Abstract
Market is increasingly demanding vegetables with high quality and nutraceutical characteristics. It was demonstrated that leafy vegetables can get benefit from biostimulants, for the reduction of nitrate concentration and the increment of antioxidants, with potential benefit for human health. The research purpose was to investigate on the role of a novel plant-based biostimulant in affecting nitrogen and carbon metabolism in wild rocket (Diplotaxis tenuifolia L.). Foliar spray treatments were performed with extracts obtained from borage (Borago officinalis L.) leaves and flowers. To evaluate the treatments effect, in vivo determinations (chlorophyll a fluorescence and chlorophyll content) were performed. At harvest, nitrate concentration, sucrose, total sugars, chlorophyll, and carotenoids levels were measured in leaves. In order to characterize the mechanism of action also at molecular level, a set of genes encoding for some of the key enzymes implicated in nitrate and carbon metabolism was selected and their expression was measured by qRT-PCR. Interesting results concerned the increment of sucrose, coherent with a high value of Fv/Fm, in addition to a significant reduction of nitrate and ABA than control, and an enhanced NR in vivo activity. Also, genes expression was influenced by extracts, with a more pronounced effect on N related genes.
Similar content being viewed by others
References
Abbas SM (2013) The influence of biostimulants on the growth and on the biochemical composition of Vicia faba cv. Giza 3 beans. Rom Biotechnol Lett 18(2):8061–8068
Anjana SU, Iqbal M (2007) Nitrate accumulation in plants, factors affecting the process, and human health implications: a review. Agron Sustain Dev 27(1):45–57
Aslam M, Huffaker RC, Rains DW (1984) Early effects of salinity on nitrate assimilation in barley seedlings. Plant Physiol 76(2):321–325
Baglieri A, Cadili V, Monterumici CM, Gennari M, Tabasso S, Montoneri E, Nardi S, Negre M (2014) Fertilization of bean plants with tomato plants hydrolysates: Effect on biomass production, chlorophyll content and N assimilation. Sci Hortic 176:194–199
Borghesi E, Ferrante A, Gordillo B, Rodríguez-Pulido FJ, Cocetta G, Trivellini A, Mensuali-Sodi A, Malorgio F, Heredia FJ (2016) Comparative physiology during ripening in tomato rich-anthocyanins fruits. Plant Growth Regul 80(2):207–214
Brewitz E, Larsson C-M, Larsson M (1995) Influence of nitrogen supply on concentrations and translocation of abscisic acid in barley (Hordeum vulgare). Physiol Plant 95:499–506
Bulgari R, Cocetta G, Trivellini A, Vernieri P, Ferrante A (2015) Biostimulants and crop responses: a review. Biol Agric Hortic 31:1–17. https://doi.org/10.1080/01448765.2014.964649
Bulgari R, Morgutti S, Cocetta G, Negrini N, Farris S, Calcante A, Spinardi A, Ferrante A (2017) Evaluation of borage extracts as potential biostimulant using a phenomic, agronomic, physiological, and biochemical approach. Front Plant Sci 8:935
Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383(1–2):3–41
Cataldo DA, Haroon M, Sehrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by titration of salicylic acid. Commun Soil Sci Plant Anal 6:71–80
Cavaiuolo M, Ferrante A (2014) Nitrates and glucosinolates as strong determinants of the nutritional quality in rocket leafy salads. Nutrients 6:1519–1538. https://doi.org/10.3390/nu6041519
Cavaiuolo M, Cocetta G, Spadafora ND, Müller CT, Rogers HJ, Ferrante A (2017) Gene expression analysis of rocket salad under pre-harvest and postharvest stresses: a transcriptomic resource for Diplotaxis tenuifolia. PloS One 12(5):e0178119
Chen BM, Wang ZH, Li SX, Wang GX, Song HX, Wang XN (2004) Effects of nitrate supply on plant growth, nitrate accumulation, metabolic nitrate concentration and nitrate reductase activity in three leafy vegetables. Plant Sci 167(3):635–643
Chow CK, Hong CB (2002) Dietary vitamin E and selenium and toxicity of nitrite and nitrate. Toxicology 180(2):195–207
Cocetta G, Rossoni M, Gardana C, Mignani I, Ferrante A, Spinardi A (2015) Methyl jasmonate affects phenolic metabolism and gene expression in blueberry (Vaccinium corymbosum). Physiol Plant 153:269–283. https://doi.org/10.1111/ppl.12243
