Effect of Agroecological Conditions on Biologically Active Compounds and Metabolome in Carrot
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
QJ1210165, QK1910235
Ministerstvo Zemědělství
RVO61388971
Institute of Microbiology, Czech Academy of Sciences
LM2018100
METROFOOD-CZ
LO1601
NPU I
PubMed
33916284
PubMed Central
PMC8066420
DOI
10.3390/cells10040784
PII: cells10040784
Knihovny.cz E-zdroje
- Klíčová slova
- 6-methoxymellein, ascorbic acid, carotenes, carrot cultivars, farming conditions, metabolomic fingerprinting, spontaneous infection,
- MeSH
- analýza hlavních komponent MeSH
- ekologie a životní prostředí - jevy * MeSH
- karotenoidy analýza MeSH
- kyselina askorbová analýza MeSH
- metabolom * MeSH
- metabolomika MeSH
- mrkev obecná metabolismus mikrobiologie MeSH
- nemoci rostlin mikrobiologie MeSH
- zemědělství * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- karotenoidy MeSH
- kyselina askorbová MeSH
Carrot serves as a source of health-beneficial phytochemicals for human diet whose content is affected by agroecological conditions. The effect of conventional, integrated and organic farming on ascorbic acid (AA) and α,β-carotene levels of new carrot cultivars Cortina F1 and Afalon F1 was investigated and their metabolomic profiles were measured by direct analysis in real time ion source coupled with a high-resolution mass spectrometer (DART-HRMS). Cortina and Afalon exhibited high levels of AA and total carotenes under all agroecological conditions tested that fluctuated in broad ranges of 215-539 and 173-456 mg AA.kg-1 dry biomass and 1069-2165 and 1683-2165 mg carotene.kg-1 dry biomass, respectively. The ratio of β- to α-carotene in both cultivars was about 1.3. The most important variable for the PCA and the partial least squares discriminant analysis (PLS-DA) models for ethyl acetate extracts measured in positive and negative ionization mode was 6-methoxymellein (6-MM). Total carotene content and 6-MM levels were higher in the organic carrot compared to the conventional one and were correlated with a higher level of spontaneous infection. Other important compounds identified were sitosterol, hexose and various organic acids including antioxidant ferulic and coumaric acids. The findings allow comparison of metabolomic profiles and the AA and carotene contents of both cultivars with those of other commercially used carrots.
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Ahmad A., Cawood M., Iqbal Q., Arino A., Batool A., Tariq R.M.S., Azam M., Akhtar S. Phytochemicals in Daucus carota and their health benefits–review article. Foods. 2019;8:424. doi: 10.3390/foods8090424. PubMed DOI PMC
Buchtová I. Situational and Development Review: Vegetables. Ministry of Agriculture of the Czech Republic, Institute of Agricultural Economics and Information; Prague, Czech Republic: 2019. [(accessed on 30 September 2020)]. Available online: http://eagri.cz/public/web/file/644345/SVZ_Zelenina_12_2019.pdf. (In Czech)
Bozalan N.K., Karadeniz F. Carotenoid profile, total phenolic content, and antioxidant activity of carrots. Int. J. Food Propert. 2011;14:1060–1068. doi: 10.1080/10942910903580918. DOI
Cwalina-Ambroziak B., Amarowicz R., Glosek M., Janiak M. Changes in the concentrations of phenolic acids in carrot plants inoculated with Alternaria radicina Meier, Drechsler & Eddy. Acta Sci. Pol. Hortorum Cultus. 2014;13:97–108.
Seljasen R., Vogt G., Olsen E., Lea P., Hogetveit L.A., Tajet T., Meadow R., Bengtsson G.B. Influence of field attack by carrot psyllid (Trioza apicalis Förster) on sensory quality, antioxidant capacity and content of terpenes, falcarindiol and 6-methoxymellein of carrots (Daucus carrota L.) J. Agric. Food Chem. 2013;61:2831–2838. doi: 10.1021/jf303979y. PubMed DOI
Lachman J., Orsák M., Pivec V. Antioxidant contents and composition in some vegetables and their role in human nutrition. Zahrad. Horticul. Sci. 2000;27:65–78.
