{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T05:47:30Z","timestamp":1790228850716,"version":"4.1.0"},"reference-count":41,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,7,15]],"date-time":"2019-07-15T00:00:00Z","timestamp":1563148800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2019,7,15]],"date-time":"2019-07-15T00:00:00Z","timestamp":1563148800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100003995","name":"Natural Science Foundation of Anhui Province","doi-asserted-by":"publisher","award":["1608085MC52"],"award-info":[{"award-number":["1608085MC52"]}],"id":[{"id":"10.13039\/501100003995","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31501368"],"award-info":[{"award-number":["31501368"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81803665"],"award-info":[{"award-number":["81803665"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81573518"],"award-info":[{"award-number":["81573518"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100009558","name":"University Natural Science Research Project of Anhui Province","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100009558","id-type":"DOI","asserted-by":"publisher"}]},{"name":"the Key Project of Natural Science Research for Colleges and Universities in Anhui Province"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p><jats:italic>In vitro<\/jats:italic> cultured seedlings or microtubers are the major starting materials for the production of potato. Currently, seedlings are cultured in media sterilized by autoclaving, which, however, consumes more electricity and takes longer for sterilization, and also requires high temperature-tolerant vessel materials. In order to identify alternative methods of sterilizing culture conditions, the disinfection effects of chlorine dioxide (CD) at 88.0, 29.3, 17.6, 12.6 and 8.8\u2009\u03bcM were evaluated in potato medium and vessels. The \u226512.6\u2009\u03bcM gaseous CD effectively disinfected vessel through a 30-min fumigation process, and its aqueous solution disinfected potato medium efficiently as well. In presence of 12.6\u2009\u03bcM CD in the medium, the potato seedlings had similar morphological features as those grown on autoclaved medium, with some exceptions. The use of 12.6\u201329.3\u2009\u03bcM aqueous CD to sterilize the medium increased antioxidant enzyme activities in potato seedlings, while the use of higher concentration decreased antioxidant enzyme activity levels. SSR analysis did not reveal significant molecular differences in potato seedlings cultured between autoclaved and CD-sterilized medium. In addition to this, CD-sterilized medium induced potato microtuber formation at a similar rate as autoclaved medium. In summary, using CD to sterilize potato medium and vessels did not compromise the growth of seedlings and microtuber induction. This study provides an economical and simplified sterilization method for media used to culture potato plantlets, and this can improve energy use of the large-scale tissue culture industry.<\/jats:p>","DOI":"10.1038\/s41598-019-46795-4","type":"journal-article","created":{"date-parts":[[2019,7,15]],"date-time":"2019-07-15T10:50:58Z","timestamp":1563187858000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Use of chlorine dioxide to sterilize medium for tissue culture of potato"],"prefix":"10.1038","volume":"9","author":[{"given":"Yongbo","family":"Duan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Han","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mengchu","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fenglan","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tao","family":"Xue","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianping","family":"Xue","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,7,15]]},"reference":[{"key":"46795_CR1","first-page":"13","volume":"4","author":"JD