In this study, we evaluated the effects of biofertilizer on primary and secondary metabolites in lettuce. Green ‘Aleppo’ and red ‘Murai’ cultivars were grown in an unheated greenhouse during winter production under biofertilizer and control (no fertilization) conditions. Main effects of cultivar showed that red ‘Murai’ exhibited higher total antioxidant capacity (TAC), total phenolic content (TPC), and total carotenoid content, myo-inositol, malic, propionic, and citric acids, and higher concentrations of chicoric and chlorogenic acids, caffeoylquinic acid glucoside, along with all quantified flavonoids except kaempferol. In contrast, green ‘Aleppo’ showed higher fructose, sucrose, total sweetness index (TSI), total soluble solids (TSS), shikimic acid, fumaric acid, lactucopicrin, and lactucopicrin-15-oxalate. Biofertilizer application significantly increased glucose by 42.9%, fructose by 39.1%, and sucrose by 57.8%, resulting in a 40.5% increase in TSI. Furthermore, malic acid increased significantly by 23.2% and fumaric acid by 36.0%, whereas myo-inositol and propionic acid significantly decreased by 23.3% and 21.6%, respectively. Biofertilizer also reduced major phenolic compounds, including chicoric acid (66.9%), chlorogenic acid (81.2%), and caffeoylquinic acid glucoside (32.6%), along with TPC (19.4%) and TAC (54.0%). All principal flavonoids were significantly reduced (30.1–70.8%) when averaged across cultivars, whereas sesquiterpene lactones showed no significant biofertilizer main effect, and lactucin was the predominant lactone. Significant cultivar × biofertilizer interactions revealed contrasting metabolic responses between cultivars. EM Aktiv reduced phenolic acids and flavonoids in ‘Murai’, whereas in ‘Aleppo’, these compounds were generally maintained or enhanced in a compound-dependent responses, alongside increases in sugars and selected organic acids. Lactones showed a crossover response, increasing under EM treatment in ‘Aleppo’ but decreasing in ‘Murai’. These results demonstrate that lettuce responses to biofertilizer treatment are strongly cultivar-dependent, highlighting the importance of genotype selection in determining metabolic responses under biofertilizer application. Overall, these changes may indicate altered allocation between primary and secondary metabolism under winter conditions.
Citation: Milica Stojanović, Dragica Milosavljević, Jelena Dragišić Maksimović, Vuk Maksimović. Biofertilizer alters primary and secondary metabolism in winter-grown lettuce in a cultivar-dependent manner[J]. AIMS Molecular Science, 2026, 13(3): 334-366. doi: 10.3934/molsci.2026016
In this study, we evaluated the effects of biofertilizer on primary and secondary metabolites in lettuce. Green ‘Aleppo’ and red ‘Murai’ cultivars were grown in an unheated greenhouse during winter production under biofertilizer and control (no fertilization) conditions. Main effects of cultivar showed that red ‘Murai’ exhibited higher total antioxidant capacity (TAC), total phenolic content (TPC), and total carotenoid content, myo-inositol, malic, propionic, and citric acids, and higher concentrations of chicoric and chlorogenic acids, caffeoylquinic acid glucoside, along with all quantified flavonoids except kaempferol. In contrast, green ‘Aleppo’ showed higher fructose, sucrose, total sweetness index (TSI), total soluble solids (TSS), shikimic acid, fumaric acid, lactucopicrin, and lactucopicrin-15-oxalate. Biofertilizer application significantly increased glucose by 42.9%, fructose by 39.1%, and sucrose by 57.8%, resulting in a 40.5% increase in TSI. Furthermore, malic acid increased significantly by 23.2% and fumaric acid by 36.0%, whereas myo-inositol and propionic acid significantly decreased by 23.3% and 21.6%, respectively. Biofertilizer also reduced major phenolic compounds, including chicoric acid (66.9%), chlorogenic acid (81.2%), and caffeoylquinic acid glucoside (32.6%), along with TPC (19.4%) and TAC (54.0%). All principal flavonoids were significantly reduced (30.1–70.8%) when averaged across cultivars, whereas sesquiterpene lactones showed no significant biofertilizer main effect, and lactucin was the predominant lactone. Significant cultivar × biofertilizer interactions revealed contrasting metabolic responses between cultivars. EM Aktiv reduced phenolic acids and flavonoids in ‘Murai’, whereas in ‘Aleppo’, these compounds were generally maintained or enhanced in a compound-dependent responses, alongside increases in sugars and selected organic acids. Lactones showed a crossover response, increasing under EM treatment in ‘Aleppo’ but decreasing in ‘Murai’. These results demonstrate that lettuce responses to biofertilizer treatment are strongly cultivar-dependent, highlighting the importance of genotype selection in determining metabolic responses under biofertilizer application. Overall, these changes may indicate altered allocation between primary and secondary metabolism under winter conditions.