Colla G, Nardi S, Cardarelli M, Ertani A, Lucini L, Canaguier R, Rouphael Y (2015) Protein hydrolysates as biostimulants in horticulture. Sci Hortic 196:28–38
Colla G, Kim HJ, Kyriacou MC, Rouphael Y (2018) Nitrate in fruits and vegetables. Sci Hortic 237:221–238
D'Anna F, Miceli A, Vetrano F (2003) First results of floating system cultivation of Eruca sativa L. In: Pardossi E et al (ed) Proceeding on greenhouse salinity, Acta Hortic, 609:361–364
D'Antuono LF, Elementi S, Neri R (2009) Exploring new potential health-promoting vegetables: glucosinolates and sensory attributes of rocket salads and related Diplotaxis and Eruca species. J Sci Food Agric 89:713–722
Di Gioia F, Gonnella M, Santamaria P (2013) Contribution of leafy vegetables to dietary nitrate intake and regulations. In: Umar S, Anjum NA, Khan NA (eds) Nitrate in leafy vegetables: toxicity and safety measures. I.K. International Publishing, New Delhi, pp 2–16
Dudaš S, Šola I, Sladonja B, Erhatić R, Ban D, Poljuha D (2016) The effect of biostimulant and fertilizer on “low input” lettuce production. Acta Bot Croat 75:253–259. https://doi.org/10.1515/botcro-2016-0023
Edwards JW, Coruzzi GM (1990) Cell-specific gene expression in plants. Annu Rev Genet 24(1):275–303
Ertani A, Cavani L, Pizzeghello D, Brandellero E, Altissimo A, Ciavatta C, Nardi S (2009) Biostimulant activity of two protein hydrolyzates in the growth and nitrogen metabolism of maize seedlings. J Plant Nutr Soil Sci 172(2):237–244
Ertani A, Schiavon M, Muscolo A, Nardi S (2013) Alfalfa plant-derived biostimulant stimulate short-term growth of salt stressed Zea mays L. plants. Plant Soil 364(1–2):145–158
Ferrante A, Incrocci L, Maggini R, Tognoni F, Serra G (2002) Preharvest and postharvest strategies for reducing nitrate content in rocket (Eruca sativa). In: XXVI international horticultural congress: issues and advances in postharvest horticulture, vol 628, pp 153–159
Fiorentino N, Ventorino V, Woo SL, Pepe O, De Rosa A, Gioia L, Romano I, Lombardi N, Napolitano M, Colla G, Rouphael Y (2018) Trichoderma-based biostimulants modulate rhizosphere microbial populations and improve N uptake efficiency, yield, and nutritional quality of leafy vegetables. Front Plant Sci 9:743
Frezza D, León A, Logegaray V, Chiesa A, Desimone M, Diaz L (2005) Soilless culture technology for high quality lettuce. Acta Hortic 697:43
Goel P, Bhuria M, Kaushal M, Singh AK (2016) Carbon: nitrogen interaction regulates expression of genes involved in N-uptake and assimilation in Brassica juncea L. PloS one 11(9):e0163061
Guan P (2017) Dancing with hormones: a current perspective of nitrate signaling and regulation in arabidopsis. Front Plant Sci 28(8):169
Jakse M, Hacin J, Kacjan NM (2013) Production of rocket (Eruca sativa Mill) on plug trays and on a floating system in relation to reduced nitrate content. Acta Agric Slov 101(1):59
Kiba T, Feria-Bourrellier AB, Lafouge F, Lezhneva L, Boutet-Mercey S, Orsel M et al (2012) The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell 24:245–258. https://doi.org/10.1105/tpc.111.092221
Kim S-J, Ishii G (2007) Effect of storage temperature and duration on glucosinolate, total vitamin C and nitrate contents in rocket salad (Eruca sativa Mill). J Sci Food Agric. 87(6):966–973
Krapp A, David LC, Chardin C, Girin T, Marmagne A, Leprince AS, Chaillou S, Ferrario-Méry S, Daniel-Vedele F (2014) Nitrate transport and signalling in Arabidopsis. J Exp Bot 65(3):789–798
Kunicki E, Grabowska A, Sekara A, Wojciechowska R (2010) The effect of cultivar type, time of cultivation, and biostimulant treatment on the yield of spinach (Spinacia oleracea L.). Folia Hortic 22:9–13
Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu Rev Plant Biol 47(1):569–593
Lancien M, Ferrario-Méry S, Roux Y, Bismuth E, Masclaux C, Hirel B, Gadal P, Hodges M (1999) Simultaneous expression of NAD-dependent isocitrate dehydrogenase and other Krebs cycle genes after nitrate resupply to short-term nitrogen-starved tobacco. Plant Physiol 120(3):717–726
