High throughput pre-breeding evaluation of Greek oregano (Origanum vulgare L. subsp. hirtum) reveals multi-purpose genotypes for different industrial uses

Eirini Sarrou1, Eftichia Martinidou1,2, Luisa Palmieri2, Ioanna Poulopoulou3, Foteini Trikka1, Domenico Masuero2, Gauly Matthias3, Ioannis Ganopoulos1, Paschalina Chatzopoulou1, Stefan Martens2
1Institute of Plant Breeding and Genetic Resources, Hellenic Agricultural Organization DEMETER, Thermi 57001, Thessaloniki, Greece
2Fondazione Edmund Mach, Centro Ricerca e Innovazione, Department of Food Quality and Nutrition, Via E. Mach, 1, 38098 San Michele all’Adige, TN, Italy
3Free University of Bozen – Bolzano, Faculty of Science and Technology, Piazza Università 5, Bolzano, 39100, Italy

Tài liệu tham khảo

Abdelqader, 2012, Anthelmintic effects of citrus peels ethanolic extracts against Ascaridia galli, Veterinary Parasitology, 188, 78, 10.1016/j.vetpar.2012.03.003 Abugri, 2017, In vitro activity of the interaction between taxifolin (dihydroquercetin) and pyrimethamine against Toxoplasma gondii, Chemical Biology & Drug Design, 91, 194, 10.1111/cbdd.13070 Ackert, 1928, Effects of the nematode Ascaridia lineate (Schneider) on growing chickens, Journal of Parasitology, 15, 1, 10.2307/3271596 Adams, 2001, Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy, Allured publishing corporation Alekseeva, 2021, Genetic and flower volatile diversity in natural populations of Origanum vulgare subsp. hirtum (Link) Ietsw. in Bulgaria: toward the development of a core collection, Frontiers in Plant Science, 12 Al-Snafi, 2016, The pharmacological activities of Cuminum cyminum-A review, IOSR Journal of Pharmacy, 6, 46 Amar, 2013, Comparative genetic study among Origanum L. plants grown in Egypt, Journal of Biodiversity & Environmental Science, 3, 208 Andi, 2021, Essential oil chemical diversity of twenty Iranian Origanum vulgare L. subsp. viride populations, Biochemical Systematics & Ecology, 98, 10.1016/j.bse.2021.104323 Azizi, 2009, Intraspecific diversity and relationship between subspecies of Origanum vulgare revealed by comparative AFLP and SAMPL marker analysis, Plant Systematics and Evolution, 281, 151, 10.1007/s00606-009-0197-1 Azizi, 2012, Correlations between genetic, morphological, and chemical diversities in a germplasm collection of the medicinal plant Origanum vulgare L, Chemistry & Biodiversity, 9, 2784, 10.1002/cbdv.201200125 Baghalian, 2010, Genetic diversity of Iranian madder (Rubia tinctorum) populations based on agro-morphological traits, phytochemical content and RAPD markers, Industrial Crops & Products, 31, 557, 10.1016/j.indcrop.2010.02.012 Baranauskaitė, 2016, Optimization of carvacrol, rosmarinic, oleanolic and ursolic acid extraction from oregano herbs (Origanum onites L., Origanum vulgare spp. hirtum and Origanum vulgare L.), Natural Products Research, 30, 672, 10.1080/14786419.2015.1038998 Bedini, 2021, Bioactivity of different chemotypes of oregano essential oil against the blowfly Calliphora vomitoria vector of foodborne pathogens, Insects, 12, 52, 10.3390/insects12010052 Bedoya-Serna, 2018, Antifungal activity of nanoemulsions encapsulating oregano (Origanum vulgare) essential oil: in vitro study and application in Minas Padrão cheese, Brazilian Journal of Microbiology, 49, 929, 10.1016/j.bjm.2018.05.004 Bonfanti, 2012, Emerging cultivation of oregano in Sicily: Sensory evaluation of plants and chemical composition of essential oils, Industrial Crops & Products, 35, 160, 10.1016/j.indcrop.2011.06.029 Carlström, 1984, New species of Alyssum, Consolida, Origanum and Umbilicus from the SE Aegean sea, Willdenowia, 15 Coles, 2006, The detection of anthelmintic