| [1] | FAOSTATCrops and livestock products (2026). Available from: https://www.fao.org/faostat/en/#data/qcl |
| [2] |
Lafarga T, Villaró S, Rivera A, et al. (2020) Bioaccessibility of polyphenols and antioxidant capacity of fresh or minimally processed modern or traditional lettuce (Lactuca sativa L.) varieties. J Food Sci Technol 57: 754-763. http://doi.org/10.1007/s13197-019-04108-7 
|
| [3] |
Medina-Lozano I, Bertolín JR, Díaz A (2021) Nutritional value of commercial and traditional lettuce (Lactuca sativa L.) and wild relatives: vitamin C and anthocyanin content. Food Chem 359: 129864. https://doi.org/10.1016/j.foodchem.2021.129864
|
| [4] |
Kim MJ, Moon Y, Tou JC, et al. (2016) Nutritional value, bioactive compounds and health benefits of lettuce (Lactuca sativa L.). J Food Compost Anal 49: 19-34. https://doi.org/10.1016/j.jfca.2016.03.004
|
| [5] |
Shi M, Gu J, Wu H, et al. (2022) Phytochemicals, nutrition, metabolism, bioavailability, and health benefits in lettuce–A comprehensive review. Antioxidants 11: 1158. http://doi.org/10.3390/antiox11061158
|
| [6] |
Stojanović M, Milosavljević D, Delcourt A, et al. (2025) Phytochemical composition and overall taste modulation in lettuce: Combination of cultivar and biofertiliser. Plants 14: 3864. https://doi.org/10.3390/plants14243864
|
| [7] |
Pandey KB, Rizvi SI (2009) Plant polyphenols as dietary antioxidants in human health and disease. Oxid Med Cell Longev 2: 897484. https://doi.org/10.4161/oxim.2.5.9498
|
| [8] |
Llorach R, Martínez-Sánchez A, Tomás-Barberán FA, et al. (2008) Characterisation of polyphenols and antioxidant properties of five lettuce varieties and escarole. Food Chem 108: 1028-1038. https://doi.org/10.1016/j.foodchem.2007.11.032
|
| [9] |
Liu X, Ardo S, Bunning M, et al. (2007) Total phenolic content and DPPH radical scavenging activity of lettuce (Lactuca sativa L.) grown in Colorado. LWT 40: 552-557. http://doi.org/10.1016/j.lwt.2005.09.007
|
| [10] |
Lemos AA, Vargas VCS, Wuilloud RG, et al. (2024) Screening of bioactive compounds in lettuce: multivariate optimization of an ultrasound-assisted solid–liquid extraction procedure. Food Anal Methods 17: 1281-1291. http://doi.org/10.1007/s12161-024-02656-z
|
| [11] |
Santander C, Vidal G, Ruiz A, et al. (2022) Salinity eustress increases the biosynthesis and accumulation of phenolic compounds that improve the functional and antioxidant quality of red lettuce. Agronomy 12: 598. https://doi.org/10.3390/agronomy12030598
|
| [12] |
Berríos D, Nahuelcura J, González F, et al. (2024) The biosynthesis, accumulation of phenolic compounds and antioxidant response in Lactuca sativa L. plants inoculated with a biofertilizer based on soil yeast and iron nanoparticles. Plants 13: 388. https://doi.org/10.3390/plants13030388
|
| [13] |
Hameed MK, Umar W, Razzaq A, et al. (2023) Quantification of total polyphenols, antioxidants, anthocyanins and secondary metabolites by UPLC VION IMS QTOF MS/MS analysis in green and red lettuce cultivars. Sci Hortic 315: 111994. https://doi.org/10.1016/j.scienta.2023.111994
|
| [14] |
Mai F, Glomb MA (2013) Isolation of phenolic compounds from iceberg lettuce and impact on enzymatic browning. J Agric Food Chem 61: 2868-2874. http://doi.org/10.1021/jf305182u
|
| [15] |
Yang X, Gil MI, Yang Q, et al. (2022) Bioactive compounds in lettuce: Highlighting the benefits to human health and impacts of preharvest and postharvest practices. Compr Rev Food Sci Food Saf 21: 4-45. http://doi.org/10.1111/1541-4337.12877
|
| [16] |
Zhou W, Liang X, Dai P, et al. (2019) Alteration of phenolic composition in lettuce (Lactuca sativa L.) by reducing nitrogen supply enhances its anti-proliferative effects on colorectal cancer cells. Int J Mol Sci 20: 4205. https://doi.org/10.3390/ijms20174205
