Abstract
The quantitative freshness assessment method for vegetables is desired to upgrade the quality management system in agricultural distribution chain. Since lipid has broad diversity in species and plays an important role in the biological metabolism of plants, there is a possibility that lipid profile indicates the freshness of harvested vegetables. The aims of this study were to clarify the lipidomic alteration of stored cabbage and identify lipid molecules indicative of freshness. Cabbage leaves stored at 5 °C, 10 °C, and 20 °C were sampled periodically for lipidomic analysis by liquid chromatography-tandem mass spectrometry. The cumulative respiratory CO2 production was determined using a flow-through method via gas chromatography. A total of 74 lipid species had a significant correlation with cumulative CO2 production. Hierarchical cluster analysis (HCA) clustered them into three main groups. A partial least squares regression (PLSR) model established the relationship between the abundance of lipid species and the cumulative CO2 production. Four lipid molecules were selected as potential freshness markers. The PLSR model with the selected markers had a better performance in predicting the cumulative CO2 production than that by ascorbic acid which is conventionally used as a quality indicator of fresh produce. Our results show that lipidomic profiling could be viable for assessing the freshness of whole cabbage.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Abhyankar V, Kaduskar B, Kamat SS et al (2018) Drosophila DNA/RNA methyltransferase contributes to robust host defense in ageing animals by regulating sphingolipid metabolism. J Exp Biol 221:1–10. https://doi.org/10.1242/jeb.187989
Agmon E, Stockwell BR (2017) Lipid homeostasis and regulated cell death. Curr Opin Chem Biol 39:83–89. https://doi.org/10.1016/j.cbpa.2017.06.002
Arce-Lopera C, Masuda T, Kimura A et al (2013) Luminance distribution as a determinant for visual freshness perception: evidence from image analysis of a cabbage leaf. Food Qual Prefer 27:202–207. https://doi.org/10.1016/j.foodqual.2012.03.005
Barth MM, Zhuang H (1996) Packaging design affects antioxidant vitamin retention and quality of broccoli florets during postharvest storage. Postharvest Biol Technol 9:141–150. https://doi.org/10.1016/S0925-5214(96)00043-9
Brash DW, Charles CM, Wright S, Bycroft BL (1995) Shelf-life of stored asparagus is strongly related to postharvest respiratory activity. Postharvest Biol Technol 5:77–81. https://doi.org/10.1016/0925-5214(94)00017-M
Brown JH, Lynch DV, Thompson JE (1987) Molecular species specificity of phospholipid breakdown in microsomal membranes of senescing carnation flowers. Plant Physiol 85:679–683. https://doi.org/10.1104/pp.85.3.679
Bustamante CA, Brotman Y, Monti LL et al (2018) Differential lipidome remodeling during postharvest of peach varieties with different susceptibility to chilling injury. Physiol Plant 163:2–17. https://doi.org/10.1111/ppl.12665
Capriotti AL, Cavaliere C, Piovesana S et al (2015) Simultaneous determination of naturally occurring estrogens and mycoestrogens in milk by ultrahigh-performance liquid chromatography-tandem mass spectrometry analysis. J Agric Food Chem 63:8940–8946. https://doi.org/10.1021/acs.jafc.5b02815
Casares D, Escribá PV, Rosselló CA (2019) Membrane lipid composition: effect on membrane and organelle structure, function and compartmentalization and therapeutic avenues. Int J Mol Sci 20:2167. https://doi.org/10.3390/ijms20092167