resistance in nematodes of veterinary importance, Veterinary Parasitology, 136, 167, 10.1016/j.vetpar.2005.11.019 Collins, 2019, Resistance to fenbendazole in Ascaridia dissimilis, an important nematode parasite of turkeys, Poultry Science, 98, 5412, 10.3382/ps/pez379 Cui, 2019, Antibacterial mechanism of oregano essential oil, Industrial Crops & Products, 139, 10.1016/j.indcrop.2019.111498 De Martino, 2009, Chemical composition and antimicrobial activity of the essential oils from three chemotypes of Origanum vulgare L. ssp. hirtum (Link) Ietswaart growing wild in Campania (Southern Italy), Molecules, 14, 2735, 10.3390/molecules14082735 De Mastro, 2017, Essential oil diversity of Origanum vulgare L. populations from Southern Italy, Food Chemistry, 235, 1, 10.1016/j.foodchem.2017.05.019 Dell'Acqua, 2014, Genome scan of Kenyan Themeda triandra populations by AFLP markers reveals a complex genetic structure and hints for ongoing environmental selection, South African Journal of Botany, 92, 28, 10.1016/j.sajb.2014.01.013 Domke, 2012, Prevalence of anthelmintic resistance in gastrointestinal nematodes of sheep and goats in Norway, Parasitology Research, 111, 185, 10.1007/s00436-012-2817-x Durán-Soria, 2021, Exploring genotype-by-environment interactions of chemical composition of raspberry by using a metabolomics approach, Metabolites, 11, 490, 10.3390/metabo11080490 Earl, 2012, STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method, Conservation genetics resources, 4, 359, 10.1007/s12686-011-9548-7 EC, 2009, Council Regulation (EC) No 1099/2009 of 24 September 2009 on the protection of animals at the time of killing relevance, Official Journal of the European Communities, 1 ECPGR, 2023. European Cooperative for Plant Genetic Resources Descriptor. Draft Descriptor List Origanum vulgare L. Accessed in November 2011. 2019, Guidance on the assessment of the safety of feed additives for the environment, EFSA Journal, 17, 5648 Evanno, 2005, Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study, Molecular Ecology, 14, 2611, 10.1111/j.1365-294X.2005.02553.x Farneti, 2015, Is there room for improving the nutraceutical composition of apple, Journal of Agriculture & Food Chemistry, 63, 2750, 10.1021/acs.jafc.5b00291 Fleisher, 1982, Oregano spices and Origanum chemotypes, Journal of the Science of Food and Agriculture, 33, 441, 10.1002/jsfa.2740330508 Gauly, 2001, Effect and repeatability of Ascaridia galli egg output in cockerels following a single low dose infection, Veterinary Parasitology, 96, 301, 10.1016/S0304-4017(00)00445-3 Gavaric, 2015, Chemical profile, antioxidant and antibacterial activity of thyme and oregano essential oils, thymol and carvacrol and their possible synergism, Journal of Essential Oil & Bearing Plants, 18, 1013, 10.1080/0972060X.2014.971069 Goliaris, 2003, Production of new Greek oregano clones and analysis of their essential oils, Journal of Herbs, Spices & Medicinal Plants, 10, 29, 10.1300/J044v10n01_04 Gordillo Jaramillo, 2021, Role of oregano and Citrus species-based essential oil preparation for the control of coccidiosis in broiler chickens, Journal of Animal Science and Biotechnology, 12, 1, 10.1186/s40104-021-00569-z Gutiérrez-Grijalva, 2017, Flavonoids and phenolic acids from oregano: occurrence, biological activity and health benefits, Plants, 7, 2, 10.3390/plants7010002 Hammer, 2001, Past: paleontological statistics software package for education and data analysis, Palaeontologia Electronica, 4, 1 Harakotr, 2021, Genotype by environment interaction effects on nutraceutical lipid compounds of pigmented Rice (Oryza sativa L. ssp. indica), International Journal of Agronomy, 1, 