|
| [17] |
Galieni A, Di Mattia C, De Gregorio M, et al. (2015) Effects of nutrient deficiency and abiotic environmental stresses on yield, phenolic compounds and antiradical activity in lettuce (Lactuca sativa L.). Sci Hortic 187: 93-101. https://doi.org/10.1016/j.scienta.2015.02.036
|
| [18] |
Liu R, Su Z, Zhou H, et al. (2020) LsHSP70 is induced by high temperature to interact with calmodulin, leading to higher bolting resistance in lettuce. Sci Rep 10: 15155. http://doi.org/10.1038/s41598-020-72443-3
|
| [19] | Todorović V, Rožić A, Marković S, et al. (2012) Influence of temperature on yield and earliness of lettuce grown in the winter period. Agroznanje 13: 475-481. http://doi.org/10.7251/AGRSR1203475T |
| [20] |
Yang X, Han Y, Huo G, et al. (2024) Integrated transcriptomic and metabolomic analysis provides insights into cold tolerance in lettuce (Lactuca sativa L.). BMC Plant Biol 24: 442. http://doi.org/10.1186/s12870-024-05099-0
|
| [21] |
Hu Y, Wu Q, Sprague SA, et al. (2015) Tomato expressing arabidopsis glutaredoxin gene AtGRXS17 confers tolerance to chilling stress via modulating cold responsive components. Hortic Res 2: 15051. http://doi.org/10.1038/hortres.2015.51
|
| [22] |
de Souza ASN, de Oliveira Schmidt H, Pagno C, et al. (2022) Influence of cultivar and season on carotenoids and phenolic compounds from red lettuce influence of cultivar and season on lettuce. Food Res Int 155: 111110. https://doi.org/10.1016/j.foodres.2022.111110
|
| [23] |
Havaux M, Kloppstech K (2001) The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. Planta 213: 953-966. http://doi.org/10.1007/s004250100572
|
| [24] |
Neugart S, Kläring HP, Zietz M, et al. (2012) The effect of temperature and radiation on flavonol aglycones and flavonol glycosides of kale (Brassica oleracea var. sabellica). Food Chem 133: 1456-1465. https://doi.org/10.1016/j.foodchem.2012.02.034
|
| [25] |
Boo HO, Heo BG, Gorinstein S, et al. (2011) Positive effects of temperature and growth conditions on enzymatic and antioxidant status in lettuce plants. Plant Sci 181: 479-484. https://doi.org/10.1016/j.plantsci.2011.07.013
|
| [26] |
Oh MM, Carey EE, Rajashekar CB (2009) Environmental stresses induce health-promoting phytochemicals in lettuce. Plant Physiol Biochem 47: 578-583. https://doi.org/10.1016/j.plaphy.2009.02.008
|
| [27] |
Chadwick M, Trewin H, Gawthrop F, et al. (2013) Sesquiterpenoids lactones: Benefits to plants and people. Int J Mol Sci 14: 12780-12805. https://doi.org/10.3390/ijms140612780
|
| [28] |
Weiss J, Gruda NS (2025) Enhancing nutritional quality in vegetables through breeding and cultivar choice in protected cultivation. Sci Hortic 339: 113914. https://doi.org/10.1016/j.scienta.2024.113914
|
| [29] |
Figiel S, Rusek P, Ryszko U, et al. (2025) Microbially enhanced biofertilizers: technologies, mechanisms of action, and agricultural applications. Agronomy 15: 1191. https://doi.org/10.3390/agronomy15051191
|
| [30] |
Negi R, Yadav N, Yadav AN (2025) Microbial biofertilizers: A paradigm shift towards gricultural ustainability. Biologia 80: 389-414. http://doi.org/10.1007/s11756-024-01848-6
|
| [31] |
Barros-Rodríguez A, Pacheco P, Peñas-Corte M, et al. (2024) Comparative study of Bacillus-based plant biofertilizers: A proposed index. Biology 13: 668. https://doi.org/10.3390/biology13090668
|
| [32] |
Melini F, Melini V, Luziatelli F, et al. (2023) Effect of microbial plant biostimulants on fruit and vegetable quality: current research lines and future perspectives. Front Plant Sci 14: 1251544. https://doi.org/10.3389/fpls.2023.1251544