Lancien M, Gadal P, Hodges M (2000) Enzyme redundancy and the importance of 2-oxoglutarate in higher plant ammonium assimilation. Plant Physiol 123(3):817–824
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic membranes. Methods Enzymol 148:350–382
Liu XQ, Lee KS (2012) Effect of mixed amino acids on crop growth. In: Aflakpui G (ed) Agricultural science. InTech Europe Publisher, Rijeka, pp 119–158
Liu XQ, Ko KY, Kim SH, Lee KS (2007) Effect of amino acid fertilization on nitrate assimilation of leafy radish and soil chemical properties in high nitrate soil. Commun Soil Sci Plant Anal 39(1–2):269–281
Lu Y, Yamaguchi J, Sato T (2015) Integration of C/N-nutrient and multiple environmental signals into the ABA signaling cascade. Plant Signal Behav 10(12):e1048940
Magnani G, Filippi F, Borghesi E, Vitale M (2007) Impact of sunlight spectrum modification on yield and quality of ready-to-use lettuce and rocket salad grown on floating system. In: International symposium on high technology for greenhouse system management: greensys, vol 801, pp 163–170
Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann Bot 105(7):1141–1157
McKnight GM, Duncan CW, Leifert C, Golden MH (1999) Dietary nitrate in man: friend or foe? Br J Nutr 81:349–358
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64(13):3983–3998
O'Brien JA, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi G, Gutiérrez RA (2016) Nitrate transport, sensing, and responses in plants. Mol Plant 9(6):837–856
Ondzighi-Assoume CA, Chakraborty S, Harris JM (2016) Environmental nitrate stimulates root tip abscisic acid accumulation via release from inactive stores. Plant Cell 28:729–745
Otori K, Tanabe N, Maruyama T, Sato S, Yanagisawa S, Tamoi M, Shigeoka S (2017) Enhanced photosynthetic capacity increases nitrogen metabolism through the coordinated regulation of carbon and nitrogen assimilation in Arabidopsis thaliana. J Plant Res 130(5):909–927
Palmer CE (1985) The relationship of abscisic acid to nitrate reductase activity in the potato plant. Plant Cell Physiol 26:1167–1174
Pao SS, Paulsen IT, Saier MH (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34
Parker JL, Newstead S (2014) Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507(7490):68–72
Peuke AD, Jeschk WD, Hartung W (1994) The uptake and flow of C, N and ions between roots and shoots in Ricinus communis L. III. Long-distance transport of abscisic acid depending on nitrogen nutrition and salt stress. J Exp Bot 45:741–747
Premuzic Z, Gárate A, Bonilla I (2001) Yield and quality of greenhouse lettuce as affected by form of N fertilizer and light supply. In: Plant nutrition, Springer, Netherlands, pp 300–301
Radin JW, Parker LL, Guinn G (1982) Water relations of cotton plants under nitrogen deficiency: V. Environmental control of abscisic acid accumulation and stomatal sensitivity to abscisic acid. Plant Physiol 70:1066–1070
Ragaert P, Verbeke W, Devlieghere F, Debevere J (2004) Consumer perception and choice of minimally processed vegetables and packaged fruits. Food Qual Prefer 15(3):259–270
Raines CA (2011) Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: current and future strategies. Plant Physiol 155(1):36–42
Ramos B, Miller FA, Brandão TR, Teixeira P, Silva CL (2013) Fresh fruits and vegetables—an overview on applied methodologies to improve its quality and safety. Innov Food Sci Emerg Technol 20:1–15
Rideout JW, Raper CD Jr, Miner GS (1992) Changes in ratio of soluble sugars and free amino nitrogen in the apical meristem during floral transition of tobacco. Int J Plant Sci 153:78–88
Romanowska-Duda Z, Grzesik M, Janas R (2019) Maximal efficiency of PSII as a marker of sorghum development fertilized with waste from a biomass biodigestion to methane. Front Plant Sci 8(9):1920. https://doi.org/10.3389/fpls.2018.01920
Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29(3):426–434
Rouphael Y, Colla G (2018) Synergistic biostimulatory action: designing the next generation of plant biostimulants for sustainable agriculture. Front Plant Sci 9:1655
Sánchez R, Flores A, Cejudo FJ (2006) Arabidopsis phosphoenolpyruvate carboxylase genes encode immunologically unrelated polypeptides and are differentially expressed in response to drought and salt stress. Planta 223(5):901–909
