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Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate

Nature volume 465, pages 316–321 (2010)Cite this article

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Abstract

A key question in developmental biology is how cells exchange positional information for proper patterning during organ development. In plant roots the radial tissue organization is highly conserved with a central vascular cylinder in which two water conducting cell types, protoxylem and metaxylem, are patterned centripetally. We show that this patterning occurs through crosstalk between the vascular cylinder and the surrounding endodermis mediated by cell-to-cell movement of a transcription factor in one direction and microRNAs in the other. SHORT ROOT, produced in the vascular cylinder, moves into the endodermis to activate SCARECROW. Together these transcription factors activate MIR165a and MIR166b. Endodermally produced microRNA165/6 then acts to degrade its target mRNAs encoding class III homeodomain-leucine zipper transcription factors in the endodermis and stele periphery. The resulting differential distribution of target mRNA in the vascular cylinder determines xylem cell types in a dosage-dependent manner.

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Figure 1: Endodermal SHR and SCR control xylem patterning via PHB.
Figure 2: SHR post-transcriptionally represses PHB.
Figure 3: miR165/6 activated by SHR in the endodermis is active in the stele.
Figure 4: Non-cell-autonomous action of MIR165a.
Figure 5: HD-ZIP III levels determine xylem type.

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Acknowledgements

We thank K. Kainulainen, M. Herpola, G.-B. Berglund and J. Jung for technical assistance; M. Prigge, S. Clark, C. Bellini, N. Sauer, J. Colinas, T. Vernoux, K. Gallagher, A. P. Mahonen, A. Bishopp, M. Bonke, N. Fedoroff, J. C. Fletcher, B. J. Reinhart, I. Pekker, ABRC and NASC for materials, and E. Richards and M. Harrison for comments on the manuscript; M. Tsiantis for sharing results before publication. This work was supported by the Boyce Thompson Institute and NSF IOS0818071 to J.-Y.L., Cornell Presidential Life Science Fellowship to J.Z., grants from the NIH (RO1-GM043778) and from the NSF ARABIDOPSIS 2010 programme to P.N.B., a fellowship from the MICINN, Spanish Government to M.A.M.-R., grants by the Academy of Finland, Tekes and ESF to Y.H., S.L. and A.V., European Molecular Biology Organisation (EMBO, ALTF 450-2007) to J.D., Estonian funding agencies (ETF7361 and SF0180071s07) to O.L., Nilsson-Ehle Foundation to C.J.R, and FORMAS and Carl Trygger’s Foundation for Scientific Research to A.C. Imaging at Boyce Thompson Institute was supported by NSF (NSF DBI-0618969) and Triad Foundation.

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Author notes

  1. Annelie Carlsbecker, Ji-Young Lee, Ykä Helariutta and Philip N. Benfey: These authors contributed equally to this work.

Authors and Affiliations

  1. Institute of Biotechnology/Department of Biosciences, University of Helsinki, FIN-00014, Finland

    Annelie Carlsbecker, Jan Dettmer, Satu Lehesranta, Ove Lindgren, Anne Vatén, Siripong Thitamadee, Ana Campilho & Ykä Helariutta

  2. Department of Physiological Botany, Evolutionary Biology Center, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden,

    Annelie Carlsbecker & Christina J. Roberts

  3. Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, New York 14853, USA ,

    Ji-Young Lee, Jing Zhou & Jose Sebastian

  4. Graduate Field of Plant Biology, Cornell University, Ithaca, New York 14853, USA ,

    Ji-Young Lee & Jing Zhou

  5. Institute of Technology, University of Tartu, Tartu 50411, Estonia

    Ove Lindgren

  6. Biology Department and IGSP Center for Systems Biology, Duke University, Durham, North Carolina 27708, USA,

    Miguel A. Moreno-Risueno & Philip N. Benfey

  7. School of Biological Sciences, Monash University, Melbourne, Victoria 3800, Australia ,

    John L. Bowman

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Contributions

A.C. and J.-Y.L. contributed equally to this work, C.J.R., J.D., S.L. and J.Z. contributed equally to this work, O.L., M.A.M.-R. and A.V. contributed equally to this work, Y.H. and P.N.B. contributed equally to this work, and the name order was determined by raffle. A.C. designed and performed experiments to characterize HD-ZIP III transcription factors and miR165/6 in vascular patterning, J.-Y.L. identified and characterized the regulatory network of SHR, SCR and miR165/6 in the xylem patterning, C.J.R. analysed the miRNA expression by in situ hybridization and participated in HD-ZIP III mutant characterization. J.D. participated in the analysis of expression of PHB (including mutant forms) and other HD-ZIP III and generated pCRE1::MIR165a as well as participated in the generation of J0571 lines to rescue scr and shr. S.L. participated in the PHB and HD-ZIP III expression analysis, phb-7d mutant characterization and generated the pSCR::MIR165a to rescue scr. J.Z. developed and characterized the xylem patterning led by non-mobile SHR and PHB-m. O.L. participated in the characterization of various HD-ZIP III mutant lines. M.A.M.-R. showed the non-cell autonomous action of non-mobile SHR. A.V. participated in positional cloning of phb-7d and establishment of the J0571 lines to rescue shr. S.T. identified the phb-7d mutant. A.C. identified the scr-6 allele. J.S. characterized shr/scr and HD-ZIP III double mutants and embryo expression patterns in GFP lines. J.L.B. shared informative non-published materials. Y.H. and P.N.B. participated in experimental design. A.C., J.-Y.L., Y.H. and P.N.B. wrote the manuscript. A.C. and J.-Y.L. are co-corresponding authors. All authors discussed the results and commented on the manuscript.

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Correspondence to Ykä Helariutta or Philip N. Benfey.

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Carlsbecker, A., Lee, JY., Roberts, C. et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465, 316–321 (2010). https://doi.org/10.1038/nature08977

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