|
| [33] |
Szepesi Á, Soares C, Fidalgo F (2024) Editorial: Working towards sustainable agriculture with biostimulants and biocides: from chemical structure to application methods. Front Plant Sci 15: 1443658. https://doi.org/10.3389/fpls.2024.1443658
|
| [34] |
Marin A, Ferreres F, Barberá GG, et al. (2015) Weather variability influences color and phenolic content of pigmented baby leaf lettuces throughout the season. J Agric Food Chem 63: 1673-1681. https://doi.org/10.1021/acs.jafc.5b00120
|
| [35] | FAOFAO highlights the vital role of soil: 95 percent of our food is directly produced on soils (2024). Available from: https://www.fao.org/countryprofiles/news-archive/detail-news/en/c/1729967/ |
| [36] |
Endo M, Fukuda N, Yoshida H, et al. (2022) Effects of light quality, photoperiod, CO2 concentration, and air temperature on chlorogenic acid and rutin accumulation in young lettuce plants. Plant Physiol Biochem 186: 290-298. https://doi.org/10.1016/j.plaphy.2022.07.010
|
| [37] |
Stojanović M, Maksimović V, Mutavdžić D, et al. (2021) Determination of antioxidative and enzymatic activity in green and red lettuce cultivars affected by microbiological fertilisers and seasons. EJFA 33: 101-112. http://doi.org/10.9755/ejfa.2021.v33.i2.2354
|
| [38] |
Lichtenthaler HK (1987) Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in enzymology . Academic Press 350-382. http://doi.org/10.1016/0076-6879(87)48036-1
|
| [39] |
Arnao MB, Cano A, Acosta M (1999) Methods to measure the antioxidant activity in plant material. A comparative discussion. Free Radic Res 31: 89-96. https://doi.org/10.1080/10715769900301371
|
| [40] |
Dragišić Maksimović JJ, Živanović BD (2012) Quantification of the antioxidant activity in salt-stressed tissues. Plant Salt Tolerance . Totowa, NJ: Humana Press 237-250. http://doi.org/10.1007/978-1-61779-986-0_16
|
| [41] |
Ntsoane LLM, Soundy P, Jifon J, et al. (2016) Variety-specific responses of lettuce grown under the different-coloured shade nets on phytochemical quality after postharvest storage. J Hortic Sci Biotechnol 91: 520-528. http://doi.org/10.1080/14620316.2016.1178080
|
| [42] |
Magwaza LS, Opara UL (2015) Analytical methods for determination of sugars and sweetness of horticultural products–A review. Sci Hortic 184: 179-192. https://doi.org/10.1016/j.scienta.2015.01.001
|
| [43] |
Fodorpataki L, Molnar K, Tompa B, et al. (2019) Priming with vitamin U enhances cold tolerance of lettuce (Lactuca sativa L.). Not Bot Horti Agrobo 47: 592-598. https://doi.org/10.15835/nbha47311433
|
| [44] |
Kalisz A, Kornaś A, Gil J, et al. (2025) Exogenously applied putrescine and chitosan–putrescine nanocomposite alleviate the negative effects of chilling stress on iceberg lettuce seedlings. Sci Rep 15: 26963. https://doi.org/10.1038/s41598-025-11180-x
|
| [45] |
Ahlawat YK, Singh M, Manorama K, et al. (2024) Plant phenolics: Neglected secondary metabolites in plant stress tolerance. Braz J Bot 47: 703-721. https://doi.org/10.1007/s40415-023-00949-x
|
| [46] |
Naikoo MI, Dar MI, Raghib F, et al. (2019) Chapter 9 - Role and regulation of plants phenolics in abiotic stress tolerance: An overview. Plant signaling molecules: Role and regulation under stressful environments . Woodhead Publishing 157-168. https://doi.org/10.1016/B978-0-12-816451-8.00009-5
|
| [47] |
Zhou P, Li Q, Liu G, et al. (2018) Integrated analysis of transcriptomic and metabolomic data reveals critical metabolic pathways involved in polyphenol biosynthesis in nicotiana tabacum under chilling stress. Funct Plant Biol 46: 30-43. https://doi.org/10.1071/FP18099
|
| [48] |
