{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,5,14]],"date-time":"2025-05-14T04:20:43Z","timestamp":1747196443844,"version":"3.40.5"},"reference-count":51,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2023,8,10]],"date-time":"2023-08-10T00:00:00Z","timestamp":1691625600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Prior to the world-wide dominance of<jats:italic>F<\/jats:italic>.<jats:italic>\u00d7ananassa<\/jats:italic>in strawberry production, native species had been cultivated in European gardens for centuries. Especially the musk strawberry (<jats:italic>F<\/jats:italic>.<jats:italic>moschata<\/jats:italic>) had been highly appreciated due to its fruit size and extraordinary aroma. Detailed studies on the diversity of the species\u2019 fruit aroma are lacking, although breeding aims to improve strawberry aroma by complex crossings during recent years. Today a few cultivars, abandoned synanthropic occurrences and native populations of this species exist in Germany. Here we characterised aroma profiles of<jats:italic>F<\/jats:italic>.<jats:italic>moschata<\/jats:italic>accessions by analysing Volatile Organic Compounds. In particular, differences between native and cultivated accessions as well as the diversity in aroma profiles of native populations were investigated. Profiles of Volatile Organic Compounds were analysed by immersion stir bar sorptive extraction-gas chromatography-quadrupol mass spectrometry (imm-SBSE-GC-qMS). These data were compared with a genetic characterisation of samples based on eight microsatellite loci using univariate and multivariate statistical analyses. High amounts of furanones and the key compound methyl anthranilate were characteristic for the aroma profile of<jats:italic>F<\/jats:italic>.<jats:italic>moschata<\/jats:italic>. We detected a considerable diversity of Volatile Organic Compounds among accessions of<jats:italic>F<\/jats:italic>.<jats:italic>moschata<\/jats:italic>, particularly among genetically distinct samples from the same population. Native accessions contained more terpenoids but less esters and were moderately differentiated from cultivated samples. The observed patterns of Volatile Organic Compounds indicate that cultivated accessions had been selected for favourable aroma profiles and thus showing traces of domestication. Moreover, native populations harbour a great diversity of Volatile Organic Compounds, which could be also considered for future breeding efforts.<\/jats:p>","DOI":"10.1371\/journal.pone.0289468","type":"journal-article","created":{"date-parts":[[2023,8,10]],"date-time":"2023-08-10T17:30:44Z","timestamp":1691688644000},"page":"e0289468","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Variation in Volatile Organic Compounds in native, synanthropic accessions and cultivars of the musk strawberry (Fragaria moschata Duchesne ex Weston)"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7246-1004","authenticated-orcid":true,"given":"Christiane M.","family":"Ritz","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Detlef","family":"Ulrich","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sebastian","family":"Buschmann","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Klaus","family":"Olbricht","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2023,8,10]]},"reference":[{"key":"pone.0289468.ref001","first-page":"1","volume-title":"The genomes of rosaceous berries and their wild relatives","author":"D. 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Vienna, Austria: R Foundation for Statistical Computing; 2015."},{"issue":"1","key":"pone.0289468.ref035","first-page":"9","article-title":"PAST: Paleontological statistics software package for education and data analysis","volume":"4","author":"\u00d8 Hammer","year":"2001","journal-title":"Palaeontologia Electronica"},{"issue":"3","key":"pone.0289468.ref036","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1111\/j.1755-0998.2011.02985.x","article-title":"POLYSAT: an R package for polyploid microsatellite analysis","volume":"11","author":"LV Clark","year":"2011","journal-title":"Molecular Ecology Resources"},{"issue":"7","key":"pone.0289468.ref037","doi-asserted-by":"crossref","first-page":"2101","DOI":"10.1111\/j.1365-294X.2004.02209.x","article-title":"A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level","volume":"13","author":"R Bruvo","year":"2004","journal-title":"Molecular Ecology"},{"key":"pone.0289468.ref038","first-page":"5","article-title":"The