Smirnoff N., Wheeler G.L. Ascorbic acid in plants: Biosynthesis and function. Crit. Rev. Biochem. Mol. Biol. 2000;35:291–314. doi: 10.1080/10409230008984166. PubMed DOI
Nicolle C., Simon G., Rock E., Amouroux P., Remesy C. Genetic variability influences carotenoid, vitamin, phenolic, and mineral content in white, yellow, purple, orange, and dark-orange carrot cultivars. J. Soc. Hortic. Sci. 2004;129:523–529. doi: 10.21273/JASHS.129.4.0523. DOI
Kim J.E., Rensing K.H., Douglas C.J., Cheng K.M. Chromoplasts ultrastructure and estimated carotene content in root secondary phloem of different carrot varieties. Planta. 2010;231:549–558. doi: 10.1007/s00425-009-1071-7. PubMed DOI
Mustafa A., Trevino L.M., Turner C. Pressurized hot ethanol extraction of carotenoids from carrot by-products. Molecules. 2012;17:1809. doi: 10.3390/molecules17021809. PubMed DOI PMC
Alasalvar C., Grigor M., Zhang D., Quantick P.C., Shadidi F. Comparison of volatiles, phenolics, sugars, antioxidant vitamins and sensory quality of different colored carrot varieties. J. Agric. Food Chem. 2001;49:410–416. doi: 10.1021/jf000595h. PubMed DOI
Metzger B.T., Barnes D.M., Reed J.D. Purple carrot (Daucus carota L. ) polyacetylenes decrease lipopolysacharide-induced expression of inflammatory proteins in macrophage and endothelial cells. J. Agric. Food Chem. 2008;56:3554–3560. doi: 10.1021/jf073494t. PubMed DOI
Seljasen R., Bengtsson G.B., Hoftun H., Vogt G. Sensory and chemical changes in five varieties of carrot (Daucus carota L.) in response to mechanical stress at harvest and post-harvest. J. Sci. Food Agric. 2001;81:436–447. doi: 10.1002/1097-0010(200103)81:4<436::AID-JSFA837>3.0.CO;2-R. DOI
Kidmose U., Hansen S.L., Christensen L.P., Edelenbos M., Larsen E., Norbaek R. Effects of genotype, root size, storage, and processing on bioactive compounds in organically grown carrots (Daucus carota L.) J. Food Sci. 2004;69:S388–S394. doi: 10.1111/j.1365-2621.2004.tb09955.x. DOI
Rico D., Martín-Diana A.B., Barat J.M., Barry-Ryan C. Extending and measuring the quality of fresh-cut fruit and vegetables: A review. Trends Food Sci. Technol. 2007;18:373–386. doi: 10.1016/j.tifs.2007.03.011. DOI
Matějková J., Petříková K. Variation in content of carotenoids and vitamin C in carrots. Not. Sci. Biol. 2010;2:88–91. doi: 10.15835/nsb245108. DOI
Stan S.D., Kar S., Stoner G.D. Bioactive food components and cancer risk reduction. J. Cell. Biochem. 2008;104:339–356. doi: 10.1002/jcb.21623. PubMed DOI
Alasalvar C., Al-Farsi M., Quantick P., Shahidi F., Wiktorowicz R. Effect of chill storage and modified atmosphere packaging (MAP) on antioxidant activity, anthocyanins, carotenoids, phenolics and sensory quality of ready-to-eat shredded orange and purple carrots. Food Chem. 2005;89:69–76. doi: 10.1016/j.foodchem.2004.02.013. DOI
Manach C., Scalbert A., Morand C., Remesy C., Jimenez L. Polyphenols: Food sources and bioavailability. Am. J. Clin. Nutr. 2004;79:727–747. doi: 10.1093/ajcn/79.5.727. PubMed DOI
Soltoft M., Nielsen J., Holst Laursen K., Husted S., Halekoh U., Knuthsen P. Effects of organic and conventional growth systems on the content of flavonoids in onions and phenolic acids in carrots and potatoes. J. Agric. Food Chem. 2010;58:10323–10329. doi: 10.1021/jf101091c. PubMed DOI
Sliwinska A., Naliwajski M.R., Pietrosiuk A., Syklowska-Baranek K. In vitro response of Polyscias filicifolia (Araliaceae) shoots to elicitation with alarmone-diadenosine triphosphate, methyl jasmonate, and salicylic acid. Cells. 2021;10:419. doi: 10.3390/cells10020419. PubMed DOI PMC
Ceglie F.G., Amodio M.L., Colelli G. Effect of organic production systems on quality and postharvest performance of horticultural produce. Horticulturae. 2016;2:4. doi: 10.3390/horticulturae2020004. DOI
Faligowska A., Panasiewicz K., Szymanska G., Ratajczak K., Sulewska H., Pszczolkowska A., Kocira L.A. Influence of farming system on weed infestation and on productivity of narrow-leaved lupin (Lupinus angustifolius L.) Agriculture. 2020;10:459. doi: 10.3390/agriculture10100459. DOI
Rembialkowska E. Organic farming as a system to provide better vegetable quality. In: Tijskens L.M.M., Vollebregt H.M., editors. Proceedings of the International Conference on Quality in Chains, Vols 1 and 2: An Integrated View on Fruit and Vegetable Quality. Volume 604. Acta Hortic; Leuven, Belgium: 2003. pp. 473–479.
