{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T03:29:12Z","timestamp":1777433352882,"version":"3.51.4"},"reference-count":88,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2021,1,7]],"date-time":"2021-01-07T00:00:00Z","timestamp":1609977600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"name":"National Science Foundation (SECRETome Project: Systematic Evaluation of CellulaR ExporT from plant cells","award":["IOS-1546879"],"award-info":[{"award-number":["IOS-1546879"]}]},{"name":"Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under","award":["390686111"],"award-info":[{"award-number":["390686111"]}]},{"name":"Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under","award":["SFB 1208\u2014Project-ID 267205415"],"award-info":[{"award-number":["SFB 1208\u2014Project-ID 267205415"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,5,5]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The leaf vasculature plays a key role in solute translocation. Veins consist of at least seven distinct cell types, with specific roles in transport, metabolism, and signaling. Little is known about leaf vascular cells, in particular the phloem parenchyma (PP). PP effluxes sucrose into the apoplasm as a basis for phloem loading, yet PP has been characterized only microscopically. Here, we enriched vascular cells from Arabidopsis leaves to generate a single-cell transcriptome atlas of leaf vasculature. We identified at least 19 cell clusters, encompassing epidermis, guard cells, hydathodes, mesophyll, and all vascular cell types, and used metabolic pathway analysis to define their roles. Clusters comprising PP cells were enriched for transporters, including SWEET11 and SWEET12 sucrose and UmamiT amino acid efflux carriers. We provide evidence that PP development occurs independently from ALTERED PHLOEM DEVELOPMENT, a transcription factor required for phloem differentiation. PP cells have a unique pattern of amino acid metabolism activity distinct from companion cells (CCs), explaining differential distribution\/metabolism of amino acids in veins. The kinship relation of the vascular clusters is strikingly similar to the vein morphology, except for a clear separation of CC from the other vascular cells including PP. In summary, our single-cell RNA-sequencing analysis provides a wide range of information into the leaf vasculature and the role and relationship of the leaf cell types.<\/jats:p>","DOI":"10.1093\/plcell\/koaa060","type":"journal-article","created":{"date-parts":[[2020,12,31]],"date-time":"2020-12-31T23:13:05Z","timestamp":1609456385000},"page":"511-530","source":"Crossref","is-referenced-by-count":331,"title":["Distinct identities of leaf phloem cells revealed by single cell transcriptomics"],"prefix":"10.1093","volume":"33","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2776-5970","authenticated-orcid":false,"given":"Ji-Yun","family":"Kim","sequence":"first","affiliation":[{"name":"Institute for Molecular Physiology and Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine-University D\u00fcsseldorf, D\u00fcsseldorf 40225, Germany"}]},{"given":"Efthymia","family":"Symeonidi","sequence":"additional","affiliation":[{"name":"Center for Plant Molecular Biology, University of T\u00fcbingen, T\u00fcbingen 72076, Germany"}]},{"given":"Tin Yau","family":"Pang","sequence":"additional","affiliation":[{"name":"Institute for Computer Science and Department of Biology, Heinrich-Heine-University D\u00fcsseldorf, D\u00fcsseldorf 40225, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7413-9855","authenticated-orcid":false,"given":"Tom","family":"Denyer","sequence":"additional","affiliation":[{"name":"Center for Plant Molecular Biology, University of T\u00fcbingen, T\u00fcbingen 72076, Germany"}]},{"given":"Diana","family":"Weidauer","sequence":"additional","affiliation":[{"name":"Institute for Molecular Physiology and Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine-University D\u00fcsseldorf, D\u00fcsseldorf 40225, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8009-3635","authenticated-orcid":false,"given":"Margaret","family":"Bezrutczyk","sequence":"additional","affiliation":[{"name":"Institute for Molecular Physiology and Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine-University D\u00fcsseldorf, D\u00fcsseldorf 40225, Germany"}]},{"given":"Manuel","family":"Miras","sequence":"additional","affiliation":[{"name":"Institute for Molecular Physiology and Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine-University D\u00fcsseldorf, D\u00fcsseldorf 