{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,6]],"date-time":"2026-05-06T14:33:56Z","timestamp":1778078036083,"version":"3.51.4"},"reference-count":112,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2023,10,7]],"date-time":"2023-10-07T00:00:00Z","timestamp":1696636800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100008530","name":"European Regional Development Fund","doi-asserted-by":"publisher","award":["NORTE-01-0246-FEDER-000063"],"award-info":[{"award-number":["NORTE-01-0246-FEDER-000063"]}],"id":[{"id":"10.13039\/501100008530","id-type":"DOI","asserted-by":"publisher"}]},{"name":"European Union\u2019s Horizon 2020 Research and Innovation Programme","award":["66898"],"award-info":[{"award-number":["66898"]}]},{"name":"European Union\u2019s Horizon 2020 Research and Innovation Programme","award":["857251"],"award-info":[{"award-number":["857251"]}]},{"name":"European Union\u2019s Horizon 2020 Research and Innovation Programme","award":["SFRH\/BD\/97590\/2013"],"award-info":[{"award-number":["SFRH\/BD\/97590\/2013"]}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["SFRH\/BD\/41907\/2007"],"award-info":[{"award-number":["SFRH\/BD\/41907\/2007"]}],"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":["CEECIND\/00399\/2017\/CP1423\/CT0004"],"award-info":[{"award-number":["CEECIND\/00399\/2017\/CP1423\/CT0004"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,1,1]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Catharanthus roseus leaves produce a range of monoterpenoid indole alkaloids (MIAs) that include low levels of the anticancer drugs vinblastine and vincristine. The MIA pathway displays a complex architecture spanning different subcellular and cell type localizations, and is under complex regulation. As a result, the development of strategies to increase the levels of the anticancer MIAs has remained elusive. The pathway involves mesophyll specialized idioblasts where the late unsolved biosynthetic steps are thought to occur. Here, protoplasts of C. roseus leaf idioblasts were isolated by fluorescence-activated cell sorting, and their differential alkaloid and transcriptomic profiles were characterized. This involved the assembly of an improved C. roseus transcriptome from short- and long-read data, IDIO+. It was observed that C. roseus mesophyll idioblasts possess a distinctive transcriptomic profile associated with protection against biotic and abiotic stresses, and indicative that this cell type is a carbon sink, in contrast to surrounding mesophyll cells. Moreover, it is shown that idioblasts are a hotspot of alkaloid accumulation, suggesting that their transcriptome may hold the key to the in-depth understanding of the MIA pathway and the success of strategies leading to higher levels of the anticancer drugs.<\/jats:p>","DOI":"10.1093\/jxb\/erad374","type":"journal-article","created":{"date-parts":[[2023,10,7]],"date-time":"2023-10-07T15:42:04Z","timestamp":1696693324000},"page":"274-299","source":"Crossref","is-referenced-by-count":17,"title":["The leaf idioblastome of the medicinal plant<i>Catharanthus roseus<\/i>is associated with stress resistance and alkaloid metabolism"],"prefix":"10.1093","volume":"75","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4082-1853","authenticated-orcid":false,"given":"Joana G","family":"Guedes","sequence":"first","affiliation":[{"name":"CIBIO, Centro de Investiga\u00e7\u00e3o em Biodiversidade e Recursos Gen\u00e9ticos, InBIO Laborat\u00f3rio Associado, Campus de Vair\u00e3o, Universidade do Porto , 4485-661 Vair\u00e3o , Portugal"},{"name":"BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO , Campus de Vair\u00e3o, 4485-661 Vair\u00e3o , Portugal"},{"name":"Programa Doutoral em Biologia Molecular e Celular (MCbiology), Instituto de Ci\u00eancias Biom\u00e9dicas Abel Salazar (ICBAS), Universidade do Porto , 4050-313 Porto , Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5468-7608","authenticated-orcid":false,"given":"Rog\u00e9rio","family":"Ribeiro","sequence":"additional","affiliation":[{"name":"CIBIO, Centro de Investiga\u00e7\u00e3o em Biodiversidade e Recursos Gen\u00e9ticos, InBIO Laborat\u00f3rio Associado, Campus de Vair\u00e3o, Universidade do Porto , 4485-661 Vair\u00e3o , Portugal"},{"name":"BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO , Campus de Vair\u00e3o, 4485-661 Vair\u00e3o , Portugal"},{"name":"Departamento de Biologia, Faculdade de Cie\u0302ncias da Universidade do Porto , 4169-007 Porto , Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9576-5556","authenticated-orcid":false,"given":"In\u00eas","family":"Carqueijeiro","sequence":"additional","affiliation":[{"name":"CIBIO, Centro de Investiga\u00e7\u00e3o em Biodiversidade e Recursos Gen\u00e9ticos, InBIO Laborat\u00f3rio Associado, Campus de Vair\u00e3o, Universidade do Porto , 4485-661 Vair\u00e3o , Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9361-9037","authenticated-orcid":false,"given":"Ana Lu\u00edsa","family":"Guimar\u00e3es","sequence":"additional","affiliation":[{"name":"Departamento de Biologia, Faculdade de Cie\u0302ncias da Universidade do Porto , 4169-007 Porto , Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4936-058X","authenticated-orcid":false,"given":"Cl\u00e1udia","family":"Bispo","sequence":"additional","affiliation":[{"name":"Instituto Gulbenkian de Ci\u00eancia , Rua da Quinta Grande 6, 2780-156 Oeiras , Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6212-0962","authenticated-orcid":false,"given":"John","family":"Archer","sequence":"additional","affiliation":[{"name":"CIBIO, Centro