10.1155/2021/8880487 Heslot, 2015, Perspectives for genomic selection applications and research in plants, Crop Science, 55, 1, 10.2135/cropsci2014.03.0249 Ietswaart, 1980, A taxonomic revision of the genus Origanum (Labiatae), Leiden Botanical Series, 4, 1 Ince, 2014, New microsatellite and CAPS-microsatellite markers for clarifying taxonomic and phylogenetic relationships within Origanum L., Molecular breeding, 34, 643, 10.1007/s11032-014-0064-9 ISO 13171:2016, 2016. International Organization for Standardization (ISO), Geneva, Switzerland. Jin, 2021, Oregano (Origanum vulgare L.) essential oil feed supplement protected broilers chickens against Clostridium perfringens induced necrotic enteritis, Agriculture, 12, 18, 10.3390/agriculture12010018 Kaplan, 2014, Antiparasitic efficacy of a novel plant-based functional food using an Ascaris suum model in pigs, Acta Tropica, 139, 15, 10.1016/j.actatropica.2014.06.008 Kapustová, 2021, Nanoencapsulated essential oils with enhanced antifungal activity for potential application on agri-food, material and environmental fields, Antibiotics, 10, 31, 10.3390/antibiotics10010031 Kashyap, 2016, Ursolic acid and oleanolic acid: pentacyclic terpenoids with promising anti-inflammatory activities, Recent Patents on Inflammation & Allergy Drug discovery, 10, 21, 10.2174/1872213X10666160711143904 Katsiotis, 2009, Phylogenetic relationships in Origanum spp. based on rDNA sequences and intra-genetic variation of Greek O. vulgare subsp. hirtum revealed by RAPD, Scientia Horticulturae, 121, 103, 10.1016/j.scienta.2009.01.015 Kaufmann, 2011, Helminth infections in laying hens kept in organic free range systems in Germany, Livestock Science, 141, 182, 10.1016/j.livsci.2011.05.015 Kholif, 2021, Essential oils and phytogenic feed additives in ruminant diet: Chemistry, ruminal microbiota and fermentation, feed utilization and productive performance, Phytochemistry Reviews, 20, 1087, 10.1007/s11101-021-09739-3 2002 Kokkini, 1996, Taxonomy, diversity and distribution of Origanum species, 12 Kokkini, 1994, Pattern of geographic variations of Origanum vulgare trichomes and essential oil content in Greece, Biochemical Systematics and Ecology, 22, 517, 10.1016/0305-1978(94)90046-9 Koldaş, 2015, Phytochemical screening, anticancer and antioxidant activities of Origanum vulgare L. ssp. viride (Boiss.) Hayek, a plant of traditional usage, Journal of the Science of Food & Agriculture, 95, 786, 10.1002/jsfa.6903 Krause, 2021, The biosynthesis of thymol, carvacrol, and thymohydroquinone in Lamiaceae proceeds via cytochrome P450s and a short-chain dehydrogenase, Proceedings of the National Academy of Sciences, 118, 10.1073/pnas.2110092118 Lambertz, 2019, Anthelmintic efficacy against gastrointestinal nematodes in goats raised under mountain farming conditions in northern Italy, BMC Veterinary Research, 15, 1, 10.1186/s12917-019-1968-8 Li, 2001, Sequence-related amplified polymorphism (SRAP), a new marker system based on a simple PCR reaction: its application to mapping and gene tagging in Brassica, Theoretical and applied genetics, 103, 455, 10.1007/s001220100570 Licata, 2015, Study of quantitative and qualitative variations in essential oils of Sicilian oregano biotypes, Journal of Essential Oil Research, 27, 293, 10.1080/10412905.2015.1045088 Lukas, 2013, Phytochemical diversity of Origanum vulgare L. subsp. vulgare (Lamiaceae) from Austria, Biochemical Systematics & Ecology, 50, 106, 10.1016/j.bse.2013.03.037 Marrelli, 2018, Origanum spp.: an update of their chemical and biological profiles, Phytochemistry Reviews, 17, 873, 10.1007/s11101-018-9566-0 Metsalu, 2015, ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap, Nucleic