40225, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0961-5680","authenticated-orcid":false,"given":"Nora","family":"Z\u00f6llner","sequence":"additional","affiliation":[{"name":"Institute for Molecular Physiology and Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine-University D\u00fcsseldorf, D\u00fcsseldorf 40225, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2707-2771","authenticated-orcid":false,"given":"Thomas","family":"Hartwig","sequence":"additional","affiliation":[{"name":"Institute for Molecular Physiology and Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine-University D\u00fcsseldorf, D\u00fcsseldorf 40225, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4332-369X","authenticated-orcid":false,"given":"Michael M","family":"Wudick","sequence":"additional","affiliation":[{"name":"Institute for Molecular Physiology and Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine-University D\u00fcsseldorf, D\u00fcsseldorf 40225, Germany"}]},{"given":"Martin","family":"Lercher","sequence":"additional","affiliation":[{"name":"Institute for Computer Science and Department of Biology, Heinrich-Heine-University D\u00fcsseldorf, D\u00fcsseldorf 40225, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0964-5388","authenticated-orcid":false,"given":"Li-Qing","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Plant Biology, School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1931-9209","authenticated-orcid":false,"given":"Marja C P","family":"Timmermans","sequence":"additional","affiliation":[{"name":"Center for Plant Molecular Biology, University of T\u00fcbingen, T\u00fcbingen 72076, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6465-0115","authenticated-orcid":false,"given":"Wolf B","family":"Frommer","sequence":"additional","affiliation":[{"name":"Institute for Molecular Physiology and Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine-University D\u00fcsseldorf, D\u00fcsseldorf 40225, Germany"},{"name":"Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Chikusa, Nagoya 464-8601, Japan"}]}],"member":"286","published-online":{"date-parts":[[2021,1,7]]},"reference":[{"key":"2021050612521209000_koaa060-B1","doi-asserted-by":"crossref","first-page":"102","DOI":"10.3389\/fpls.2013.00102","article-title":"Phloem parenchyma transfer cells in Arabidopsis - an experimental system to identify transcriptional regulators of wall ingrowth formation","volume":"4","author":"Arun Chinnappa","year":"2013","journal-title":"Front Plant Sci"},{"key":"2021050612521209000_koaa060-B2","first-page":"531","article-title":"Biochemical aspects of assimilate transfers along the phloem path: N-solutes in lupins","volume":"27","author":"Atkins","year":"2000","journal-title":"Austr J Plant Physiol"},{"key":"2021050612521209000_koaa060-B3","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1104\/pp.126.2.643","article-title":"The Arabidopsis ATHB-8 HD-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems","volume":"126","author":"Baima","year":"2001","journal-title":"Plant Physiol"},{"key":"2021050612521209000_koaa060-B4","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1071\/PP99172","article-title":"Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse","volume":"27","author":"van Bel","year":"2000","journal-title":"Funct Plant Biol"},{"key":"2021050612521209000_koaa060-B5","doi-asserted-by":"crossref","DOI":"10.1093\/plcell\/koaa055","article-title":"Evidence for phloem loading via the abaxial bundle sheath cells in maize leaves","volume":"33","author":"Bezrutczyk","year":"2021","journal-title":"The Plant Cell"},{"key":"2021050612521209000_koaa060-B6","doi-asserted-by":"crossref","first-page":"1956","DOI":"10.1126\/science.1090022","article-title":"A gene expression map of the Arabidopsis root","volume":"302","author":"Birnbaum","year":"2003","journal-title":"Science"},{"key":"2021050612521209000_koaa060-B7","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1038\/nature02100","article-title":"APL regulates vascular tissue identity in Arabidopsis","volume":"426","author":"Bonke","year":"2003","journal-title":"Nature"},{"key":"2021050612521209000_koaa060-B8","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1126\/science.1146265","article-title":"A high-resolution root spatiotemporal map reveals dominant expression patterns","volume":"318","author":"Brady","year":"2007","journal-title":"Science"},{"key":"2021050612521209000_koaa060-B9","doi-asserted-by":"crossref","first-page":"e47182","DOI":"10.15252\/embr.201847182","article-title":"Multiple C2 