{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,16]],"date-time":"2026-03-16T15:23:58Z","timestamp":1773674638665,"version":"3.50.1"},"reference-count":121,"publisher":"Wiley","license":[{"start":{"date-parts":[[2010,1,1]],"date-time":"2010-01-01T00:00:00Z","timestamp":1262304000000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/3.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["SFRH\/BPD\/13850\/2003"],"award-info":[{"award-number":["SFRH\/BPD\/13850\/2003"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["SFRH\/BPD\/27122\/2006"],"award-info":[{"award-number":["SFRH\/BPD\/27122\/2006"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["SFRH\/BPD\/13850\/2003"],"award-info":[{"award-number":["SFRH\/BPD\/13850\/2003"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["SFRH\/BPD\/27122\/2006"],"award-info":[{"award-number":["SFRH\/BPD\/27122\/2006"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Journal of Biomedicine and Biotechnology"],"published-print":{"date-parts":[[2010]]},"abstract":"<jats:p>The usage of<jats:italic>Humulus lupulus<\/jats:italic>for brewing increased the demand for high-quality plant material. Simultaneously, hop has been used in traditional medicine and recently recognized with anticancer and anti-infective properties. Tissue culture techniques have been reported for a wide range of species, and open the prospect for propagation of disease-free, genetically uniform and massive amounts of plants<jats:italic>in vitro.<\/jats:italic>Moreover, the development of large-scale culture methods using bioreactors enables the industrial production of secondary metabolites. Reliable and efficient tissue culture protocol for shoot regeneration through organogenic nodule formation was established for hop. The present review describes the histological, and biochemical changes occurring during this morphogenic process, together with an analysis of transcriptional and metabolic profiles. We also discuss the existence of common molecular factors among three different morphogenic processes: organogenic nodules and somatic embryogenesis, which strictly speaking depend exclusively on intrinsic developmental reprogramming, and legume nitrogen-fixing root nodules, which arises in response to symbiosis. The review of the key factors that participate in hop nodule organogenesis and the comparison with other morphogenic processes may have merit as a study presenting recent advances in complex molecular networks occurring during morphogenesis and together, these provide a rich framework for biotechnology applications.<\/jats:p>","DOI":"10.1155\/2010\/583691","type":"journal-article","created":{"date-parts":[[2010,8,3]],"date-time":"2010-08-03T05:36:35Z","timestamp":1280813795000},"page":"1-16","source":"Crossref","is-referenced-by-count":8,"title":["Organogenic Nodule Formation in Hop: A Tool to Study Morphogenesis in Plants with Biotechnological and Medicinal Applications"],"prefix":"10.1155","volume":"2010","author":[{"given":"Ana M.","family":"Fortes","sequence":"first","affiliation":[{"name":"Plant Systems Biology Lab, ICAT, Center for Biodiversity and Functional Integrative Genomics, Science Faculty of Lisbon University, Campo Grande, 1749-016 Lisboa, Portugal"}]},{"given":"Filipa","family":"Santos","sequence":"additional","affiliation":[{"name":"Plant Systems Biology Lab, ICAT, Center for Biodiversity and Functional Integrative Genomics, Science Faculty of Lisbon University, Campo Grande, 1749-016 Lisboa, Portugal"},{"name":"Institute of Biology II\/Botany, Faculty of Biology, Albert-Ludwigs-University of Freiburg, Sch\u00e4nzlestra\u00dfe 1, 79104 Freiburg, Germany"}]},{"given":"Maria S.","family":"Pais","sequence":"additional","affiliation":[{"name":"Plant Systems Biology Lab, ICAT, Center for Biodiversity and Functional Integrative Genomics, Science Faculty of Lisbon University, Campo Grande, 1749-016 Lisboa, Portugal"}]}],"member":"311","reference":[{"key":"1","doi-asserted-by":"publisher","DOI":"10.1021\/np800740m"},{"key":"2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jep.2008.01.011"},{"issue":"5","key":"3","first-page":"591","volume":"4","year":"2009","journal-title":"Natural