de Investiga\u00e7\u00e3o em Biodiversidade e Recursos Gen\u00e9ticos, InBIO Laborat\u00f3rio Associado, Campus de Vair\u00e3o, Universidade do Porto , 4485-661 Vair\u00e3o , Portugal"},{"name":"BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO , Campus de Vair\u00e3o, 4485-661 Vair\u00e3o , Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9324-3030","authenticated-orcid":false,"given":"Herlander","family":"Azevedo","sequence":"additional","affiliation":[{"name":"CIBIO, Centro de Investiga\u00e7\u00e3o em Biodiversidade e Recursos Gen\u00e9ticos, InBIO Laborat\u00f3rio Associado, Campus de Vair\u00e3o, Universidade do Porto , 4485-661 Vair\u00e3o , Portugal"},{"name":"BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO , Campus de Vair\u00e3o, 4485-661 Vair\u00e3o , Portugal"},{"name":"Departamento de Biologia, Faculdade de Cie\u0302ncias da Universidade do Porto , 4169-007 Porto , Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4832-578X","authenticated-orcid":false,"given":"Nuno A","family":"Fonseca","sequence":"additional","affiliation":[{"name":"CIBIO, Centro de Investiga\u00e7\u00e3o em Biodiversidade e Recursos Gen\u00e9ticos, InBIO Laborat\u00f3rio Associado, Campus de Vair\u00e3o, Universidade do Porto , 4485-661 Vair\u00e3o , Portugal"},{"name":"BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO , Campus de Vair\u00e3o, 4485-661 Vair\u00e3o , Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2411-710X","authenticated-orcid":false,"given":"Mariana","family":"Sottomayor","sequence":"additional","affiliation":[{"name":"CIBIO, Centro de Investiga\u00e7\u00e3o em Biodiversidade e Recursos Gen\u00e9ticos, InBIO Laborat\u00f3rio Associado, Campus de Vair\u00e3o, Universidade do Porto , 4485-661 Vair\u00e3o , Portugal"},{"name":"BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO , Campus de Vair\u00e3o, 4485-661 Vair\u00e3o , Portugal"},{"name":"Departamento de Biologia, Faculdade de Cie\u0302ncias da Universidade do Porto , 4169-007 Porto , Portugal"}]}],"member":"286","published-online":{"date-parts":[[2023,10,7]]},"reference":[{"key":"2023122122461522500_CIT0001","doi-asserted-by":"crossref","first-page":"112110","DOI":"10.1016\/j.phytochem.2019.112110","article-title":"The genuine localization of indole alkaloids in Vinca minor and Catharanthus roseus","volume":"168","author":"Abouzeid","year":"2019","journal-title":"Phytochemistry"},{"key":"2023122122461522500_CIT0002","doi-asserted-by":"crossref","first-page":"1600","DOI":"10.1093\/bioinformatics\/btl140","article-title":"Improved scoring of functional groups from gene expression data by decorrelating GO graph structure","volume":"22","author":"Alexa","year":"2006","journal-title":"Bioinformatics"},{"key":"2023122122461522500_CIT0003","doi-asserted-by":"crossref","first-page":"R106","DOI":"10.1186\/gb-2010-11-10-r106","article-title":"Differential expression analysis for sequence count data","volume":"11","author":"Anders","year":"2010","journal-title":"Genome Biology"},{"key":"2023122122461522500_CIT0004","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/978-3-642-74551-5_17","article-title":"Distribution of catharanthine, vindoline and 3\u02b9,4\u02b9-anhydrovinblastine in the aerial parts of some Catharanthus roseus plants and the significance thereof in relation to alkaloid production in cultured cells","volume-title":"Primary and secondary metabolism of plant cell cultures","author":"Balsevich","year":"1989"},{"key":"2023122122461522500_CIT0005","doi-asserted-by":"crossref","first-page":"5533","DOI":"10.1007\/s00253-019-09887-9","article-title":"Antifungal and antimicrobial proteins and peptides of potato (Solanum tuberosum L.) tubers and their applications","volume":"103","author":"B\u00e1rtov\u00e1","year":"2019","journal-title":"Applied Microbiology and Biotechnology"},{"key":"2023122122461522500_CIT0006","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/s00425-014-2056-8","article-title":"Benzylisoquinoline alkaloid biosynthesis in opium poppy","volume":"240","author":"Beaudoin","year":"2014","journal-title":"Planta"},{"key":"2023122122461522500_CIT0007","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the false discovery rate: a practical and powerful approach to multiple testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"Journal of the Royal Statistical Society: Series B"},{"key":"2023122122461522500_CIT0008","doi-asserted-by":"crossref","first-page":"D344","DOI":"10.1093\/nar\/gkaa977","article-title":"The InterPro protein families and domains database: 20 years on","volume":"49","author":"Blum","year":"2021","journal-title":"Nucleic Acids Research"},{"key":"2023122122461522500_CIT0009","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: a flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"2023122122461522500_CIT0010","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nmeth.3176","article-title":"Fast and sensitive protein alignment using DIAMOND","volume":"12","author":"Buchfink","year":"2015","journal-title":"Nature Methods"},{"key":"2023122122461522500_CIT0011","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1186\/s13059-016-0924-1","article-title":"JBrowse: a dynamic web platform for genome visualization and analysis","volume":"17","author":"Buels","year":"2016","journal-title":"Genome Biology"},{"key":"2023122122461522500_CIT0012","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1111\/j.1365-313X.2004.02030.x","article-title":"Co-expression