Apical growth in plants initiates upon seed germination, whereas radial growth is primed only during early ontogenesis in procambium cells and activated later by the vascular cambium1. Although it is not known how radial growth is organized and regulated in plants, this system resembles the developmental competence observed in some animal systems, in which pre-existing patterns of developmental potential are established early on2,3. Here we show that in Arabidopsis the initiation of radial growth occurs around early protophloem-sieve-element cell files of the root procambial tissue. In this domain, cytokinin signalling promotes the expression of a pair of mobile transcription factors—PHLOEM EARLY DOF 1 (PEAR1) and PHLOEM EARLY DOF 2 (PEAR2)—and their four homologues (DOF6, TMO6, OBP2 and HCA2), which we collectively name PEAR proteins. The PEAR proteins form a short-range concentration gradient that peaks at protophloem sieve elements, and activates gene expression that promotes radial growth. The expression and function of PEAR proteins are antagonized by the HD-ZIP III proteins, well-known polarity transcription factors4—the expression of which is concentrated in the more-internal domain of radially non-dividing procambial cells by the function of auxin, and mobile miR165 and miR166 microRNAs. The PEAR proteins locally promote transcription of their inhibitory HD-ZIP III genes, and thereby establish a negative-feedback loop that forms a robust boundary that demarks the zone of cell division. Taken together, our data establish that during root procambial development there exists a network in which a module that links PEAR and HD-ZIP III transcription factors integrates spatial information of the hormonal domains and miRNA gradients to provide adjacent zones of dividing and more-quiescent cells, which forms a foundation for further radial growth.
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All lines and data supporting the findings of this study are available from the corresponding authors upon request. The transcriptomics data files are available at Gene Expression Omnibus (GEO), under accession number GSE115183. A list of putative direct targets of PEAR1 and/or PEAR2 with their description as well as individual P values for Tukey’s HSD test and two-sided Student’s t-test are provided as Supplementary Information.
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We thank E. Scarpella, ABRC and NASC for materials, K. Kainulainen, K. Blajecka, M. Herpola and A. Mainardi for technical assistance, N. Clark for assisting with the scanning FCS analysis, J. Jansen for technical assistance with microarray hybridizations, O. Kambur and L. Kalmbach for assistance in generating the heat map, and D. Weijers and T. Kakimoto for helpful discussions, A. Groenheide, E. Cornelissen, M. Chu, A. Korppoo and A. Rodriguez Diez for technical support. This works was supported by Finnish Centre of Excellence in Molecular Biology of Primary Producers (Academy of Finland CoE program 2014-2019) decision #271832, the Gatsby Foundation (GAT3395/PR3)), University of Helsinki (award 799992091) and the European Research Council Advanced Investigator Grant SYMDEV (No. 323052) to Y.H., a NSF-BBSRC MCSB 1517058 to R. Sozzani and Y.H., an ERC Consolidator grant (PLANTSTEMS), a Heisenberg Professorship of the German Research Foundation (DFG, GR2104/5-1) and the SFB 873 (DFG) to T.G., the Netherlands Organization for Scientific Research (NWO; VIDI-864.13.001) and The Research Foundation - Flanders (FWO; Odysseus II G0D0515N and 12D1815N) to W.S. and B.D.R., respectively, a JSPS postdoctoral fellowship for research abroad and JSPS KAKENHI Grant (17K15138) to S.M., Swiss National Science Foundation Postdoc Mobility Grant (P300P3_147894) to P.R., a JSPS Research Fellowship for Young Scientists and JSPS KAKENHI Grant (JP16J00131) to K.T., Bayer Science and Education Foundation, German Academic Exchange Service (DAAD) to B.B., The Finnish Academy of Science to J.-o.H., and Herchel Smith Postdoctoral Research Fellowship (Herchel Smith Fund) to S.O.
Nature thanks S. Sabatini, S. Turner and the other anonymous reviewer(s) for their contribution to the peer review of this work.