Li","year":"2017","unstructured":"Li, J. D., Li, X. D. & Wang, S. H. Analysis on financialization of potato price fluctuation under background of developing potato as staple food. J Huazhong Agri Univ 4, 13\u201321 (2017).","journal-title":"J Huazhong Agri Univ"},{"key":"46795_CR2","doi-asserted-by":"publisher","first-page":"1117","DOI":"10.1016\/j.cropro.2011.04.001","volume":"30","author":"B Wang","year":"2011","unstructured":"Wang, B. et al. Potato viruses in China. Crop Prot 30, 1117\u20131123 (2011).","journal-title":"Crop Prot"},{"key":"46795_CR3","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-017-17059-w","volume":"7","author":"YL Li","year":"2017","unstructured":"Li, Y. L. et al. Integrated miRNA and microRNA transcriptome analysis reveals miRNA regulation in response to PVA in potato. Sci Rep 7, 16925 (2017).","journal-title":"Sci Rep"},{"key":"46795_CR4","first-page":"6375","volume":"8","author":"EP Venkatasalam","year":"2013","unstructured":"Venkatasalam, E. P. et al. Development of low cost technology for in vitro mass multiplication of potato (Solanum tuberosum L.). Afr J Agr Res 8, 6375\u20136382 (2013).","journal-title":"Afr J Agr Res"},{"key":"46795_CR5","first-page":"82","volume":"2","author":"J Dobr\u00e1nszki","year":"2008","unstructured":"Dobr\u00e1nszki, J., Magyar-T\u00e1bori, K. & Hud\u00e1k, I. In vitro tuberization in hormone-free systems on solidified medium and dormancy of potato microtubers. Fruit Veg Cereal Sci Biotechnol 2, 82\u201394 (2008).","journal-title":"Fruit Veg Cereal Sci Biotechnol"},{"key":"46795_CR6","unstructured":"IAEA-TECDOC. Low cost options for tissue culture technology in developing countries. IAEA-TECDOC-1384, AEA (2004)."},{"key":"46795_CR7","first-page":"703","volume":"6","author":"J Manuel","year":"2013","unstructured":"Manuel, J. Low cost tissue culture technology for the regeneration of some economically important plants for developing countries. International Journal of Agriculture Environment & Biotechnology 6, 703\u2013711 (2013).","journal-title":"International Journal of Agriculture Environment & Biotechnology"},{"key":"46795_CR8","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1007\/BF00232040","volume":"10","author":"N Schenk","year":"1991","unstructured":"Schenk, N., Hsiao, K. & Bornman, C. H. Avoidance of precipitation and carbohydrate breakdown in autoclaved plant tissue culture media. Plant Cell Rep 10, 115\u2013119 (1991).","journal-title":"Plant Cell Rep"},{"key":"46795_CR9","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1007\/s11627-012-9470-z","volume":"49","author":"GA Venturieri","year":"2013","unstructured":"Venturieri, G. A., Venturieri, A. R. & Leopoldo, G. Sterilization of culture media for orchids using a microwave oven. In Vitro Cell Dev-Pl 49, 137\u2013144 (2013).","journal-title":"In Vitro Cell Dev-Pl"},{"key":"46795_CR10","first-page":"1038","volume":"78","author":"W Deein","year":"2013","unstructured":"Deein, W., Thepsithar, C. & Thongpukdee, A. In vitro culture medium sterilization by chemicals and essential oils without autoclaving and growth of chrysanthemum nodes. World Acad Sci Engin Technol 78, 1038\u20131041 (2013).","journal-title":"World Acad Sci Engin Technol"},{"key":"46795_CR11","first-page":"257","volume":"41","author":"ALL Silva","year":"2013","unstructured":"Silva, A. L. L., Brondani, G. E., Oliveira, L. S. & Gon\u00e7alves, N. A. Chemical sterilization of culture medium: a low cost alternative to in vitro establishment of plants. Sci For 41, 257\u2013264 (2013).","journal-title":"Sci For"},{"key":"46795_CR12","doi-asserted-by":"publisher","first-page":"885","DOI":"10.1007\/BF02447733","volume":"8","author":"T Macek","year":"1994","unstructured":"Macek, T., Kr\u00e1l, J., Van\u011bk, T., Bla\u017eek, J. & Mackov\u00e1, M. Chemical sterilization of nutrient media for plant cell cultures