of three MEP pathway genes and geraniol 10-hydroxylase in internal phloem parenchyma of Catharanthus roseus implicates multicellular translocation of intermediates during the biosynthesis of monoterpene indole alkaloids and isoprenoid-derived primary metabolites","volume":"38","author":"Burlat","year":"2004","journal-title":"The Plant Journal"},{"key":"2023122122461522500_CIT0013","doi-asserted-by":"crossref","first-page":"515","DOI":"10.3389\/fpls.2015.00515","article-title":"Comparative analysis of the phytocyanin gene family in 10 plant species: a focus on Zea mays","volume":"6","author":"Cao","year":"2015","journal-title":"Frontiers in Plant Science"},{"key":"2023122122461522500_CIT0014","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1126\/science.aat4100","article-title":"Missing enzymes in the biosynthesis of the anticancer drug vinblastine in Madagascar periwinkle","volume":"360","author":"Caputi","year":"2018","journal-title":"Science"},{"key":"2023122122461522500_CIT0015","doi-asserted-by":"crossref","first-page":"2371","DOI":"10.1104\/pp.16.01028","article-title":"Isolation of cells specialized in anticancer alkaloid metabolism by fluorescence-activated cell sorting","volume":"171","author":"Carqueijeiro","year":"2016","journal-title":"Plant Physiology"},{"key":"2023122122461522500_CIT0016","doi-asserted-by":"crossref","first-page":"1486","DOI":"10.1104\/pp.113.220558","article-title":"Vacuolar transport of the medicinal alkaloids from Catharanthus roseus is mediated by a proton-driven antiport","volume":"162","author":"Carqueijeiro","year":"2013","journal-title":"Plant Physiology"},{"key":"2023122122461522500_CIT0017","doi-asserted-by":"crossref","first-page":"1024","DOI":"10.3389\/fpls.2015.01024","article-title":"Overexpression of soybean isoflavone reductase (GmIFR) enhances resistance to Phytophthora sojae in soybean","volume":"6","author":"Cheng","year":"2015","journal-title":"Frontiers in Plant Science"},{"key":"2023122122461522500_CIT0018","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.phytochem.2016.08.006","article-title":"Regulation of plant secondary metabolism and associated specialized cell development by MYBs and bHLHs","volume":"131","author":"Chezem","year":"2016","journal-title":"Phytochemistry"},{"key":"2023122122461522500_CIT0019","doi-asserted-by":"crossref","first-page":"687406","DOI":"10.3389\/fpls.2021.687406","article-title":"Subfunctionalization of paralog transcription factors contributes to regulation of alkaloid pathway branch choice in Catharanthus roseus","volume":"12","author":"Colinas","year":"2021","journal-title":"Frontiers in Plant Science"},{"key":"2023122122461522500_CIT0020","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1104\/pp.107.107060","article-title":"Molecular cloning and characterization of a vacuolar class III peroxidase involved in the metabolism of anticancer alkaloids in Catharanthus roseus","volume":"146","author":"Costa","year":"2008","journal-title":"Plant Physiology"},{"key":"2023122122461522500_CIT0021","doi-asserted-by":"crossref","first-page":"2145","DOI":"10.1039\/D0NP00092B","article-title":"Metabolic engineering for plant natural products biosynthesis: new procedures, concrete achievements and remaining limits","volume":"38","author":"Courdavault","year":"2021","journal-title":"Natural Product Reports"},{"key":"2023122122461522500_CIT0022","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.pbi.2014.03.010","article-title":"A look inside an alkaloid multisite plant: the Catharanthus logistics","volume":"19","author":"Courdavault","year":"2014","journal-title":"Current Opinion in Plant Biology"},{"key":"2023122122461522500_CIT0023","doi-asserted-by":"crossref","first-page":"1541","DOI":"10.12688\/f1000research.129212.1","article-title":"An updated version of the Madagascar periwinkle genome","volume":"11","author":"Cuello","year":"2022","journal-title":"F1000Research"},{"key":"2023122122461522500_CIT0024","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1104\/pp.19.00565","article-title":"Purine permease-type benzylisoquinoline alkaloid transporters in opium poppy","volume":"181","author":"Dastmalchi","year":"2019","journal-title":"Plant Physiology"},{"key":"2023122122461522500_CIT0025","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.pbi.2014.03.006","article-title":"Making iridoids\/secoiridoids and monoterpenoid indole alkaloids: progress on pathway elucidation","volume":"19","author":"De Luca","year":"2014","journal-title":"Current Opinion in Plant Biology"},{"key":"2023122122461522500_CIT0026","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1093\/pcp\/pct198","article-title":"Emerging functions of nodulin-like proteins in non-nodulating plant species","volume":"55","author":"Denanc\u00e9","year":"2014","journal-title":"Plant and Cell Physiology"},{"key":"2023122122461522500_CIT0027","doi-asserted-by":"crossref","first-page":"40453","DOI":"10.1038\/srep40453","article-title":"Folivory elicits a strong defense reaction in Catharanthus roseus: metabolomic and transcriptomic analyses reveal distinct local and systemic responses","volume":"7","author":"Dug\u00e9 de Bernonville","year":"2017","journal-title":"Scientific Reports"},{"key":"2023122122461522500_CIT0028","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.phytochem.2014.07.023","article-title":"Phytochemical genomics of the Madagascar periwinkle: unravelling the last twists of the alkaloid engine","volume":"113","author":"Dug\u00e9 de