Product Communications"},{"issue":"1","key":"5","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1007\/BF02823011","volume":"32","year":"1996","journal-title":"In Vitro Cellular and Developmental Biology\u2014Plant"},{"key":"6","doi-asserted-by":"publisher","DOI":"10.1023\/A:1017901817063"},{"issue":"2","key":"7","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1007\/BF02921085","volume":"36","year":"1994","journal-title":"Biologia Plantarum"},{"issue":"7","key":"8","doi-asserted-by":"crossref","first-page":"971","DOI":"10.2307\/2656996","volume":"87","year":"2000","journal-title":"American Journal of Botany"},{"key":"9","doi-asserted-by":"publisher","DOI":"10.1016\/S0168-9452(99)00196-X"},{"key":"10","first-page":"149","volume-title":"Nodule culture: a developmental pathway with high potencial for regeneration, automated micropropagation, and plant metabolite production from woody plants","year":"1988"},{"key":"11","doi-asserted-by":"publisher","DOI":"10.1007\/BF00232338"},{"key":"12","doi-asserted-by":"publisher","DOI":"10.1007\/s002990050259"},{"issue":"1-2","key":"13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0304-4238(93)90132-A","volume":"53","year":"1993","journal-title":"Scientia Horticulturae"},{"key":"14","doi-asserted-by":"publisher","DOI":"10.1007\/s00299-008-0537-6"},{"key":"15","first-page":"57","volume":"1","year":"2007","journal-title":"Pharmacognosy Reviews"},{"key":"17","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-8137.1996.tb04921.x"},{"key":"18","doi-asserted-by":"publisher","DOI":"10.1016\/S0168-9452(02)00050-X"},{"key":"19","doi-asserted-by":"publisher","DOI":"10.1078\/0176-1617-01116"},{"key":"20","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.107.055178"},{"key":"21","doi-asserted-by":"publisher","DOI":"10.1021\/jf9043106"},{"key":"125","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1111\/j.1399-3054.1962.tb08052.x","volume":"15","year":"1962","journal-title":"Physiologia Plantarum"},{"key":"22","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-9-445"},{"key":"23","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/S0079-6603(02)72070-9","volume":"72","year":"2002","journal-title":"Progress in Nucleic Acid Research and Molecular Biology"},{"key":"24","doi-asserted-by":"publisher","DOI":"10.1093\/aob\/mcm079"},{"key":"25","doi-asserted-by":"crossref","first-page":"S185","DOI":"10.1105\/tpc.010455","volume":"14","year":"2002","journal-title":"Plant Cell"},{"key":"26","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/erj027"},{"key":"27","doi-asserted-by":"publisher","DOI":"10.1104\/pp.107.106955"},{"key":"28","doi-asserted-by":"publisher","DOI":"10.1016\/j.tplants.2008.06.006"},{"key":"29","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-313X.2009.03871.x"},{"key":"30","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-313X.2003.01823.x"},{"key":"31","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-8137.2008.02511.x"},{"key":"32","doi-asserted-by":"publisher","DOI":"10.1126\/scisignal.149re11"},{"key":"33","doi-asserted-by":"publisher","DOI":"10.1016\/j.tplants.2007.10.003"},{"key":"34","doi-asserted-by":"publisher","DOI":"10.1007\/s11103-008-9374-9"},{"key":"35","doi-asserted-by":"publisher","DOI":"10.1515\/BC.2001.142"},{"issue":"5244","key":"36","doi-asserted-by":"crossref","first-page":"1988","DOI":"10.1126\/science.270.5244.1988","volume":"270","year":"1995","journal-title":"Science"},{"key":"38","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.106.046581"},{"key":"39","doi-asserted-by":"publisher","DOI":"10.1104\/pp.108.131557"},{"key":"40","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.106.048298"},{"key":"41","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.108.058032"},{"issue":"4","key":"42","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1093\/mp\/ssn029","volume":"1","year":"2008","journal-title":"Molecular Plant"},{"issue":"2","key":"43","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/0092-8674(95)90401-8","volume":"80","year":"1995","journal-title":"Cell"},{"issue":"4","key":"44","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1165\/ajrcmb.24.4.4290","volume":"24","year":"2001","journal-title":"American