{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,3]],"date-time":"2026-05-03T02:09:52Z","timestamp":1777774192993,"version":"3.51.4"},"reference-count":87,"publisher":"Public Library of Science (PLoS)","issue":"4","license":[{"start":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T00:00:00Z","timestamp":1777420800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100010663","name":"H2020 European Research Council","doi-asserted-by":"publisher","award":["810131"],"award-info":[{"award-number":["810131"]}],"id":[{"id":"10.13039\/100010663","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["433194101"],"award-info":[{"award-number":["433194101"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Dr. Elisabeth Appuhn-Stiftung","award":["\/"],"award-info":[{"award-number":["\/"]}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>\n                    In plants, long-distance transport and phloem-mediated signal distribution play crucial roles in regulating stress adaptation and development. Phloem sap contains various types of RNAs, including small RNAs (sRNAs), messenger RNAs (mRNAs), and long noncoding RNAs (lncRNAs). Recently, endogenous circular RNAs have been identified in phloem sap of apple trees. Some phloem RNAs have been shown to have long-distance signaling functions, but for most, no functions have yet been determined. Due to their stability, circRNAs are interesting candidates with potential functions in long-distance signaling. Therefore, we aimed to characterize the circRNA content in the phloem sap of the crop plant\n                    <jats:italic>Brassica napus<\/jats:italic>\n                    . To achieve this, we performed Illumina sequencing of rRNA-depleted, circRNA-enriched, and sRNA libraries. The analysis revealed 1,734 distinct circRNAs in the phloem sap of\n                    <jats:italic>B. napus<\/jats:italic>\n                    . Of these, we validated ten circRNAs by PCR amplification and Sanger sequencing of their back-splicing junctions (BSJs). Using circ-Panel Nanopore sequencing, we investigated the full-length sequences of 14 circRNAs from phloem sap and leaf samples, identifying seven high-confidence candidates that exhibit potential intron retention and isoform variation across the two tissues. The investigation of potential interaction partners from phloem circRNA identified miRNA target sites on multiple circRNAs, particularly for known phloem-mobile miRNAs like miR156, miR169, and miR395. With Microscale Thermophoresis (MST), we were able to show the ability of the abundant RNA-binding protein BnGRP7 to bind the phloem circRNA circBnaANL2(7,8) with a dissociation constant of around 1 \u00b5M, raising questions about the involvement of RBPs in circRNA transport, stabilization, and function in phloem sap.\n                  <\/jats:p>","DOI":"10.1371\/journal.pone.0347473","type":"journal-article","created":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T17:38:45Z","timestamp":1777484325000},"page":"e0347473","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Characterizing the circular RNA landscape in phloem sap of Brassica napus"],"prefix":"10.1371","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0009-0008-8741-958X","authenticated-orcid":true,"given":"Kim Lara","family":"L\u00fchmann","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9086-5459","authenticated-orcid":true,"given":"Zs\u00f3fia","family":"Fekete","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rita","family":"Fernandes","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Julia","family":"Kehr","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2026,4,29]]},"reference":[{"issue":"2","key":"pone.0347473.ref001","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1007\/BF00391189","article-title":"Determination of phytohormones in phloem exudate from tree species by radioimmunoassay","volume":"152","author":"EW Weiler","year":"1981","journal-title":"Planta"},{"issue":"12","key":"pone.0347473.ref002","doi-asserted-by":"crossref","first-page":"1795","DOI":"10.1016\/j.phytochem.2004.04.006","article-title":"Proteomics of curcurbit phloem exudate reveals a