Plant cells are totipotent and competent to regenerate from differentiated organs. It has been shown that two phytohormones, auxin and cytokinin, play critical roles within this process. As in animals, the regenerative capacity declines with age in plants, but the molecular basis for this phenomenon remains elusive. Here, we demonstrate that an age-regulated microRNA, miR156, regulates shoot regenerative capacity. As a plant ages, the gradual increase in miR156-targeted SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factors leads to the progressive decline in shoot regenerative capacity. In old plants, SPL reduces shoot regenerative capacity by attenuating the cytokinin response through binding with the B-type ARABIDOPSIS RESPONSE REGULATORs, which encode the transcriptional activators in the cytokinin signaling pathway. Consistently, the increased amount of exogenous cytokinin complements the reduced shoot regenerative capacity in old plants. Therefore, the recruitment of age cues in response to cytokinin contributes to shoot regenerative competence.

National Key Laboratory of Plant Molecular Genetics Institute of Plant Physiology and Ecology Shanghai Institutes for Biological Sciences Shanghai 200032 People's Republic of China

National Key Laboratory of Plant Molecular Genetics Institute of Plant Physiology and Ecology Shanghai Institutes for Biological Sciences Shanghai 200032 People's Republic of China University of the Chinese Academy of Sciences Shanghai 200032 People's Republic of China

Umeå Plant Science Centre Department of Forest Genetics and Plant Physiology Swedish University of Agricultural Sciences SE 901 83 Umeå Sweden

Umeå Plant Science Centre Department of Forest Genetics and Plant Physiology Swedish University of Agricultural Sciences SE 901 83 Umeå Sweden Laboratory of Growth Regulators Institute of Experimental Botany Academy of Sciences of the Czech Republic 78371 Olomouc Czech Republic Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University 78371 Olomouc Czech Republic

Zobrazit více v PubMed

Ambros V. (2011). MicroRNAs and developmental timing. Curr. Opin. Genet. Dev. 21: 511–517. PubMed PMC

Axtell M.J., Bowman J.L. (2008). Evolution of plant microRNAs and their targets. Trends Plant Sci. 13: 343–349. PubMed

Berdowski J.J.M., Siepel H. (1998). Vegetative regeneration of Calluna vulgaris at different ages and fertilizer levels. Biol. Conserv. 46: 85–93.

Bergonzi S., Albani M.C., Ver Loren van Themaat E., Nordström K.J., Wang R., Schneeberger K., Moerland P.D., Coupland G. (2013). Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 340: 1094–1097. PubMed

Birnbaum K.D., Sánchez Alvarado A. (2008). Slicing across kingdoms: Regeneration in plants and animals. Cell 132: 697–710. PubMed PMC

Chuck G., Cigan A.M., Saeteurn K., Hake S. (2007). The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat. Genet. 39: 544–549. PubMed

Clough S.J., Bent A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735–743. PubMed

Duclercq J., Sangwan-Norreel B., Catterou M., Sangwan R.S. (2011). De novo shoot organogenesis: From art to science. Trends Plant Sci. 16: 597–606. PubMed

Franco-Zorrilla J.M., Valli A., Todesco M., Mateos I., Puga M.I., Rubio-Somoza I., Leyva A., Weigel D., García J.A., Paz-Ares J. (2007). Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39: 1033–1037. PubMed

Gou J.Y., Felippes F.F., Liu C.J., Weigel D., Wang J.W. (2011). Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23: 1512–1522. PubMed PMC

Hellens R.P., Allan A.C., Friel E.N., Bolitho K., Grafton K., Templeton M.D., Karunairetnam S., Gleave A.P., Laing W.A. (2005). Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1: 13. PubMed PMC

Heyl A., Schmülling T. (2003). Cytokinin signal perception and transduction. Curr. Opin. Plant Biol. 6: 480–488. PubMed

Hwang I., Sheen J. (2001). Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413: 383–389. PubMed

Hwang I., Sheen J., Müller B. (2012). Cytokinin signaling networks. Annu. Rev. Plant Biol. 63: 353–380. PubMed

Ishida K., Yamashino T., Yokoyama A., Mizuno T. (2008). Three type-B response regulators, ARR1, ARR10 and ARR12, play essential but redundant roles in cytokinin signal transduction throughout the life cycle of Arabidopsis thaliana. Plant Cell Physiol. 49: 47–57. PubMed

Kartsonas E., Papafotiou M. (2007). Mother plant age and seasonal influence on in vitro propagation of Quercus euboica Pap, an endemic, rare and endangered oak species of Greece. Plant Cell Tissue Organ Cult. 90: 111–116.