Santamaria P, Gonnella M, Elia A, Parente A, Serio F (2001) Ways of reducing rocket salad nitrate content. Acta Hortic. 548:529–536. https://doi.org/10.17660/ActaHortic.2001.548.64
Santi C, Zamboni A, Varanini Z, Pandolfini T (2017) Growth stimulatory effects and genome-wide transcriptional changes produced by protein hydrolysates in maize seedlings. Front Plant Sci 8:433
Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027–1038
Shi J, Yi K, Liu Y, Xie L, Zhou Z, Chen Y, Hu Z, Zheng T, Liu R, Chen Y, Chen J (2015) Phosphoenolpyruvate carboxylase in Arabidopsis leaves plays a crucial role in carbon and nitrogen metabolism. Plant Physiol 167:671–681
Schiavon M, Ertani A, Nardi S (2008) Effects of an alfaalfa protein hydrolysate on the gene expression and activity of enzymes of TCA cycle and N metabolism in Zea mays L. J Agric Food Chem 56:11800–11808
Signora L, De Smet I, Foyer CH, Zhang H (2001) ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J 28:655–662
Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Ann Rev Plant Biol 53(1):449–475
Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2:178–186
Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY et al (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19(5):765–777
Tarantino E, Disciglio G, Frabboni L, Libutti A, Gatta G, Gagliaridi A, Tarantino A (2015) Effect of biostimulants application on quali-quantitative characteristics of cauliflower, pepper, and fennel crops under organic and conventional fertilization. Environment 10:13
Temple SJ, Vance CP, Gantt JS (1998) Glutamate synthase and nitrogen assimilation. Trends Plant Sci 3(2):51–56
Tripodi P, Francese G, Mennella G (2017) Rocket salad: crop description, bioactive compounds and breeding perspectives. Adv Hortic Sci 31(2):107–113
Vance CP, Gantt JS (1992) Control of nitrogen and carbon metabolism in root nodules. Physiol Plant 85(2):266–274
Vernieri P, Borghesi E, Ferrante A, Magnani G (2005) Application of biostimulants in floating system for improving rocket quality. J Food Agric Environ 3:86–88
Vernieri P, Perata P, Armellini D, Bugnoli M, Presentini R, Lorenzi R et al (1989) Solid phase radioimmunoassay for the quantitation of abscisic acid in plant crude extracts using a new monoclonal antibody. J Plant Physiol 134:441–446
Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant, Cell Env 25:195–210
Wood CW, Reeves DW, Himelrick DG (1993) Relationships between chlorophyll meter readings and leaf chlorophyll concentration, N status, and crop yield: a review. In: Proceedings of the agronomy society of New Zealand, vol 23, pp 1–9
Xu D, Shen Y (2005) External and internal factors responsible for midday depression of photosynthesis. In: Pessarakli M (ed) Handbook of photosynthesis, 2nd edn. CRC Press, Boca Raton, pp 287–297
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514. https://doi.org/10.3389/fpls.2016.02049
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329
Zodape ST, Gupta A, Bhandari SC, Rawat US, Chaudhary DR, Eswaran K, Chikara J (2011) Foliar application of seaweed sap as biostimulant for enhancement of yield and quality of tomato (Lycopersicon esculentum Mill.). J Sci Ind Res 70:215–219
Author information
Authors and Affiliations
Contributions
RB: performed the experiment and analytical determinations, the elaboration and the interpretation of data, and contributed to manuscript writing; GC: contributed to molecular analysis, data interpretation and manuscript writing; AT: contributed to ABA extraction and determination, and manuscript writing; AF: responsible for the research activities, experimental plan, and revision of the final manuscript. All authors read and approved the final version of the manuscript.
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bulgari, R., Cocetta, G., Trivellini, A. et al. Borage extracts affect wild rocket quality and influence nitrate and carbon metabolism. Physiol Mol Biol Plants 26, 649–660 (2020). https://doi.org/10.1007/s12298-020-00783-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-020-00783-5