Glucosinolate Content Varies and Transcriptome Analysis in Different Kale Cultivars (Brassica oleracea var. acephala) Grown in a Vertical Farm

Thi Kim Loan Nguyen; Ga Oun Lee; Jung Su Jo; Jun Gu Lee; Shin-Woo Lee; Ki-Ho Son

doi:10.12791/KSBEC.2022.31.4.332

All Issue

2022 Vol.31, Issue 4 Preview Page Next Page

Original Articles

Glucosinolate Content Varies and Transcriptome Analysis in Different Kale Cultivars (Brassica oleracea var. acephala) Grown in a Vertical Farm 수직농장에서 자란 케일(Brassica oleracea var. acephala) 품종에 따른 글루코시놀레이트 함량의 변화 및 전사체 분석

31 October 2022. pp. 332-342

PDF XML

Abstract

Kale (Brassica oleracea var. acephala) is one of the most frequently consumed leafy vegetables globally, as it contains numerous nutrients; essential amino acids, phenolics, vitamins, and minerals, and is particularly rich in glucosinolates. However, the differences in the biosynthesis of glucosinolates and related gene expression among kale cultivars has been poorly reported. In this study, we investigated glucosinolates profile and content in three different kale cultivars, including green (‘Man-Choo’ and ‘Mat-Jjang’) and red kale (‘Red-Curled’) cultivars grown in a vertical farm, using transcriptomic and metabolomic analyses. The growth and development of the green kale cultivars were higher than those of the red kale cultivar at 6 weeks after cultivation. High-performance liquid chromatography (HPLC) analysis revealed five glucosinolates in the ‘Man-Choo’ cultivar, and four glucosinolates in the ‘Mat-Jjang’ and ‘Red-Curled’ cultivars. Glucobrassicin was the most predominant glucosinolate followed by gluconastrutiin in all the cultivars. In contrast, other glucosinolates were highly dependent to the genotypes. The highest total glucosinolates was found in the ‘Red-Curled’ cultivar, which followed by ‘Man-Choo’ and ‘Mat-Jjang’. Based on transcriptome analysis, eight genes were involved in glucosinolate biosynthesis. The overall results suggest that the glucosinolate content and accumulation patterns differ according to the kale cultivar and differential expression of glucosinolate biosynthetic genes.

Keywords

glucosinolates

growth

kale

metabolome

transcriptome

vertical farms

케일(Brassica oleracea var. acephala)은 필수 아미노산, 비타민, 미네랄과 같은 수많은 영양소를 함유하고 특히 글루코시놀레이트가 풍부하기 때문에 전 세계적으로 가장 많이 소비되는 잎 채소 중 하나이다. 그러나 케일 품종 간의 글루코시놀레이트 합성과 관련된 유전자 발현에 대한 연구는 미비한 실정이다. 본 연구에서는 전사체 및 대사체 분석을 사용하여 식물공장에서 재배된 녹색(만추 및 맛짱) 및 적색 케일 품종(적곱슬)을 포함한 3 가지 케일 품종에서 글루코시놀레이트를 조사하였다. 재배 후 6주된 녹색 케일 품종의 생육 및 발달이 적색 케일 품종에 비해 높았다. High-performance liquid chromatography (HPLC) 분석에서 7가지 글루코시놀레이트를 분석하였다; 만추 품종에서는 5종의 글루코시놀레이트가, 맛짱과 적곱슬 품종에서는 4종의 글루코시놀레이트가 분류되었다. Glucobrassicin은 3가지 케일 품종에서 가장 높은 글루코시놀레이트 였다. 총 글루코시놀레이트 함량은 적곱슬 품종에서 가장 높았다. 전사체 분석에서는 8개의 유전자가 글루코시놀레이트 합성에 관여됨을 확인할 수 있었다. 이러한 결과는 케일 품종에 따라 글루코시놀레이트 함량과 축적 패턴이 다르다는 것을 시사한다.