Bernonville","year":"2015","journal-title":"Phytochemistry"},{"key":"2023122122461522500_CIT0029","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1186\/s12864-015-1678-y","article-title":"Characterization of a second secologanin synthase isoform producing both secologanin and secoxyloganin allows enhanced de novo assembly of a Catharanthus roseus transcriptome","volume":"16","author":"Dug\u00e9 de Bernonville","year":"2015","journal-title":"BMC Genomics"},{"key":"2023122122461522500_CIT0030","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.tips.2019.12.006","article-title":"Identifying missing biosynthesis enzymes of plant natural products","volume":"41","author":"Dug\u00e9 de Bernonville","year":"2020","journal-title":"Trends in Pharmacological Sciences"},{"key":"2023122122461522500_CIT0031","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1093\/nar\/30.1.207","article-title":"Gene Expression Omnibus: NCBI gene expression and hybridization array data repository","volume":"30","author":"Edgar","year":"2002","journal-title":"Nucleic Acids Research"},{"key":"2023122122461522500_CIT0032","doi-asserted-by":"crossref","first-page":"2841","DOI":"10.1093\/jxb\/erq458","article-title":"Phenolic compounds and class III peroxidase in leaf vacuoles\u2014an H2O2 affair","volume":"62","author":"Ferreres","year":"2011","journal-title":"Journal of Experimental Botany"},{"key":"2023122122461522500_CIT0033","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1007\/BF01248877","article-title":"Plant idioblasts\u2014remarkable examples of cell specialization","volume":"46","author":"Foster","year":"1956","journal-title":"Protoplasma"},{"key":"2023122122461522500_CIT0034","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1002\/cbic.201800592","article-title":"Gene discovery in Gelsemium highlights conserved gene clusters in monoterpene indole alkaloid biosynthesis","volume":"20","author":"Franke","year":"2019","journal-title":"ChemBioChem"},{"key":"2023122122461522500_CIT0035","doi-asserted-by":"crossref","first-page":"110856","DOI":"10.1016\/j.plantsci.2021.110856","article-title":"Review: Biological functions of major latex-like proteins in plants","volume":"306","author":"Fujita","year":"2021","journal-title":"Plant Science"},{"key":"2023122122461522500_CIT0036","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00299-020-02599-9","article-title":"Membrane transporters: the key drivers of transport of secondary metabolites in plants","volume":"40","author":"Gani","year":"2020","journal-title":"Plant Cell Reports"},{"key":"2023122122461522500_CIT0037","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1007\/s00425-015-2446-6","article-title":"A novel cinnamyl alcohol dehydrogenase (CAD)-like reductase contributes to the structural diversity of monoterpenoid indole alkaloids in Rauvolfia","volume":"243","author":"Geissler","year":"2016","journal-title":"Planta"},{"key":"2023122122461522500_CIT0038","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1038\/nature11692","article-title":"An alternative route to cyclic terpenes by reductive cyclization in iridoid biosynthesis","volume":"492","author":"Geu-Flores","year":"2012","journal-title":"Nature"},{"key":"2023122122461522500_CIT0039","doi-asserted-by":"crossref","first-page":"17077","DOI":"10.3390\/ijms131217077","article-title":"Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores","volume":"13","author":"Glas","year":"2012","journal-title":"International Journal of Molecular Sciences"},{"key":"2023122122461522500_CIT0040","doi-asserted-by":"crossref","first-page":"e107117","DOI":"10.1371\/journal.pone.0107117","article-title":"Tomato ABSCISIC ACID STRESS RIPENING (ASR) gene family revisited","volume":"9","author":"Golan","year":"2014","journal-title":"PLoS One"},{"key":"2023122122461522500_CIT0041","doi-asserted-by":"crossref","first-page":"e52506","DOI":"10.1371\/journal.pone.0052506","article-title":"Development of transcriptomic resources for interrogating the biosynthesis of monoterpene indole alkaloids in medicinal plant species","volume":"7","author":"G\u00f3ngora-Castillo","year":"2012","journal-title":"PLoS One"},{"key":"2023122122461522500_CIT0042","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1007\/978-1-0716-2185-1_16","article-title":"Isolation of specialized plant cells by fluorescence-activated cell sorting","volume":"2469","author":"Guedes","year":"2022","journal-title":"Methods in Molecular Biology"},{"key":"2023122122461522500_CIT0043","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1186\/1471-2229-10-182","article-title":"Strictosidine activation in Apocynaceae: towards a \u2018nuclear time bomb?\u2019","volume":"10","author":"Guirimand","year":"2010","journal-title":"BMC Plant Biology"},{"key":"2023122122461522500_CIT0044","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1111\/j.1742-4658.2010.07994.x","article-title":"The subcellular organization of strictosidine biosynthesis in Catharanthus roseus epidermis highlights several trans-tonoplast translocations of intermediate metabolites","volume":"278","author":"Guirimand","year":"2011","journal-title":"The FEBS Journal"},{"key":"2023122122461522500_CIT0045","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1016\/j.jplph.2010.08.018","article-title":"Spatial organization of the vindoline biosynthetic pathway in Catharanthus roseus","volume":"168","author":"Guirimand","year":"2011","journal-title":"Journal of Plant