del Aguila JS, Sasaki FF, Heiffig LS et al (2006) Fresh-cut radish using different cut types and storage temperatures. Postharvest Biol Technol 40:149–154. https://doi.org/10.1016/j.postharvbio.2005.12.010
Dufourc EJ (2008) The role of phytosterols in plant adaptation to temperature. Plant Signal Behav 3:133–134. https://doi.org/10.4161/psb.3.2.5051
Dunn WB, Broadhurst D, Begley P et al (2011) Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat Protoc 6:1060–1083. https://doi.org/10.1038/nprot.2011.335
Fahmy K, Nakano K (2014) Optimal design of modified atmosphere packaging for alleviating chilling injury in cucumber fruit. Environ Control Biol 52:233–240. https://doi.org/10.2525/ecb.52.233
Ferrer A, Altabella T, Arró M, Boronat A (2017) Emerging roles for conjugated sterols in plants. Prog Lipid Res 67:27–37. https://doi.org/10.1016/j.plipres.2017.06.002
Fonseca SC, Oliveira FAR, Brecht JK (2002) Modelling respiration rate of fresh fruits and vegetables for modified atmosphere packages: a review. J Food Eng 52:99–119. https://doi.org/10.1016/S0260-8774(01)00106-6
Galani JHY, Patel JS, Patel NJ, Talati JG (2017) Storage of fruits and vegetables in refrigerator increases their phenolic acids but decreases the total phenolics, anthocyanins and vitamin C with subsequent loss of their antioxidant capacity. Antioxidants 6:59. https://doi.org/10.3390/antiox6030059
Gao F, Dong Y, Xiao W et al (2016) LED-induced fluorescence spectroscopy technique for apple freshness and quality detection. Postharvest Biol Technol 119:27–32. https://doi.org/10.1016/j.postharvbio.2016.04.020
Gao H, Mao H, Ullah I (2020) Analysis of metabolomic changes in lettuce leaves under low nitrogen and phosphorus deficiencies stresses. Agric 10:1–14. https://doi.org/10.3390/agriculture10090406
Gorassini A, Verardo G, Fregolent SC, Bortolomeazzi R (2017) Rapid determination of cholesterol oxidation products in milk powder based products by reversed phase SPE and HPLC-APCI-MS/MS. Food Chem 230:604–610. https://doi.org/10.1016/j.foodchem.2017.03.080
Hammann S, Korf A, Bull ID et al (2019) Lipid profiling and analytical discrimination of seven cereals using high temperature gas chromatography coupled to high resolution quadrupole time-of-flight mass spectrometry. Food Chem 282:27–35. https://doi.org/10.1016/j.foodchem.2018.12.109
Harayama T, Riezman H (2018) Understanding the diversity of membrane lipid composition. Nat Rev Mol Cell Biol 19:281–296. https://doi.org/10.1038/nrm.2017.138
Hasperué JH, Guardianelli L, Rodoni LM et al (2016) Continuous white-blue LED light exposition delays postharvest senescence of broccoli. LWT - Food Sci Technol 65:495–502. https://doi.org/10.1016/j.lwt.2015.08.041
Howard LA, Wong AD, Perry AK, Klein BP (1999) β-Carotene and ascorbic acid retention in fresh and processed vegetables. J Food Sci 64:929–936. https://doi.org/10.1111/j.1365-2621.1999.tb15943.x
Jia Y, Li W (2015) Characterisation of lipid changes in ethylene-promoted senescence and its retardation by suppression of phospholipase Dδ in Arabidopsis leaves. Front Plant Sci 6:1045. https://doi.org/10.3389/fpls.2015.01045
Jia Y, Tao F, Li W (2013) Lipid profiling demonstrates that suppressing Arabidopsis phospholipase Dδ Retards ABA-promoted leaf senescence by attenuating lipid degradation. PLoS ONE 8:e65687. https://doi.org/10.1371/journal.pone.0065687
Kader A (2002) Postharvest biology and technology: an overview. Postharvest technology of horticultural crops. In A. A. K. University of California, Division of Agriculture and Natural Resources, California, pp 39–48.