키워드

글루코시놀레이트

생육

케일

대사체

식물공장

전사체

References

Awasthi S., and N.T. Saraswathi 2016, Elucidating the molecular interaction of sinigrin, a potent anticancer glucosinolate from cruciferous vegetables with bovine serum albumin: effect of methylglyoxal modification. J Biomol Struct Dyn 34:2224-2232. doi:10.1080/07391102.2015.1110835 10.1080/07391102.2015.111083526488200

Ayaz F.A., R.H. Glew, M. Millson, H.S. Huang , L.T. Chuang, C. Sanz , and S. Hayırlıoglu-Ayaz 2006, Nutrient contents of kale (Brassica oleraceae L. var. acephala DC.). Food Chem 96:572-579. doi:10.1016/j.foodchem.2005.03.011 10.1016/j.foodchem.2005.03.011

Bak S., and R. Feyereisen 2001, The involvement of two P450 enzymes, CYP83B1 and CYP83A1, in auxin homeostasis and glucosinolate biosynthesis. Plant Physiol 127:108-118. doi:10.1104/pp.127.1.108 10.1104/pp.127.1.10811553739PMC117967

Burger J., and G.E. Edwards 1996, Photosynthetic efficiency, and photodamage by UV and visible radiation, in red versus green leaf coleus varieties. Plant Cell Physiol 37:395-399. doi:10.1093/oxfordjournals.pcp.a028959 10.1093/oxfordjournals.pcp.a028959

Grubb C.D., and S. Abel 2006, Glucosinolate metabolism and its control. Trends Plant Sci 11:89-100. doi:10.1016/j.tplants.2005.12.006 10.1016/j.tplants.2005.12.00616406306

Grubb C.D., B.J. Zipp, J. Kopycki, M. Schubert, M. Quint, E. K. Lim, D.J. Bowles, M.S.C. Pedras, and S. Abel 2014, Comparative analysis of Arabidopsis UGT 74 glucosyltransferases reveals a special role of UGT 74C1 in glucosinolate biosynthesis. Plant J 79:92-105. doi:10.1111/tpj.12541 10.1111/tpj.1254124779768

Grubb C.D., B.J. Zipp, J. Ludwig‐Müller, M.N. Masuno, T.F. Molinski, and S. Abel 2004, Arabidopsis glucosyltransferase UGT74B1 functions in glucosinolate biosynthesis and auxin homeostasis. Plant J 40:893-908. doi:10.1111/j.1365-313X.2004.02261.x 10.1111/j.1365-313X.2004.02261.x15584955

Herr I., and M.W. Büchler 2010, Dietary constituents of broccoli and other cruciferous vegetables: implications for prevention and therapy of cancer. Cancer Treat Rev 36:377-383. doi:10.1016/j.ctrv.2010.01.002 10.1016/j.ctrv.2010.01.00220172656

Hull A.K., R. Vij, and J.L. Celenza 2000, Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis. Proc Natl Acad Sci 97:2379-2384. doi:10.1073/pnas.040569997 10.1073/pnas.04056999710681464PMC15809

Jahangir M., H.K. Kim, Y.H. Choi, and R. Verpoorte 2009, Health‐affecting compounds in Brassicaceae. Compr Rev Food Sci Food Saf 8:31-43. doi:10.1111/j.1541-4337.2008.00065.x 10.1111/j.1541-4337.2008.00065.x

Jeon J., J.K. Kim, H. Kim H,Y.J. Kim, Y.J. Park, S.J. Kim, C.S. Kim, and S.U. Park 2018, Transcriptome analysis and metabolic profiling of green and red kale (Brassica oleracea var. acephala) seedlings. Food Chem 241:7-13. doi:10.1016/j.foodchem.2017.08.067 10.1016/j.foodchem.2017.08.06728958560

Kim K.H., and S.O. Chung 2018, Comparison of plant growth and glucosinolates of Chinese cabbage and kale crops under three cultivation conditions. J Biosyst Eng 43:30-36. doi:10.5307/JBE.2018.43.1.030 10.5307/JBE.2018.43.1.030