Khakbazan M., Henry R., Haung J., Mohr R., Peters R., Fillmore S., Rodd V., Mills A. Economics of organically managed and conventional potato production systems in Atlantic Canada. Can. J. Plant Sci. 2015;95:161–174. doi: 10.4141/cjps-2014-050. DOI
Mitchell A.E., Hong Y.J., Koh E., Barret D.M., Bryant D.E., Denison R.F., Kaffka S. Ten-year comparison of the influence of organic and conventional crop management practices on the content of flavonoids in tomatoes. J. Agric. Food Chem. 2007;55:6154–6159. doi: 10.1021/jf070344+. PubMed DOI
Sink N., Mikulic-Petrovsek M., Veberic R., Kacjan Marsic N. Chemical composition and morphometric traits and yield of carrots grown in organic and integrated farming systems. Turk. J. Agric. For. 2017;41:452–462. doi: 10.3906/tar-1705-8. DOI
Soltoft M., Bysted A., Madsen K.H., Mark A.B., Bűgel S.G., Nielsen J., Knuthsen P. Effects of organic and conventional growth on the content of carotenoids in carrot roots, and on intake and plasma status of carotenoids in humans. J. Sci. Food Agric. 2011;91:767–775. doi: 10.1002/jsfa.4248. PubMed DOI
Pacifico D., Onofri C., Parisi B., Ostano P., Mandolino G. Influence of organic farming on the potato transcriptome. Sustainability. 2017;9:779. doi: 10.3390/su9050779. DOI
Ierna A., Parisi B. Crop growth and tuber yield of “early” potato crop under organic and conventional farming. Scient. Horticult. 2014;165:260–265. doi: 10.1016/j.scienta.2013.11.032. DOI
Brazinskiene V., Asakaviciute R., Miezeliene A., Alencikiene G., Ivanauskas L., Jakstas V., Viskelis P., Razukas A. Effect of farming systems on the yield, quality parameters and sensory properties of conventionally and organically grown potato (Solanum tuberosum L.) tubers. Food Chem. 2014;145:903–909. doi: 10.1016/j.foodchem.2013.09.011. PubMed DOI
Tein B., Kauer K., Runno-Paurson E., Eremeev V., Luik A., Selge A., Loit E. The potato tuber disease occurrence as affected by conventional and organic farming systems. Am. J. Potato Res. 2015;92:662–672. doi: 10.1007/s12230-015-9481-5. DOI
Lazzaro I., Moretti A., Giorni P., Brera C., Battilani P. Organic vs. conventional farming: Differences in infection by mycotoxin-producing fungi on maize and wheat in Northern and Central Italy. Crop Prot. 2015;72:22–30. doi: 10.1016/j.cropro.2015.03.001. DOI
Farrar J.J., Pryor B.M., Davis R.M. Alternaria diseases of carrot. Plant Dis. 2004;88:776–784. doi: 10.1094/PDIS.2004.88.8.776. PubMed DOI
Gugino B.K., Carroll J., Chen J., Ludwig J., Abawi G. NYS Integrated Pest Management Program. New York State IPM Program; Geneva, NY, USA: 2004. [(accessed on 1 April 2021)]. Carrot Leaf Blight Diseases and Their Management in New York. Available online: www.nysipm.cornell.edu/factsheets/vegetables/misc/clb.pdf.
Harding V.K., Heale J.B. Isolation and identification of the antifungal compounds accumulating in the induced resistence response of carrot root slices to Botrytis cinerea. Physiol. Plant Pathol. 1980;17:277–289.