using diethylpyrocarbonate. Biotechnol Tech 8, 885\u2013888 (1994).","journal-title":"Biotechnol Tech"},{"key":"46795_CR13","doi-asserted-by":"publisher","first-page":"785","DOI":"10.1590\/S0100-204X2009000700020","volume":"44","author":"JC Cardoso","year":"2009","unstructured":"Cardoso, J. C. Chemical sterilization of culture medium for anthurium in vitro culture. Pesqui Agropecu Bras 44, 785\u2013788 (2009).","journal-title":"Pesqui Agropecu Bras"},{"key":"46795_CR14","doi-asserted-by":"publisher","first-page":"362","DOI":"10.1007\/s11627-011-9418-8","volume":"48","author":"JC Cardoso","year":"2012","unstructured":"Cardoso, J. C. & Silva, J. A. T. D. Micropropagation of gerbera using chlorine dioxide (ClO2) to sterilize the culture medium. In Vitro Cell Dev-Pl 48, 362\u2013368 (2012).","journal-title":"In Vitro Cell Dev-Pl"},{"key":"46795_CR15","doi-asserted-by":"crossref","unstructured":"Cardoso, J. C., Sheng Gerald, L. T. & Teixeira da Silva, J. A. Micropropagation in the Twenty-First Century. In: Loyola-Vargas, V. & Ochoa-Alejo, N. (eds) Plant Cell Culture Protocols. Methods in Molecular Biology, vol 1815. Humana Press, New York, NY, 17\u201331 (2018).","DOI":"10.1007\/978-1-4939-8594-4_2"},{"key":"46795_CR16","doi-asserted-by":"publisher","first-page":"218","DOI":"10.14295\/oh.v24i3.1222","volume":"3","author":"JC Cardoso","year":"2018","unstructured":"Cardoso, J. C. & Imthurn, A. C. P. Easy and efficient chemical sterilization of the culture medium for in vitro growth of gerbera using chlorine dioxide (ClO2). Ornam Hortic 3, 218\u2013224 (2018).","journal-title":"Ornam Hortic"},{"key":"46795_CR17","doi-asserted-by":"publisher","first-page":"375","DOI":"10.1007\/s11240-006-9121-3","volume":"86","author":"SL Teixeira","year":"2006","unstructured":"Teixeira, S. L., Ribeiro, J. M. & Teixeira, M. T. Influence of NaOCl on nutrient medium sterilization and on pineapple (Ananas comosus, cv Smooth cayenne) behavior. PCTOC 86, 375\u2013378 (2006).","journal-title":"PCTOC"},{"key":"46795_CR18","doi-asserted-by":"publisher","first-page":"1995","DOI":"10.5897\/AJB2016.15405","volume":"15","author":"AK Pais","year":"2016","unstructured":"Pais, A. K. et al. Sodium hypochlorite sterilization of culture medium in micropropagation of Gerbera hybrida cv. Essandre. Afr J Biotechnol 15, 1995\u20131998 (2016).","journal-title":"Afr J Biotechnol"},{"key":"46795_CR19","first-page":"33","volume":"10","author":"T Yanagawa","year":"1995","unstructured":"Yanagawa, T., Nagai, M., Ogino, T. & Maeguchi, R. Application of disinfectants to orchid seeds, plantlets and media as a means to prevent in vitro contamination. Lindleyana 10, 33\u201336 (1995).","journal-title":"Lindleyana"},{"key":"46795_CR20","doi-asserted-by":"publisher","first-page":"628","DOI":"10.1111\/j.1472-765X.2011.03156.x","volume":"53","author":"H Morino","year":"2011","unstructured":"Morino, H., Fukuda, T., Miura, T. & Shibata, T. Effect of low-concentration chlorine dioxide gas against bacteria and viruses on a glass surface in wet environments. Lett Appl Microbiol 53, 628\u2013634 (2011).","journal-title":"Lett Appl Microbiol"},{"key":"46795_CR21","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1016\/j.hpj.2016.08.006","volume":"2","author":"X Song","year":"2016","unstructured":"Song, X. et al. SSR Analysis of genetic diversity among 192 diploid potato cultivars. Hort Plant J 2, 163\u2013171 (2016).","journal-title":"Hort Plant J"},{"key":"46795_CR22","doi-asserted-by":"publisher","first-page":"1921","DOI":"10.1007\/s11270-014-1921-1","volume":"225","author":"FX Simon","year":"2014","unstructured":"Simon, F. X., Berdalet, E., Gracia, F. A., Espa\u00f1a, F. & Llorens, J. Seawater disinfection by chlorine dioxide and sodium hypochlorite-A comparison of biofilm formation. Water Air Soil Poll 225, 1921 (2014).","journal-title":"Water Air Soil