Physiology"},{"key":"2023122122461522500_CIT0046","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1038\/nprot.2013.084","article-title":"De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis","volume":"8","author":"Haas","year":"2013","journal-title":"Nature Protocols"},{"key":"2023122122461522500_CIT0047","doi-asserted-by":"crossref","first-page":"20120426","DOI":"10.1098\/rstb.2012.0426","article-title":"Plant P450s as versatile drivers for evolution of species-specific chemical diversity","volume":"368","author":"Hamberger","year":"2013","journal-title":"Philosophical Transactions of the Royal Society B: Biological Sciences"},{"key":"2023122122461522500_CIT0048","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1111\/j.1365-313X.2000.00922.x","article-title":"Indole alkaloid biosynthesis in Catharanthus roseus: new enzyme activities and identification of cytochrome P450 CYP72A1 as secologanin synthase","volume":"24","author":"Irmler","year":"2000","journal-title":"The Plant Journal"},{"key":"2023122122461522500_CIT0049","doi-asserted-by":"crossref","first-page":"78","DOI":"10.3389\/fpls.2012.00078","article-title":"An expanding role for purine uptake permease-like transporters in plant secondary metabolism","volume":"3","author":"Jelesko","year":"2012","journal-title":"Frontiers in Plant Science"},{"key":"2023122122461522500_CIT0050","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1093\/pcp\/pcy235","article-title":"Roles of cytosolic glutamine synthetases in Arabidopsis development and stress responses","volume":"60","author":"Ji","year":"2019","journal-title":"Plant and Cell Physiology"},{"key":"2023122122461522500_CIT0051","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1186\/1471-2229-12-54","article-title":"Arabidopsis senescence-associated protein DMP1 is involved in membrane remodeling of the ER and tonoplast","volume":"12","author":"Kasaras","year":"2012","journal-title":"BMC Plant Biology"},{"key":"2023122122461522500_CIT0052","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1093\/molbev\/mst010","article-title":"MAFFT multiple sequence alignment software version 7: improvements in performance and usability","volume":"30","author":"Katoh","year":"2013","journal-title":"Molecular Biology and Evolution"},{"key":"2023122122461522500_CIT0053","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1111\/tpj.12827","article-title":"Genome-guided investigation of plant natural product biosynthesis","volume":"82","author":"Kellner","year":"2015","journal-title":"The Plant Journal"},{"key":"2023122122461522500_CIT0054","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1038\/s41587-019-0201-4","article-title":"Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype","volume":"37","author":"Kim","year":"2019","journal-title":"Nature Biotechnology"},{"key":"2023122122461522500_CIT0055","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1186\/s13059-019-1910-1","article-title":"Transcriptome assembly from long-read RNA-seq alignments with StringTie2","volume":"20","author":"Kovaka","year":"2019","journal-title":"Genome Biology"},{"key":"2023122122461522500_CIT0056","doi-asserted-by":"crossref","first-page":"102200","DOI":"10.1016\/j.pbi.2022.102200","article-title":"More than a Catharanthus plant: a multicellular and pluri-organelle alkaloid-producing factory","volume":"67","author":"Kulagina","year":"2022","journal-title":"Current Opinion in Plant Biology"},{"key":"2023122122461522500_CIT0057","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1186\/1471-2105-9-559","article-title":"WGCNA: an R package for weighted correlation network analysis","volume":"9","author":"Langfelder","year":"2008","journal-title":"BMC Bioinformatics"},{"key":"2023122122461522500_CIT0058","doi-asserted-by":"crossref","first-page":"1507","DOI":"10.1093\/pcp\/pcx097","article-title":"Identification of iridoid glucoside transporters in Catharanthus roseus","volume":"58","author":"Larsen","year":"2017","journal-title":"Plant and Cell Physiology"},{"key":"2023122122461522500_CIT0059","doi-asserted-by":"crossref","first-page":"2422","DOI":"10.1093\/molbev\/msx149","article-title":"SMS: smart model selection in PhyML","volume":"34","author":"Lefort","year":"2017","journal-title":"Molecular Biology and Evolution"},{"key":"2023122122461522500_CIT0060","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1038\/s41589-023-01327-0","article-title":"Single-cell multi-omics in the medicinal plant Catharanthus roseus","volume":"19","author":"Li","year":"2023","journal-title":"Nature Chemical Biology"},{"key":"2023122122461522500_CIT0061","doi-asserted-by":"crossref","first-page":"3094","DOI":"10.1093\/bioinformatics\/bty191","article-title":"Minimap2: pairwise alignment for nucleotide sequences","volume":"34","author":"Li","year":"2018","journal-title":"Bioinformatics"},{"key":"2023122122461522500_CIT0062","doi-asserted-by":"crossref","first-page":"1336","DOI":"10.1104\/pp.19.00489","article-title":"GATA and phytochrome interacting factor transcription factors regulate light-induced vindoline biosynthesis in Catharanthus roseus","volume":"180","author":"Liu","year":"2019","journal-title":"Plant Physiology"},{"key":"2023122122461522500_CIT0063","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biology"},{"key":"2023122122461522500_CIT0064","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1002\/prot.22396","article-title":"Structures of two Arabidopsis thaliana major latex proteins represent novel helix-grip