Mercier J., Kuc J. Elicitation of 6-methoxymellein in carrot leaves by Cercospora carotae. J. Sci. Food Agric. 1997;73:60–62. doi: 10.1002/(SICI)1097-0010(199701)73:1<60::AID-JSFA704>3.0.CO;2-E. DOI
Lecomte M., Berruyer R., Hamama L., Boedo C., Hudhomme P., Bersihand S., Arul J., N’Guyen G., Gatto J., Guilet D., et al. Inhibitory effects of the carrot metabolites 6-methoxymellein and falcarindiol on development of the fungal leaf blight pathogen Alternaria dauci. Physiol. Mol. Plant Pathol. 2012;80:58–67. doi: 10.1016/j.pmpp.2012.10.002. DOI
Louarn S., Nawrocki A., Edelenbos M., Jensen D.F., Jensen O.N., Collinge D.B., Jensen B. The influence of the fungal pathogen Mycocentrospora acerina on the proteome and polyacetylenes and 6-methoxymellein in organic and conventionally cultivated carrots (Daucus carota) during postharvest storage. J. Proteom. 2012;75:962–977. doi: 10.1016/j.jprot.2011.10.014. PubMed DOI
Mercier J., Roussel D., Charles M.T., Arul J. Systemic and local responses associated with UV and pathogen induced resistance to Botrytis cinerea in stored carrot. Phytopathology. 2000;90:981–986. doi: 10.1094/PHYTO.2000.90.9.981. PubMed DOI
Kouassi N., Corcuff R., Arul J., Tweddell R.J. Effect of storage temperature and age after harvest on the accumulation of the phytoalexin 6-methoxymellein in UV-C treated carrots. Acta Hortic. 2012;945:135–138. doi: 10.17660/ActaHortic.2012.945.17. DOI
Fan X., Mattheis J.P., Roberts R.G. Biosynthesis of phytoalexin in carrot root requires ethylene action. Physiol. Plant. 2000;110:450–454. doi: 10.1111/j.1399-3054.2000.1100404.x. DOI
Kramer M., Bufler G., Ulrich D., Leitenberger M., Conrad J., Carle R., Kammerer D.R. Effect of ethylene and 1-methylcyclopropene on bitter compounds in carrots (Daucus carota L.) Postharvest. Biol. Technol. 2012;73:28–36. doi: 10.1016/j.postharvbio.2012.05.009. DOI
Eisebai M.F., Ghabbour H.A., Legrave N., Fontaine-Vive F., Mehiri M. New bioactive chlorinated cyclopentene derivatives from the marine-derived fungus Phoma sp. Med. Chem. Res. 2018;27:1885–1892. doi: 10.1007/s00044-018-2201-1. DOI
Medical T. Isolation and antimicrobial activity of the phytoalexin 6-methoxymellein from cultured carrot cells. Phytochemistry. 1983;22:669–672.
Mercier J., Arul J., Julien C. Effect of food preparation on the isocoumarin, 6-methoxymellein content of UV-treated carrots. Food Res. Int. 1994;27:401–404. doi: 10.1016/0963-9969(94)90196-1. DOI
Jayaraj J., Rahman M., Wan A., Punja Z.K. Enhanced resistance to foliar fungal pathogens in carrot by application of elicitors. Ann. Appl. Biol. 2009;155:71–80. doi: 10.1111/j.1744-7348.2009.00321.x. DOI
Amin M., Kurosaki F., Nishi A. Extracellular pectinolytic enzymes of fungi elicit phytoalexin accumulation in carrot suspension culture. J. Gen. Microbiol. 1986;132:771–777.
De Girolamo A., Solfrizzo M., Vitti C., Visconti A. Occurrence of 6-methoxymellein in fresh and processed carrots and relevant effect of storage and processing. J. Agric. Food Chem. 2004;52:6478–6484. doi: 10.1021/jf0491660. PubMed DOI
Liu R., Choi H.S., Kim S.L., Kim J.H., Yun B.S., Lee B.S. 6-Methoxymellein isolated from carrot (Daucus carota L.) targets breast cancer stem cells by regulating NF-κB signaling. Molecules. 2020;25:4374. doi: 10.3390/molecules25194374. PubMed DOI PMC
Pawelec A., Dubourg C., Briard M. Evaluation of carrot resistance to alternaria leaf blight in controlled environments. Plant Pathol. 2006;55:68–72. doi: 10.1111/j.1365-3059.2006.01290.x. DOI
Lundegardh B., Botek P., Schulzová V., Hajšlová J., Stromnerg A., Andersson C. Impact of different green manures on the content of S-alk(en)yl-L-cysteine sulfoxides and L-ascorbic acid in leek (Allium porrum) J. Agric. Food Chem. 2008;56:2102–2111. doi: 10.1021/jf071710s. PubMed DOI
Bhave A., Schulzova V., Chmelarova H., Mrnka L., Hajslova J. Assessment of the rosehips based on their biologically active compound content. J. Food Drug Anal. 2017;25:681–690. doi: 10.1016/j.jfda.2016.12.019. PubMed DOI PMC
Sharma K.D., Karki S., Thakur N.S., Attri S. Chemical composition, functional properties and processing of carrot–A review. J. Food Sci. Technol. 2012;49:22–32. doi: 10.1007/s13197-011-0310-7. PubMed DOI PMC
Bratu M., Avram D., Buruleanu L. The minerals and vitamin content variation from different vegetables raw materials. Appl. Sci. Res. Coll. Lith. 2006;4:86–88.