Francini A, Sebastiani L (2019) Abiotic stress effects on performance of horticultural crops. Horticulturae 5: 67. https://doi.org/10.3390/horticulturae5040067
|
| [49] |
Derzelle S, Hallet B, Ferain T, et al. (2003) Improved adaptation to cold-shock, stationary-phase, and freezing stresses in Lactobacillus plantarum overproducing cold-shock proteins. Appl Environ Microbiol 69: 4285-4290. https://doi.org/10.1128/AEM.69.7.4285-4290.2003
|
| [50] |
Rizvi A, Ahmed B, Khan MS, et al. (2021) Psychrophilic bacterial phosphate-biofertilizers: A novel extremophile for sustainable crop production under cold environment. Microorganisms 9: 2451. https://doi.org/10.3390/microorganisms9122451
|
| [51] |
Ait Barka E, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 72: 7246-7252. https://doi.org/10.1128/AEM.01047-06
|
| [52] |
Asadi M, Rasouli F, Amini T, et al. (2022) Improvement of photosynthetic pigment characteristics, mineral content, and antioxidant activity of lettuce (Lactuca sativa L.) by arbuscular mycorrhizal fungus and seaweed extract foliar application. Agronomy 12: 1943. https://doi.org/10.3390/agronomy12081943
|
| [53] |
Sarkar MD, Rahman MJ, Uddain J, et al. (2021) Estimation of yield, photosynthetic rate, biochemical, and nutritional content of red leaf lettuce (Lactuca sativa L.) grown in organic substrates. Plants 10: 1220. https://doi.org/10.3390/plants10061220
|
| [54] |
Kimura M, Rodriguez-Amaya DB (2003) Carotenoid composition of hydroponic leafy vegetables. J Agric Food Chem 51: 2603-2607. http://doi.org/10.1021/jf020539b
|
| [55] |
López A, Javier GA, Fenoll J, et al. (2014) Chemical composition and antioxidant capacity of lettuce: comparative study of regular-sized (Romaine) and baby-sized (Little Gem and Mini Romaine) types. J Food Compost Anal 33: 39-48. https://doi.org/10.1016/j.jfca.2013.10.001
|
| [56] |
Ayoub I, Bigatton ED, Vázquez C, et al. (2024) Use of Bacillus velezensis RI3 and Pseudomonas psychrophila P10 strains as plant growth-promoting rhizobacteria in lettuce (Lactuca sativa L.). Agriscientia 41: 27-35. https://doi.org/10.31047/1668.298x.v41.n2.46344
|
| [57] |
Gutiérrez-Chávez A, Robles-Hernández L, Guerrero BI, et al. (2025) Potential of Trichoderma asperellum as a growth promoter in hydroponic lettuce cultivated in a floating-root system. Plants 14: 382. http://doi.org/10.3390/plants14030382
|
| [58] |
Hernández-Huerta J, Guerrero BI, Acevedo-Barrera AA, et al. (2025) Biostimulant effects of Trichoderma asperellum in hydroponic spinach production. Life 15: 428. https://doi.org/10.3390/life15030428
|
| [59] |
Demir H, Saka AK, Uçan U, et al. (2024) Impact of effective micro-organisms (EM) on the yield, growth and bio-chemical properties of lettuce when applied to soil and leaves. BMC Plant Biol 24: 1189. http://doi.org/10.1186/s12870-024-05980-y
|
| [60] |
Wichaphian A, Kamngoen A, Pathom-aree W, et al. (2025) Integrating microalgal Chlorella biomass and biorefinery residues into sustainable agriculture and food production: insights from lettuce cultivation. Foods 14: 808. https://doi.org/10.3390/foods14050808
|
| [61] |
Consentino BB, Aprile S, Rouphael Y, et al. (2022) Application of PGPB combined with variable N doses affects growth, yield-related traits, N-fertilizer efficiency and nutritional status of lettuce grown under controlled condition. Agronomy 12: 236. http://doi.org/10.3390/agronomy12020236
|
| [62] |
Pagliarini E, Gaggìa F, Quartieri M, et al. (2023) Yield and nutraceutical value of lettuce and basil improved by a microbial inoculum in greenhouse experiments. Plants 12: 1700. https://doi.org/10.3390/plants12081700
|
| [63] |
