{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,30]],"date-time":"2026-05-30T01:29:35Z","timestamp":1780104575937,"version":"3.54.0"},"reference-count":34,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2019,3,29]],"date-time":"2019-03-29T00:00:00Z","timestamp":1553817600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81673527"],"award-info":[{"award-number":["81673527"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Ministry of science and technology of People's Republic of China","award":["2017YFC1702702"],"award-info":[{"award-number":["2017YFC1702702"]}]},{"name":"Ministry of science and technology of People's Republic of China","award":["2017YFC1700705"],"award-info":[{"award-number":["2017YFC1700705"]}]},{"name":"Department of Science and Technology of Shandong Provincial","award":["2017GSF19115"],"award-info":[{"award-number":["2017GSF19115"]}]},{"name":"Department of Science and Technology of Shandong Provincial","award":["2017CXGC1303"],"award-info":[{"award-number":["2017CXGC1303"]}]},{"DOI":"10.13039\/501100005892","name":"China Academy of Chinese Medical Sciences","doi-asserted-by":"publisher","award":["2060302"],"award-info":[{"award-number":["2060302"]}],"id":[{"id":"10.13039\/501100005892","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Molecules"],"abstract":"<jats:p>Although smoke-isolated karrikins (KAR1) could regulate secondary metabolism in medicinal plants, the signal transduction mechanism has not been reported. This study highlights the influence of KAR1 on tanshinone I (T-I) production in Salvia miltiorrhiza and the involved signal molecules. Results showed KAR1-induced generation of nitric oxide (NO), jasmonic acid (JA) and T-I in S. miltiorrhiza hairy root. KAR1-induced increase of T-I was suppressed by NO-specific scavenger (cPTIO) and NOS inhibitors (PBITU); JA synthesis inhibitor (SHAM) and JA synthesis inhibitor (PrGall), which indicated that NO and JA play essential roles in KAR1-induced T-I. NO inhibitors inhibited KAR1-induced generation of NO and JA, suggesting NO was located upstream of JA signal pathway. NO-induced T-I production was inhibited by SHAM and PrGall, implying JA participated in transmitting signal NO to T-I accumulation. In other words, NO mediated the KAR1-induced T-I production through a JA-dependent signaling pathway. The results helped us understand the signal transduction mechanism involved in KAR1-induced T-I production and provided helpful information for the production of S. miltiorrhiza hairy root.<\/jats:p>","DOI":"10.3390\/molecules24071229","type":"journal-article","created":{"date-parts":[[2019,3,29]],"date-time":"2019-03-29T03:50:21Z","timestamp":1553831421000},"page":"1229","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Smoke-Isolated Karrikins Stimulated Tanshinones Biosynthesis in Salvia miltiorrhiza through Endogenous Nitric Oxide and Jasmonic Acid"],"prefix":"10.3390","volume":"24","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1241-2876","authenticated-orcid":false,"given":"Jie","family":"Zhou","sequence":"first","affiliation":[{"name":"School of Biological Science and Technology, University of Jinan, Jinan 250022, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zi-xin","family":"Xu","sequence":"additional","affiliation":[{"name":"School of Biological Science and Technology, University of Jinan, Jinan 250022, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hui","family":"Sun","sequence":"additional","affiliation":[{"name":"School of Biological Science and Technology, University of Jinan, Jinan 250022, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lan-ping","family":"Guo","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,3,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1016\/j.sajb.2011.02.004","article-title":"Smoke-water improves shoot growth and indigo accumulation in shoots of Isatis indigotica seedlings","volume":"77","author":"Zhou","year":"2011","journal-title":"S. Afr. J. Bot."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1126\/science.1099944","article-title":"A compound from smoke that promotes seed germination","volume":"305","author":"Flematti","year":"2004","journal-title":"Science"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"654","DOI":"10.1016\/S0254-6299(15)30206-4","article-title":"Isolation of the major germination cue from plant-derived smoke","volume":"70","author":"Light","year":"2004","journal-title":"S. Afr. J. Bot."