domains and transmembrane region proteins (MCTPs) tether membranes at plasmodesmata","volume":"20","author":"Brault","year":"2019","journal-title":"EMBO Rep"},{"key":"2021050612521209000_koaa060-B10","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1046\/j.1365-313X.2003.01700.x","article-title":"Transport of cytokinins mediated by purine transporters of the PUP family expressed in phloem, hydathodes, and pollen of Arabidopsis","volume":"34","author":"B\u00fcrkle","year":"2003","journal-title":"Plant J"},{"key":"2021050612521209000_koaa060-B11","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1038\/nbt.4096","article-title":"Integrating single-cell transcriptomic data across different conditions, technologies, and species","volume":"36","author":"Butler","year":"2018","journal-title":"Nat Biotech"},{"key":"2021050612521209000_koaa060-B12","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1007\/978-1-4939-9562-2_8","article-title":"Live-cell imaging of fluorescently tagged phloem proteins with confocal microscopy","volume":"2014","author":"Cayla","year":"2019","journal-title":"Methods Mol Biol"},{"key":"2021050612521209000_koaa060-B13","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1038\/nature09606","article-title":"Sugar transporters for intercellular exchange and nutrition of pathogens","volume":"468","author":"Chen","year":"2010","journal-title":"Nature"},{"key":"2021050612521209000_koaa060-B14","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1105\/tpc.114.134585","article-title":"A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis 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J"},{"key":"2021050612521209000_koaa060-B27","doi-asserted-by":"crossref","first-page":"13979","DOI":"10.1073\/pnas.250473797","article-title":"Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters","volume":"97","author":"Gottwald","year":"2000","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021050612521209000_koaa060-B28","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1016\/j.cub.2019.12.043","article-title":"A reservoir of pluripotent phloem cells safeguards the linear developmental trajectory of protophloem sieve elements","volume":"30","author":"Gujas","year":"2020","journal-title":"Curr Biol"},{"key":"2021050612521209000_koaa060-B29","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1186\/s13059-019-1874-1","article-title":"Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression","volume":"20","author":"Hafemeister","year":"2019","journal-title":"Genome 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brassinosteroid-responsive transcription factor BZR1 in Arabidopsis Roots","volume":"31","author":"Kim","year":"2019","journal-title":"Plant Cell"},{"key":"2021050612521209000_koaa060-B37","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1111\/j.1365-313X.2010.04339.x","article-title":"Glucosinolate-accumulating S-cells in Arabidopsis leaves and flower stalks undergo programmed cell death at early stages of differentiation","volume":"64","author":"Koroleva","year":"2010","journal-title":"Plant J"},{"key":"2021050612521209000_koaa060-B38","doi-asserted-by":"crossref","first-page":"1298","DOI":"10.1126\/science.275.5304.1298","article-title":"Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements","volume":"275","author":"K\u00fchn","year":"1997","journal-title":"Science"},{"key":"2021050612521209000_koaa060-B39","doi-asserted-by":"crossref","first-page":"2917","DOI":"10.1104\/pp.17.01562","article-title":"VASCULAR PLANT ONE-ZINC FINGER1 (VOZ1) and VOZ2 interact with CONSTANS and promote photoperiodic flowering transition","volume":"176","author":"Kumar","year":"2018","journal-title":"Plant Physiol"},{"key":"2021050612521209000_koaa060-B40","doi-asserted-by":"crossref","first-page":"1587","DOI":"10.1104\/pp.114.235556","article-title":"Intertissue signal transfer of abscisic acid from vascular cells to guard cells","volume":"164","author":"Kuromori","year":"2014","journal-title":"Plant Physiol"},{"key":"2021050612521209000_koaa060-B41","doi-asserted-by":"crossref","first-page":"1643","DOI":"10.1104\/pp.111.192583","article-title":"Siliques are Red1 from Arabidopsis acts as a bidirectional amino acid transporter that is crucial for the amino acid homeostasis of siliques","volume":"158","author":"Ladwig","year":"2012","journal-title":"Plant Physiol"},{"key":"2021050612521209000_koaa060-B42","doi-asserted-by":"crossref","first-page":"3353","DOI":"10.1105\/tpc.111.087742","article-title":"A 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