Differential expression of major genes involved in the biosynthesis of aliphatic glucosinolates in intergeneric Baemoochae (Brassicaceae) and its parents during development
- 25 Downloads
Thus study found the temporal and spatial relationship between production of aliphatic glucosinolate compounds and the expression profile of glucosinolate-related genes during growth and development in radish, Chinese cabbage, and their intergeneric hybrid baemoochae plants.
Glucosinolates (GSLs) are one of major bioactive compounds in Brassicaceae plants. GSLs play a role in defense against microbes as well as chemo-preventative activity against cancer, which draw attentions from plant scientists. We investigated the temporal relationship between production of aliphatic Glucosinolate (GSLs) compounds and the expression profile of GSL related genes during growth and development in radish, Chinese cabbage, and their intergeneric hybrid, baemoochae. Over the complete life cycle, Glucoraphasatin (GRH) and glucoraphanin (GRE) predominated in radish, whereas gluconapin (GNP), glucobrassicanapin (GBN), and glucoraphanin (GRA) abounded in Chinese cabbage. Baemoochae contained intermediate levels of all GSLs studied, indicating inheritance from both radish and Chinese cabbage. Expression patterns of BCAT4, CYP79F1, CYP83A1, UGT74B1, GRS1, FMOgs-ox1, and AOP2 genes showed a correlation to their corresponding encoded proteins in radish, Chinese cabbage, and baemoochae. Interestingly, there is a sharp change in gene expression pattern involved in side chain modification, particularly GRS1, FMOgs-ox1, and AOP2, among these plants during the vegetative and reproductive stage. For instance, the GRS1 was strongly expressed during leaf development, while both of FMOgs-ox1 and AOP2 was manifested high in floral tissues. Furthermore, expression of GRS1 gene which is responsible for GRH production was predominantly expressed in leaf tissues of radish and baemoochae, whereas it was only slightly detected in Chinese cabbage root tissue, explaining why radish has an abundance of GRH compared to other Brassica plants. Altogether, our comprehensive and comparative data proved that aliphatic GSLs biosynthesis is dynamically and precisely regulated in a tissue- and development-dependent manner in Brassicaceae family members.
KeywordsRadish Chinese cabbage Baemoochae Glucosinolates GRS1 FMOgs-ox1 AOP2
Glucoraphasatin synthase 1
Flavin monooxygenase 1
2-Oxoglutarate-dependent dioxygenase 2
Ultra-high performance liquid chromatography
Quantitative Real-Time PCR
This research was supported by the CAYSS Program of Chung-Ang University to A.B.D.N. and A.N.P., IPET (Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries) through the Agri-Bio Industry Technology Development Program, funded by the Ministry of Agriculture, Food and Rural Affairs (MAFRA) (112011-5) to J.K. and the start-up funds (201801238-001-00) from Chung-Ang University to D.-H. K.
ABDN and ANP planted all plant materials and performed molecular experiments; NH and ABDN performed U-HPLC and LC–ESI–MS experiments. ABDN and JK planned the experiments; ABDN, NH, D-HK, and JK analyzed the data and wrote the manuscript.
Compliance with ethical standards
Conflict of interest
All authors declare that they have no conflict of interest.