network of defence proteins","volume":"65","author":"C Walz","year":"2004","journal-title":"Phytochemistry"},{"issue":"2","key":"pone.0347473.ref003","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1074\/mcp.M800420-MCP200","article-title":"Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function","volume":"8","author":"M-K Lin","year":"2009","journal-title":"Mol Cell Proteomics"},{"issue":"3","key":"pone.0347473.ref004","doi-asserted-by":"crossref","first-page":"896","DOI":"10.1002\/pmic.200500155","article-title":"Towards the proteome of Brassica napus phloem sap","volume":"6","author":"P Giavalisco","year":"2006","journal-title":"Proteomics"},{"issue":"5","key":"pone.0347473.ref005","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1111\/j.1365-313X.2007.03368.x","article-title":"Identification and characterization of small RNAs from the phloem of Brassica napus","volume":"53","author":"A Buhtz","year":"2008","journal-title":"Plant J"},{"issue":"12","key":"pone.0347473.ref006","doi-asserted-by":"crossref","first-page":"3183","DOI":"10.1093\/jxb\/erl082","article-title":"A phloem-enriched cDNA library from Ricinus: insights into phloem function","volume":"57","author":"C Doering-Saad","year":"2006","journal-title":"J Exp Bot"},{"key":"pone.0347473.ref007","doi-asserted-by":"crossref","first-page":"257","DOI":"10.3389\/fpls.2013.00257","article-title":"Phloem-mobile messenger RNAs and root development","volume":"4","author":"DJ Hannapel","year":"2013","journal-title":"Front Plant Sci"},{"issue":"1","key":"pone.0347473.ref008","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1093\/jxb\/erm176","article-title":"Long distance transport and movement of RNA through the phloem","volume":"59","author":"J Kehr","year":"2008","journal-title":"J Exp Bot"},{"issue":"1","key":"pone.0347473.ref009","doi-asserted-by":"crossref","DOI":"10.1146\/annurev-arplant-070121-033601","article-title":"Long-Distance Transported RNAs: From Identity to Function","volume":"73","author":"J Kehr","year":"2022","journal-title":"Annu Rev Plant Biol"},{"issue":"1","key":"pone.0347473.ref010","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1104\/pp.108.134767","article-title":"The phloem-delivered RNA pool contains small noncoding RNAs and interferes with translation","volume":"150","author":"S Zhang","year":"2009","journal-title":"Plant Physiol"},{"issue":"7","key":"pone.0347473.ref011","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1007\/BF02878295","article-title":"Development and structure of the phloem tissue","volume":"5","author":"K Esau","year":"1939","journal-title":"Bot Rev"},{"issue":"1","key":"pone.0347473.ref012","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1146\/annurev.pp.32.060181.002341","article-title":"Phloem Structure and Function","volume":"32","author":"J Cronshaw","year":"1981","journal-title":"Annu Rev Plant Physiol"},{"key":"pone.0347473.ref013","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1186\/1471-2229-10-64","article-title":"Phloem small RNAs, nutrient stress responses, and systemic mobility","volume":"10","author":"A Buhtz","year":"2010","journal-title":"BMC Plant Biol"},{"issue":"8","key":"pone.0347473.ref014","doi-asserted-by":"crossref","first-page":"1979","DOI":"10.1105\/tpc.104.023614","article-title":"A systemic small RNA signaling system in plants","volume":"16","author":"B-C Yoo","year":"2004","journal-title":"Plant Cell"},{"key":"pone.0347473.ref015","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1186\/1471-2229-10-159","article-title":"Characterisation of microRNAs from apple (Malus domestica \u2019Royal Gala\u2019) vascular tissue and phloem sap","volume":"10","author":"E Varkonyi-Gasic","year":"2010","journal-title":"BMC Plant Biol"},{"issue":"15","key":"pone.0347473.ref016","doi-asserted-by":"crossref","first-page":"2782","DOI":"10.3390\/plants12152782","article-title":"The Small RNA Component of Arabidopsis thaliana Phloem Sap and Its Response to Iron Deficiency","volume":"12","author":"A Bakirbas","year":"2023","journal-title":"Plants"},{"issue":"8","key":"pone.0347473.ref017","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1093\/oxfordjournals.pcp.a029451","article-title":"Detection