Journal of Respiratory Cell and Molecular Biology"},{"key":"45","doi-asserted-by":"publisher","DOI":"10.1023\/A:1006405929082"},{"key":"46","doi-asserted-by":"publisher","DOI":"10.1078\/0171-9335-00397"},{"key":"47","doi-asserted-by":"publisher","DOI":"10.1093\/emboj\/18.3.664"},{"key":"48","doi-asserted-by":"publisher","DOI":"10.1104\/pp.103.019968"},{"issue":"2","key":"49","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1177\/002215540405200211","volume":"52","year":"2004","journal-title":"Journal of Histochemistry and Cytochemistry"},{"key":"50"},{"key":"51","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.arplant.55.031903.141701"},{"key":"52","doi-asserted-by":"publisher","DOI":"10.1104\/pp.106.079186"},{"issue":"3-4","key":"53","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1515\/znc-1996-3-401","volume":"51","year":"1996","journal-title":"Zeitschrift f\u00fcr Naturforschung C"},{"key":"54","doi-asserted-by":"publisher","DOI":"10.1104\/pp.010787"},{"key":"55","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbamcr.2006.08.031"},{"key":"56","doi-asserted-by":"publisher","DOI":"10.1034\/j.1399-3054.2002.1160114.x"},{"key":"57","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-8137.2007.02292.x"},{"key":"58","doi-asserted-by":"publisher","DOI":"10.1093\/pcp\/pci187"},{"key":"59","doi-asserted-by":"publisher","DOI":"10.1093\/aob\/mcg098"},{"key":"60","doi-asserted-by":"publisher","DOI":"10.1034\/j.1399-3054.1997.1000327.x"},{"key":"61","doi-asserted-by":"publisher","DOI":"10.1007\/s10529-006-9179-3"},{"issue":"2","key":"62","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1007\/PL00000852","volume":"58","year":"2001","journal-title":"Cellular and Molecular Life Sciences"},{"key":"63","doi-asserted-by":"publisher","DOI":"10.1104\/pp.106.083030"},{"issue":"3","key":"64","first-page":"106","volume":"16","year":"2001","journal-title":"News in Physiological Sciences"},{"key":"65","doi-asserted-by":"publisher","DOI":"10.1093\/treephys\/tpp063"},{"key":"66","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1007\/978-1-4684-5637-0_42","volume":"250","year":"1988","journal-title":"Advances in Experimental Medicine and Biology"},{"key":"67","doi-asserted-by":"publisher","DOI":"10.1104\/pp.108.134932"},{"key":"68","doi-asserted-by":"publisher","DOI":"10.1104\/pp.104.055756"},{"key":"69","doi-asserted-by":"publisher","DOI":"10.1111\/j.1399-3054.2006.00799.x"},{"key":"70","doi-asserted-by":"publisher","DOI":"10.1038\/nrm2020"},{"key":"71","doi-asserted-by":"publisher","DOI":"10.1016\/j.tplants.2009.01.006"},{"key":"72","doi-asserted-by":"publisher","DOI":"10.1126\/science.1121356"},{"key":"73","doi-asserted-by":"publisher","DOI":"10.1126\/science.1123542"},{"key":"75","doi-asserted-by":"publisher","DOI":"10.1007\/s00018-006-6116-5"},{"key":"76","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.93.17.9282"},{"key":"77","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.107.055798"},{"key":"78","doi-asserted-by":"publisher","DOI":"10.1104\/pp.000810"},{"issue":"2","key":"79","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1093\/mp\/ssm021","volume":"1","year":"2008","journal-title":"Molecular Plant"},{"issue":"6","key":"80","first-page":"715","volume":"83","year":"2002","journal-title":"Current Science"},{"key":"81","doi-asserted-by":"publisher","DOI":"10.1016\/S0168-9452(01)00334-X"},{"key":"82","doi-asserted-by":"publisher","DOI":"10.1104\/pp.104.042069"},{"key":"83","doi-asserted-by":"publisher","DOI":"10.1104\/pp.104.044784"},{"key":"84","doi-asserted-by":"publisher","DOI":"10.1016\/j.pbi.2004.07.006"},{"key":"85","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-5-39"},{"key":"86","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0401572101"},{"key":"87","doi-asserted-by":"publisher","DOI":"10.1016\/j.jplph.2009.01.012"},{"issue":"10","key":"88","doi-asserted-by":"crossref","first-page":"1257","DOI":"10.1093\/treephys\/26.10.1257","volume":"26","year":"2006","journal-title":"Tree