acids research, 43(W1), W566, 10.1093/nar/gkv468 Morshedloo, 2017, Chemical composition and antioxidant activity of essential oils in Origanum vulgare subsp. gracile at different phenological stages and plant parts, Journal of Food Processing & Preservation, 42 Napoli, 2009, Screening the essential oil composition of wild Sicilian oregano, Biochemical Systematics & Ecology, 37, 484, 10.1016/j.bse.2009.07.008 Noshita, 2022, Model-based plant phenomics on morphological traits using morphometric descriptors, Breeding Science, 72, 19, 10.1270/jsbbs.21078 Novak, 2008, Identification and characterization of simple sequence repeat markers from a glandular Origanum vulgare expressed sequence tag, Molecular Ecology Resources, 8, 599, 10.1111/j.1471-8286.2007.02059.x Oka, 2000, Nematicidal activity of essential oils and their components against the root-knot nematode, Phytopathology, 90, 710, 10.1094/PHYTO.2000.90.7.710 Palmieri, 2017, Genotype‐by‐environment effect on bioactive compounds in strawberry (Fragaria x ananassa Duch.), Journal of the Science of Food and Agriculture, 97, 4180, 10.1002/jsfa.8290 Papaioannou, 2020, Genetic profiling and volatile oil content of oregano genotypes from Greece, Revista Brasileira Délelőtt Farmacognosia, 30, 295, 10.1007/s43450-020-00016-6 Partridge, 2017, Dihydrobenz[e][1,4]oxazepin-2(3H)-ones, a new anthelmintic chemotype immobilising whipworm and reducing infectivity in vivo, PLoS Neglected Tropical Diseases, 11, 10.1371/journal.pntd.0005359 Plata-Rueda, 2021, Origanum vulgare essential oil against Tenebrio molitor (Coleoptera: Tenebrionidae): composition, insecticidal activity, and behavioral response, Plants, 10, 2513, 10.3390/plants10112513 Poulopoulou, 2022, In vitro evaluation of the effects of methanolic plant extracts on the embryonation rate of Ascaridia galli eggs, Veterinary Research Communications Pritchard, 2000, Inference of population structure using multilocus genotype data, Genetics, 155, 945, 10.1093/genetics/155.2.945 Rahimian, 2016, Embryonation ability of Ascaridia galli eggs isolated from worm uteri or host faeces, Veterinary Parasitology, 215, 29, 10.1016/j.vetpar.2015.10.026 Rajković, 2019, Ascaridia galli infection in laying hens and the results of in vitro efficacy of levamisole, piperazine and carvacrol, whether is necessary to change the deworming protocols?, Acta Veterinaria-Beograd, 6, 414, 10.2478/acve-2019-0035 Russo, 1998, Essential oil chemical composition of wild populations of Italian oregano spice (Origanum vulgare ssp. hirtum (Link) Ietswaart): a preliminary evaluation of their use in chemotaxonomy by cluster analysis. 1. Inflorescences, Journal of Agriculture & Food Chemistry, 46, 3741, 10.1021/jf980087w Sarrou, 2017, Conventional breeding of Greek oregano (Origanum vulgare ssp. hirtum) and development of improved cultivars for yield potential and essential oil quality, Euphytica, 213, 1, 10.1007/s10681-017-1889-1 Scutari, 2014 Sharma, 2019, The impacts of Ascaridia galli on performance, health, and immune responses of laying hens: new insights into an old problem, Poultry Science, 98, 6517, 10.3382/ps/pez422 Sharma, 2017, Ascaridia galli challenge model in laying hens, Journal of Advances in Parasitology, 4, 41 Shen, 2010, LC-MS method for the simultaneous quantitation of the anti-inflammatory constituents in oregano (Origanum species), Journal of Agriculture & Food Chemistry, 58, 7119, 10.1021/jf100636h Sultana, 2008, Oleanolic acid and related derivatives as medicinally important compounds, Journal of Enzyme Inhibition & Medical Chemistry, 23, 739, 10.1080/14756360701633187 Symeonidou, 2018, Botanicals: a natural approach to control