ade4 package I: One-table methods","volume":"4","author":"D Chessel","year":"2004","journal-title":"R News"},{"issue":"2","key":"pone.0289468.ref039","first-page":"47","volume":"7","author":"S Dray","year":"2007","journal-title":"The ade4 package II: Two-table and K-table methods R News"},{"key":"pone.0289468.ref040","doi-asserted-by":"crossref","DOI":"10.1007\/978-1-4939-8850-1","volume-title":"Multivariate analysis of ecological data with ade4","author":"J Thioulouse","year":"2018"},{"issue":"19","key":"pone.0289468.ref041","doi-asserted-by":"crossref","first-page":"9123","DOI":"10.1021\/jf901693j","article-title":"Aroma Development during Ripening of Fragaria chiloensis Fruit and Participation of an Alcohol Acyltransferase (FcAAT1) Gene","volume":"57","author":"M Gonzalez","year":"2009","journal-title":"Journal of Agricultural and Food Chemistry"},{"volume-title":"Das Buch der Erdbeeren: Eine practische Anleitung von Cultur derselben im freien Lande wie auch zum Treiben in K\u00fcsten und H\u00e4usern nebst Mittheilungen \u00fcber Botanik, Geschichte, Classification der Erdbeeren und Beschreibung aller in G\u00e4rten bekannten Arten und Variet\u00e4ten","year":"1874","author":"G. Goeschke","key":"pone.0289468.ref042"},{"volume-title":"Untersuchungen zum Z\u00fcchtungswert der Fragaria moschata Weston","year":"2017","author":"N. B\u00f6lke","key":"pone.0289468.ref043"},{"key":"pone.0289468.ref044","doi-asserted-by":"crossref","first-page":"3110","DOI":"10.1105\/tpc.104.023895","article-title":"Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species","volume":"16","author":"A Aharoni","year":"2004","journal-title":"The Plant Cell"},{"key":"pone.0289468.ref045","first-page":"223","article-title":"A search for the ideal flavor of strawberry\u2014Comparison of consumer acceptance and metabolite patterns in Fragaria \u00d7ananassa Duch","volume":"89","author":"D Ulrich","year":"2016","journal-title":"Journal of Applied Botany and Food Quality"},{"key":"pone.0289468.ref046","doi-asserted-by":"crossref","DOI":"10.1016\/j.phytochem.2020.112590","article-title":"Early transcriptional response of terpenoid metabolism to Colletotrichum gloeosporioides in a resistant wild strawberry Fragaria nilgerrensis","volume":"181","author":"N Mehmood","year":"2021","journal-title":"Phytochemistry"},{"key":"pone.0289468.ref047","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2021.615749","article-title":"Genetic analysis of methyl anthranilate, mesifurane, linalool, and other flavor compounds in cultivated strawberry (Fragaria \u00d7ananassa)","volume":"12","author":"CR Barbey","year":"2021","journal-title":"Frontiers in Plant Science"},{"key":"pone.0289468.ref048","first-page":"215","article-title":"Fruit diversity in a natural European habitat of Fragaria moschata Weston","volume":"1156","author":"SS Lesemann","year":"2015","journal-title":"Acta Horticulturae"},{"key":"pone.0289468.ref049","doi-asserted-by":"crossref","first-page":"61","DOI":"10.17660\/ActaHortic.2017.1156.8","article-title":"Domestication effects in European breeding history of strawberry demonstrated by aroma compound pattern","volume":"1156","author":"K Olbricht","year":"2017","journal-title":"Acta Horticulturae"},{"key":"pone.0289468.ref050","doi-asserted-by":"crossref","first-page":"139","DOI":"10.17660\/ActaHortic.2021.1309.20","article-title":"Breeding potential of underutilized Fragaria species","volume":"1309","author":"K Olbricht","year":"2021","journal-title":"Acta Horticulturae"},{"key":"pone.0289468.ref051","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1007\/s10681-005-3496-9","article-title":"Interspecific hybridization of Fragaria moschata with two diploid species, F. nubicola and F. viridis","volume":"143","author":"RH Bors","year":"2005","journal-title":"Euphytica"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0289468","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,12,18]],"date-time":"2023-12-18T21:31:42Z","timestamp":1702935102000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0289468"}},"subtitle":[],"editor":[{"given":"Branislav T.","family":"\u0160iler","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2023,8,10]]},"references-count":51,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,8,10]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0289468","relation":{},"ISSN":["1932-6203"],"issn-type":[{"type":"electronic","value":"1932-6203"}],"subject":[],"published":{"date-parts":[[2023,8,10]]}}}