Kaup MT, Froese CD, Thompson JE (2002) A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiol 129:1616–1626. https://doi.org/10.1104/pp.003087
Kong X, Wei B, Gao Z et al (2018) Changes in membrane lipid composition and function accompanying chilling injury in bell peppers. Plant Cell Physiol 59:167–178. https://doi.org/10.1093/pcp/pcx171
Li L, Zhao J, Zhao Y et al (2016) Comprehensive investigation of tobacco leaves during natural early senescence via multi-platform metabolomics analyses. Sci Rep 6:2–11. https://doi.org/10.1038/srep37976
Li X, Sekiyama Y, Nakamura N et al (2021) Estimation of komatsuna freshness using visible and near-infrared spectroscopy based on the interpretation of NMR metabolomics analysis. Food Chem 364:130381. https://doi.org/10.1016/j.foodchem.2021.130381
Li Y, Wang X, Li C et al (2020) Exploration of chemical markers using a metabolomics strategy and machine learning to study the different origins of Ixeris denticulata (Houtt.) Stebb. Food Chem 330:127232. https://doi.org/10.1016/j.foodchem.2020.127232
Lin W, Oliver DJ (2008) Role of triacylglycerols in leaves. Plant Sci 175:233–237. https://doi.org/10.1016/j.plantsci.2008.04.003
Liu J, Li Q, Chen J, Jiang Y (2020) Revealing further insights on chilling injury of postharvest bananas by untargeted lipidomics. Foods 9:894. https://doi.org/10.3390/foods9070894
Matyash V, Liebisch G, Kurzchalia TV et al (2008) Lipid extraction by methyl-terf-butyl ether for high-throughput lipidomics. J Lipid Res 49:1137–1146. https://doi.org/10.1194/jlr.D700041-JLR200
Mazurek A, Pankiewicz U (2012) Changes of dehydroascorbic acid content in relation to total content of vitamin C in selected fruits and vegetables. Acta Sci Pol Hortorum Cultus 11:169–177.
Medina MS, Tudela JA, Marín A et al (2012) Short postharvest storage under low relative humidity improves quality and shelf life of minimally processed baby spinach (Spinacia oleracea L.). Postharvest Biol Technol 67:1–9. https://doi.org/10.1016/j.postharvbio.2011.12.002
Mendez KM, Reinke SN, Broadhurst DI (2019) A comparative evaluation of the generalised predictive ability of eight machine learning algorithms across ten clinical metabolomics data sets for binary classification. Metabolomics 15:1–15. https://doi.org/10.1007/s11306-019-1612-4
Mueller SP, Unger M, Guender L et al (2017) Phospholipid: diacylglycerol acyltransferase-mediated triacylglyerol synthesis augments basal thermotolerance. Plant Physiol 175:486–497. https://doi.org/10.1104/pp.17.00861
Nekvapil F, Brezestean I, Barchewitz D et al (2018) Citrus fruits freshness assessment using raman spectroscopy. Food Chem 242:560–567. https://doi.org/10.1016/j.foodchem.2017.09.105
Paliyath G, Droillard M (1992) The mechanisms of membrane deterioration and disassembly during senescence. Plant Physiol Biochem 30:789–812.
Paliyath G, Tiwari K, Sitbon C, Whitaker BD (2012) Biochemistry of fruits. Food biochemistry and food processing. Wiley-Blackwell, Oxford, UK, pp 531–553.