Poll"},{"key":"46795_CR23","doi-asserted-by":"publisher","first-page":"186","DOI":"10.1016\/j.lwt.2014.09.031","volume":"60","author":"SH Park","year":"2015","unstructured":"Park, S. H. & Kang, D. H. Antimicrobial effect of chlorine dioxide gas against foodborne pathogens under differing conditions of relative humidity. LWT-Food Sci Technol 60, 186\u2013191 (2015).","journal-title":"LWT-Food Sci Technol"},{"key":"46795_CR24","doi-asserted-by":"publisher","first-page":"796","DOI":"10.1080\/10962247.2012.735212","volume":"63","author":"CS Hsu","year":"2013","unstructured":"Hsu, C. S. & Huang, D. J. Disinfection efficiency of chlorine dioxide gas in student cafeterias in Taiwan. J Air. Waste Manage 63, 796\u2013805 (2013).","journal-title":"Waste Manage"},{"key":"46795_CR25","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s10661-014-4167-x","volume":"187","author":"CS Hsu","year":"2015","unstructured":"Hsu, C. S., Lu, M. C. & Huang, D. J. Disinfection of indoor air microorganisms in stack room of university library using gaseous chlorine dioxide. Environ Monit Assess 187, 1\u201311 (2015).","journal-title":"Environ Monit Assess"},{"key":"46795_CR26","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1007\/s11627-015-9736-3","volume":"52","author":"YB Duan","year":"2016","unstructured":"Duan, Y. B. et al. Evaluation of aqueous chlorine dioxide for disinfecting plant explants. In Vitro Cell Dev-Pl 52, 38\u201344 (2016).","journal-title":"In Vitro Cell Dev-Pl"},{"key":"46795_CR27","first-page":"100","volume":"47","author":"ZB Mo","year":"2017","unstructured":"Mo, Z. B., Hu, S. T. & Hu, D. D. Experimental research on the manufacture of chlorine dioxide by sodium chlorite and hydrochloric acid at low concentration. J Shandong Univ 47, 100\u2013105 (2017).","journal-title":"J Shandong Univ"},{"key":"46795_CR28","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1177\/153567601201700107","volume":"17","author":"D Gordon","year":"2012","unstructured":"Gordon, D., Carruthers, B. A. & Theriault, S. Gaseous decontamination methods in high-containment laboratories. Applied Biosafety 17, 31\u201339 (2012).","journal-title":"Applied Biosafety"},{"key":"46795_CR29","doi-asserted-by":"publisher","first-page":"401","DOI":"10.3109\/10903127.2013.792889","volume":"17","author":"JJ Lowe","year":"2013","unstructured":"Lowe, J. J., Hewlett, A. L., Iwen, P. C., Smith, P. W. & Gibbs, S. G. Evaluation of ambulance decontamination using gaseous chlorine dioxide. Prehosp Emerg Care 17, 401\u2013408 (2013).","journal-title":"Prehosp Emerg Care"},{"key":"46795_CR30","first-page":"33","volume":"37","author":"HQ Jia","year":"2013","unstructured":"Jia, H. Q. et al. Evaluation of gaseous chlorine dioxide fumigation for enclosed space decontamination. Milit Med Sci 37, 33\u201338 (2013).","journal-title":"Milit Med Sci"},{"key":"46795_CR31","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1007\/s12355-011-0072-6","volume":"13","author":"RA Sawant","year":"2011","unstructured":"Sawant, R. A. & Tawar, P. N. Use of sodium hypochlorite as media sterilant in sugarcane micropropagation at commercial scale. Sugar Tech 13, 27\u201335 (2011).","journal-title":"Sugar Tech"},{"key":"46795_CR32","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1016\/j.scienta.2017.05.022","volume":"222","author":"A Chumyam","year":"2017","unstructured":"Chumyam, A., Shank, L., Faiyue, B., Uthaibutra, J. & Saengnil, K. Effects of chlorine dioxide fumigation on redox balancing potential of antioxidative ascorbate-glutathione cycle in \u2018Daw\u2019 longan fruit during storage. Sci Hortic 222, 76\u201383 (2017).","journal-title":"Sci Hortic"},{"key":"46795_CR33","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1007\/s13197-011-0464-3","volume":"49","author":"R Choudhary","year":"2012","unstructured":"Choudhary, R., Saroha, A. E. & Swarnkar, P. L. Effect of abscisic acid