369-4
28
Schuhr C A, Radykewicz T, Sagner S, Latzel C, Zenk M H, Arigoni D, Bacher A, Rohdich F, Eisenreich W. Quantitative assessment of crosstalk between the two isoprenoid biosynthesis pathways in plants by NMR spectroscopy. Phytochemistry Reviews, 2003, 2(1−2): 3–16
https://doi.org/10.1023/B:PHYT.0000004180.25066.62
29
Sriram G, González-Rivera O, Shanks J V. Determination of biomass composition of Catharanthus roseus hairy roots for metabolic flux analysis. Biotechnology Progress, 2006, 22(6): 1659–1663
pmid: 17137315
30
Fukushima A, Kusano M, Redestig H, Arita M, Saito K. Integrated omics approaches in plant systems biology. Current Opinion in Chemical Biology, 2009, 13(5−6): 532–538
https://doi.org/10.1016/j.cbpa.2009.09.022
pmid: 19837627
31
Urbanczyk-Wochniak E, Luedemann A, Kopka J, Selbig J, Roessner-Tunali U, Willmitzer L, Fernie A R. Parallel analysis of transcript and metabolic profiles: a new approach in systems biology. EMBO Reports, 2003, 4(10): 989–993
https://doi.org/10.1038/sj.embor.embor944
pmid: 12973302
32
Okazaki Y, Shimojima M, Sawada Y, Toyooka K, Narisawa T, Mochida K, Tanaka H, Matsuda F, Hirai A, Hirai M Y, Ohta H, Saito K. A chloroplastic UDP-glucose pyrophosphorylase from Arabidopsis is the committed enzyme for the first step of sulfolipid biosynthesis. Plant Cell, 2009, 21(3): 892–909
https://doi.org/10.1105/tpc.108.063925
pmid: 19286968
33
Lackman P, González-Guzmán M, Tilleman S, Carqueijeiro I, Pérez A C, Moses T, Seo M, Kanno Y, Häkkinen S T, Van Montagu M C, Thevelein J M, Maaheimo H, Oksman-Caldentey K M, Rodriguez P L, Rischer H, Goossens A. Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(14): 5891–5896
https://doi.org/10.1073/pnas.1103010108
pmid: 21436041
34
Rischer H, Orešič M, Seppänen-Laakso T, Katajamaa M, Lammertyn F, Ardiles-Diaz W, Van Montagu M C, Inzé D, Oksman-Caldentey K M, Goossens A. Gene-to-metabolite networks for terpenoid indole alkaloid biosynthesis in Catharanthus roseus cells. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(14): 5614–5619
https://doi.org/10.1073/pnas.0601027103
pmid: 16565214