of several mRNA species in rice phloem sap","volume":"39","author":"T Sasaki","year":"1998","journal-title":"Plant Cell Physiol"},{"issue":"13","key":"pone.0347473.ref018","doi-asserted-by":"crossref","first-page":"3645","DOI":"10.1093\/jxb\/erm214","article-title":"Characterization of phloem-sap transcription profile in melon plants","volume":"58","author":"A Omid","year":"2007","journal-title":"J Exp Bot"},{"issue":"5","key":"pone.0347473.ref019","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1111\/j.1365-313X.2007.03363.x","article-title":"MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis","volume":"53","author":"BD Pant","year":"2008","journal-title":"Plant J"},{"issue":"6","key":"pone.0347473.ref020","first-page":"1046","article-title":"MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana","volume":"62","author":"G Liang","year":"2010","journal-title":"Plant J"},{"issue":"3","key":"pone.0347473.ref021","doi-asserted-by":"crossref","first-page":"1541","DOI":"10.1104\/pp.109.139139","article-title":"Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing","volume":"150","author":"BD Pant","year":"2009","journal-title":"Plant Physiol"},{"issue":"12","key":"pone.0347473.ref022","doi-asserted-by":"crossref","first-page":"3443","DOI":"10.1105\/tpc.106.042473","article-title":"Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway","volume":"18","author":"AK Banerjee","year":"2006","journal-title":"Plant Cell"},{"issue":"1","key":"pone.0347473.ref023","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1111\/j.1365-313X.2005.02351.x","article-title":"Phloem long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development","volume":"42","author":"V Haywood","year":"2005","journal-title":"Plant J"},{"issue":"11","key":"pone.0347473.ref024","doi-asserted-by":"crossref","first-page":"3852","DOI":"10.1073\/pnas.73.11.3852","article-title":"Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures","volume":"73","author":"HL Sanger","year":"1976","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"2","key":"pone.0347473.ref025","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1261\/rna.035667.112","article-title":"Circular RNAs are abundant, conserved, and associated with ALU repeats","volume":"19","author":"WR Jeck","year":"2013","journal-title":"RNA"},{"issue":"1","key":"pone.0347473.ref026","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1016\/j.cell.2014.09.001","article-title":"Complementary sequence-mediated exon circularization","volume":"159","author":"X-O Zhang","year":"2014","journal-title":"Cell"},{"issue":"7","key":"pone.0347473.ref027","doi-asserted-by":"crossref","first-page":"485","DOI":"10.2174\/1389202922666210331130722","article-title":"A Brief Review of circRNA Biogenesis, Detection, and Function","volume":"22","author":"Y Liang","year":"2021","journal-title":"Curr Genomics"},{"issue":"1","key":"pone.0347473.ref028","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/0042-6822(87)90260-1","article-title":"Potato spindle tuber viroid: Investigation of the long-distance, intra-plant transport route","volume":"158","author":"P Palukaitis","year":"1987","journal-title":"Virology"},{"issue":"1","key":"pone.0347473.ref029","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1006\/viro.2000.0724","article-title":"Cellular basis of potato spindle tuber viroid systemic movement","volume":"279","author":"Y Zhu","year":"2001","journal-title":"Virology"},{"issue":"1","key":"pone.0347473.ref030","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1111\/nph.13585","article-title":"Widespread noncoding circular RNAs in plants","volume":"208","author":"C-Y Ye","year":"2015","journal-title":"New Phytol"},{"issue":"12","key":"pone.0347473.ref031","doi-asserted-by":"crossref","first-page":"2076","DOI":"10.1261\/rna.052282.115","article-title":"Transcriptome-wide investigation of circular RNAs in rice","volume":"21","author":"T Lu","year":"2015","journal-title":"RNA"},{"issue":"2","key":"pone.0347473.ref032","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.bbrc.2016.07.032","article-title":"Deciphering the roles of circRNAs on