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Potent inhibition of TCP transcription factors by miR319 ensures proper root growth in Arabidopsis

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Abstract

Key message

Proper root growth depends on the clearance of TCP transcripts from the root apical meristem by microRNA miR319.

Abstract

The evolutionarily conserved microRNA miR319 regulates genes encoding TCP transcription factors in angiosperms. The miR319-TCP module controls cell proliferation and differentiation in leaves and other aerial organs. The current model sustains that miR319 quantitatively tunes TCP activity during leaf growth and development, ultimately affecting its size. In this work we studied how this module participates in Arabidopsis root development. We found that misregulation of TCP activity through impairment of miR319 binding decreased root meristem size and root length. Cellular and molecular analyses revealed that high TCP activity affects cell number and cyclin expression but not mature cell length, indicating that, in roots, unchecking the expression of miR319-regulated TCPs significantly affects cell proliferation. Conversely, tcp multiple mutants showed no obvious effect on root growth, but strong defects in leaf morphogenesis. Therefore, in contrast to the quantitative regulation of the TCPs by miR319 in leaves, our data suggest that miR319 clears TCP transcripts from root cells. Hence, we provide new insights into the functions of the miR319-TCP regulatory system in Arabidopsis development, highlighting a different modus operandi for its action mechanism in roots and shoots.

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Vectors and mutant lines generated in this study are available on request.

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References

  • Alonso-Peral MM, Sun C, Millar AA (2012) MicroRNA159 can act as a switch or tuning microRNA independently of its abundance in Arabidopsis. PLoS ONE 7:e34751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bao M, Bian H, Zha Y, Li F, Sun Y, Bai B, Chen Z, Wang J, Zhu M, Han N (2014) miR396a-mediated basic helix-loop-helix transcription factor bHLH74 repression acts as a regulator for root growth in Arabidopsis seedlings. Plant Cell Physiol 55:1343–1353

    Article  CAS  PubMed  Google Scholar 

  • Bell E, Creelman RA, Mullet JE (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc Natl Acad Sci U S A 92:8675–8679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801–806

    Article  CAS  PubMed  Google Scholar 

  • Bresso EG, Chorostecki U, Rodriguez RE, Palatnik JF, Schommer C (2018) Spatial control of gene expression by miR319-regulated TCP transcription factors in leaf development. Plant Physiol 176:1694–1708

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33:e179

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, Wang B, Chen R, Jiang H, Qi J, Li X, Palme K, Li C (2011) The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23:3335–3352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Citerne HL, Luo D, Pennington RT, Coen E, Cronk QC (2003) A phylogenomic investigation of CYCLOIDEA-like TCP genes in the Leguminosae. Plant Physiol 131:1042–1053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Colon-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20:503–508

    Article  CAS  PubMed  Google Scholar 

  • Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222

    Article  CAS  PubMed  Google Scholar 

  • Danisman S, van Dijk AD, Bimbo A, van der Wal F, Hennig L, de Folter S, Angenent GC, Immink RG (2013) Analysis of functional redundancies within the Arabidopsis TCP transcription factor family. J Exp Bot 64:5673–5685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384

    Article  CAS  Google Scholar 

  • Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419

    Article  CAS  PubMed  Google Scholar 

  • Efroni I, Blum E, Goldshmidt A, Eshed Y (2008) A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 20:2293–2306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ercoli MF, Vena R, Goldy C, Palatnik JF, Rodriguez RE (2018a) Analysis of expression gradients of developmental regulators in Arabidopsis thaliana roots. Methods Mol Biol 1863:3–17

    Article  CAS  PubMed  Google Scholar 

  • Ercoli MF, Ferela A, Debernardi JM, Perrone AP, Rodriguez RE, Palatnik JF (2018b) GIF transcriptional coregulators control root meristem homeostasis. Plant Cell 30:347–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flynt AS, Lai EC (2008) Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat Rev Genet 9:831–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh Dastidar M, Mosiolek M, Bleckmann A, Dresselhaus T, Nodine MD, Maizel A (2016) Sensitive whole mount in situ localization of small RNAs in plants. Plant J 88:694–702

    Article  CAS  PubMed  Google Scholar 

  • Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15:1899–1911

    Article  CAS  PubMed  Google Scholar 

  • Ichihashi Y, Kawade K, Usami T, Horiguchi G, Takahashi T, Tsukaya H (2011) Key proliferative activity in the junction between the leaf blade and leaf petiole of Arabidopsis. Plant Physiol 157:1151–1162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jarvis P, Chen LJ, Li H, Peto CA, Fankhauser C, Chory J (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282:100–103

    Article  CAS  PubMed  Google Scholar 

  • Klepikova AV, Kasianov AS, Gerasimov ES, Logacheva MD, Penin AA (2016) A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. Plant J 88:1058–1070

    Article  CAS  PubMed  Google Scholar 

  • Koyama T, Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2010) TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22:3574–3588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S (2015) The Arabidopsis thaliana TCP transcription factors: a broadening horizon beyond development. Plant Signal Behav 10:e1044192

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lucas JR, Shaw SL (2012) MAP65-1 and MAP65-2 promote cell proliferation and axial growth in Arabidopsis roots. Plant J 71:454–463

