The MADS transcription factor XAL2/AGL14 modulates auxin transport during Arabidopsis root development by regulating PIN expression

Elucidating molecular links between cell‐fate regulatory networks and dynamic patterning modules is a key for understanding development. Auxin is important for plant patterning, particularly in roots, where it establishes positional information for cell‐fate decisions. PIN genes encode plasma membrane proteins that serve as auxin efflux transporters; mutations in members of this gene family exhibit smaller roots with altered root meristems and stem‐cell patterning. Direct regulators of PIN transcription have remained elusive. Here, we establish that a MADS‐box gene (XAANTAL2, XAL2/AGL14) controls auxin transport via PIN transcriptional regulation during Arabidopsis root development; mutations in this gene exhibit altered stem‐cell patterning, root meristem size, and root growth. XAL2 is necessary for normal shootward and rootward auxin transport, as well as for maintaining normal auxin distribution within the root. Furthermore, this MADS‐domain transcription factor upregulates PIN1 and PIN4 by direct binding to regulatory regions and it is required for PIN4‐dependent auxin response. In turn, XAL2 expression is regulated by auxin levels thus establishing a positive feedback loop between auxin levels and PIN regulation that is likely to be important for robust root patterning.

[1]  Philip N Benfey,et al.  The SHORT-ROOT Gene Controls Radial Patterning of the Arabidopsis Root through Radial Signaling , 2000, Cell.

[2]  A. Müller,et al.  Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. , 1998, Science.

[3]  S. Sabatini,et al.  SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. , 2003, Genes & development.

[4]  Klaus Palme,et al.  AtPIN4 Mediates Sink-Driven Auxin Gradients and Root Patterning in Arabidopsis , 2002, Cell.

[5]  H. Burstrom Auxin and the mechanism of root growth. , 1957, Symposia of the Society for Experimental Biology.

[6]  Ben Scheres,et al.  Cell fate and cell differentiation status in the Arabidopsis root , 1998, Planta.

[7]  E. Davidson,et al.  Gene Regulatory Networks and the Evolution of Animal Body Plans , 2006, Science.

[8]  G. Fink,et al.  EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. , 1998, Genes & development.

[9]  Tom Beeckman,et al.  Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression , 2005, Development.

[10]  D. Shasha,et al.  A Gene Expression Map of the Arabidopsis Root , 2003, Science.

[11]  C. Gutiérrez,et al.  Arabidopsis ORC1 is a PHD-containing H3K4me3 effector that regulates transcription , 2009, Proceedings of the National Academy of Sciences.

[12]  Hiroaki Kitano,et al.  Biological robustness , 2008, Nature Reviews Genetics.

[13]  E. Groisman,et al.  Positive feedback in cellular control systems , 2008, BioEssays : news and reviews in molecular, cellular and developmental biology.

[14]  E. Meyerowitz,et al.  Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[16]  Claudia van den Berg,et al.  Short-range control of cell differentiation in the Arabidopsis root meristem , 1997, Nature.

[17]  D. Weijers,et al.  Auxin control of embryo patterning. , 2009, Cold Spring Harbor perspectives in biology.

[18]  A. Murphy,et al.  Relocalization of the PIN1 Auxin Efflux Facilitator Plays a Role in Phototropic Responses1[w] , 2004, Plant Physiology.

[19]  Mariusz Kowalczyk,et al.  An Auxin Gradient and Maximum in the Arabidopsis Root Apex Shown by High-Resolution Cell-Specific Analysis of IAA Distribution and Synthesis[W] , 2009, The Plant Cell Online.

[20]  E. Álvarez-Buylla,et al.  An AGAMOUS-Related MADS-Box Gene, XAL1 (AGL12), Regulates Root Meristem Cell Proliferation and Flowering Transition in Arabidopsis1[W][OA] , 2008, Plant Physiology.

[21]  J. G. Dubrovsky,et al.  The lateral root initiation index: an integrative measure of primordium formation. , 2009, Annals of botany.

[22]  Tobias I. Baskin,et al.  On the constancy of cell division rate in the root meristem , 2000, Plant Molecular Biology.

[23]  Stefan de Folter,et al.  SEPALLATA3: the 'glue' for MADS box transcription factor complex formation , 2009, Genome Biology.

[24]  Eugenio Azpeitia,et al.  Single-cell and coupled GRN models of cell patterning in the Arabidopsis thaliana root stem cell niche , 2010, BMC Systems Biology.

[25]  J. G. Dubrovsky,et al.  Root growth, developmental changes in the apex, and hydraulic conductivity for Opuntia ficus‐indica during drought , 1998 .

[26]  V. B. Ivanov,et al.  Longitudinal zonation pattern in plant roots: conflicts and solutions. , 2013, Trends in plant science.

[27]  A. Murphy,et al.  Multidrug Resistance–like Genes of Arabidopsis Required for Auxin Transport and Auxin-Mediated Development Article, publication date, and citation information can be found at www.aspb.org/cgi/doi/10.1105/tpc.010350. , 2001, The Plant Cell Online.

[28]  Renze Heidstra,et al.  Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. , 2007, Genes & development.

[29]  Renze Heidstra,et al.  PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development , 2007, Nature.

[30]  P. Benfey,et al.  Organization and cell differentiation in lateral roots of Arabidopsis thaliana. , 1997, Development.