Faisal N.A., Chatha S.A.S., Hussain A.I., Ikram M., Bukhari S.A. Liaison of phenolic acid and biological activity of escalating cultivars of Daucus carota. Int. J. Food Prop. 2017;20:2782–2792. doi: 10.1080/10942912.2016.1252390. DOI
Seljasen R., Lea P., Torp T., Riley H., Berentsen E., Thomsen M., Bengtsson G.B. Effect of genotype, soil, type, year and fertilization on sensory and morphological attributes of carrots (Daucus carrota L.) J. Sci. Food. Agric. 2012;92:1786–1799. doi: 10.1002/jsfa.5548. PubMed DOI
Perrin F., Dubois-Laurent C., Gibon Y., Citerne S., Huet S., Suel A., Le Clerc V., Briard M., Hamama L., Peltier D., et al. Combined Alternaria dauci infection and water stresses impact carotenoid content of carrot leaves and roots. Environ. Exp. Bot. 2017;142:125–134. doi: 10.1016/j.envexpbot.2017.09.004. DOI
Novotný Č., Schulzová V., Krmela A., Hajšlová J., Svobodová K., Koudela M. Ascorbic acid and glucosinolate levels in new Czech cabbage cultivars: Effect of production system and fungal infection. Molecules. 2018;23:1855. doi: 10.3390/molecules23081855. PubMed DOI PMC
Fjelkner-Modig S., Bengtsson H., Stegmark R., Nystrom S. The influence of organic and integrated production on nutritional, sensory and agricultural aspects of vegetable raw materials for food production. Acta Agric. Scand. Sect. B Soil Plant Sci. 2001;50:102–113. doi: 10.1080/090647100750374250. DOI
Middleton E.M., Teramura A.H. The role of flavonol glycosides and carotenoids in protecting soybean from ultraviolet-B damage. Plant Physiol. 1993;103:741–752. doi: 10.1104/pp.103.3.741. PubMed DOI PMC
Evers A.M., Tuuri H., Hagg M., Plaami S., Hakkinen U., Talvitie H. Soil forming and plant density effects on carrot yield and internal quality. Plant Foods Hum. Nutr. 1997;51:283–294. doi: 10.1023/A:1007955818503. PubMed DOI
Heinonen M.I., Ollilainen V., Linkola E.K., Varo P.T., Koivistoinen P.E. Carotenoids in Finnish foods: Vegetables, fruits, and berries. J. Agric. Food Chem. 1989;37:655–659. doi: 10.1021/jf00087a017. DOI
Simon P.W., Wolff X.Y. Carotenes in typical and dark orange carrots. J. Agric. Food Chem. 1987;35:1017–1022. doi: 10.1021/jf00078a038. DOI
Brandt K., Leifert C., Sanderson R., Seal J.S. Agroecosystem management and nutritional quality of plant foods: The case of organic fruits and vegetables. Crit. Rev. Plan Sci. 2011;30:177–197. doi: 10.1080/07352689.2011.554417. DOI
Novotná H., Kmiecik O., Galazka M., Krtková V., Hurajová A., Schulzová V., Hallmann E., Rembialkowska E., Hajšlová J. Metabolomic fingerprinting employing DART-TOFMS for authentication of tomatoes and peppers from organic and conventional farming. Food Add. Contam. Part A. 2012;29:1335–1346. doi: 10.1080/19440049.2012.690348. PubMed DOI
Hart D.J., Scott K.J. Development and evaluation of an HPLC method for the analysis of carotenoids in foods, and the measurement of the carotenoid content of vegetables and fruits commonly consumed in the UK. Food Chem. 1995;54:101–111. doi: 10.1016/0308-8146(95)92669-B. DOI
Maiani G., Periago Caston M.J., Catasta G., Toti E., Goni I., Cambrodon A.B., Granado-Lorencio F., Olmedilla-Alonso B., Knuthsen P., Valoti M., et al. Carotenoids: Actual knowledge on food sources, intakes, stability and bioavailability and their protective role in humans. Molec. Nutr. Food Res. 2009;53:S194–S218. doi: 10.1002/mnfr.200800053. PubMed DOI
