Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis.
The periodic formation of plant organs such as leaves and flowers gives rise to intricate patterns that have fascinated biologists and mathematicians alike for hundreds of years [1]. The plant hormone auxin plays a central role in establishing these patterns by promoting organ formation at sites where it accumulates due to its polar, cell-to-cell transport [2-6]. Although experimental evidence as well as modeling suggest that feedback from auxin to its transport direction may help specify phyllotactic patterns [7-12], the nature of this feedback remains unclear [13]. Here we reveal that polarization of the auxin efflux carrier PIN-FORMED 1 (PIN1) is regulated by the auxin response transcription factor MONOPTEROS (MP) [14]. We find that in the shoot, cell polarity patterns follow MP expression, which in turn follows auxin distribution patterns. By perturbing MP activity both globally and locally, we show that localized MP activity is necessary for the generation of polarity convergence patterns and that localized MP expression is sufficient to instruct PIN1 polarity directions non-cell autonomously, toward MP-expressing cells. By expressing MP in the epidermis of mp mutants, we further show that although MP activity in a single-cell layer is sufficient to promote polarity convergence patterns, MP in sub-epidermal tissues helps anchor these polarity patterns to the underlying cells. Overall, our findings reveal a patterning module in plants that determines organ position by orienting transport of the hormone auxin toward cells with high levels of MP-mediated auxin signaling. We propose that this feedback process acts broadly to generate periodic plant architectures.
European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany.
Neha
N
Bhatia
Computational Biology and Biological Physics Group, Department of Astronomy and Theoretical Physics, Lund University, Sölvegatan 14A, SE-223 62 Lund, Sweden.
Behruz
B
Bozorg
Computational Biology and Biological Physics Group, Department of Astronomy and Theoretical Physics, Lund University, Sölvegatan 14A, SE-223 62 Lund, Sweden.
André
A
Larsson
European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany.
Carolyn
C
Ohno
Computational Biology and Biological Physics Group, Department of Astronomy and Theoretical Physics, Lund University, Sölvegatan 14A, SE-223 62 Lund, Sweden; Sainsbury Laboratory and Department of Applied Mathematics and Theoretical Physics, University of Cambridge, Cambridge CB2 1TN, UK.
Henrik
H
Jönsson
European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany; Biological Sciences, The University of Sydney, Sydney, NSW 2006, Australia. Electronic address: heisler@embl.de.
Marcus G
MG
Heisler
D017360:Arabidopsis / Q000166:cytology / Q000254:growth & development*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D001692:Biological Transport; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant / Q000502:physiology*; D007210:Indoleacetic Acids / Q000378:metabolism*; D009154:Mutation; D010507:Periodicity; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*
D029681:Arabidopsis Proteins; D004268:DNA-Binding Proteins; D007210:Indoleacetic Acids; C111371:MONOPTEROS protein, Arabidopsis; D014157:Transcription Factors
ARF5; Arabidopsis; MONOPTEROS; PIN1; auxin; cell polarity; organ positioning; organogenesis; pattern formation; phyllotaxis