folds","volume":"76","author":"Lytle","year":"2009","journal-title":"Proteins"},{"key":"2023122122461522500_CIT0065","doi-asserted-by":"crossref","first-page":"giy131","DOI":"10.1093\/gigascience\/giy131","article-title":"Efficient and accurate detection of splice junctions from RNA-seq with Portcullis","volume":"7","author":"Mapleson","year":"2018","journal-title":"GigaScience"},{"key":"2023122122461522500_CIT0066","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1139\/b86-141","article-title":"Differential distribution of specific indole alkaloids in leaves of Catharanthus roseus","volume":"64","author":"Mersey","year":"1986","journal-title":"Canadian Journal of Botany"},{"key":"2023122122461522500_CIT0067","doi-asserted-by":"crossref","first-page":"3606","DOI":"10.1038\/ncomms4606","article-title":"The seco-iridoid pathway from Catharanthus roseus","volume":"5","author":"Miettinen","year":"2014","journal-title":"Nature Communications"},{"key":"2023122122461522500_CIT0068","doi-asserted-by":"crossref","DOI":"10.1145\/2016741.2016785","article-title":"The CIPRES science gateway: a community resource for phylogenetic analyses","author":"Miller","year":"2011"},{"key":"2023122122461522500_CIT0069","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1111\/j.1365-313X.2005.02557.x","article-title":"Localization of tabersonine 16-hydroxylase and 16-OH tabersonine-16-O-methyltransferase to leaf epidermal cells defines them as a major site of precursor biosynthesis in the vindoline pathway in Catharanthus roseus","volume":"44","author":"Murata","year":"2005","journal-title":"The Plant Journal"},{"key":"2023122122461522500_CIT0070","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1105\/tpc.107.056630","article-title":"The leaf epidermome of Catharanthus roseus reveals its biochemical specialization","volume":"20","author":"Murata","year":"2008","journal-title":"The Plant Cell"},{"key":"2023122122461522500_CIT0071","doi-asserted-by":"crossref","first-page":"1451","DOI":"10.1016\/0031-9422(91)84184-T","article-title":"Growth related dimerization of vindoline and catharanthine in Catharanthus roseus and effect of wounding on the process","volume":"30","author":"Naaranlahti","year":"1991","journal-title":"Phytochemistry"},{"key":"2023122122461522500_CIT0072","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1104\/pp.79.2.499","article-title":"Identification and characterization of latex- specific proteins in opium poppy","volume":"79","author":"Nessler","year":"1985","journal-title":"Plant Physiology"},{"key":"2023122122461522500_CIT0073","doi-asserted-by":"crossref","first-page":"15059","DOI":"10.1038\/s41598-018-33415-w","article-title":"Expression analysis of cell wall invertase under abiotic stress conditions influencing specialized metabolism in Catharanthus roseus","volume":"8","author":"Nishanth","year":"2018","journal-title":"Scientific Reports"},{"key":"2023122122461522500_CIT0074","doi-asserted-by":"crossref","first-page":"1939","DOI":"10.1104\/pp.105.064352","article-title":"Characterization of vacuolar transport of the endogenous alkaloid berberine in Coptis japonica","volume":"138","author":"Otani","year":"2005","journal-title":"Plant Physiology"},{"key":"2023122122461522500_CIT0075","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.jchromb.2016.01.034","article-title":"A simple and rapid HPLC-DAD method for simultaneously monitoring the accumulation of alkaloids and precursors in different parts and different developmental stages of Catharanthus roseus plants","volume":"1014","author":"Pan","year":"2016","journal-title":"Journal of Chromatography. B. Analytical Technologies in the Biomedical and Life Sciences"},{"key":"2023122122461522500_CIT0076","doi-asserted-by":"crossref","first-page":"931","DOI":"10.3389\/fpls.2019.00931","article-title":"CrERF5, an AP2\/erf transcription factor, positively regulates the biosynthesis of bisindole alkaloids and their precursors in Catharanthus roseus","volume":"10","author":"Pan","year":"2019","journal-title":"Frontiers in Plant Science"},{"key":"2023122122461522500_CIT0077","doi-asserted-by":"crossref","first-page":"1566","DOI":"10.1111\/nph.14910","article-title":"A network of jasmonate-responsive bHLH factors modulate monoterpenoid indole alkaloid biosynthesis in Catharanthus roseus","volume":"217","author":"Patra","year":"2018","journal-title":"New Phytologist"},{"key":"2023122122461522500_CIT0078","doi-asserted-by":"crossref","first-page":"16208","DOI":"10.1038\/nplants.2016.208","article-title":"An NPF transporter exports a central monoterpene indole alkaloid intermediate from the vacuole","volume":"3","author":"Payne","year":"2017","journal-title":"Nature Plants"},{"key":"2023122122461522500_CIT0079","doi-asserted-by":"crossref","first-page":"304","DOI":"10.12688\/f1000research.23297.1","article-title":"GFF Utilities: GffRead and GffCompare","volume":"9","author":"Pertea","year":"2020","journal-title":"F1000Research"},{"key":"2023122122461522500_CIT0080","doi-asserted-by":"crossref","first-page":"1096","DOI":"10.1038\/nmeth.2639","article-title":"Smart-seq2 for sensitive full-length transcriptome profiling in single cells","volume":"10","author":"Picelli","year":"2013","journal-title":"Nature Methods"},{"key":"2023122122461522500_CIT0081","doi-asserted-by":"crossref","first-page":"6224","DOI":"10.1073\/pnas.1501821112","article-title":"Completion of the seven-step pathway from tabersonine to the anticancer drug precursor vindoline and its assembly in yeast","volume":"112","author":"Qu","year":"2015","journal-title":"Proceedings of the