chilling injury in tomato","volume":"479","author":"J Zuo","year":"2016","journal-title":"Biochem Biophys Res Commun"},{"key":"pone.0347473.ref033","doi-asserted-by":"crossref","first-page":"776","DOI":"10.3389\/fpls.2016.00776","article-title":"Identification of Circular RNAs from the Parental Genes Involved in Multiple Aspects of Cellular Metabolism in Barley","volume":"7","author":"B Darbani","year":"2016","journal-title":"Front Plant Sci"},{"issue":"4","key":"pone.0347473.ref034","doi-asserted-by":"crossref","first-page":"712","DOI":"10.3390\/genes13040712","article-title":"Expression Characteristics in Roots, Phloem, Leaves, Flowers and Fruits of Apple circRNA","volume":"13","author":"D Wang","year":"2022","journal-title":"Genes (Basel)"},{"issue":"7441","key":"pone.0347473.ref035","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1038\/nature11993","article-title":"Natural RNA circles function as efficient microRNA sponges","volume":"495","author":"TB Hansen","year":"2013","journal-title":"Nature"},{"issue":"4","key":"pone.0347473.ref036","article-title":"The circular RNA circANK suppresses rice resistance to bacterial blight by inhibiting microRNA398b-mediated defense","volume":"37","author":"X Liu","year":"2025","journal-title":"Plant Cell"},{"issue":"6","key":"pone.0347473.ref037","doi-asserted-by":"crossref","first-page":"2846","DOI":"10.1093\/nar\/gkw027","article-title":"Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2","volume":"44","author":"WW Du","year":"2016","journal-title":"Nucleic Acids Res"},{"key":"pone.0347473.ref038","doi-asserted-by":"crossref","first-page":"17053","DOI":"10.1038\/nplants.2017.53","article-title":"A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation","volume":"3","author":"VM Conn","year":"2017","journal-title":"Nat Plants"},{"issue":"4","key":"pone.0347473.ref039","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1111\/tpj.14267","article-title":"A large-scale circular RNA profiling reveals universal molecular mechanisms responsive to drought stress in maize and Arabidopsis","volume":"98","author":"P Zhang","year":"2019","journal-title":"Plant J"},{"issue":"1","key":"pone.0347473.ref040","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1186\/s12870-019-1712-3","article-title":"Identification of cucumber circular RNAs responsive to salt stress","volume":"19","author":"Y-X Zhu","year":"2019","journal-title":"BMC Plant Biol"},{"issue":"3","key":"pone.0347473.ref041","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1007\/s11103-017-0684-7","article-title":"Heat stress alters genome-wide profiles of circular RNAs in Arabidopsis","volume":"96","author":"T Pan","year":"2018","journal-title":"Plant Mol Biol"},{"issue":"2","key":"pone.0347473.ref042","doi-asserted-by":"crossref","first-page":"966","DOI":"10.1104\/pp.18.01331","article-title":"Characterization and Cloning of Grape Circular RNAs Identified the Cold Resistance-Related Vv-circATS1","volume":"180","author":"Z Gao","year":"2019","journal-title":"Plant Physiol"},{"issue":"19","key":"pone.0347473.ref043","doi-asserted-by":"crossref","first-page":"10297","DOI":"10.3390\/ijms221910297","article-title":"Circular RNAs Repertoire and Expression Profile during Brassica rapa Pollen Development","volume":"22","author":"S Babaei","year":"2021","journal-title":"Int J Mol Sci"},{"issue":"131","key":"pone.0347473.ref044","first-page":"57097","article-title":"Phloem Sap Sampling from Brassica napus for 3D-PAGE of Protein and Ribonucleoprotein Complexes","author":"S Pahlow","year":"2018","journal-title":"J Vis Exp"},{"issue":"7","key":"pone.0347473.ref045","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1007\/s00122-024-04678-x","article-title":"Comparative genome-wide analysis of circular RNAs in Brassica napus L.: target-site versus non-target-site resistance to herbicide stress","volume":"137","author":"Y Guo","year":"2024","journal-title":"Theor Appl Genet"},{"key":"pone.0347473.ref046","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.gene.2018.05.014","article-title":"Genome-wide identification, characterization and expression analysis of long non-coding RNAs in different tissues of