Cell-by-cell dissection of phloem development links a maturation gradient to cell specialization

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In the plant meristem, tissue-wide maturation gradients are coordinated with specialized cell networks to establish various developmental phases required for indeterminate growth. Here, we used single-cell transcriptomics to reconstruct the protophloem developmental trajectory from birth of cell progenitors to terminal differentiation in the Arabidopsis root. PHLOEM EARLY DNA-BINDING-WITH-ONE-FINGER (PEAR) transcription factors mediate lineage bifurcation by activating GTPase signaling and prime a transcriptional differentiation program. This program is initially repressed by a meristem-wide gradient of PLETHORA transcription factors. Only the dissipation of PLETHORA gradient permits activation of the differentiation program that involves mutual inhibition of early vs. late meristem regulators. Thus, for phloem development, broad maturation gradients interface with cell-type specific transcriptional regulators to stage cellular differentiation.

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Arabidopsis, Arabidopsis Proteins, Cell Differentiation, GTP-Binding Proteins, Meristem, Phloem, Plant Roots, RNA-Seq, Signal Transduction, Single-Cell Analysis, Transcription Factors, Transcriptome
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American Association for the Advancement of Science
European Research Council (323052)
Gatsby Charitable Foundation (GAT3395/PR3)
Biotechnology and Biological Sciences Research Council (BB/N013158/1)
Gatsby Charitable Foundation (GAT3395/PR3B)
Wellcome Trust (105031/D/14/Z)
Medical Research Council (MR/M008975/1)
Wellcome Trust (203151/Z/16/Z)
Medical Research Council (MC_PC_17230)
Finnish CoE in Molecular Biology of Primary Producers (Academy of Finland CoE program 2014-2019) decision #271832 (YH) Gatsby Foundation GAT3395/PR3 (YH) University of Helsinki award 799992091 (YH) ERC Advanced Investigator Grant SYMDEV No. 323052 (YH) NSF-BBSRC MCSB grant 1517058 (RS, YH) NSF CAREER MCB grant 1453130 (RS) NIH grant GM078279 (KDB) NFS IOS grant 1934388 (KDB, DS) NIH grant R35GM136362 (KDB) MRC Clinical Research Infrastructure award MR/M008975/1 (BG) Core funding from the Wellcome and MRC to the Cambridge Stem Cell Institute (BG) Academy of Finland grants 266431 and 307335 (APM, XW) NWO Horizon grant 050-71-054 (RH) ERC Starting Grant TORPEDO; 714055 (BDR) Research Foundation - Flanders (FWO; Odysseus II G0D0515N) (BDR) Gatsby Foundation CDF grant (SEA) BOF postdoctoral fellowship from Ghent University (JRW) Wallenberg Academy Fellowship KAW 2016.0274 (CWM) Wellcome Strategic Award 105031/D/14/Z (FH) JSPS Research Fellowship for Young Scientists (KT) JSPS KAKENHI grant JP16J00131 (KT) JSPS Overseas Research Fellowship (YS) MEXT KAKENHI grant 16H06280, 19H05677 (YO) The Finnish Academy of Science (JH)