title: Cytokinin and Auxin Display Distinct but Interconnected Distribution and Signaling Profiles to Stimulate Cambial Activity.
abstract: Despite the crucial roles of phytohormones in plant development, comparison of the exact distribution profiles of different hormones within plant meristems has thus far remained scarce. Vascular cambium, a wide lateral meristem with an extensive developmental zonation, provides an optimal system for hormonal and genetic profiling. By taking advantage of this spatial resolution, we show here that two major phytohormones, cytokinin and auxin, display different yet partially overlapping distribution profiles across the cambium. In contrast to auxin, which has its highest concentration in the actively dividing cambial cells, cytokinins peak in the developing phloem tissue of a Populus trichocarpa stem. Gene expression patterns of cytokinin biosynthetic and signaling genes coincided with this hormonal gradient. To explore the functional significance of cytokinin signaling for cambial development, we engineered transgenic Populus tremula × tremuloides trees with an elevated cytokinin biosynthesis level. Confirming that cytokinins function as major regulators of cambial activity, these trees displayed stimulated cambial cell division activity resulting in dramatically increased (up to 80% in dry weight) production of the lignocellulosic trunk biomass. To connect the increased growth to hormonal status, we analyzed the hormone distribution and genome-wide gene expression profiles in unprecedentedly high resolution across the cambial zone. Interestingly, in addition to showing an elevated cambial cytokinin content and signaling level, the cambial auxin concentration and auxin-responsive gene expression were also increased in the transgenic trees. Our results indicate that cytokinin signaling specifies meristematic activity through a graded distribution that influences the amplitude of the cambial auxin gradient.
authors.affiliation: Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland; Department of Biosciences, University of Helsinki, 00014 Helsinki, Finland.
authors.forename: Juha
authors.initials: J
authors.lastname: Immanen
authors.affiliation: Green Technology, Natural Resources Institute Finland (Luke), Jokiniemenkuja 1, 01301 Vantaa, Finland. Electronic address: kaisa.nieminen@luke.fi.
authors.forename: Kaisa
authors.initials: K
authors.lastname: Nieminen
authors.affiliation: Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland.
authors.forename: Olli-Pekka
authors.initials: OP
authors.lastname: Smolander
authors.affiliation: RIKEN Center for Sustainable Resource Science, 1-7-22, Suehiro, Tsurumi, Yokohama 230-0045, Japan.
authors.forename: Mikiko
authors.initials: M
authors.lastname: Kojima
authors.affiliation: Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland; Department of Biosciences, University of Helsinki, 00014 Helsinki, Finland.
authors.forename: Juan
authors.initials: J
authors.lastname: Alonso Serra
authors.affiliation: Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland.
authors.forename: Patrik
authors.initials: P
authors.lastname: Koskinen
authors.affiliation: Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland; Department of Biosciences, University of Helsinki, 00014 Helsinki, Finland; Sainsbury Laboratory, Cambridge University, Bateman Street, Cambridge CB2 1LR, UK.
authors.forename: Jing
authors.initials: J
authors.lastname: Zhang
authors.affiliation: Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland; Department of Biosciences, University of Helsinki, 00014 Helsinki, Finland.
authors.forename: Annakaisa
authors.initials: A
authors.lastname: Elo
authors.affiliation: Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland; Department of Biosciences, University of Helsinki, 00014 Helsinki, Finland.
authors.forename: Ari Pekka
authors.initials: AP
authors.lastname: Mähönen
authors.affiliation: Umeå Plant Science Center and Department of Forest Genetics and Plant Physiology, SLU, Umeå 901 87, Sweden.
authors.forename: Nathaniel
authors.initials: N
authors.lastname: Street
authors.affiliation: Umeå Plant Science Center and Department of Forest Genetics and Plant Physiology, SLU, Umeå 901 87, Sweden; Department of Biology, King Saud University, Riyadh 11451, Saudi Arabia.
authors.forename: Rishikesh P
authors.initials: RP
authors.lastname: Bhalerao
authors.affiliation: Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland.
authors.forename: Lars
authors.initials: L
authors.lastname: Paulin
authors.affiliation: Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland.
authors.forename: Petri
authors.initials: P
authors.lastname: Auvinen
authors.affiliation: RIKEN Center for Sustainable Resource Science, 1-7-22, Suehiro, Tsurumi, Yokohama 230-0045, Japan.
authors.forename: Hitoshi
authors.initials: H
authors.lastname: Sakakibara
authors.affiliation: Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland; Department of Biosciences, University of Helsinki, 00014 Helsinki, Finland; Sainsbury Laboratory, Cambridge University, Bateman Street, Cambridge CB2 1LR, UK. Electronic address: yrjo.helariutta@slcu.cam.ac.uk.
authors.forename: Ykä
authors.initials: Y
authors.lastname: Helariutta
mesh_terms: D058506:Cambium / Q000254:growth & development*; D003583:Cytokinins / Q000378:metabolism*; D018745:Genome, Plant; D007210:Indoleacetic Acids / Q000378:metabolism*; D010937:Plant Growth Regulators / Q000378:metabolism*; D030821:Plants, Genetically Modified / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D032107:Populus / Q000235:genetics / Q000254:growth & development / Q000502:physiology*; D015398:Signal Transduction; D059467:Transcriptome
chemical_list: D003583:Cytokinins; D007210:Indoleacetic Acids; D010937:Plant Growth Regulators