apple","volume":"666","author":"N An","year":"2018","journal-title":"Gene"},{"issue":"8","key":"pone.0347473.ref047","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1038\/s41592-023-01944-6","article-title":"Large-scale benchmarking of circRNA detection tools reveals large differences in sensitivity but not in precision","volume":"20","author":"M Vromman","year":"2023","journal-title":"Nat Methods"},{"issue":"10","key":"pone.0347473.ref048","doi-asserted-by":"crossref","first-page":"1208","DOI":"10.1038\/s41592-022-01487-2","article-title":"Best practice standards for circular RNA research","volume":"19","author":"AF Nielsen","year":"2022","journal-title":"Nat Methods"},{"issue":"1","key":"pone.0347473.ref049","doi-asserted-by":"crossref","DOI":"10.1093\/bib\/bbac612","article-title":"Systematic benchmarking of statistical methods to assess differential expression of circular RNAs","volume":"24","author":"A Buratin","year":"2023","journal-title":"Brief Bioinform"},{"issue":"1","key":"pone.0347473.ref050","doi-asserted-by":"crossref","first-page":"4825","DOI":"10.1038\/s41467-021-24975-z","article-title":"Nanopore sequencing of brain-derived full-length circRNAs reveals circRNA-specific exon usage, intron retention and microexons","volume":"12","author":"K Rahimi","year":"2021","journal-title":"Nat Commun"},{"issue":"6","key":"pone.0347473.ref051","doi-asserted-by":"crossref","first-page":"1795","DOI":"10.1038\/s41596-023-00815-w","article-title":"Full-length circular RNA profiling by nanopore sequencing with CIRI-long","volume":"18","author":"L Hou","year":"2023","journal-title":"Nat Protoc"},{"issue":"2","key":"pone.0347473.ref052","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1093\/bib\/bbs017","article-title":"Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration","volume":"14","author":"H Thorvaldsd\u00f3ttir","year":"2013","journal-title":"Brief Bioinform"},{"issue":"1","key":"pone.0347473.ref053","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1038\/nbt.1754","article-title":"Integrative genomics viewer","volume":"29","author":"JT Robinson","year":"2011","journal-title":"Nat Biotechnol"},{"issue":"8","key":"pone.0347473.ref054","doi-asserted-by":"crossref","first-page":"2628","DOI":"10.1093\/bioinformatics\/btz931","article-title":"ShinyGO: a graphical gene-set enrichment tool for animals and plants","volume":"36","author":"SX Ge","year":"2020","journal-title":"Bioinformatics"},{"key":"pone.0347473.ref055","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1007\/978-1-60327-005-2_4","article-title":"miRNA Target Prediction in Plants.","volume-title":"Plant MicroRNAs: Methods and Protocols","author":"N Fahlgren","year":"2010"},{"key":"pone.0347473.ref056","article-title":"psRNATarget: a plant small RNA target analysis server (2017 release)","volume":"46","author":"X Dai","year":"2018","journal-title":"Nucleic Acids Res"},{"key":"pone.0347473.ref057","article-title":"psRNATarget: a plant small RNA target analysis server","volume":"39","author":"X Dai","year":"2011","journal-title":"Nucleic Acids Res"},{"issue":"2","key":"pone.0347473.ref058","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1093\/bib\/bbq065","article-title":"Computational analysis of miRNA targets in plants: current status and challenges","volume":"12","author":"X Dai","year":"2011","journal-title":"Brief Bioinform"},{"issue":"1","key":"pone.0347473.ref059","doi-asserted-by":"crossref","first-page":"16018","DOI":"10.1038\/s41598-024-66955-5","article-title":"The glycine-rich domain of GRP7 plays a crucial role in binding long RNAs and facilitating phase separation","volume":"14","author":"KL L\u00fchmann","year":"2024","journal-title":"Sci Rep"},{"issue":"13","key":"pone.0347473.ref060","doi-asserted-by":"crossref","first-page":"2326","DOI":"10.1093\/bioinformatics\/bty948","article-title":"circtools-a one-stop software solution for circular RNA research","volume":"35","author":"T Jakobi","year":"2019","journal-title":"Bioinformatics"},{"issue":"7","key":"pone.0347473.ref061","doi-asserted-by":"crossref","first-page":"1094","DOI":"10.1093\/bioinformatics\/btv656","article-title":"Specific identification and quantification