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      A map of cell type-specific auxin responses

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          Abstract

          • The majority of the thousands of auxin-responsive genes in the Arabidopsis thaliana root show a spatial bias in their induction or repression by auxin treatment.

          • Auxin promotes the expression of cell-identity markers for the developing xylem and quiescent center, whereas it inhibits markers for the maturing xylem, cortex and trichoblasts.

          • Relative induction or repression by auxin predicts expression along the longitudinal axis of the root.

          Abstract

          In plants, changes in local auxin concentrations can trigger a range of developmental processes as distinct tissues respond differently to the same auxin stimulus. However, little is known about how auxin is interpreted by individual cell types. We performed a transcriptomic analysis of responses to auxin within four distinct tissues of the Arabidopsis thaliana root and demonstrate that different cell types show competence for discrete responses. The majority of auxin-responsive genes displayed a spatial bias in their induction or repression. The novel data set was used to examine how auxin influences tissue-specific transcriptional regulation of cell-identity markers. Additionally, the data were used in combination with spatial expression maps of the root to plot a transcriptomic auxin-response gradient across the apical and basal meristem. The readout revealed a strong correlation for thousands of genes between the relative response to auxin and expression along the longitudinal axis of the root. This data set and comparative analysis provide a transcriptome-level spatial breakdown of the response to auxin within an organ where this hormone mediates many aspects of development.

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          Most cited references41

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          Local, efflux-dependent auxin gradients as a common module for plant organ formation.

          Plants, compared to animals, exhibit an amazing adaptability and plasticity in their development. This is largely dependent on the ability of plants to form new organs, such as lateral roots, leaves, and flowers during postembryonic development. Organ primordia develop from founder cell populations into organs by coordinated cell division and differentiation. Here, we show that organ formation in Arabidopsis involves dynamic gradients of the signaling molecule auxin with maxima at the primordia tips. These gradients are mediated by cellular efflux requiring asymmetrically localized PIN proteins, which represent a functionally redundant network for auxin distribution in both aerial and underground organs. PIN1 polar localization undergoes a dynamic rearrangement, which correlates with establishment of auxin gradients and primordium development. Our results suggest that PIN-dependent, local auxin gradients represent a common module for formation of all plant organs, regardless of their mature morphology or developmental origin.
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            A high-resolution root spatiotemporal map reveals dominant expression patterns.

            Transcriptional programs that regulate development are exquisitely controlled in space and time. Elucidating these programs that underlie development is essential to understanding the acquisition of cell and tissue identity. We present microarray expression profiles of a high-resolution set of developmental time points within a single Arabidopsis root and a comprehensive map of nearly all root cell types. These cell type-specific transcriptional signatures often predict previously unknown cellular functions. A computational pipeline identified dominant expression patterns that demonstrate transcriptional similarity between disparate cell types. Dominant expression patterns along the root's longitudinal axis do not strictly correlate with previously defined developmental zones, and in many cases, we observed expression fluctuation along this axis. Both robust co-regulation of gene expression and potential phasing of gene expression were identified between individual roots. Methods that combine these profiles demonstrate transcriptionally rich and complex programs that define Arabidopsis root development in both space and time.
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              Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19.

              The AUXIN RESPONSE FACTOR (ARF) gene family products, together with the AUXIN/INDOLE-3-ACETIC ACID proteins, regulate auxin-mediated transcriptional activation/repression. The biological function(s) of most ARFs is poorly understood. Here, we report the identification and characterization of T-DNA insertion lines for 18 of the 23 ARF gene family members in Arabidopsis thaliana. Most of the lines fail to show an obvious growth phenotype except of the previously identified arf2/hss, arf3/ett, arf5/mp, and arf7/nph4 mutants, suggesting that there are functional redundancies among the ARF proteins. Subsequently, we generated double mutants. arf7 arf19 has a strong auxin-related phenotype not observed in the arf7 and arf19 single mutants, including severely impaired lateral root formation and abnormal gravitropism in both hypocotyl and root. Global gene expression analysis revealed that auxin-induced gene expression is severely impaired in the arf7 single and arf7 arf19 double mutants. For example, the expression of several genes, such as those encoding members of LATERAL ORGAN BOUNDARIES domain proteins and AUXIN-REGULATED GENE INVOLVED IN ORGAN SIZE, are disrupted in the double mutant. The data suggest that the ARF7 and ARF19 proteins play essential roles in auxin-mediated plant development by regulating both unique and partially overlapping sets of target genes. These observations provide molecular insight into the unique and overlapping functions of ARF gene family members in Arabidopsis.
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                Author and article information

                Journal
                Mol Syst Biol
                Mol. Syst. Biol
                Molecular Systems Biology
                Nature Publishing Group
                1744-4292
                2013
                10 September 2013
                10 September 2013
                : 9
                : 688
                Affiliations
                [1 ]Biology Department, Center for Genomics and Systems Biology, New York University , New York, NY, USA
                [2 ]Department of Cell and Developmental Biology, UCSD , La Jolla, CA, USA
                [3 ]Department of Plant Systems Biology, VIB , Ghent, Belgium
                [4 ]Department of Plant Biotechnology and Bioinformatics, Ghent University , Ghent, Belgium
                [5 ]Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes—Claude Grignon , Montpellier, France
                [6 ]Institute of Science and Technology Austria (IST Austria) , Klosterneuburg, Austria
                [7 ]Howard Hughes Medical Institute, Stanford University, Stanford , CA, USA
                Author notes
                [a ]Biology Department, Center for Genomics and Systems Biology, New York University , New York, NY 10003, USA. Tel.:+1 212 998 8257; Fax:+1 212 995 4015; ken.birnbaum@ 123456nyu.edu
                Article
                msb201340
                10.1038/msb.2013.40
                3792342
                24022006
                4be88a83-7217-47a4-ad3e-a887063adba9
                Copyright © 2013, EMBO and Macmillan Publishers Limited

                This is an open-access article distributed under the terms of the Creative Commons Attribution Noncommercial Share Alike 3.0 Unported License, which allows readers to alter, transform, or build upon the article and then distribute the resulting work under the same or similar license to this one. The work must be attributed back to the original author and commercial use is not permitted without specific permission.

                History
                : 13 March 2013
                : 23 July 2013
                Categories
                Article

                Quantitative & Systems biology
                arabidopsis,development,root apical meristem,signaling gradient
                Quantitative & Systems biology
                arabidopsis, development, root apical meristem, signaling gradient

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