Yan O. Zubo, Ivory Clabaugh Blakley, Maria V. Yamburenko, Jennifer M. Worthen, Ian H. Street, José M. Franco-Zorrilla, Wenjing Zhang, Kristine Hill, Tracy Raines, Roberto Solano, Joseph J. Kieber, Ann E. Loraine, and G. Eric Schaller (2017). Cytokinin induces genome-wide binding of the type-B response regulator ARR10 to regulate growth and development in Arabidopsis. Proceedings of the National Academy of Sciences.
Department of Biological Sciences, Dartmouth College, Hanover, NH 03755;
Department of Bioinformatics and Genomics, University of North Carolina at Charlotte, Kannapolis, NC 28081;
Genomics Unit, Centro Nacional de Biotecnología (CNB)-Consejo Superior de Investigaciones Científicas (CSIC), 28049 Madrid, Spain;
Department of Biology, University of North Carolina at Chapel Hill, NC 27599;
Department of Plant Molecular Genetics, CNB-CSIC, 28049 Madrid, Spain
The plant hormone cytokinin affects a diverse array of growth and development processes and responses to the environment. How a signaling molecule mediates such a diverse array of outputs and how these response pathways are integrated with other inputs remain fundamental questions in plant biology. To this end, we characterized the transcriptional network initiated by the type-B ARABIDOPSIS RESPONSE REGULATORs (ARRs) that mediate the cytokinin primary response, making use of chromatin immunoprecipitation sequencing (ChIP-seq), protein-binding microarrays, and transcriptomic approaches. By ectopic overexpression of ARR10, Arabidopsis lines hypersensitive to cytokinin were generated and used to clarify the role of cytokinin in regulation of various physiological responses. ChIP-seq was used to identify the cytokinin-dependent targets for ARR10, thereby defining a crucial link between the cytokinin primary-response pathway and the transcriptional changes that mediate physiological responses to this phytohormone. Binding of ARR10 was induced by cytokinin with binding sites enriched toward the transcriptional start sites for both induced and repressed genes. Three type-B ARR DNA-binding motifs, determined by use of protein-binding microarrays, were enriched at ARR10 binding sites, confirming their physiological relevance. WUSCHEL was identified as a direct target of ARR10, with its cytokinin-enhanced expression resulting in enhanced shooting in tissue culture. Results from our analyses shed light on the physiological role of the type-B ARRs in regulating the cytokinin response, mechanism of type-B ARR activation, and basis by which cytokinin regulates diverse aspects of growth and development as well as responses to biotic and abiotic factors.