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Auxin-driven patterning with unidirectional fluxes.

ABSTRACT: The plant hormone auxin plays an essential role in the patterning of plant structures. Biological hypotheses supported by computational models suggest that auxin may fulfil this role by regulating its own transport, but the plausibility of previously proposed models has been questioned. We applied the notion of unidirectional fluxes and the formalism of Petri nets to show that the key modes of auxin-driven patterning-the formation of convergence points and the formation of canals-can be implemented by biochemically plausible networks, with the fluxes measured by dedicated tally molecules or by efflux and influx carriers themselves. Common elements of these networks include a positive feedback of auxin efflux on the allocation of membrane-bound auxin efflux carriers (PIN proteins), and a modulation of this allocation by auxin in the extracellular space. Auxin concentration in the extracellular space is the only information exchanged by the cells. Canalization patterns are produced when auxin efflux and influx act antagonistically: an increase in auxin influx or concentration in the extracellular space decreases the abundance of efflux carriers in the adjacent segment of the membrane. In contrast, convergence points emerge in networks in which auxin efflux and influx act synergistically. A change in a single reaction rate may result in a dynamic switch between these modes, suggesting plausible molecular implementations of coordinated patterning of organ initials and vascular strands predicted by the dual polarization theory.

SUBMITTER: Cieslak M

PROVIDER: S-EPMC4513925 | biostudies-literature | 2015 Aug

REPOSITORIES: biostudies-literature

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Auxin-driven patterning with unidirectional fluxes.

Cieslak Mikolaj M Runions Adam A Prusinkiewicz Przemyslaw P

Journal of experimental botany 20150627 16

The plant hormone auxin plays an essential role in the patterning of plant structures. Biological hypotheses supported by computational models suggest that auxin may fulfil this role by regulating its own transport, but the plausibility of previously proposed models has been questioned. We applied the notion of unidirectional fluxes and the formalism of Petri nets to show that the key modes of auxin-driven patterning-the formation of convergence points and the formation of canals-can be implemen ...[more]

PMID: 26116915

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Project description:BackgroundIn plant roots, auxin is critical for patterning and morphogenesis. It regulates cell elongation and division, the development and maintenance of root apical meristems, and other processes. In Arabidopsis, auxin distribution along the central root axis has several maxima: in the root tip, in the basal meristem and at the shoot/root junction. The distal maximum in the root tip maintains the stem cell niche. Proximal maxima may trigger lateral or adventitious root initiation.ResultsWe propose a reflected flow mechanism for the formation of the auxin maximum in the root apical meristem. The mechanism is based on auxin's known activation and inhibition of expressed PIN family auxin carriers at low and high auxin levels, respectively. Simulations showed that these regulatory interactions are sufficient for self-organization of the auxin distribution pattern along the central root axis under varying conditions. The mathematical model was extended with rules for discontinuous cell dynamics so that cell divisions were also governed by auxin, and by another morphogen Division Factor which combines the actions of cytokinin and ethylene on cell division in the root. The positional information specified by the gradients of these two morphogens is able to explain root patterning along the central root axis.ConclusionWe present here a plausible mechanism for auxin patterning along the developing root, that may provide for self-organization of the distal auxin maximum when the reverse fountain has not yet been formed or has been disrupted. In addition, the proximal maxima are formed under the reflected flow mechanism in response to periods of increasing auxin flow from the growing shoot. These events may predetermine lateral root initiation in a rhyzotactic pattern. Another outcome of the reflected flow mechanism - the predominance of lateral or adventitious roots in different plant species - may be based on the different efficiencies with which auxin inhibits its own transport in different species, thereby distinguishing two main types of plant root architecture: taproot vs. fibrous.

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Auxin-driven patterning with unidirectional fluxes.

Publications

Auxin-driven patterning with unidirectional fluxes.

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