    CAS  PubMed  Google Scholar 

  • Martin-Trillo M, Cubas P (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15:31–39

    Article  CAS  PubMed  Google Scholar 

  • Nawy T, Lee JY, Colinas J, Wang JY, Thongrod SC, Malamy JE, Birnbaum K, Benfey PN (2005) Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell 17:1908–1925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Article  CAS  PubMed  Google Scholar 

  • Palatnik JF, Wollmann H, Schommer C, Schwab R, Boisbouvier J, Rodriguez R, Warthmann N, Allen E, Dezulian T, Huson D, Carrington JC, Weigel D (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev Cell 13:115–125

    Article  CAS  PubMed  Google Scholar 

  • Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63:563–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubio-Somoza I, Zhou CM, Confraria A, Martinho C, von Born P, Baena-Gonzalez E, Wang JW, Weigel D (2014) Temporal control of leaf complexity by miRNA-regulated licensing of protein complexes. Curr Biol 24:2714–2719

    Article  CAS  PubMed  Google Scholar 

  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682

    Article  CAS  PubMed  Google Scholar 

  • Schommer C, Palatnik JF, Aggarwal P, Chetelat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6:e230

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schommer C, Debernardi JM, Bresso EG, Rodriguez RE, Palatnik JF (2014) Repression of cell proliferation by miR319-regulated TCP4. Mol Plant 7:1533–1544

    Article  CAS  PubMed  Google Scholar 

  • Shimotohno A, Heidstra R, Blilou I, Scheres B (2018) Root stem cell niche organizer specification by molecular convergence of PLETHORA and SCARECROW transcription factor modules. Genes Dev 32:1085–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian Q, Uhlir NJ, Reed JW (2002) Arabidopsis SHY2/IAA3 inhibits auxin-regulated gene expression. Plant Cell 14:301–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616

    Article  CAS  PubMed  Google Scholar 

  • Uberti-Manassero NG, Lucero LE, Viola IL, Vegetti AC, Gonzalez DH (2012) The class I protein AtTCP15 modulates plant development through a pathway that overlaps with the one affected by CIN-like TCP proteins. J Exp Bot 63:809–823

    Article  CAS  PubMed  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687

    Article  CAS  PubMed  Google Scholar 

  • Weigel D, Glazebrook J (2009) Quick miniprep for plant DNA isolation. Cold Spring Harb Protoc 2009, pdb prot5179.

  • Wen B, Nieuwland J, Murray JA (2013) The Arabidopsis CDK inhibitor ICK3/KRP5 is rate limiting for primary root growth and promotes growth through cell elongation and endoreduplication. J Exp Bot 64:1135–1144

    CAS  PubMed  Google Scholar 

  • Zhou W, Lozano-Torres JL, Blilou I, Zhang X, Zhai Q, Smant G, Li C, Scheres B (2019a) A jasmonate signaling network activates root stem cells and promotes regeneration. Cell 177(942–956):e914

    Google Scholar 

  • Zhou Y, Xun Q, Zhang D, Lv M, Ou Y, Li J (2019b) TCP transcription factors associate with PHYTOCHROME INTERACTING FACTOR 4 and CRYPTOCHROME 1 to regulate thermomorphogenesis in Arabidopsis thaliana. iScience 15:600–610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Ramiro Rodriguez for helpful discussions and Rodrigo Vena for technical assistance in image acquisition. EGB, JLB and CG were supported by fellowships from CONICET. JFP and CS are members of CONICET. This work was supported by Grants to JFP (ICGEB CRP/ARG17-01) and CS (Project: IO-345-17 of Agencia Santafesina de Ciencia Tecnología e Innovación and project: PICT 2019-03571 of Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación).

Funding

EGB, JLB and CG were supported by fellowships from CONICET. JFP and CS are members of CONICET. This work was supported by Grants to JFP (ICGEB CRP/ARG17-01) and CS (Project: IO-345-17 of Agencia Santafesina de Ciencia Tecnología e Innovación; and project: PICT 2019-03571 of Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación).

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Author notes

  1. Julia L. Baulies and Edgardo G. Bresso have contributed equally to this work and share first authorship.

Authors and Affiliations

  1. Instituto de Biología Molecular y Celular de Rosario, Ocampo y Esmeralda s/n, 2000, Rosario, Argentina

    Julia L. Baulies, Edgardo G. Bresso, Camila Goldy, Javier F. Palatnik & Carla Schommer

  2. Centro de Estudios Interdisciplinarios (CEI), Universidad Nacional de Rosario, Maipú 1065, 2000, Rosario, Argentina

    Javier F. Palatnik & Carla Schommer

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  1. Julia L. Baulies
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  2. Edgardo G. Bresso
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  3. Camila Goldy
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  4. Javier F. Palatnik
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  5. Carla Schommer
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Contributions

EGB, JLB, CG and CS performed the experiments. EGB, JFP and CS conceived the experiments. EGB, JLB, JFP and CS wrote the manuscript.

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Correspondence to Carla Schommer.

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Baulies, J.L., Bresso, E.G., Goldy, C. et al. Potent inhibition of TCP transcription factors by miR319 ensures proper root growth in Arabidopsis. Plant Mol Biol 108, 93–103 (2022). https://doi.org/10.1007/s11103-021-01227-8

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