of circular RNAs from sequencing data","volume":"32","author":"J Cheng","year":"2016","journal-title":"Bioinformatics"},{"issue":"5","key":"pone.0347473.ref062","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1093\/bib\/bbx014","article-title":"Circular RNA identification based on multiple seed matching","volume":"19","author":"Y Gao","year":"2018","journal-title":"Brief Bioinform"},{"issue":"6","key":"pone.0347473.ref063","first-page":"984","article-title":"Comprehensive characterization of tissue-specific circular RNAs in the human and mouse genomes","volume":"18","author":"S Xia","year":"2017","journal-title":"Brief Bioinform"},{"issue":"1","key":"pone.0347473.ref064","doi-asserted-by":"crossref","first-page":"14544","DOI":"10.1038\/s41598-019-51190-0","article-title":"Transcriptome-Wide Identification and Characterization of Circular RNAs in Leaves of Chinese Cabbage (Brassica rapa L. ssp. pekinensis) in Response to Calcium Deficiency-Induced Tip-burn","volume":"9","author":"W Wang","year":"2019","journal-title":"Sci Rep"},{"issue":"1","key":"pone.0347473.ref065","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1186\/s12870-023-04319-3","article-title":"Circular RNAs modulate the floral fate acquisition in soybean shoot apical meristem","volume":"23","author":"S Babaei","year":"2023","journal-title":"BMC Plant Biol"},{"issue":"2","key":"pone.0347473.ref066","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0030733","article-title":"Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types","volume":"7","author":"J Salzman","year":"2012","journal-title":"PLoS One"},{"issue":"4","key":"pone.0347473.ref067","doi-asserted-by":"crossref","first-page":"100343","DOI":"10.1016\/j.xplc.2022.100343","article-title":"PlantcircBase 7.0: Full-length transcripts and conservation of plant circRNAs","volume":"3","author":"X Xu","year":"2022","journal-title":"Plant Commun"},{"issue":"12","key":"pone.0347473.ref068","doi-asserted-by":"crossref","first-page":"1823","DOI":"10.1111\/jipb.13002","article-title":"Profiling of circular RNA N6 -methyladenosine in moso bamboo (Phyllostachys edulis) using nanopore-based direct RNA sequencing","volume":"62","author":"Y Wang","year":"2020","journal-title":"J Integr Plant Biol"},{"issue":"1","key":"pone.0347473.ref069","doi-asserted-by":"crossref","DOI":"10.1002\/tpg2.20429","article-title":"Long- and short-read sequencing methods discover distinct circular RNA pools in Lotus japonicus","volume":"17","author":"A Budnick","year":"2024","journal-title":"Plant Genome"},{"issue":"1","key":"pone.0347473.ref070","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1104\/pp.19.00716","article-title":"circRNAs Are Involved in the Rice-Magnaporthe oryzae Interaction","volume":"182","author":"J Fan","year":"2020","journal-title":"Plant Physiol"},{"issue":"1","key":"pone.0347473.ref071","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1186\/s13059-018-1462-9","article-title":"From squiggle to basepair: computational approaches for improving nanopore sequencing read accuracy","volume":"19","author":"FJ Rang","year":"2018","journal-title":"Genome Biol"},{"key":"pone.0347473.ref072","doi-asserted-by":"crossref","first-page":"591806","DOI":"10.3389\/fgene.2020.591806","article-title":"Genome-Wide Identification of Circular RNAs in Response to Low-Temperature Stress in Tomato Leaves","volume":"11","author":"X Yang","year":"2020","journal-title":"Front Genet"},{"key":"pone.0347473.ref073","doi-asserted-by":"crossref","first-page":"1678","DOI":"10.3389\/fpls.2017.01678","article-title":"Genome-Wide Identification of Circular RNAs in Arabidopsis thaliana","volume":"8","author":"G Chen","year":"2017","journal-title":"Front Plant Sci"},{"issue":"6","key":"pone.0347473.ref074","doi-asserted-by":"crossref","first-page":"1240","DOI":"10.1111\/pbi.13544","article-title":"Efficient deletion of multiple circle RNA loci by CRISPR-Cas9 reveals Os06circ02797 as a putative sponge for OsMIR408 in rice","volume":"19","author":"J Zhou","year":"2021","journal-title":"Plant Biotechnol J"},{"issue":"18","key":"pone.0347473.ref075","doi-asserted-by":"crossref","first-page":"10104","DOI":"10.1128\/JVI.78.18.10104-10110.2004","article-title":"A