Zhao Y, Han Q, Ding C, et al. (2020) Effect of low temperature on chlorophyll biosynthesis and chloroplast biogenesis of rice seedlings during greening. Int J Mol Sci 21: 1390. https://doi.org/10.3390/ijms21041390
|
| [64] |
Stojanović M, Dinić Z, Dragišić Maksimović J, et al. (2025) Comparative analysis of lettuce morphological and physiological traits: Effects of cultivar, biofertiliser, and seasonal variations in different soil types. Horticulturae 11: 1372. https://doi.org/10.3390/horticulturae11111372
|
| [65] |
Zapata-Vahos IC, Rojas-Rodas F, David D, et al. (2020) Comparison of antioxidant contents of green and red leaf lettuce cultivated in hydroponic systems in greenhouses and conventional soil cultivation. Rev Fac Nac Agron Medellín 73: 9077-9088. http://doi.org/10.15446/rfnam.v73n1.77279
|
| [66] |
Kim DE, Shang X, Assefa AD, et al. (2018) Metabolite profiling of green, green/red, and red lettuce cultivars: variation in health beneficial compounds and antioxidant potential. Food Res Int 105: 361-370. https://doi.org/10.1016/j.foodres.2017.11.028
|
| [67] |
Papoui E, Bantis F, Kapoulas N, et al. (2022) A sustainable intercropping system for organically produced lettuce and green onion with the use of arbuscular mycorrhizal inocula. Horticulturae 8: 466. https://doi.org/10.3390/horticulturae8050466
|
| [68] |
Zuzunaga-Rosas J, Calone R, Mircea DM, et al. (2024) Mitigation of salt stress in lettuce by a biostimulant that protects the root absorption zone and improves biochemical responses. Front Plant Sci 15: 1341714. https://doi.org/10.3389/fpls.2024.1341714
|
| [69] |
Vargas-Arcila M, Cartagena-Valenzuela JR, Franco G, et al. (2017) Changes in the physico-chemical properties of four lettuce (Lactuca sativa L.) varieties during storage. Cienc Tecnol Agropecuaria 18: 257-273. https://doi.org/10.21930/rcta.vol18_num2_art:632
|
| [70] |
Chen X, Wang L, Li T, et al. (2019) Sugar accumulation and growth of lettuce exposed to different lighting modes of red and blue led light. Sci Rep 9: 6926. http://doi.org/10.1038/s41598-019-43498-8
|
| [71] |
Lanzotti V, Anzano A, Grauso L, et al. (2022) NMR metabolomics and chemometrics of lettuce, Lactuca sativa L., under different foliar organic fertilization treatments. Plants 11: 2164. https://doi.org/10.3390/plants11162164
|
| [72] |
Ciriello M, Formisano L, Pannico A, et al. (2021) Nutrient solution deprivation as a tool to improve hydroponics sustainability: Yield, physiological, and qualitative response of lettuce. Agronomy 11: 1469. https://doi.org/10.3390/agronomy11081469
|
| [73] |
Miceli A, Vetrano F, Moncada A (2021) Influence of Ecklonia maxima extracts on growth, yield, and postharvest quality of hydroponic leaf lettuce. Horticulturae 7: 440. https://doi.org/10.3390/horticulturae7110440
|
| [74] |
Fedeli R, Vannini A, Guarnieri M, et al. (2022) Bio-based solutions for agriculture: foliar application of wood distillate alone and in combination with other plant-derived corroborants results in different effects on lettuce (Lactuca sativa L.). Biology 11: 404. https://doi.org/10.3390/biology11030404
|
| [75] |
Becker C, Urlić B, Jukić Špika M, et al. (2015) Nitrogen limited red and green leaf lettuce accumulate flavonoid glycosides, caffeic acid derivatives, and sucrose while losing chlorophylls, β-carotene and xanthophylls. PLoS One 10: e0142867. https://doi.org/10.1371/journal.pone.0142867
|
| [76] |
Wang F, Wang X, Zhang Y, et al. (2022) SlFHY3 and SlHY5 act compliantly to enhance cold tolerance through the integration of myo-inositol and light signaling in tomato. New Phytol 233: 2127-2143. https://doi.org/10.1111/nph.17934
|
| [77] |