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.jplph.2017.04.021","article-title":"Synthesis of tricyclic butenolides and comparison their effects with known smoke-butenolide, KAR1","volume":"215","author":"Krawczyk","year":"2017","journal-title":"J. Plant Physiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1016\/j.tplants.2017.03.011","article-title":"Strigolactones in Plant Interactions with Beneficial and Detrimental Organisms: The Yin and Yang","volume":"22","author":"Shirasu","year":"2017","journal-title":"Trends Plant Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.plaphy.2017.09.013","article-title":"Bacteria and smoke-water extract improve growth and induce the synthesis of volatile defense mechanisms in Vitis vinifera L.","volume":"120","author":"Salomon","year":"2017","journal-title":"Plant Physiol. Biochem."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.flora.2016.04.014","article-title":"Plant-derived smoke and temperature effects on seed germination of five Helianthemum (Cistaceae)","volume":"223","author":"Carlon","year":"2016","journal-title":"Flora"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/j.tig.2016.01.002","article-title":"Smoke and Hormone Mirrors: Action and Evolution of Karrikin and Strigolactone Signaling","volume":"32","author":"Morffy","year":"2016","journal-title":"Trends Genet."},{"key":"ref_9","unstructured":"China Pharmacopoeia Committee (2015). Pharmacopoeia of Peoples Republic of China, China Medical Science and Technology Press."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1016\/j.indcrop.2016.09.058","article-title":"Pathogenic fungal elicitors enhance ginsenoside biosynthesis of adventitious roots in Panax quinquefolius during bioreactor culture","volume":"94","author":"Yu","year":"2016","journal-title":"Ind. Crop Prod."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1016\/j.plaphy.2016.06.028","article-title":"Comparative proteomic analysis of the response to silver ions and yeast extract in salvia miltiorrhiza hairy root cultures","volume":"107","author":"Wang","year":"2016","journal-title":"Plant Physiol. Biochem."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1142\/S0192415X16500488","article-title":"Cytotoxicity of salvia miltiorrhiza against multidrug-resistant cancer cells","volume":"44","author":"Wu","year":"2016","journal-title":"Am. J. Chin. Me."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1007\/s11103-008-9435-0","article-title":"Role of plant hormones in plant defence responses","volume":"69","author":"Bari","year":"2009","journal-title":"Plant Mol. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.jprot.2015.12.005","article-title":"Proteomic analysis of Magnolia sieboldii K. Koch seed germination","volume":"133","author":"Lu","year":"2016","journal-title":"J. Proteomics."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.jplph.2014.11.010","article-title":"Germination induction of dormant Avena fatua caryopses by KAR1 and GA3 involving the control of reactive oxygen species (H2O2 and O2\u2022\u2212) and enzymatic antioxidants (superoxide dismutase and catalase) both in the embryo and the aleurone layers","volume":"176","author":"Koprowski","year":"2015","journal-title":"J. Plant Physiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1111\/jipb.12087","article-title":"Nitric oxide and brassinosteroids mediated fungal endophyte-lnduced volatile oil production through protein phosphorylation pathways in Atractylodes lancea plantlets","volume":"55","author":"Ren","year":"2013","journal-title":"J. Integr. Plant Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/j.foodchem.2014.08.014","article-title":"UV-B irradiation alleviates the deterioration of cold-stored mangoes by enhancing endogenous nitric oxide levels","volume":"169","author":"Ruan","year":"2015","journal-title":"Food Chem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1016\/j.indcrop.2018.03.044","article-title":"Salicylic acid-induced flavonoid accumulation in Ginkgo biloba leaves is dependent on red and far-red light","volume":"118","author":"Ni","year":"2018","journal-title":"Ind. Crop Prod."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.postharvbio.2011.10.008","article-title":"Cold-induced endogenous nitric oxide generation plays a role in chilling tolerance of loquat fruit during postharvest storage","volume":"65","author":"Xu","year":"2012","journal-title":"Postharvest Biol. Tec."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1007\/s11434-015-0813-0","article-title":"JA-mediated transcriptional regulation of secondary metabolism in medicinal plants","volume":"60","author":"Afrin","year":"2015","journal-title":"Sci. Bull."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1663","DOI":"10.1093\/jxb\/erx484","article-title":"SmJAZ8 acts as a core repressor regulating JA-induced biosynthesis of salvianolic acids and tanshinones in Salvia miltiorrhiza hairy roots","volume":"69","author":"Pei","year":"2018","journal-title":"J. Exp. Bot."