The Arabidopsis bZIP11 transcription factor links low-energy signalling to auxin-mediated control of primary root growth.
Plants have to tightly control their energy homeostasis to ensure survival and fitness under constantly changing environmental conditions. Thus, it is stringently required that energy-consuming stress-adaptation and growth-related processes are dynamically tuned according to the prevailing energy availability. The evolutionary conserved SUCROSE NON-FERMENTING1 RELATED KINASES1 (SnRK1) and the downstream group C/S1 basic leucine zipper (bZIP) transcription factors (TFs) are well-characterised central players in plants' low-energy management. Nevertheless, mechanistic insights into plant growth control under energy deprived conditions remains largely elusive. In this work, we disclose the novel function of the low-energy activated group S1 bZIP11-related TFs as regulators of auxin-mediated primary root growth. Whereas transgenic gain-of-function approaches of these bZIPs interfere with the activity of the root apical meristem and result in root growth repression, root growth of loss-of-function plants show a pronounced insensitivity to low-energy conditions. Based on ensuing molecular and biochemical analyses, we propose a mechanistic model, in which bZIP11-related TFs gain control over the root meristem by directly activating IAA3/SHY2 transcription. IAA3/SHY2 is a pivotal negative regulator of root growth, which has been demonstrated to efficiently repress transcription of major auxin transport facilitators of the PIN-FORMED (PIN) gene family, thereby restricting polar auxin transport to the root tip and in consequence auxin-driven primary root growth. Taken together, our results disclose the central low-energy activated SnRK1-C/S1-bZIP signalling module as gateway to integrate information on the plant's energy status into root meristem control, thereby balancing plant growth and cellular energy resources.
Julius-von-Sachs-Institut, Pharmazeutische Biologie, Julius-Maximilians-Universität Würzburg, Würzburg, Germany.
Christoph
C
Weiste
Julius-von-Sachs-Institut, Pharmazeutische Biologie, Julius-Maximilians-Universität Würzburg, Würzburg, Germany.
Lorenzo
L
Pedrotti
Department of Molecular Plant Physiology, Utrecht University, Utrecht, Netherlands.
Jebasingh
0000-0001-8352-0586
J
Selvanayagam
Julius-von-Sachs-Institut, Pharmazeutische Biologie, Julius-Maximilians-Universität Würzburg, Würzburg, Germany.
Prathibha
P
Muralidhara
Julius-von-Sachs-Institut, Pharmazeutische Biologie, Julius-Maximilians-Universität Würzburg, Würzburg, Germany.
Christian
0000-0001-9266-7897
C
Fröschel
Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden.
Ondřej
0000-0003-3452-0154
O
Novák
Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden.
Karin
K
Ljung
Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, Sweden.
Johannes
0000-0002-5605-7984
J
Hanson
Julius-von-Sachs-Institut, Pharmazeutische Biologie, Julius-Maximilians-Universität Würzburg, Würzburg, Germany.
Wolfgang
W
Dröge-Laser
D017360:Arabidopsis / Q000235:genetics* / Q000254:growth & development; D029681:Arabidopsis Proteins / Q000096:biosynthesis / Q000235:genetics*; D050976:Basic-Leucine Zipper Transcription Factors / Q000096:biosynthesis / Q000235:genetics*; D018506:Gene Expression Regulation, Plant; D007210:Indoleacetic Acids / Q000378:metabolism; D026901:Membrane Transport Proteins / Q000235:genetics; D018519:Meristem / Q000235:genetics / Q000254:growth & development; D009687:Nuclear Proteins / Q000096:biosynthesis / Q000235:genetics*; D010937:Plant Growth Regulators / Q000235:genetics / Q000378:metabolism; D018517:Plant Roots / Q000235:genetics* / Q000254:growth & development; D017346:Protein Serine-Threonine Kinases / Q000235:genetics*; D015398:Signal Transduction
D029681:Arabidopsis Proteins; D050976:Basic-Leucine Zipper Transcription Factors; D007210:Indoleacetic Acids; D026901:Membrane Transport Proteins; D009687:Nuclear Proteins; D010937:Plant Growth Regulators; D017346:Protein Serine-Threonine Kinases; C112599:ATB2 protein, Arabidopsis; C116363:PIN1 protein, Arabidopsis; C117994:SHY2 protein, Arabidopsis; C531469:At3g01090 protein, Arabidopsis