Paoletti F., Raffo A., Kristensen H.L., Thorup-Kristensen A., Ploeger A., Kahl J. Multi-method comparison of carrot quality from a conventional and three organic cropping systems with increasing levels of nutrient recycling. J. Sci. Food Agric. 2012;92:2855–2869. doi: 10.1002/jsfa.5819. PubMed DOI
Kotíková Z., Hejtmánková A., Lachman J., Hamouz K., Trnková E., Dvořák P. Effect of selected factors on total carotenoid content in potato tubers (Solanum tuberosum L.) Plant Soil Environ. 2007;53:355–360. doi: 10.17221/2214-PSE. DOI
Brdar-Jokanovič M., Koren A., Ljevnaič-Mašič B., Kiprovski B., Sikora V. Yield and quality parameters of Hokkaido type pumpkins grown in Serbia. Genetika. 2019;51:377–387. doi: 10.2298/GENSR1902377B. DOI
Nisar N., Li L., Lu S., Khin N.C., Pogson B.J. Carotenoid metabolism in plants. Molec. Plant. 2015;8:68–82. doi: 10.1016/j.molp.2014.12.007. PubMed DOI
Diretto G., Tavazza R., Welsch R., Pizzichini D., Mourgues F., Papacchioli V., Beyer P., Giuliano G. Metabolic engineering of potato tuber carotenoids through tuber-specific silencing of lycopene epsilon cyclase. BMC Plant Biol. 2006;6:13. doi: 10.1186/1471-2229-6-13. PubMed DOI PMC
Yu B., Lydiate D., Young L., Schäfer U., Hannoufa A. Enhancing the carotenoid content of Brassica napus seeds by downregulating lycopene epsilon cyclase. Transgen. Res. 2008;17:573–585. doi: 10.1007/s11248-007-9131-x. PubMed DOI
Kim S.H., Kim Y.H., Ahn Y.O., Jeong J.C., Lee H.S., Kwak S.S. Downregulation of the lycopene ε-cyclase gene increases carotenoid synthesis via the β-branch-specific pathway and enhances salt-stress tolerance in sweet potato transgenic calli. Physiol. Plant. 2013;147:432–442. doi: 10.1111/j.1399-3054.2012.01688.x. PubMed DOI
Hajslova J., Cajka T., Vaclavik L. Challenging applications offered by direct analysis in real time (DART) in food-quality and safety analysis. TrAC Trends Analyt. Chem. 2011;30:204–218. doi: 10.1016/j.trac.2010.11.001. DOI
Cody R.B., Laramée J.A., Durst H.D. Versatile new ion source for the analysis of materials in open air under ambient conditions. Anal. Chem. 2005;77:2297–2302. doi: 10.1021/ac050162j. PubMed DOI
Guilherme R., Aires A., Rodrigues N., Peres A.M., Pereira J.A. Phenolics and antioxidant activity of green and red sweet peppers from organic and conventional agriculture: A comparative study. Agriculture. 2020;10:652. doi: 10.3390/agriculture10120652. DOI
Rotem J. The Genus Alternaria: Biology, Epidemiology and Pathogenicity. American Phytopathological Society; St. Paul, MN, USA: 1994.
Carvalho A.M.G., Junqueira A.M., Vieira J.V., Reis A., Silva J.B.C. Produtividade, florescimento premature, e queima-das-folhas em cenou-ra cultivada em Sistema organico e convencional. Hortic. Bras. 2005;23:250–254. doi: 10.1590/S0102-05362005000200017. DOI
Gugino T.L., Caroll J.E., Widmer T.L., Chen P., Abawi G.S. Field evaluation of carrot cultivars susceptibility to fungal leaf blight diseases in New York. Crop Prot. 2007;26:709–714. doi: 10.1016/j.cropro.2006.06.009. DOI