Parijadi AAR, Putri SP, Ridwani S et al (2018) Metabolic profiling of Garcinia mangostana (mangosteen) based on ripening stages. J Biosci Bioeng 125:238–244. https://doi.org/10.1016/j.jbiosc.2017.08.013
Péneau S, Hoehn E, Roth H-R et al (2006) Importance and consumer perception of freshness of apples. Food Qual Prefer 17:9–19. https://doi.org/10.1016/j.foodqual.2005.05.002
Péneau S, Brockhoff PB, Escher F, Nuessli J (2007) A comprehensive approach to evaluate the freshness of strawberries and carrots. Postharvest Biol Technol 45:20–29. https://doi.org/10.1016/j.postharvbio.2007.02.001
Peršurić Ž, Saftić L, Mašek T, Pavelić SK (2018) Comparison of triacylglycerol analysis by MALDI-TOF/MS, fatty acid analysis by GC-MS and non-selective analysis by NIRS in combination with chemometrics for determination of extra virgin olive oil geographical origin. A Case Study Lwt 95:326–332. https://doi.org/10.1016/j.lwt.2018.04.072
Piironen V, Toivo J, Puupponen-Pimiä R, Lampi AM (2003) Plant sterols in vegetables, fruits and berries. J Sci Food Agric 83:330–337. https://doi.org/10.1002/jsfa.1316
Qiu Y, Zhao Y, Liu J, Guo Y (2017) A statistical analysis of the freshness of postharvest leafy vegetables with application of water based on chlorophyll fluorescence measurement. Inf Process Agric 4:269–274. https://doi.org/10.1016/j.inpa.2017.08.001
Righetti L, Rubert J, Galaverna G et al (2018) A novel approach based on untargeted lipidomics reveals differences in the lipid pattern among durum and common wheat. Food Chem 240:775–783. https://doi.org/10.1016/j.foodchem.2017.08.020
Saito M, Rai DR, Masuda R (2000) Effect of modified atmosphere packaging on glutathione and ascorbic acid content of asparagus spears. J Food Process Preserv 24:243–251. https://doi.org/10.1111/j.1745-4549.2000.tb00416.x
Slavin JL, Lloyd B (2012) Health benefits of fruits and vegetables. Adv Nutr 3:506–516. https://doi.org/10.3945/an.112.002154
Sud M, Fahy E, Cotter D et al (2007) Lmsd: lipid maps structure database. Nucleic Acids Res 35:D527–D532. https://doi.org/10.1093/nar/gkl838
Sun F, Chen H, Chen D et al (2020) Lipidomic changes in banana ( Musa cavendish ) during ripening and comparison of extraction by folch and bligh–dyer methods. J Agric Food Chem 68:11309–11316. https://doi.org/10.1021/acs.jafc.0c04236
Syukri D, Thammawong M, Naznin HA et al (2018) Identification of a freshness marker metabolite in stored soybean sprouts by comprehensive mass-spectrometric analysis of carbonyl compounds. Food Chem 269:588–594. https://doi.org/10.1016/j.foodchem.2018.07.036
Takahashi D, Imai H, Kawamura Y, Uemura M (2016) Lipid profiles of detergent resistant fractions of the plasma membrane in oat and rye in association with cold acclimation and freezing tolerance. Cryobiology 72:123–134. https://doi.org/10.1016/j.cryobiol.2016.02.003
Tarazona P, Feussner K, Feussner I (2015) An enhanced plant lipidomics method based on multiplexed liquid chromatography-mass spectrometry reveals additional insights into cold- and drought-induced membrane remodeling. Plant J 84:621–633. https://doi.org/10.1111/tpj.13013
Techavuthiporn C, Nakano K, Maezawa S (2008) Prediction of ascorbic acid content in broccoli using a model equation of respiration. Postharvest Biol Technol 47:373–381. https://doi.org/10.1016/j.postharvbio.2007.07.007
Thammawong M, Kasai E, Syukri D, Nakano K (2019) Effect of a low oxygen storage condition on betacyanin and vitamin C retention in red amaranth leaves. Sci Hortic 246:765–768. https://doi.org/10.1016/j.scienta.2018.11.046
Tonutti P, Bonghi C (2014) Innovative and integrated approaches to investigating postharvest stress physiology and the biological basis of fruit quality during storage. In: Postharvest Handling: A system approach. Elsevier, USA, 3rd ed, pp 519–526.