ascaridiosis in poultry, Journal of the Hellenic Veterinary Medical Society, 69, 711, 10.12681/jhvms.16383 Tabari, 2015, Carvacrol as a potent natural acaricide against Dermanyssus gallinae, Parasitology Research, 114, 3801, 10.1007/s00436-015-4610-0 Taşcıoğlu, 2018, Molecular genetic diversity in the Origanum genus: EST-SSR and SRAP marker analyses of the 22 species in eight sections that naturally occur in Turkey, Industrial Crops & Products, 123, 746, 10.1016/j.indcrop.2018.07.027 Ter Braak, 1986, Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis, Ecology, 67, 1167, 10.2307/1938672 Tiersch, 2013, The role of culture media on embryonation and subsequent infectivity of Capillaria obsignata eggs, Parasitology Research, 357, 10.1007/s00436-012-3143-z Traboulsi, 2002, Insecticidal properties of essential plant oils against the mosquito Culex pipiens molestus (Diptera: Culicidae), Pest management science, 58, 491, 10.1002/ps.486 Tsivelika, 2018, Phenotypic variation of wild Chamomile (Matricaria chamomilla L.) populations and their evaluation for medicinally important essential oil, Biochemical Systematics & Ecology, 80, 21, 10.1016/j.bse.2018.06.001 Vallverdú-Queralt, 2014, A comprehensive study on the phenolic profile of widely used culinary herbs and spices: Rosemary, thyme, oregano, cinnamon, cumin and bay, Food Chemistry, 154, 299, 10.1016/j.foodchem.2013.12.106 Verma, 2010, Chemical diversity in Indian oregano (Origanum vulgare L.), Chemistry & Biodivesity, 7, 2054, 10.1002/cbdv.200900419 Vokou, 1993, Geographic variation of Greek oregano (Origanum vulgare ssp. hirtum) essential oils, Biochemical Systematics and Ecology, 21, 287, 10.1016/0305-1978(93)90047-U Vrhovsek, 2012, A versatile targeted metabolomics method for the rapid quantification of multiple classes of phenolics in fruits and beverages, Journal of Agriculture & Food Chemistry, 60, 8831, 10.1021/jf2051569 Williams, 2014, Assessment of the anthelmintic activity of medicinal plant extracts and purified condensed tannins against free-living and parasitic stages of Oesophagostomum dentatum, Parasites Vectors, 7, 518, 10.1186/s13071-014-0518-2 Woźniak, 2015, Ursolic acid—a pentacyclic triterpenoid with a wide spectrum of pharmacological activities, Molecules, 20, 20614, 10.3390/molecules201119721 Wu, 2021, ZnO nanoparticles stabilized oregano essential oil Pickering emulsion for functional cellulose nanofibrils packaging films with antimicrobial and antioxidant activity, International Journal of Biological Macromolecules, 190, 433, 10.1016/j.ijbiomac.2021.08.210 Yan, 2016, Antioxidant capacity variation in the oregano (Origanum vulgare L.) collection of the German National Genebank, Industrial Crops & Products, 92, 19, 10.1016/j.indcrop.2016.07.038 Zajičkova, 2020, Anthelmintics in the future: current trends in the discovery and development of new drugs against gastrointestinal nematodes, Drug Discovery Today, 25, 430, 10.1016/j.drudis.2019.12.007 Zaman, 2020, Role of secondary metabolites of medicinal plants against Ascaridia galli, World’s Poultry Science Journal, 76, 639, 10.1080/00439339.2020.1782801 Zanzani, 2014, Gastrointestinal nematodes of dairy goats, anthelmintic resistance and practices of parasite control in Northern Italy, BMC Veterinary Research, 10 Zhang, 2021, Effects of oregano essential oil as an antibiotic growth promoter alternative on growth performance, antioxidant status, and intestinal health of broilers, Poultry Science, 100, 10.1016/j.psj.2021.101163 Zhao, 2021, Effects of the substitution of oregano essential oil for antibiotics in the plateau-broiler diet, Italian Journal of Animal Science, 20, 1328, 10.1080/1828051X.2021.1967208