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Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis.

ABSTRACT: 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.

SUBMITTER: Bhatia N

PROVIDER: S-EPMC5154752 | biostudies-literature | 2016 Dec

REPOSITORIES: biostudies-literature

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Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis.

Bhatia Neha N Bozorg Behruz B Larsson André A Ohno Carolyn C Jönsson Henrik H Heisler Marcus G MG

Current biology : CB 20161103 23

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 phyllo ...[more]

PMID: 27818174

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Project description:Phyllotaxis, the arrangement of leaves on a plant stem, is well known because of its beautiful geometric configuration, which is derived from the constant spacing between leaf primordia. This phyllotaxis is established by mutual interaction between a diffusible plant hormone auxin and its efflux carrier PIN1, which cooperatively generate a regular pattern of auxin maxima, small regions with high auxin concentrations, leading to leaf primordia. However, the molecular mechanism of the regular pattern of auxin maxima is still largely unknown. To better understand how the phyllotaxis pattern is controlled, we investigated mathematical models based on the auxin-PIN1 interaction through linear stability analysis and numerical simulations, focusing on the spatial regularity control of auxin maxima. As in previous reports, we first confirmed that this spatial regularity can be reproduced by a highly simplified and abstract model. However, this model lacks the extracellular region and is not appropriate for considering the molecular mechanism. Thus, we investigated how auxin maxima patterns are affected under more realistic conditions. We found that the spatial regularity is eliminated by introducing the extracellular region, even in the presence of direct diffusion between cells or between extracellular spaces, and this strongly suggests the existence of an unknown molecular mechanism. To unravel this mechanism, we assumed a diffusible molecule to verify various feedback interactions with auxin-PIN1 dynamics. We revealed that regular patterns can be restored by a diffusible molecule that mediates the signaling from auxin to PIN1 polarization. Furthermore, as in the one-dimensional case, similar results are observed in the two-dimensional space. These results provide a great insight into the theoretical and molecular basis for understanding the phyllotaxis pattern. Our theoretical analysis strongly predicts a diffusible molecule that is pivotal for the phyllotaxis pattern but is yet to be determined experimentally.

Dataset Information

Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis.

Publications

Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis.

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