Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis.
The plant hormones auxin and cytokinin mutually coordinate their activities to control various aspects of development [1-9], and their crosstalk occurs at multiple levels [10, 11]. Cytokinin-mediated modulation of auxin transport provides an efficient means to regulate auxin distribution in plant organs. Here, we demonstrate that cytokinin does not merely control the overall auxin flow capacity, but might also act as a polarizing cue and control the auxin stream directionality during plant organogenesis. Cytokinin enhances the PIN-FORMED1 (PIN1) auxin transporter depletion at specific polar domains, thus rearranging the cellular PIN polarities and directly regulating the auxin flow direction. This selective cytokinin sensitivity correlates with the PIN protein phosphorylation degree. PIN1 phosphomimicking mutations, as well as enhanced phosphorylation in plants with modulated activities of PIN-specific kinases and phosphatases, desensitize PIN1 to cytokinin. Our results reveal conceptually novel, cytokinin-driven polarization mechanism that operates in developmental processes involving rapid auxin stream redirection, such as lateral root organogenesis, in which a gradual PIN polarity switch defines the growth axis of the newly formed organ.
Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium; Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria.
Peter
P
Marhavý
Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium.
Jérôme
J
Duclercq
Plant Systems Biology, Technische Universität München, 85354 Freising, Germany.
Benjamin
B
Weller
Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium.
Elena
E
Feraru
Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium.
Agnieszka
A
Bielach
Department of Molecular and Developmental Genetics, Institute Biology Leiden, Leiden University, 2333 AL Leiden, the Netherlands.
Remko
R
Offringa
Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium; Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria.
Jiří
J
Friml
Plant Systems Biology, Technische Universität München, 85354 Freising, Germany.
Claus
C
Schwechheimer
Plant Science and Landscape Architecture, University of Maryland, College Park, MD 20742, USA.
Angus
A
Murphy
Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium; Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria. Electronic address: eva.benkova@ist.ac.at.
Eva
E
Benková
D017360:Arabidopsis / Q000196:embryology / Q000378:metabolism* / Q000502:physiology; D029681:Arabidopsis Proteins / Q000096:biosynthesis / Q000235:genetics / Q000378:metabolism*; D001692:Biological Transport; D003583:Cytokinins / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D000071677:Histidine Kinase; D007210:Indoleacetic Acids / Q000378:metabolism*; D026901:Membrane Transport Proteins / Q000235:genetics / Q000378:metabolism*; D063246:Organogenesis, Plant; D010766:Phosphorylation; D010937:Plant Growth Regulators / Q000378:metabolism; D018517:Plant Roots / Q000254:growth & development* / Q000378:metabolism; D011494:Protein Kinases / Q000096:biosynthesis / Q000378:metabolism; D011956:Receptors, Cell Surface / Q000096:biosynthesis / Q000378:metabolism; D015398:Signal Transduction
D029681:Arabidopsis Proteins; D003583:Cytokinins; D007210:Indoleacetic Acids; D026901:Membrane Transport Proteins; C116363:PIN1 protein, Arabidopsis; D010937:Plant Growth Regulators; D011956:Receptors, Cell Surface; D011494:Protein Kinases; D000071677:Histidine Kinase; C421783:WOL protein, Arabidopsis