National Academy of Sciences, USA"},{"key":"2023122122461522500_CIT0082","doi-asserted-by":"crossref","first-page":"3180","DOI":"10.1073\/pnas.1719979115","article-title":"Solution of the multistep pathway for assembly of corynanthean, strychnos, iboga, and aspidosperma monoterpenoid indole alkaloids from 19E-geissoschizine","volume":"115","author":"Qu","year":"2018","journal-title":"Proceedings of the National Academy of Sciences, USA"},{"key":"2023122122461522500_CIT0083","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1111\/tpj.14111","article-title":"Completion of the canonical pathway for assembly of anticancer drugs vincristine\/vinblastine in Catharanthus roseus","volume":"97","author":"Qu","year":"2019","journal-title":"The Plant Journal"},{"key":"2023122122461522500_CIT0084","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1007\/s00425-017-2812-7","article-title":"Geissoschizine synthase controls flux in the formation of monoterpenoid indole alkaloids in a Catharanthus roseus mutant","volume":"247","author":"Qu","year":"2018","journal-title":"Planta"},{"key":"2023122122461522500_CIT0085","doi-asserted-by":"crossref","first-page":"W116","DOI":"10.1093\/nar\/gki442","article-title":"InterProScan: protein domains identifier","volume":"33","author":"Quevillon","year":"2005","journal-title":"Nucleic Acids Research"},{"key":"2023122122461522500_CIT0086","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1895\/wormbook.1.67.2","article-title":"Small GTPases","volume":"2018","author":"Reiner","year":"2018","journal-title":"WormBook"},{"key":"2023122122461522500_CIT0087","doi-asserted-by":"crossref","first-page":"15287","DOI":"10.1073\/pnas.0911451107","article-title":"Vinca drug components accumulate exclusively in leaf exudates of Madagascar periwinkle","volume":"107","author":"Roepke","year":"2010","journal-title":"Proceedings of the National Academy of Sciences, USA"},{"key":"2023122122461522500_CIT0088","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.ymben.2018.05.016","article-title":"An engineered combinatorial module of transcription factors boosts production of monoterpenoid indole alkaloids in Catharanthus roseus","volume":"48","author":"Schweizer","year":"2018","journal-title":"Metabolic Engineering"},{"key":"2023122122461522500_CIT0089","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1007\/978-1-4939-9173-0_14","article-title":"BUSCO: assessing genome assembly and annotation completeness","volume":"1962","author":"Seppey","year":"2019","journal-title":"Methods in Molecular Biology"},{"key":"2023122122461522500_CIT0090","first-page":"1309","article-title":"Specialized vacuoles of myrosin cells: chemical defense strategy in Brassicales plants","volume":"59","author":"Shirakawa","year":"2018","journal-title":"Plant and Cell Physiology"},{"key":"2023122122461522500_CIT0091","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1073\/pnas.0134257100","article-title":"Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica","volume":"100","author":"Shitan","year":"2003","journal-title":"Proceedings of the National Academy of Sciences, USA"},{"key":"2023122122461522500_CIT0092","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.phytochem.2012.02.012","article-title":"Characterization of Coptis japonica CjABCB2, an ATP-binding cassette protein involved in alkaloid transport","volume":"91","author":"Shitan","year":"2013","journal-title":"Phytochemistry"},{"key":"2023122122461522500_CIT0093","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1104\/pp.108.132811","article-title":"Multidrug and toxic compound extrusion-type transporters implicated in vacuolar sequestration of nicotine in tobacco roots","volume":"149","author":"Shoji","year":"2009","journal-title":"Plant Physiology"},{"key":"2023122122461522500_CIT0094","doi-asserted-by":"crossref","first-page":"1521","DOI":"10.12688\/f1000research.7563.1","article-title":"Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences","volume":"4","author":"Soneson","year":"2015","journal-title":"F1000Research"},{"key":"2023122122461522500_CIT0095","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/S0014-5793(98)00551-1","article-title":"Purification and characterization of alpha-3',4'-anhydrovinblastine synthase (peroxidase-like) from Catharanthus roseus (L.) G. Don","volume":"428","author":"Sottomayor","year":"1998","journal-title":"FEBS Letters"},{"key":"2023122122461522500_CIT0096","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1093\/bioinformatics\/btu033","article-title":"RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies","volume":"30","author":"Stamatakis","year":"2014","journal-title":"Bioinformatics"},{"key":"2023122122461522500_CIT0097","doi-asserted-by":"crossref","first-page":"12116","DOI":"10.1038\/ncomms12116","article-title":"Structural investigation of heteroyohimbine alkaloid synthesis reveals active site elements that control stereoselectivity","volume":"7","author":"Stavrinides","year":"2016","journal-title":"Nature Communications"},{"key":"2023122122461522500_CIT0098","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1016\/j.chembiol.2015.02.006","article-title":"Unlocking the diversity of alkaloids in Catharanthus roseus: nuclear localization suggests metabolic channeling in secondary metabolism","volume":"22","author":"Stavrinides","year":"2015","journal-title":"Chemistry & Biology"},{"key":"2023122122461522500_CIT0099","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1105\/tpc.11.5.887","article-title":"Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate","volume":"11","author":"St-Pierre","year":"1999","journal-title":"The