[31]  Michael Sauer,et al.  Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis , 2003, Nature.

[32]  M. Lenhard,et al.  Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers , 2007, Nature.

[33]  Klaus Palme,et al.  Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis , 2002, Nature.

[34]  Koji Goto,et al.  Complexes of MADS-box proteins are sufficient to convert leaves into floral organs , 2001, Nature.

[35]  J. Friml,et al.  Polar auxin transport – old questions and new concepts? , 2002, Plant Molecular Biology.

[36]  Ben Scheres,et al.  Polar PIN Localization Directs Auxin Flow in Plants , 2006, Science.

[37]  Dirk Inzé,et al.  GATEWAY vectors for Agrobacterium-mediated plant transformation. , 2002, Trends in plant science.

[38]  H. Bohnert,et al.  yucca6, a Dominant Mutation in Arabidopsis, Affects Auxin Accumulation and Auxin-Related Phenotypes1[W][OA] , 2007, Plant Physiology.

[39]  A. Murphy,et al.  A New Vertical Mesh Transfer Technique for Metal-Tolerance Studies in Arabidopsis (Ecotypic Variation and Copper-Sensitive Mutants) , 1995, Plant physiology.

[40]  A. Murphy,et al.  Flavonoids and auxin transport: modulators or regulators? , 2007, Trends in plant science.

[41]  R. Amasino,et al.  The PLETHORA Genes Mediate Patterning of the Arabidopsis Root Stem Cell Niche , 2004, Cell.

[42]  E. Álvarez-Buylla,et al.  An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[43]  A. Depicker,et al.  Update on Recombinational Cloning with Plant Gateway Vectors Recombinational Cloning with Plant Gateway Vectors , 2007 .

[44]  J. Tomasi Improving the Technic of the Feulgen Stain , 1936 .

[45]  E. Álvarez-Buylla,et al.  MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. , 2000, The Plant journal : for cell and molecular biology.

[46]  Detlef Weigel,et al.  Comprehensive Interaction Map of the Arabidopsis MADS Box Transcription Factorsw⃞ , 2005, The Plant Cell Online.

[47]  Ottoline Leyser,et al.  An Auxin-Dependent Distal Organizer of Pattern and Polarity in the Arabidopsis Root , 1999, Cell.

[48]  P. Doerner,et al.  Pericycle cell proliferation and lateral root initiation in Arabidopsis. , 2000, Plant physiology.

[49]  H. Saedler,et al.  Successful PCR-based reverse genetic screens using an En-1-mutagenised Arabidopsis thaliana population generated via single-seed descent , 1998, Theoretical and Applied Genetics.

[50]  Steffen Vanneste,et al.  Auxin: A Trigger for Change in Plant Development , 2009, Cell.

[51]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[52]  Tal Nawy,et al.  Transcriptional Profile of the Arabidopsis Root Quiescent Centerw⃞ , 2005, The Plant Cell Online.

[53]  Johannes Jaeger,et al.  Regulative feedback in pattern formation: towards a general relativistic theory of positional information , 2008, Development.

[54]  W. J. Lucas,et al.  Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. , 1999, Development.

[55]  N. Goldman,et al.  A codon-based model of nucleotide substitution for protein-coding DNA sequences. , 1994, Molecular biology and evolution.

[56]  Gema López-Torrejón,et al.  The Arabidopsis Cell Cycle F-Box Protein SKP2A Binds to Auxin[C][W] , 2010, Plant Cell.

[57]  E. Álvarez-Buylla,et al.  Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[58]  V. B. Ivanov,et al.  Estimation of the Cell-Cycle Duration in the Root Apical Meristem: A Model of Linkage between Cell-Cycle Duration, Rate of Cell Production, and Rate of Root Growth , 1997, International Journal of Plant Sciences.

[59]  Nadejda V. Mezentseva,et al.  Cell state switching factors and dynamical patterning modules: complementary mediators of plasticity in development and evolution , 2009, Journal of Biosciences.

[60]  E. Coen,et al.  The war of the whorls: genetic interactions controlling flower development , 1991, Nature.

[61]  Michael Sauer,et al.  Interactions among PIN-FORMED and P-Glycoprotein Auxin Transporters in Arabidopsis[W] , 2007, The Plant Cell Online.

[62]  Elena R. Alvarez-Buylla,et al.  MADS-box gene expression in lateral primordia, meristems and differentiated tissues of Arabidopsis thaliana roots , 2014, Planta.

[63]  R. Sablowski,et al.  Hypersensitivity to DNA damage in plant stem cell niches , 2009, Proceedings of the National Academy of Sciences.

[64]  B. Scheres,et al.  Cellular organisation of the Arabidopsis thaliana root. , 1993, Development.

[65]  Jan Petrásek,et al.  Cytokinin regulates root meristem activity via modulation of the polar auxin transport , 2009, Proceedings of the National Academy of Sciences.

[66]  Jing Zhang,et al.  Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter , 2009, Nature.

[67]  P. Hogeweg,et al.  Auxin transport is sufficient to generate a maximum and gradient guiding root growth , 2007, Nature.

[68]  S. Filleur,et al.  Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana , 2005, Planta.

[69]  Klaus Palme,et al.  The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots , 2005, Nature.

[70]  S. Baum,et al.  Root apical organization inArabidopsis thaliana 1. Root cap and protoderm , 1996, Protoplasma.