long-distance translocatable phloem protein from cucumber forms a ribonucleoprotein complex in vivo with Hop stunt viroid RNA","volume":"78","author":"G G\u00f3mez","year":"2004","journal-title":"J Virol"},{"issue":"12","key":"pone.0347473.ref076","doi-asserted-by":"crossref","first-page":"102631","DOI":"10.1016\/j.jbc.2022.102631","article-title":"Intrinsically disordered plant protein PARCL colocalizes with RNA in phase-separated condensates whose formation can be regulated by mutating the PLD","volume":"298","author":"A Ostendorp","year":"2022","journal-title":"J Biol Chem"},{"issue":"5","key":"pone.0347473.ref077","doi-asserted-by":"crossref","first-page":"1863","DOI":"10.1093\/plcell\/koac043","article-title":"Arabidopsis apoplastic fluid contains sRNA- and circular RNA-protein complexes that are located outside extracellular vesicles","volume":"34","author":"H Zand Karimi","year":"2022","journal-title":"Plant Cell"},{"issue":"3","key":"pone.0347473.ref078","doi-asserted-by":"crossref","DOI":"10.1186\/gb-2009-10-3-r25","article-title":"Ultrafast and memory-efficient alignment of short DNA sequences to the human genome","volume":"10","author":"B Langmead","year":"2009","journal-title":"Genome Biol"},{"issue":"4","key":"pone.0347473.ref079","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with Bowtie 2","volume":"9","author":"B Langmead","year":"2012","journal-title":"Nat Methods"},{"key":"pone.0347473.ref080","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1186\/1471-2105-13-140","article-title":"miREvo: an integrative microRNA evolutionary analysis platform for next-generation sequencing experiments","volume":"13","author":"M Wen","year":"2012","journal-title":"BMC Bioinformatics"},{"issue":"1","key":"pone.0347473.ref081","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1093\/nar\/gkr688","article-title":"miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades","volume":"40","author":"MR Friedl\u00e4nder","year":"2012","journal-title":"Nucleic Acids Res"},{"key":"pone.0347473.ref082","doi-asserted-by":"crossref","DOI":"10.1093\/nar\/gkn188","article-title":"The Vienna RNA websuite","volume":"36","author":"AR Gruber","year":"2008","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"pone.0347473.ref083","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1748-7188-6-26","article-title":"ViennaRNA Package 2.0","volume":"6","author":"R Lorenz","year":"2011","journal-title":"Algorithms Mol Biol"},{"issue":"1","key":"pone.0347473.ref084","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: ultrafast universal RNA-seq aligner","volume":"29","author":"A Dobin","year":"2013","journal-title":"Bioinformatics"},{"key":"pone.0347473.ref085","doi-asserted-by":"crossref","unstructured":"Md V, Misra S, Li H, Aluru S. Efficient architecture-aware acceleration of BWA-MEM for multicore systems. Proc - 2019 IEEE 33rd Int Parallel Distrib Process Symp IPDPS 2019. 2019. p. 314\u201324.","DOI":"10.1109\/IPDPS.2019.00041"},{"issue":"18","key":"pone.0347473.ref086","doi-asserted-by":"crossref","first-page":"3094","DOI":"10.1093\/bioinformatics\/bty191","article-title":"Minimap2: pairwise alignment for nucleotide sequences","volume":"34","author":"H Li","year":"2018","journal-title":"Bioinformatics"},{"issue":"6","key":"pone.0347473.ref087","doi-asserted-by":"crossref","DOI":"10.1093\/nar\/gkaa1256","article-title":"Characterizing and circumventing sequence restrictions for synthesis of circular RNA in vitro","volume":"49","author":"JW Rausch","year":"2021","journal-title":"Nucleic Acids Res"}],"container-title":["PLOS One"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0347473","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T17:39:05Z","timestamp":1777484345000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0347473"}},"subtitle":[],"editor":[{"given":"Xiaoyong","family":"Sun","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2026,4,29]]},"references-count":87,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2026,4,29]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0347473","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,4,29]]}}}