Kozai T. 2013, Sustainable plant factory: Closed plant production systems with artificial light for high resource use efficiencies and quality produce. Acta Hortic 1004:27-40. doi:10.17660/ActaHortic.2013.1004.2 10.17660/ActaHortic.2013.1004.2

Lännenpää M. 2014, Heterologous expression of AtMYB12 in kale (Brassica oleracea var. acephala) leads to high flavonol accumulation. Plant Cell Rep 33:1377-1388. doi:10.1007/s00299-014-1623-6 10.1007/s00299-014-1623-624792422

Lee G.J, J.W. Heo, C.R. Jung, H.H. Kim, J.S. Jo, J.G. Lee, G.J. Lee, S.Y. Nam, and E.Y. Hong 2016, Effects of artificial light sources on growth and glucosinolate contents of hydroponically grown kale in plant factory. Protected Hort Plant Fac 25:77-82. (in Korean) doi:10.12791/KSBEC.2016.25.2.77 10.12791/KSBEC.2016.25.2.77

Lee H.H., S.C. Yang, M.K. Lee, D.K. Ryu, S. Park, S.O. Chung, S.U. Park, and S.J. Kim 2015, Effect of developmental stages on glucosinolate contents in kale (Brassica oleracea var. acephala). Hortic Sci Technol 33:177-185. (in Korean) doi:10.7235/hort.2015.14017 10.7235/hort.2015.14017

Liu Z., A.H. Hirani, P.B.E. McVetty, F. Daayf, C.F. Quiros, and G. Li 2012, Reducing progoitrin and enriching glucoraphanin in Braasica napus seeds through silencing of the GSL-ALK gene family. Plant Mol Biol 79:179-189. doi:10.1007/s11103-012-9905-2 10.1007/s11103-012-9905-222477389

Lu N., E.L. Bernardo, C. Tippayadarapanich, M. Takagaki, N. Kagawa, and W. Yamori 2017, Growth and accumulation of secondary metabolites in perilla as affected by photosynthetic photon flux density and electrical conductivity of the nutrient solution. Front Plant Sci 8:708. doi:10.3389/fpls.2017.00708 10.3389/fpls.2017.0070828523012PMC5416839

Mayne S.T. 1996, Beta‐carotene, carotenoids, and disease prevention in humans. FASEB J 10:690-701. doi:10.1096/fasebj.10.7.8635686 10.1096/fasebj.10.7.86356868635686

Mikkelsen M.D., C.H. Hansen, U. Wittstock, B.A. Halkier 2000, Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. J Biol Chem 275:33712-33717. doi:10.1074/jbc.M001667200 10.1074/jbc.M00166720010922360

Mikkelsen M.D., P. Naur, and B.A. Halkier 2004, Arabidopsis mutants in the C-S lyase of glucosinolate biosynthesis establish a critical role for indole‐3‐acetaldoxime in auxin homeostasis. Plant J 37:770-777. doi:10.1111/j.1365-313X.2004.02002.x 10.1111/j.1365-313X.2004.02002.x14871316

Naur P., B.L. Petersen, M.D. Mikkelsen, S. Bak, H. Rasmussen, C.E. Olsen, and B.A. Halkier 2003, CYP83A1 and CYP83B1, two nonredundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis. Plant Physiol 133:63-72. doi:10.1104/pp.102.019240 10.1104/pp.102.01924012970475PMC196579

Neugart S., S. Baldermann, F.S. Hanschen, R. Klopsch, M. Wiesner-Reinhold, and M. Schreiner 2018, The intrinsic quality of brassicaceous vegetables: How secondary plant metabolites are affected by genetic, environmental, and agronomic factors. Sci Hortic 233:460-478. doi:10.1016/j.scienta.2017.12.038 10.1016/j.scienta.2017.12.038