Physiology"},{"key":"89","doi-asserted-by":"publisher","DOI":"10.1104\/pp.127.3.803"},{"issue":"10","key":"90","doi-asserted-by":"crossref","first-page":"2049","DOI":"10.1242\/dev.124.10.2049","volume":"124","year":"1997","journal-title":"Development"},{"key":"91","doi-asserted-by":"publisher","DOI":"10.1016\/j.plaphy.2003.10.008"},{"key":"92","doi-asserted-by":"publisher","DOI":"10.1007\/s00425-005-1534-4"},{"key":"93","doi-asserted-by":"publisher","DOI":"10.1007\/s00299-008-0588-8"},{"key":"94","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/erp046"},{"key":"95","doi-asserted-by":"publisher","DOI":"10.1016\/j.ygeno.2007.07.007"},{"key":"96","doi-asserted-by":"publisher","DOI":"10.1101\/gad.220402"},{"key":"97","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.cellbio.18.012502.083431"},{"key":"98","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.105.039412"},{"key":"99","doi-asserted-by":"publisher","DOI":"10.1093\/pcp\/pci026"},{"key":"100","doi-asserted-by":"publisher","DOI":"10.1016\/j.tplants.2008.09.008"},{"key":"101","doi-asserted-by":"publisher","DOI":"10.1104\/pp.103.037747"},{"key":"102","doi-asserted-by":"publisher","DOI":"10.1126\/science.1115581"},{"key":"103","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0911006107"},{"key":"104","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.13.6.1305"},{"key":"105","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.13.6.1293"},{"key":"106","doi-asserted-by":"publisher","DOI":"10.1007\/s11103-007-9234-z"},{"key":"107","doi-asserted-by":"publisher","DOI":"10.1104\/pp.105.070326"},{"issue":"5","key":"108","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1094\/MPMI.2002.15.5.411","volume":"15","year":"2002","journal-title":"Molecular Plant-Microbe Interactions"},{"key":"109","doi-asserted-by":"publisher","DOI":"10.1094\/MPMI-21-6-0843"},{"key":"110","doi-asserted-by":"publisher","DOI":"10.1126\/science.1132397"},{"key":"111","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-313X.1998.00090.x"},{"key":"112","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.105.038232"},{"key":"113","doi-asserted-by":"publisher","DOI":"10.1007\/s11033-009-9764-3"},{"key":"114","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/erj184"},{"key":"115","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2229-7-21"},{"key":"116","doi-asserted-by":"publisher","DOI":"10.1128\/JB.187.1.168-174.2005"},{"key":"117","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-8137.2004.01285.x"},{"key":"118","doi-asserted-by":"publisher","DOI":"10.1007\/s00299-003-0611-z"},{"key":"119","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2818.2008.02040.x"},{"key":"120","doi-asserted-by":"crossref","first-page":"1332","DOI":"10.1104\/pp.88.4.1332","volume":"88","year":"1988","journal-title":"Plant Physiology"},{"issue":"12","key":"121","doi-asserted-by":"crossref","first-page":"1283","DOI":"10.1094\/MPMI.2004.17.12.1283","volume":"17","year":"2004","journal-title":"Molecular Plant-Microbe Interactions"},{"key":"122","doi-asserted-by":"publisher","DOI":"10.1093\/pcp\/pci222"},{"key":"123","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-313X.2006.02751.x"},{"key":"124","doi-asserted-by":"publisher","DOI":"10.1046\/j.0028-646X.2001.00246.x"}],"container-title":["Journal of Biomedicine and Biotechnology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/downloads.hindawi.com\/journals\/bmri\/2010\/583691.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/downloads.hindawi.com\/journals\/bmri\/2010\/583691.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/downloads.hindawi.com\/journals\/bmri\/2010\/583691.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,11,2]],"date-time":"2021-11-02T21:55:18Z","timestamp":1635890118000},"score":1,"resource":{"primary":{"URL":"http:\/\/www.hindawi.com\/journals\/bmri\/2010\/583691\/"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2010]]},"references-count":121,"alternative-id":["583691","583691"],"URL":"https:\/\/doi.org\/10.1155\/2010\/583691","relation":{},"ISSN":["1110-7243","1110-7251"],"issn-type":[{"value":"1110-7243","type":"print"},{"value":"1110-7251","type":"electronic"}],"subject":[],"published":{"date-parts":[[2010]]}}}