Tudela JA, Espín JC, Gil MI (2002) Vitamin C retention in fresh-cut potatoes. Postharvest Biol Technol 26:75–84. https://doi.org/10.1016/S0925-5214(02)00002-9
Uematsu M, Shimizu T (2021) Raman microscopy-based quantification of the physical properties of intracellular lipids. Commun Biol 4:3–14. https://doi.org/10.1038/s42003-021-02679-w
Van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112–124. https://doi.org/10.1038/nrm2330
Wanner L, Keller F, Matile P (1991) Metabolism of radiolabelled galactolipids in senescent barley leaves. Plant Sci 78:199–206. https://doi.org/10.1016/0168-9452(91)90199-I
Watanabe M, Balazadeh S, Tohge T et al (2013) Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol 162:1290–1310. https://doi.org/10.1104/pp.113.217380
Wei F, Hu N, Lv X et al (2015) Quantitation of triacylglycerols in edible oils by off-line comprehensive two-dimensional liquid chromatography-atmospheric pressure chemical ionization mass spectrometry using a single column. J Chromatogr A 1404:60–71. https://doi.org/10.1016/j.chroma.2015.05.058
Wewer V, Dombrink I, Vom Dorp K, Dörmann P (2011) Quantification of sterol lipids in plants by quadrupole time-of-flight mass spectrometry. J Lipid Res 52:1039–1054. https://doi.org/10.1194/jlr.D013987
Wieland K, Masri M, von Poschinger J et al (2021) Non-invasive Raman spectroscopy for time-resolved in-line lipidomics. RSC Adv 11:28565–28572. https://doi.org/10.1039/d1ra04254h
Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183. https://doi.org/10.1007/978-81-322-1542-4-11
Xu D, Lam SM, Zuo J et al (2021) Lipidomics reveals the difference of membrane lipid catabolism between chilling injury sensitive and non-sensitive green bell pepper in response to chilling. Postharvest Biol Technol 182:111714. https://doi.org/10.1016/j.postharvbio.2021.111714
Yamauchi N, Kusabe A (2001) Involvement of ascorbate-glutathione cycle in senescence of stored broccoli (Brassica oleracea L.). J Japan Soc Hort Sci 70:704–708. https://doi.org/10.2503/jjshs.70.704
Zhou Y, Kim SY, Lee JS et al (2021) Discrimination of the geographical origin of soybeans using nmr-based metabolomics. Foods 10:1–16. https://doi.org/10.3390/foods10020435
Funding
This work was supported by Cabinet Office, Government of Japan, Cross-ministerial Strategic Innovation Promotion Program (SIP), “Technologies for Smart Bio-industry and Agriculture” (funding agency: Bio-oriented Technology Research Advancement Institution, NARO), and JSPS KAKENHI Grant Number 16H02581 and 22H0389.
Author information
Authors and Affiliations
Contributions
Putri Wulandari Zainal: Investigation, Formal analysis, Software, Writing—original draft. Daimon Syukri: Methodology, Investigation. Khandra Fahmy: Writing—review & editing. Teppei Imaizumi: Formal analysis. Manasikan Thammawong: Formal analysis. Mizuki Tsuta: Software, Writing—review & editing. Masayasu Nagata: Writing—review & editing. Kohei Nakano: Conceptualization, Methodology, Supervision, Writing—review & editing, Funding acquisition.
Corresponding author
Ethics declarations
Ethics Approval
This study does not involve usage of sample related to human participants or animals.
Consent to Participate
Not applicable.
Conflict of Interest
Putri Wulandari Zainal declares that she has no conflict of interest. Daimon Syukri declares that he has no conflict of interest. Khandra Fahmy declares that he has no conflict of interest. Teppei Imaizumi declares that he has no conflict of interest. Manasikan Thammawong declares that she has no conflict of interest. Mizuki Tsuta declares that he has no conflict of interest. Masayasu Nagata declares that he has no conflict of interest. Kohei Nakano declares that he has no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zainal, P.W., Syukri, D., Fahmy, K. et al. Lipidomic Profiling to Assess the Freshness of Stored Cabbage. Food Anal. Methods 16, 304–317 (2023). https://doi.org/10.1007/s12161-022-02422-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12161-022-02422-z