Nguyen T.K.L., and M.M. Oh 2021, Physiological and biochemical responses of green and red perilla to LED‐based light. J Sci Food Agric 101:240-252. doi:10.1002/jsfa.10636 10.1002/jsfa.1063633460178

Palani K., B. Harbaum-Piayda, D. Meske, J.K. Keppler, W. Bockelmann, K.J. Heller, and K. Schwarz 2016, Influence of fermentation on glucosinolates and glucobrassicin degradation products in sauerkraut. Food Chem 190:755-762. doi:10.1016/j.foodchem.2015.06.012 10.1016/j.foodchem.2015.06.01226213035

Piotrowski M., A. Schemenewitz, A. Lopukhina, A. Müller, T. Janowitz, E.W. Weiler, and C. Oecking 2004, Desulfoglucosinolate sulfotransferases from Arabidopsis thaliana catalyze the final step in the biosynthesis of the glucosinolate core structure. J Biol Chem 279:50717-50725. doi:10.1074/jbc.M407681200 10.1074/jbc.M40768120015358770

Sawada Y., A. Kuwahara, M. Nagano, T. Narisawa, A. Sakata, K. Saito, and M. Y. Hirai 2009a, Omics-based approaches to methionine side chain elongation in Arabidopsis: characterization of the genes encoding methylthioalkylmalate isomerase and methylthioalkylmalate dehydrogenase. Plant Cell Physiol 50:1181-1190. doi:10.1093/pcp/pcp079 10.1093/pcp/pcp07919493961PMC2709551

Sawada Y., K. Toyooka, A. Kuwahara, A. Sakata, M. Nagano, K. Saito, and M.Y. Hirai 2009b, Arabidopsis bile acid:sodium symporter family protein 5 is involved in methionine-derived glucosinolate biosynthesis. Plant Cell Physiol 50:1579-1586. doi:10.1093/pcp/pcp110 10.1093/pcp/pcp11019633020PMC2739670

Smillie R.M., and S.E. Hetherington 1999, Photoabatement by anthocyanin shields photosynthetic systems from light stress. Photosynthetica 36:451-463. doi:10.1023/A:1007084321859 10.1023/A:1007084321859

Sønderby I.E., F. Geu-Flores, and B.A. Halkier 2010, Biosynthesis of glucosinolates-gene discovery and beyond. Trends Plant Sci 15:283-290. doi:10.1016/j.tplants.2010.02.005 10.1016/j.tplants.2010.02.00520303821

Waterland N.L., Y. Moon, J.C. Tou, D.A. Kopsell, M.J. Kim, and S. Park 2019, Differences in leaf color and stage of development at harvest influenced phytochemical content in three cultivars of kale (Brassica oleracea L. and B. napus). J Agric Sci 11:14-21. doi:10.5539/jas.v11n3p14 10.5539/jas.v11n3p14

Yan X., and S. Chen 2007, Regulation of plant glucosinolate metabolism. Planta 226:1343-1352. doi:10.1007/s00425-007-0627-7. 10.1007/s00425-007-0627-717899172

Yi G.E., A.H.K. Robin, K. Yang, J.I. Park, J.G. Kang, T.J. Yang, and I.S. Nou 2015, Identification and expression analysis of glucosinolate biosynthetic genes and estimation of glucosinolate contents in edible organs of Brassica oleracea subspecies. Molecules 20:13089-13111. doi:10.3390/molecules200713089 10.3390/molecules20071308926205053PMC6332298

Information

Publisher :The Korean Society for Bio-Environment Control
Publisher(Ko) :(사)한국생물환경조절학회
Journal Title :Journal of Bio-Environment Control
Journal Title(Ko) :생물환경조절학회지
Volume : 31
No :4
Pages :332-342
Received Date : 2022-07-22
Revised Date : 2022-10-11
Accepted Date : 2022-10-14
DOI :https://doi.org/10.12791/KSBEC.2022.31.4.332

Journal of Bio-Environment Control ISSN:1229-4675(Print) 2765-3641(Online) 생물환경조절학회지

All Issue