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1016\/j.phymed.2011.09.076","article-title":"Tanshinone IIA and tanshinone I production by Trichoderma atroviride D16, an endophytic fungus in Salvia miltiorrhiza","volume":"19","author":"Ming","year":"2012","journal-title":"Phytomedicine"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1016\/j.plantsci.2004.09.012","article-title":"Tanshinone production and isoprenoid pathways in Salvia miltiorrhiza hairy roots induced by Ag+ and yeast elicitor","volume":"168","author":"Ge","year":"2005","journal-title":"Plant Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1016\/S1002-0721(10)60486-3","article-title":"Effects of LaCl3 on photosynthesis and the accumulation of tanshinones and salvianolic acids in Salvia miltiorrhiza seedlings","volume":"29","author":"Zhou","year":"2011","journal-title":"J. Rare Earth."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Gao, W., Sun, H.X., Xiao, H.B., Cui, G.H., Hillwig, M.L., Jackson, A., Wang, X., Shen, Y., Zhou, N., and Zhang, L.X. (2014). Combining metabolomics and transcriptomics to characterize tanshinone biosynthesis in Salvia miltiorrhiza. BMC Genomics., 15.","DOI":"10.1186\/1471-2164-15-73"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.jphotobiol.2016.01.012","article-title":"Synergistic effects of ultraviolet-B and methyl jasmonate on tanshinone biosynthesis in Salvia miltiorrhiza hairy roots","volume":"159","author":"Wang","year":"2016","journal-title":"J. Photochem. Photobiol. B"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.sajb.2013.12.001","article-title":"Smoke\u2013water stimulates secondary metabolites during in vitro seedling development in Tulbaghia species","volume":"9","author":"Aremu","year":"2014","journal-title":"S. Afr. J. Bot."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"So\u00f3s, V., Sebesty\u00e9n, E., Juh\u00e1sz, A., Szalai, G., Tandori, J., Light, M.E., Kohout, L., Van Staden, J., and Bal\u00e1zs, E. (2010). Transcriptome analysis of germinating maize kernels exposed to smoke\u2013water and the active compound KAR1. BMC Plant Biol., 10.","DOI":"10.1186\/1471-2229-10-236"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1111\/j.1744-7909.2007.00570.x","article-title":"Synergistic action between jasmonic acid and nitric oxide in inducing matrine accumulation of Sophora flavescens suspension cells","volume":"50","author":"Xu","year":"2008","journal-title":"J. Integr. Plant Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"21843","DOI":"10.1038\/srep21843","article-title":"Jasmonic acid is a crucial signal transducer in heat shock induced sesquiterpene formation in Aquilaria sinensis","volume":"6","author":"Xu","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1016\/j.jbiosc.2013.10.013","article-title":"Selective responses of enzymes in the two parallel pathways of rosmarinic acid biosynthetic pathway to elicitors in Salvia miltiorrhiza hairy root cultures","volume":"117","author":"Zhang","year":"2014","journal-title":"J. Biosci. Bioeng."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.sajb.2008.10.004","article-title":"Smoke-derived butenolide: Towards understanding its biological effects","volume":"75","author":"Light","year":"2009","journal-title":"S. Afr. J. Bot."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2","DOI":"10.3390\/molecules22030478","article-title":"Quality Evaluation and Chemical Markers Screening of Salvia miltiorrhiza Bge. (Danshen) Based on HPLC Fingerprints and HPLC-MS (n) Coupled with Chemometrics","volume":"22","author":"Liang","year":"2017","journal-title":"Molecules"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.jplph.2017.04.005","article-title":"Nitric oxide mediates brassinosteroid-induced flavonoid biosynthesis in Camellia sinensis L.","volume":"214","author":"Li","year":"2017","journal-title":"J. Plant Physiol."}],"container-title":["Molecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1420-3049\/24\/7\/1229\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T12:41:22Z","timestamp":1760186482000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1420-3049\/24\/7\/1229"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,3,29]]},"references-count":34,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2019,4]]}},"alternative-id":["molecules24071229"],"URL":"https:\/\/doi.org\/10.3390\/molecules24071229","relation":{},"ISSN":["1420-3049"],"issn-type":[{"value":"1420-3049","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,3,29]]}}}