- Andersen TG, Nour-Eldin HH, Fuller VL, Olsen CE, Burow M, Halkier BA (2013) Integration of biosynthesis and long-distance transport establish organ-specific glucosinolate profiles in vegetative Arabidopsis. Plant Cell 25:3133–3145. https://doi.org/10.1105/tpc.113.110890 CrossRefPubMedPubMedCentralGoogle Scholar
- Baek SA, Jung YH, Lim SH, Park SU, Kim JK (2016) Metabolic profiling in Chinese cabbage (Brassica rapa L. subsp. pekinensis) cultivars reveals that glucosinolate content is correlated with carotenoid content. J Agric Food Chem 64:4426–4434. https://doi.org/10.1021/acs.jafc.6b01323 CrossRefPubMedGoogle Scholar
- Fahey JW, Haristoy X, Dolan PM, Kensler TW, Scholtus I, Stephenson KK et al (2002) Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobacter pylori and prevents benzo[a]pyrene-induced stomach tumors. Proc Natl Acad Sci USA 99:7610–7615. https://doi.org/10.1073/PNAS.112203099 CrossRefPubMedGoogle Scholar
- Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol. https://doi.org/10.1146/annurev.arplant.57.032905.105228 CrossRefPubMedGoogle Scholar
- Ishida M, Kakizaki T, Morimitsu Y, Ohara T, Hatakeyama K, Yoshiaki H et al (2015) Novel glucosinolate composition lacking 4-methylthio-3-butenyl glucosinolate in Japanese white radish (Raphanus sativus L.). Theor Appl Genet 128:2037–2046. https://doi.org/10.1007/s00122-015-2564-3 CrossRefPubMedGoogle Scholar
- Kliebenstein DJ, Lambrix VM, Reichelt M, Gershenzon J, Mitchell-Olds T (2001) Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 13:681–693. https://doi.org/10.1105/TPC.13.3.681 CrossRefPubMedPubMedCentralGoogle Scholar
- Kumar S, Chauhan J, Andy A, Meena M (2010) Pattern of glucosinolate changes in Indian mustard (Brassica Juncea L.) during different developmental stages. Indian J Plant Physiol 15:69–72Google Scholar
- Kusznierewicz B, Iori R, Piekarska A, Namieśnik J, Bartoszek A (2013) Convenient identification of desulfoglucosinolates on the basis of mass spectra obtained during liquid chromatography–diode array–electrospray ionisation mass spectrometry analysis: method verification for sprouts of different Brassicaceae species extracts. J Chromatogr A 1278:108–115. https://doi.org/10.1016/J.CHROMA.2012.12.075 CrossRefPubMedGoogle Scholar
- Lee S-S, Choi W-J, Woo J-G (2002) Development of a new vegetable crop in x brassicoraphanus by hybridization of Brassica campestris and Raphanus sativus. Korean J Hortic Sci Technol 43:693–698Google Scholar
- Lee SS, Lee SA, Yang J, Kim J (2011) Developing stable progenies of × Brassicoraphanus, an intergeneric allopolyploid between Brassica rapa and Raphanus sativus, through induced mutation using microspore culture. Theor Appl Genet 122:885–891. https://doi.org/10.1007/s00122-010-1494-3 CrossRefPubMedGoogle Scholar
- Liang X, Lee HW, Li Z, Lu Y, Zou L, Ong CN (2018) Simultaneous quantification of 22 glucosinolates in 12 brassicaceae vegetables by hydrophilic interaction chromatography-tandem mass spectrometry. ACS Omega 3:15546–15553. https://doi.org/10.1021/acsomega.8b01668 CrossRefPubMedPubMedCentralGoogle Scholar
- Mithen RF, Dekker M, Verkerk R, Rabot S, Johnson IT (2000) The nutritional significance, biosynthesis and bioavailability of glucosinolates in human foods. J Sci Food Agric 80:967–984. https://doi.org/10.1002/(SICI)1097-0010(20000515)80:7%3c967:AID-JSFA597%3e3.0.CO;2-V CrossRefGoogle Scholar
- Sotelo T, Soengas P, Velasco P, Rodríguez VM, Cartea ME (2014) Identification of metabolic QTLs and candidate genes for glucosinolate synthesis in Brassica oleracea leaves, seeds and flower buds. PLoS ONE 9:e91428. https://doi.org/10.1371/journal.pone.0091428 CrossRefPubMedPubMedCentralGoogle Scholar
- Wang J, Qiu Y, Wang X, Yue Z, Yang X, Chen X et al (2017) Insights into the species-specific metabolic engineering of glucosinolates in radish (Raphanus sativus L.) based on comparative genomic analysis. Sci Rep 7:1–9. https://doi.org/10.1038/s41598-017-16306-4 CrossRefPubMedPubMedCentralGoogle Scholar
- Zhang Y, Huai D, Yang Q, Cheng Y, Ma M, Kliebenstein DJ et al (2015b) Overexpression of three glucosinolate biosynthesis genes in Brassica napus identifies enhanced resistance to Sclerotinia sclerotiorum and Botrytis cinerea. PLoS ONE 10:1–17. https://doi.org/10.1371/journal.pone.0140491 CrossRefGoogle Scholar
- Zou Z, Ishida M, Li F, Kakizaki T, Suzuki S, Kitashiba H et al (2013) QTL analysis using SNP markers developed by next-generation sequencing for identification of candidate genes controlling 4-methylthio-3-butenyl glucosinolate contents in roots of radish Raphanus sativus L. PLoS One 8:e53541. https://doi.org/10.1371/journal.pone.0053541 CrossRefPubMedPubMedCentralGoogle Scholar
- Zukalová H, Va J (2002) The role and effects of glucosinolates of Brassica species—a review. Rostl. Výroba 48:175–180Google Scholar