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Open Access Methodology article

Monitoring the regulation of gene expression in a growing organ using a fluid mechanics formalism

Rémy Merret1, Bruno Moulia2, Irène Hummel1, David Cohen1, Erwin Dreyer1 and Marie-Béatrice Bogeat-Triboulot1*

Author Affiliations

1 INRA, Nancy Université, UMR1137 Ecologie et Ecophysiologie Forestières, IFR 110 EFABA, F-54280 Champenoux, France

2 INRA, Université Blaise Pascal, UMR_A547 Physique et Physiologie Intégratives de l'Arbre Fruitier et Forestier, Domaine de Crouelle, F-63039 Clermont Ferrand, France

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BMC Biology 2010, 8:18  doi:10.1186/1741-7007-8-18

Published: 4 March 2010

Abstract

Background

Technological advances have enabled the accurate quantification of gene expression, even within single cell types. While transcriptome analyses are routinely performed, most experimental designs only provide snapshots of gene expression. Molecular mechanisms underlying cell fate or positional signalling have been revealed through these discontinuous datasets. However, in developing multicellular structures, temporal and spatial cues, known to directly influence transcriptional networks, get entangled as the cells are displaced and expand. Access to an unbiased view of the spatiotemporal regulation of gene expression occurring during development requires a specific framework that properly quantifies the rate of change of a property in a moving and expanding element, such as a cell or an organ segment.

Results

We show how the rate of change in gene expression can be quantified by combining kinematics and real-time polymerase chain reaction data in a mechanistic model which considers any organ as a continuum. This framework was applied in order to assess the developmental regulation of the two reference genes Actin11 and Elongation Factor 1-β in the apex of poplar root. The growth field was determined by time-lapse photography and transcript density was obtained at high spatial resolution. The net accumulation rates of the transcripts of the two genes were found to display highly contrasted developmental profiles. Actin11 showed pulses of up and down regulation in the accelerating and decelerating parts of the growth zone while the dynamic of EF1β were much slower. This framework provides key information about gene regulation in a developing organ, such as the location, the duration and the intensity of gene induction/repression.

Conclusions

We demonstrated that gene expression patterns can be monitored using the continuity equation without using mutants or reporter constructions. Given the rise of imaging technologies, this framework in our view opens a new way to dissect the molecular basis of growth regulation, even in non-model species or complex structures.