and hydrogen peroxide on antioxidant enzymes in Syzygium cumini plant. J Food Sci Tech 49, 649\u2013652 (2012).","journal-title":"J Food Sci Tech"},{"key":"46795_CR34","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1111\/jfq.12082","volume":"37","author":"P Tsouvaltzis","year":"2014","unstructured":"Tsouvaltzis, P. & Brecht, J. K. Changes in quality and antioxidant enzyme activities of bunched and topped radish (Raphanus sativus L.) plants during storage at 5 or 10 C. J Food Quality 37, 157\u2013167 (2014).","journal-title":"J Food Quality"},{"key":"46795_CR35","doi-asserted-by":"publisher","first-page":"282","DOI":"10.2135\/cropsci2016.07.0636","volume":"57","author":"F Saeidnia","year":"2017","unstructured":"Saeidnia, F., Majidi, M. M., Mirlohi, A. & Soltan, S. Physiological and tolerance indices useful for drought tolerance selection in smooth bromegrass. Crop Sci 57, 282\u2013289 (2017).","journal-title":"Crop Sci"},{"key":"46795_CR36","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1016\/j.ab.2005.09.041","volume":"347","author":"MW Davey","year":"2005","unstructured":"Davey, M. W., Stals, E., Panis, B., Keulemans, J. & Swennen, R. L. High-throughput determination of malondialdehyde in plant tissues. Anal Biochem 347, 201\u2013207 (2005).","journal-title":"Anal Biochem"},{"key":"46795_CR37","doi-asserted-by":"publisher","first-page":"786","DOI":"10.1016\/j.plaphy.2008.04.018","volume":"46","author":"Y Yamauchi","year":"2008","unstructured":"Yamauchi, Y., Furutera, A., Toyoda, Y., Tanaka, K. & Sugimoto, Y. Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. Plant Physiol Bioch 46, 786\u2013793 (2008).","journal-title":"Plant Physiol Bioch"},{"key":"46795_CR38","doi-asserted-by":"publisher","first-page":"1989","DOI":"10.1080\/01904167.2015.1105263","volume":"39","author":"M Moustafa-Farag","year":"2015","unstructured":"Moustafa-Farag, M. et al. Boron in I: activated antioxidant enzymes-reduced malondialdehyde concentration, and improved mineral uptake-promoted watermelon seedlings growth under boron deficiency. J Plant Nutr 39, 1989\u20132001 (2015).","journal-title":"J Plant Nutr"},{"key":"46795_CR39","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1111\/j.1399-3054.1962.tb08052.x","volume":"15","author":"T Murashige","year":"1962","unstructured":"Murashige, T. & Skoog, F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Phys Plant 15, 473\u2013497 (1962).","journal-title":"Phys Plant"},{"key":"46795_CR40","unstructured":"Zhang, Z. L., Qu, W. J. & Li, X. F. Plant physiology experimental guidance [M]. Fourth edition. Beijing: Higher Education Press, 2009."},{"key":"46795_CR41","doi-asserted-by":"publisher","first-page":"9848","DOI":"10.1021\/jf051201v","volume":"53","author":"DS Smith","year":"2005","unstructured":"Smith, D. S., Maxwell, P. W. & De Boer, S. H. Comparison of several methods for the extraction of DNA from potatoes and potato-derived products. J Agric Food Chem 53, 9848\u20139859 (2005).","journal-title":"J Agric Food Chem"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-46795-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-46795-4","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-46795-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,17]],"date-time":"2022-12-17T11:37:43Z","timestamp":1671277063000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-46795-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,7,15]]},"references-count":41,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,12]]}},"alternative-id":["46795"],"URL":"https:\/\/doi.org\/10.1038\/s41598-019-46795-4","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,7,15]]},"assertion":[{"value":"26 March 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 July 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 July 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"10232"}}