Kieber J.J., Schaller G.E. (2014). Cytokinins. The Arabidopsis Book 12: e0168, doi/10.1199/tab.0168. PubMed PMC

Mason M.G., Mathews D.E., Argyros D.A., Maxwell B.B., Kieber J.J., Alonso J.M., Ecker J.R., Schaller G.E. (2005). Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17: 3007–3018. PubMed PMC

Müller B., Sheen J. (2008). Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453: 1094–1097. PubMed PMC

Nodine M.D., Bartel D.P. (2010). MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev. 24: 2678–2692. PubMed PMC

Nordström A., Tarkowski P., Tarkowska D., Norbaek R., Astot C., Dolezal K., Sandberg G. (2004). Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: A factor of potential importance for auxin-cytokinin-regulated development. Proc. Natl. Acad. Sci. USA 101: 8039–8044. PubMed PMC

Papp I., Mette M.F., Aufsatz W., Daxinger L., Schauer S.E., Ray A., van der Winden J., Matzke M., Matzke A.J. (2003). Evidence for nuclear processing of plant microRNA and short interfering RNA precursors. Plant Physiol. 132: 1382–1390. PubMed PMC

Poethig R.S. (2013). Vegetative phase change and shoot maturation in plants. Curr. Top. Dev. Biol. 105: 125–152. PubMed PMC

Porrello E.R., Mahmoud A.I., Simpson E., Hill J.A., Richardson J.A., Olson E.N., Sadek H.A. (2011). Transient regenerative potential of the neonatal mouse heart. Science 331: 1078–1080. PubMed PMC

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

Ruckh J.M., Zhao J.W., Shadrach J.L., van Wijngaarden P., Rao T.N., Wagers A.J., Franklin R.J. (2012). Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell 10: 96–103. PubMed PMC

Sabatini S., Beis D., Wolkenfelt H., Murfett J., Guilfoyle T., Malamy J., Benfey P., Leyser O., Bechtold N., Weisbeek P., Scheres B. (1999). An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99: 463–472. PubMed

Schwarz S., Grande A.V., Bujdoso N., Saedler H., Huijser P. (2008). The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol. Biol. 67: 183–195. PubMed PMC

Shyh-Chang N., Zhu H., Yvanka de Soysa T., Shinoda G., Seligson M.T., Tsanov K.M., Nguyen L., Asara J.M., Cantley L.C., Daley G.Q. (2013). Lin28 enhances tissue repair by reprogramming cellular metabolism. Cell 155: 778–792. PubMed PMC

Skoog F., Miller C.O. (1957). Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 11: 118–130. PubMed

Sugimoto K., Gordon S.P., Meyerowitz E.M. (2011). Regeneration in plants and animals: Dedifferentiation, transdifferentiation, or just differentiation? Trends Cell Biol. 21: 212–218. PubMed

Wang J.W., Czech B., Weigel D. (2009). miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: 738–749. PubMed

Wang J.W., Park M.Y., Wang L.J., Koo Y., Chen X.Y., Weigel D., Poethig R.S. (2011). miRNA control of vegetative phase change in trees. PLoS Genet. 7: e1002012. PubMed PMC

Wang J.W., Schwab R., Czech B., Mica E., Weigel D. (2008). Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20: 1231–1243. PubMed PMC

Werner T., Schmülling T. (2009). Cytokinin action in plant development. Curr. Opin. Plant Biol. 12: 527–538. PubMed

Wu G., Poethig R.S. (2006). Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133: 3539–3547. PubMed PMC

Wu G., Park M.Y., Conway S.R., Wang J.W., Weigel D., Poethig R.S. (2009). The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138: 750–759. PubMed PMC

Xing S., Salinas M., Höhmann S., Berndtgen R., Huijser P. (2010). miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell 22: 3935–3950. PubMed PMC

Yang L., Xu M., Koo Y., He J., Poethig R.S. (2013). Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. eLife 2: e00260. PubMed PMC

Yu N., Cai W.J., Wang S., Shan C.M., Wang L.J., Chen X.Y. (2010). Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22: 2322–2335. PubMed PMC

Yu S., Cao L., Zhou C.M., Zhang T.Q., Lian H., Sun Y., Wu J., Huang J., Wang G., Wang J.W. (2013). Sugar is an endogenous cue for juvenile-to-adult phase transition in plants. eLife 2: e00269. PubMed PMC

Yu S., Galvão V.C., Zhang Y.C., Horrer D., Zhang T.Q., Hao Y.H., Feng Y.Q., Wang S., Schmid M., Wang J.W. (2012). Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell 24: 3320–3332. PubMed PMC

Zhou C.M., Zhang T.Q., Wang X., Yu S., Lian H., Tang H., Feng Z.Y., Zozomova-Lihová J., Wang J.W. (2013). Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science 340: 1097–1100. PubMed

Cytokinin depends on GA biosynthesis and signaling to regulate different aspects of vegetative phase change in Arabidopsis

Epigenetics and plant hormone dynamics: a functional and methodological perspective

Cytokinins - regulators of de novo shoot organogenesis