Yan L, Zeng L, Raza A, et al. (2022) Inositol improves cold tolerance through inhibiting CBL1 and increasing Ca2+ influx in rapeseed (Brassica napus L.). Front Plant Sci 13: 775692. https://doi.org/10.3389/fpls.2022.775692
|
| [78] |
Chadwick M, Gawthrop F, Michelmore RW, et al. (2016) Perception of bitterness, sweetness and liking of different genotypes of lettuce. Food Chem 197: 66-74. https://doi.org/10.1016/j.foodchem.2015.10.105
|
| [79] |
Keskin B, Akhoundnejad Y, Dasgan HY, et al. (2025) Fulvic acid, amino acids, and vermicompost enhanced yield and improved nutrient profile of soilless iceberg lettuce. Plants 14: 609. https://doi.org/10.3390/plants14040609
|
| [80] |
Sthapit Kandel J, Simko I, Hayes RJ, et al. (2025) Concentration and retention of ascorbic acid, carotenoids, and sugars in fresh-cut lettuce in modified atmosphere packaging. Hortic Plant J 11: 303-313. https://doi.org/10.1016/j.hpj.2023.07.008
|
| [81] |
Bhandari SR, Choi CS, Rhee J, et al. (2021) Seasonal variation in agronomic characteristics and sugar content of cabbage genotypes. Chil J Agr Res 81: 80-91. http://doi.org/10.4067/S0718-58392021000100080
|
| [82] |
Zhou L, Ullah F, Zou J, et al. (2025) Molecular and physiological responses of plants that enhance cold tolerance. Int J Mol Sci 26: 1157. https://doi.org/10.3390/ijms26031157
|
| [83] |
Taïbi K, Del Campo AD, Vilagrosa A, et al. (2018) Distinctive physiological and molecular responses to cold stress among cold-tolerant and cold-sensitive pinus halepensis seed sources. BMC Plant Biol 18: 236. http://doi.org/10.1186/s12870-018-1464-5
|
| [84] |
Chandra D, Matsui T, Suzuki H, et al. (2007) Seasonal changes in texture, sugar and organic acid contents and activities of some ammonia-assimilating enzymes in lettuce. J Appl Hortic 9: 101-107. https://doi.org/10.37855/jah.2007.v09i02.22
|
| [85] |
Bogdanović J, Mojović M, Milosavić N, et al. (2008) Role of fructose in the adaptation of plants to cold-induced oxidative stress. Eur Biophys J 37: 1241-1246. http://doi.org/10.1007/s00249-008-0260-9
|
| [86] |
Zhou W, Liang X, Li K, et al. (2021) Metabolomics analysis reveals potential mechanisms of phenolic accumulation in lettuce (Lactuca sativa L.) induced by low nitrogen supply. Plant Physiol Biochem 158: 446-453. https://doi.org/10.1016/j.plaphy.2020.11.027
|
| [87] |
Giordano M, El-Nakhel C, Carillo P, et al. (2022) Plant-derived biostimulants differentially modulate primary and secondary metabolites and improve the yield potential of red and green lettuce cultivars. Agronomy 12: 1361. https://doi.org/10.3390/agronomy12061361
|
| [88] |
Zrig A, Alsherif EA, Aloufi AS, et al. (2025) The biomass and health-enhancing qualities of lettuce are amplified through the inoculation of arbuscular mycorrhizal fungi. BMC Plant Biol 25: 521. https://doi.org/10.1186/s12870-025-06317-z
|
| [89] |
de Oliveira HO, Siqueira JA, Medeiros DB, et al. (2025) Harnessing the dynamics of plant organic acids metabolism following abiotic stresses. Plant Physiol Biochem 220: 109465. https://doi.org/10.1016/j.plaphy.2024.109465
|
| [90] |
Huang H, Jian Q, Jiang Y, et al. (2016) Enhanced chilling tolerance of banana fruit treated with malic acid prior to low-temperature storage. Postharvest Biol Technol 111: 209-213. https://doi.org/10.1016/j.postharvbio.2015.09.008
|
| [91] |
Ferreres F, Gil MI, Castañer M, et al. (1997) Phenolic metabolites in red pigmented lettuce (Lactuca sativa). Changes with minimal processing and cold storage. J Agric Food Chem 45: 4249-4254. http://doi.org/10.1021/jf970399j
|
| [92] |
Brazaitytė A, Vaštakaitė-Kairienė V, Sutulienė R, et al. (2022) Phenolic compounds content evaluation of lettuce grown under short-term preharvest daytime or nighttime supplemental LEDs. Plants 11: 1123. https://doi.org/10.3390/plants11091123
