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DOF2.1 Controls Cytokinin-Dependent Vascular Cell Proliferation Downstream of TMO5/LHW

2019; Elsevier BV; Volume: 29; Issue: 3 Linguagem: Inglês

10.1016/j.cub.2018.12.041

1879-0445

Wouter Smet, Iris Sevilem, María Angels de Luis Balaguer, Brecht Wybouw, Eliana Mor, Shunsuke Miyashima, Bernhard Blob, Pawel Roszak, Thomas B. Jacobs, Mark V. Boekschoten, Guido Hooiveld, Rosangela Sozzani, Ykä Helariutta, Bert De Rybel,

RNA modifications and cancer

To create a three-dimensional structure, plants rely on oriented cell divisions and cell elongation. Oriented cell divisions are specifically important in procambium cells of the root to establish the different vascular cell types [1Dolan L. Janmaat K. Willemsen V. Linstead P. Poethig S. Roberts K. Scheres B. Cellular organisation of the Arabidopsis thaliana root.Development. 1993; 119: 71-84Crossref PubMed Google Scholar, 2Jürgens G.M.U. Arabidopsis. In Embryos: Colour Atlas of Development - Bard,Jbl.Nature. 1994; 370 (190–190)Google Scholar]. These divisions are in part controlled by the auxin-controlled TARGET OF MONOPTEROS5 (TMO5) and LONESOME HIGHWAY (LHW) transcription factor complex [3De Rybel B. Adibi M. Breda A.S. Wendrich J.R. Smit M.E. Novák O. Yamaguchi N. Yoshida S. Van Isterdael G. Palovaara J. et al.Plant development. Integration of growth and patterning during vascular tissue formation in Arabidopsis.Science. 2014; 345: 1255215Crossref PubMed Scopus (210) Google Scholar, 4De Rybel B. Möller B. Yoshida S. Grabowicz I. Barbier de Reuille P. Boeren S. Smith R.S. Borst J.W. Weijers D. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis.Dev. Cell. 2013; 24: 426-437Abstract Full Text Full Text PDF PubMed Scopus (186) Google Scholar, 5Ohashi-Ito K. Matsukawa M. Fukuda H. An atypical bHLH transcription factor regulates early xylem development downstream of auxin.Plant Cell Physiol. 2013; 54: 398-405Crossref PubMed Scopus (55) Google Scholar, 6Ohashi-Ito K. Saegusa M. Iwamoto K. Oda Y. Katayama H. Kojima M. Sakakibara H. Fukuda H. A bHLH complex activates vascular cell division via cytokinin action in root apical meristem.Curr. Biol. 2014; 24: 2053-2058Abstract Full Text Full Text PDF PubMed Scopus (114) Google Scholar, 7Ohashi-Ito K. Oguchi M. Kojima M. Sakakibara H. Fukuda H. Auxin-associated initiation of vascular cell differentiation by LONESOME HIGHWAY.Development. 2013; 140: 765-769Crossref PubMed Scopus (54) Google Scholar]. Loss-of-function of tmo5 or lhw clade members results in strongly reduced vascular cell file numbers, whereas ectopic expression of both TMO5 and LHW can ubiquitously induce periclinal and radial cell divisions in all cell types of the root meristem. TMO5 and LHW interact only in young xylem cells, where they promote expression of two direct target genes involved in the final step of cytokinin (CK) biosynthesis, LONELY GUY3 (LOG3) and LOG4 [8Kuroha T. Tokunaga H. Kojima M. Ueda N. Ishida T. Nagawa S. Fukuda H. Sugimoto K. Sakakibara H. Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis.Plant Cell. 2009; 21: 3152-3169Crossref PubMed Scopus (278) Google Scholar, 9Tokunaga H. Kojima M. Kuroha T. Ishida T. Sugimoto K. Kiba T. Sakakibara H. Arabidopsis lonely guy (LOG) multiple mutants reveal a central role of the LOG-dependent pathway in cytokinin activation.Plant J. 2012; 69: 355-365Crossref PubMed Scopus (131) Google Scholar] Therefore, CK was hypothesized to act as a mobile signal from the xylem to trigger divisions in the neighboring procambium cells [3De Rybel B. Adibi M. Breda A.S. Wendrich J.R. Smit M.E. Novák O. Yamaguchi N. Yoshida S. Van Isterdael G. Palovaara J. et al.Plant development. Integration of growth and patterning during vascular tissue formation in Arabidopsis.Science. 2014; 345: 1255215Crossref PubMed Scopus (210) Google Scholar, 6Ohashi-Ito K. Saegusa M. Iwamoto K. Oda Y. Katayama H. Kojima M. Sakakibara H. Fukuda H. A bHLH complex activates vascular cell division via cytokinin action in root apical meristem.Curr. Biol. 2014; 24: 2053-2058Abstract Full Text Full Text PDF PubMed Scopus (114) Google Scholar]. To unravel how TMO5/LHW-dependent cytokinin regulates cell proliferation, we analyzed the transcriptional responses upon simultaneous induction of both transcription factors. Using inferred network analysis, we identified AT2G28510/DOF2.1 as a cytokinin-dependent downstream target gene. We further showed that DOF2.1 controls specific procambium cell divisions without inducing other cytokinin-dependent effects such as the inhibition of vascular differentiation. In summary, our results suggest that DOF2.1 and its closest homologs control vascular cell proliferation, thus leading to radial expansion of the root.