Plant Cell"},{"key":"2023122122461522500_CIT0100","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1104\/pp.121.1.1","article-title":"Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning","volume":"121","author":"Sturm","year":"1999","journal-title":"Plant Physiology"},{"key":"2023122122461522500_CIT0101","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1038\/s41477-022-01291-y","article-title":"Single-cell RNA sequencing provides a high-resolution roadmap for understanding the multicellular compartmentation of specialized metabolism","volume":"9","author":"Sun","year":"2023","journal-title":"Nature Plants"},{"key":"2023122122461522500_CIT0102","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/s10725-008-9320-5","article-title":"Variations of vinblastine accumulation and redox state affected by exogenous H2O2 in Catharanthus roseus (L.) G. Don","volume":"57","author":"Tang","year":"2009","journal-title":"Plant Growth Regulators"},{"key":"2023122122461522500_CIT0103","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1038\/s41467-017-00154-x","article-title":"A three enzyme system to generate the Strychnos alkaloid scaffold from a central biosynthetic intermediate","volume":"8","author":"Tatsis","year":"2017","journal-title":"Nature Communications"},{"key":"2023122122461522500_CIT0104","doi-asserted-by":"crossref","first-page":"W84","DOI":"10.1093\/nar\/gky350","article-title":"PANNZER2: a rapid functional annotation web server","volume":"46","author":"Toronen","year":"2018","journal-title":"Nucleic Acids Research"},{"key":"2023122122461522500_CIT0105","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1007\/s10265-022-01380-1","article-title":"Differential regulation of fluorescent alkaloid metabolism between idioblast and lacticifer cells during leaf development in Catharanthus roseus seedlings","volume":"135","author":"Uzaki","year":"2022","journal-title":"Journal of Plant Research"},{"key":"2023122122461522500_CIT0106","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1104\/pp.111.189514","article-title":"Dissecting plant genomes with the PLAZA comparative genomics platform","volume":"158","author":"Van Bel","year":"2012","journal-title":"Plant Physiology"},{"key":"2023122122461522500_CIT0107","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1093\/pcp\/pct039","article-title":"CathaCyc, a metabolic pathway database built from Catharanthus roseus RNA-Seq data","volume":"54","author":"Van Moerkercke","year":"2013","journal-title":"Plant and Cell Physiology"},{"key":"2023122122461522500_CIT0108","doi-asserted-by":"crossref","first-page":"giy093","DOI":"10.1093\/gigascience\/giy093","article-title":"Leveraging multiple transcriptome assembly methods for improved gene structure annotation","volume":"7","author":"Venturini","year":"2018","journal-title":"GigaScience"},{"key":"2023122122461522500_CIT0109","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1111\/nph.16138","article-title":"The complexity of intercellular localisation of alkaloids revealed by single-cell metabolomics","volume":"224","author":"Yamamoto","year":"2019","journal-title":"New Phytologist"},{"key":"2023122122461522500_CIT0110","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.1002\/j.1537-2197.1976.tb13202.x","article-title":"Reactions of alkaloid and histochemical indicators in laticifers and specialized parenchyma cells of Catharanthus roseus (Apocynaceae)","volume":"63","author":"Yoder","year":"1976","journal-title":"American Journal of Botany"},{"key":"2023122122461522500_CIT0111","doi-asserted-by":"crossref","first-page":"15830","DOI":"10.1073\/pnas.1307504110","article-title":"ATP-binding cassette transporter controls leaf surface secretion of anticancer drug components in Catharanthus roseus","volume":"110","author":"Yu","year":"2013","journal-title":"Proceedings of the National Academy of Sciences, USA"},{"key":"2023122122461522500_CIT0112","doi-asserted-by":"crossref","first-page":"4619","DOI":"10.1093\/jxb\/erz203","article-title":"Research advances in cytochrome P450-catalysed pharmaceutical terpenoid biosynthesis in plants","volume":"70","author":"Zheng","year":"2019","journal-title":"Journal of Experimental Botany"}],"container-title":["Journal of Experimental Botany"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jxb\/advance-article-pdf\/doi\/10.1093\/jxb\/erad374\/53402524\/erad374.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jxb\/article-pdf\/75\/1\/274\/54732029\/erad374.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jxb\/article-pdf\/75\/1\/274\/54732029\/erad374.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,30]],"date-time":"2024-10-30T07:54:10Z","timestamp":1730274850000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jxb\/article\/75\/1\/274\/7297638"}},"subtitle":[],"editor":[{"given":"Sonia","family":"Osorio","sequence":"additional","affiliation":[{"name":"University of Malaga , Spain"}]}],"short-title":[],"issued":{"date-parts":[[2023,10,7]]},"references-count":112,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,10,7]]},"published-print":{"date-parts":[[2024,1,1]]}},"URL":"https:\/\/doi.org\/10.1093\/jxb\/erad374","relation":{},"ISSN":["0022-0957","1460-2431"],"issn-type":[{"value":"0022-0957","type":"print"},{"value":"1460-2431","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024,1,1]]},"published":{"date-parts":[[2023,10,7]]}}}