|
| [93] |
Senizza B, Zhang L, Miras-Moreno B, et al. (2020) The strength of the nutrient solution modulates the functional profile of hydroponically grown lettuce in a genotype-dependent manner. Foods 9: 1156. https://doi.org/10.3390/foods9091156
|
| [94] |
Simko I (2024) Spatio-temporal dynamics of lettuce metabolome: A framework for targeted nutritional quality improvement. Plants 13: 3316. https://doi.org/10.3390/plants13233316
|
| [95] |
Ninkuu V, Aluko OO, Yan J, et al. (2025) Phenylpropanoids metabolism: recent insight into stress tolerance and plant development cues. Front Plant Sci 16: 1571825. https://doi.org/10.3389/fpls.2025.1571825
|
| [96] |
Xiao J, Cao B, Tang W, et al. (2025) The CaCAD1-CaPOA1 module positively regulates pepper resistance to cold stress by increasing lignin accumulation. Int J Biol Macromol 290: 139979. https://doi.org/10.1016/j.ijbiomac.2025.139979
|
| [97] |
Ayuso-Calles M, García-Estévez I, Jiménez-Gómez A, et al. (2020) Rhizobium laguerreae improves productivity and phenolic compound content of lettuce (Lactuca sativa L.) under saline stress conditions. Foods 9: 1166. https://doi.org/10.3390/foods9091166
|
| [98] |
Abdalla MA, Li F, Wenzel-Storjohann A, et al. (2021) Comparative metabolite profile, biological activity and overall quality of three lettuce (Lactuca sativa L., Asteraceae) cultivars in response to sulfur nutrition. Pharmaceutics 13: 713. https://doi.org/10.3390/pharmaceutics13050713
|
| [99] | Díaz-Pérez M, Cantón Ramos JM, Velázquez Martí B, et al. (2024) Commercial quality of ‘Little Gem’ lettuce hearts. J Agric Food Res 16: 101168. https://doi.org/10.1016/j.jafr.2024.101168 |
| [100] |
Sung J-S, Hur O-S, Ryu K-Y, et al. (2016) Variation in phenotypic characteristics and contents of sesquiterpene lactones in lettuce (Lactuca sativa L.) germplasm. Korean J Plant Res 29: 679-689. http://doi.org/10.7732/kjpr.2016.29.6.679
|
| [101] |
Seo MW, Yang DS, Kays SJ, et al. (2009) Sesquiterpene lactones and bitterness in Korean leaf lettuce cultivars. HortScience 44: 246-249. http://doi.org/10.21273/HORTSCI.44.2.246
|
| [102] |
Dyson BC, Miller MAE, Feil R, et al. (2016) FUM2, a cytosolic fumarase, is essential for acclimation to low temperature in Arabidopsis thaliana. Plant Physiol 172: 118-127. http://doi.org/10.1104/pp.16.00852
|
| [103] |
Sun X, Han G, Meng Z, et al. (2019) Roles of malic enzymes in plant development and stress responses. Plant Signal Behav 14: e1644596. https://doi.org/10.1080/15592324.2019.1644596
|
| [104] |
Hameed MK, Umar W, Razzaq A, et al. (2022) Differential metabolic responses of lettuce grown in soil, substrate and hydroponic cultivation systems under NH4+/NO3⁻ application. Metabolites 12: 444. https://doi.org/10.3390/metabo12050444
|
| [105] |
Seo MW, Yang DS, Kays SJ, et al. (2009) Effects of nutrient solution electrical conductivity and sulfur, magnesium, and phosphorus concentration on sesquiterpene lactones in hydroponically grown lettuce (Lactuca sativa L.). Sci Hortic 122: 369-374. https://doi.org/10.1016/j.scienta.2009.06.013
|
| [106] |
Frey M, Vahabi K, Cankar K, et al. (2024) Sesquiterpene lactones – insights into biosynthesis, regulation and signalling roles. Crit Rev Plant Sci 43: 131-157. http://doi.org/10.1080/07352689.2024.2307240
|
 molsci-13-03-016-s001.xlsx |
 |
Figures(7) / Tables(6)
Milica Stojanović, Dragica Milosavljević, Jelena Dragišić Maksimović, Vuk Maksimović. Biofertilizer alters primary and secondary metabolism in winter-grown lettuce in a cultivar-dependent manner[J]. AIMS Molecular Science, 2026, 13(3): 334-366. doi: 10.3934/molsci.2026016
DownLoad: