Cross-species functional diversity within the PIN auxin efflux protein family

O'Connor, Devin Lee; Elton, Samuel; Ticchiarelli, Fabrizio; Hsia, Mon Mandy; Vogel, John P.; Leyser, Ottoline

doi:10.7554/eLife.31804

Title: Cross-species functional diversity within the PIN auxin efflux protein family

Journal Article · 24 October 2017 · eLife

DOI: https://doi.org/10.7554/eLife.31804 · OSTI ID:1417010

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Univ. of Cambridge (United Kingdom). Sainsbury Lab.
US Dept. of Agriculture (USDA)., Albany, CA (United States). Agricultural Research Service, Western Regional Research Center
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology

In Arabidopsis, development during flowering is coordinated by transport of the hormone auxin mediated by polar-localized PIN-FORMED1 (AtPIN1). However Arabidopsis has lost a PIN clade sister to AtPIN1, Sister-of-PIN1 (SoPIN1), which is conserved in flowering plants. Here, we previously proposed that the AtPIN1 organ initiation and vein patterning functions are split between the SoPIN1 and PIN1 clades in grasses. Here we show that in the grass Brachypodium sopin1 mutants have organ initiation defects similar to Arabidopsis atpin1, while loss of PIN1 function in Brachypodium has little effect on organ initiation but alters stem growth. Heterologous expression of Brachypodium SoPIN1 and PIN1b in Arabidopsis provides further evidence of functional specificity. SoPIN1 but not PIN1b can mediate flower formation in null atpin1 mutants, although both can complement a missense allele. The behavior of SoPIN1 and PIN1b in Arabidopsis illustrates how membrane and tissue-level accumulation, transport activity, and interaction contribute to PIN functional specificity.

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Research Organization:: Agricultural Research Service, Albany, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AI02-07ER64452

OSTI ID:: 1417010

Journal Information:: eLife, Vol. 6; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 36 works

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References (69)

Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis Bhatia, Neha; Bozorg, Behruz; Larsson, André Current Biology, Vol. 26, Issue 23 https://doi.org/10.1016/j.cub.2016.09.044	journal	December 2016
Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism Abas, Lindy; Benjamins, René; Malenica, Nenad Nature Cell Biology, Vol. 8, Issue 3 https://doi.org/10.1038/ncb1369	journal	February 2006
Auxin Regulates the Initiation and Radial Position of Plant Lateral Organs Reinhardt, Didier; Mandel, Therese; Kuhlemeier, Cris The Plant Cell, Vol. 12, Issue 4 https://doi.org/10.1105/tpc.12.4.507	journal	April 2000
Patterning of Leaf Vein Networks by Convergent Auxin Transport Pathways Sawchuk, Megan G.; Edgar, Alexander; Scarpella, Enrico PLoS Genetics, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pgen.1003294	journal	February 2013
ERECTA Family Genes Regulate Auxin Transport in the Shoot Apical Meristem and Forming Leaf Primordia Chen, Ming-Kun; Wilson, Rebecca L.; Palme, Klaus Plant Physiology, Vol. 162, Issue 4 https://doi.org/10.1104/pp.113.218198	journal	July 2013
The dynamics of plant plasma membrane proteins: PINs and beyond Luschnig, C.; Vert, G. Development, Vol. 141, Issue 15 https://doi.org/10.1242/dev.103424	journal	July 2014
Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation Benková, Eva; Michniewicz, Marta; Sauer, Michael Cell, Vol. 115, Issue 5 https://doi.org/10.1016/S0092-8674(03)00924-3	journal	November 2003
Loss of an MDR Transporter in Compact Stalks of Maize br2 and Sorghum dw3 Mutants Multani, D. S. Science, Vol. 302, Issue 5642 https://doi.org/10.1126/science.1086072	journal	October 2003
Polar PIN Localization Directs Auxin Flow in Plants Wisniewska, J. Science, Vol. 312, Issue 5775 https://doi.org/10.1126/science.1121356	journal	May 2006
Dynamic PIN-FORMED auxin efflux carrier phosphorylation at the plasma membrane controls auxin efflux-dependent growth Weller, Benjamin; Zourelidou, Melina; Frank, Lena Proceedings of the National Academy of Sciences, Vol. 114, Issue 5 https://doi.org/10.1073/pnas.1614380114	journal	January 2017
A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta Barkoulas, Michalis; Hay, Angela; Kougioumoutzi, Evagelia Nature Genetics, Vol. 40, Issue 9 https://doi.org/10.1038/ng.189	journal	August 2008
Control of vein network topology by auxin transport Verna, Carla; Sawchuk, Megan G.; Linh, Nguyen Manh BMC Biology, Vol. 13, Issue 1 https://doi.org/10.1186/s12915-015-0208-3	journal	November 2015
The Power of Auxin in Plants: Figure 1. Leyser, Ottoline Plant Physiology, Vol. 154, Issue 2 https://doi.org/10.1104/pp.110.161323	journal	October 2010
Auxin efflux by PIN-FORMED proteins is activated by two different protein kinases, D6 PROTEIN KINASE and PINOID Zourelidou, Melina; Absmanner, Birgit; Weller, Benjamin eLife, Vol. 3 https://doi.org/10.7554/eLife.02860	journal	June 2014
Regulation of phyllotaxis by polar auxin transport Reinhardt, Didier; Pesce, Eva-Rachele; Stieger, Pia Nature, Vol. 426, Issue 6964 https://doi.org/10.1038/nature02081	journal	November 2003
Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting Kleine-Vehn, J.; Leitner, J.; Zwiewka, M. Proceedings of the National Academy of Sciences, Vol. 105, Issue 46 https://doi.org/10.1073/pnas.0808073105	journal	November 2008
A sister of PIN1 gene in tomato ( Solanum lycopersicum) defines leaf and flower organ initiation patterns by maintaining epidermal auxin flux Martinez, Ciera C.; Koenig, Daniel; Chitwood, Daniel H. Developmental Biology, Vol. 419, Issue 1 https://doi.org/10.1016/j.ydbio.2016.08.011	journal	November 2016
Formation of polarity convergences underlying shoot outgrowths Abley, Katie; Sauret-Güeto, Susanna; Marée, Athanasius FM eLife, Vol. 5 https://doi.org/10.7554/eLife.18165	journal	August 2016
Auxin-driven patterning with unidirectional fluxes Cieslak, Mikolaj; Runions, Adam; Prusinkiewicz, Przemyslaw Journal of Experimental Botany, Vol. 66, Issue 16 https://doi.org/10.1093/jxb/erv262	journal	June 2015
Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity Sauer, M.; Balla, J.; Luschnig, C. Genes & Development, Vol. 20, Issue 20 https://doi.org/10.1101/gad.390806	journal	October 2006
Model for the regulation of Arabidopsis thaliana leaf margin development Bilsborough, G. D.; Runions, A.; Barkoulas, M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 8 https://doi.org/10.1073/pnas.1015162108	journal	February 2011
The PIN auxin efflux facilitators: evolutionary and functional perspectives Paponov, I.; Teale, W.; Trebar, M. Trends in Plant Science, Vol. 10, Issue 4 https://doi.org/10.1016/j.tplants.2005.02.009	journal	April 2005
Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1 Lenhard, M. Development, Vol. 130, Issue >14 https://doi.org/10.1242/dev.00525	journal	July 2003
The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Torii, K. U.; Mitsukawa, N.; Oosumi, T. The Plant Cell, Vol. 8, Issue 4 https://doi.org/10.1105/tpc.8.4.735	journal	April 1996
The Arabidopsis MAX Pathway Controls Shoot Branching by Regulating Auxin Transport Bennett, Tom; Sieberer, Tobias; Willett, Barbara Current Biology, Vol. 16, Issue 6 https://doi.org/10.1016/j.cub.2006.01.058	journal	March 2006
D6PK AGCVIII Kinases Are Required for Auxin Transport and Phototropic Hypocotyl Bending in Arabidopsis Willige, Björn C.; Ahlers, Siv; Zourelidou, Melina The Plant Cell, Vol. 25, Issue 5 https://doi.org/10.1105/tpc.113.111484	journal	May 2013
A Molecular Framework for Plant Regeneration Xu, Jian; Hofhuis, Hugo; Heidstra, Renze Science, Vol. 311, Issue 5759 https://doi.org/10.1126/science.1121790	journal	January 2006
Alignment between PIN1 Polarity and Microtubule Orientation in the Shoot Apical Meristem Reveals a Tight Coupling between Morphogenesis and Auxin Transport Heisler, Marcus G.; Hamant, Olivier; Krupinski, Pawel PLoS Biology, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pbio.1000516	journal	October 2010
A plausible model of phyllotaxis Smith, R. S.; Guyomarc'h, S.; Mandel, T. Proceedings of the National Academy of Sciences, Vol. 103, Issue 5 https://doi.org/10.1073/pnas.0510457103	journal	January 2006
Functional redundancy of PIN proteins is accompanied by auxin-dependentcross-regulation of PIN expression Vieten, A.; Vanneste, S.; Wisniewska, J. Development, Vol. 132, Issue 20 https://doi.org/10.1242/dev.02027	journal	September 2005
The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots Blilou, Ikram; Xu, Jian; Wildwater, Marjolein Nature, Vol. 433, Issue 7021 https://doi.org/10.1038/nature03184	journal	January 2005
Improving CRISPR-Cas nuclease specificity using truncated guide RNAs Fu, Yanfang; Sander, Jeffry D.; Reyon, Deepak Nature Biotechnology, Vol. 32, Issue 3 https://doi.org/10.1038/nbt.2808	journal	January 2014
Paralogous Radiations of PIN Proteins with Multiple Origins of Noncanonical PIN Structure Bennett, Tom; Brockington, Samuel F.; Rothfels, Carl Molecular Biology and Evolution, Vol. 31, Issue 8 https://doi.org/10.1093/molbev/msu147	journal	April 2014
A transcription activation system for regulated gene expression in transgenic plants Moore, I.; Galweiler, L.; Grosskopf, D. Proceedings of the National Academy of Sciences, Vol. 95, Issue 1 https://doi.org/10.1073/pnas.95.1.376	journal	January 1998
Brachytic2/ZmABCB1 functions in IAA export from intercalary meristems Knöller, Anne Sophie; Blakeslee, Joshua J.; Richards, Elizabeth L. Journal of Experimental Botany, Vol. 61, Issue 13 https://doi.org/10.1093/jxb/erq180	journal	June 2010
Targeted mutagenesis in rice using CRISPR-Cas system Miao, Jin; Guo, Dongshu; Zhang, Jinzhe Cell Research, Vol. 23, Issue 10 https://doi.org/10.1038/cr.2013.123	journal	September 2013
A Division in PIN-Mediated Auxin Patterning during Organ Initiation in Grasses O'Connor, Devin L.; Runions, Adam; Sluis, Aaron PLoS Computational Biology, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pcbi.1003447	journal	January 2014
Strigolactone Can Promote or Inhibit Shoot Branching by Triggering Rapid Depletion of the Auxin Efflux Protein PIN1 from the Plasma Membrane Shinohara, Naoki; Taylor, Catherine; Leyser, Ottoline PLoS Biology, Vol. 11, Issue 1 https://doi.org/10.1371/journal.pbio.1001474	journal	January 2013
Auxin Distribution and Plant Pattern Formation: How Many Angels Can Dance on the Point of PIN? Leyser, Ottoline Cell, Vol. 121, Issue 6 https://doi.org/10.1016/j.cell.2005.06.005	journal	June 2005
Connective Auxin Transport in the Shoot Facilitates Communication between Shoot Apices Bennett, Tom; Hines, Geneviève; van Rongen, Martin PLOS Biology, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pbio.1002446	journal	April 2016
A novel sensor to map auxin response and distribution at high spatio-temporal resolution Brunoud, Géraldine; Wells, Darren M.; Oliva, Marina Nature, Vol. 482, Issue 7383 https://doi.org/10.1038/nature10791	journal	January 2012
PIN-Dependent Auxin Transport: Action, Regulation, and Evolution Adamowski, Maciek; Friml, Jiří The Plant Cell, Vol. 27, Issue 1 https://doi.org/10.1105/tpc.114.134874	journal	January 2015
Pattern formation during de novo assembly of the Arabidopsis shoot meristem Gordon, S. P.; Heisler, M. G.; Reddy, G. V. Development, Vol. 134, Issue 19 https://doi.org/10.1242/dev.010298	journal	October 2007
An auxin-driven polarized transport model for phyllotaxis Jonsson, H.; Heisler, M. G.; Shapiro, B. E. Proceedings of the National Academy of Sciences, Vol. 103, Issue 5 https://doi.org/10.1073/pnas.0509839103	journal	January 2006
Developmental Analysis of a Medicago truncatula smooth leaf margin1 Mutant Reveals Context-Dependent Effects on Compound Leaf Development Zhou, Chuanen; Han, Lu; Hou, Chunyan The Plant Cell, Vol. 23, Issue 6 https://doi.org/10.1105/tpc.111.085464	journal	June 2011
Integration of transport-based models for phyllotaxis and midvein formation Bayer, E. M.; Smith, R. S.; Mandel, T. Genes & Development, Vol. 23, Issue 3 https://doi.org/10.1101/gad.497009	journal	February 2009
Brachypodium distachyon Bragg, Jennifer N.; Anderton, Amy; Nieu, Rita Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-1695-5_2	book	September 2014
The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia: Epidermal expression of transgenes in meristems Sessions, Allen; Weigel, Detlef; Yanofsky, Martin F. The Plant Journal, Vol. 20, Issue 2 https://doi.org/10.1046/j.1365-313x.1999.00594.x	journal	October 1999
Strigolactones enhance competition between shoot branches by dampening auxin transport Crawford, S.; Shinohara, N.; Sieberer, T. Development, Vol. 137, Issue 17 https://doi.org/10.1242/dev.051987	journal	July 2010
The Polar Transport of Auxin and Vein Patterns in Plants [and Discussion] Mitchison, G. J.; Hanke, D. E.; Sheldrake, A. R. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 295, Issue 1078 https://doi.org/10.1098/rstb.1981.0154	journal	October 1981
Mitogen-Activated Protein Kinase Cascade MKK7-MPK6 Plays Important Roles in Plant Development and Regulates Shoot Branching by Phosphorylating PIN1 in Arabidopsis Jia, Weiyan; Li, Baohua; Li, Shujia PLOS Biology, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pbio.1002550	journal	September 2016
Morphogenesis in pinoid mutants of Arabidopsis thaliana Bennett, Sally R. M.; Alvarez, John; Bossinger, Gerd The Plant Journal, Vol. 8, Issue 4 https://doi.org/10.1046/j.1365-313X.1995.8040505.x	journal	October 1995
Dynamic Integration of Auxin Transport and Signalling Leyser, Ottoline Current Biology, Vol. 16, Issue 11 https://doi.org/10.1016/j.cub.2006.05.014	journal	June 2006
Phyllotaxis involves auxin drainage through leaf primordia Deb, Y.; Marti, D.; Frenz, M. Development, Vol. 142, Issue 11 https://doi.org/10.1242/dev.121244	journal	May 2015
TRANSPORT OF INDOLEACETIC ACID IN PLANT CELLS IN RELATION TO pH AND ELECTRICAL POTENTIAL GRADIENTS, AND ITS SIGNIFICANCE FOR POLAR IAA TRANSPORT Raven, J. A. New Phytologist, Vol. 74, Issue 2 https://doi.org/10.1111/j.1469-8137.1975.tb02602.x	journal	March 1975
Interaction between Meristem Tissue Layers Controls Phyllotaxis Kierzkowski, Daniel; Lenhard, Michael; Smith, Richard Developmental Cell, Vol. 26, Issue 6 https://doi.org/10.1016/j.devcel.2013.08.017	journal	September 2013
Patterns of Auxin Transport and Gene Expression during Primordium Development Revealed by Live Imaging of the Arabidopsis Inflorescence Meristem Heisler, Marcus G.; Ohno, Carolyn; Das, Pradeep Current Biology, Vol. 15, Issue 21 https://doi.org/10.1016/j.cub.2005.09.052	journal	November 2005
PIN-driven polar auxin transport in plant developmental plasticity: a key target for environmental and endogenous signals Habets, Myckel E. J.; Offringa, Remko New Phytologist, Vol. 203, Issue 2 https://doi.org/10.1111/nph.12831	journal	May 2014
Control of bud activation by an auxin transport switch Prusinkiewicz, P.; Crawford, S.; Smith, R. S. Proceedings of the National Academy of Sciences, Vol. 106, Issue 41 https://doi.org/10.1073/pnas.0906696106	journal	September 2009
MORE SPIKELETS1 Is Required for Spikelet Fate in the Inflorescence of Brachypodium Derbyshire, Paul; Byrne, Mary E. Plant Physiology, Vol. 161, Issue 3 https://doi.org/10.1104/pp.112.212340	journal	January 2013
Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation. Okada, K.; Ueda, J.; Komaki, M. K. The Plant Cell https://doi.org/10.1105/tpc.3.7.677	journal	July 1991
ARF GEF-Dependent Transcytosis and Polar Delivery of PIN Auxin Carriers in Arabidopsis Kleine-Vehn, Jürgen; Dhonukshe, Pankaj; Sauer, Michael Current Biology, Vol. 18, Issue 7 https://doi.org/10.1016/j.cub.2008.03.021	journal	April 2008
Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway Wang, Renhou; Estelle, Mark Current Opinion in Plant Biology, Vol. 21 https://doi.org/10.1016/j.pbi.2014.06.006	journal	October 2014
Regulation of Polar Auxin Transport by AtPIN1 in Arabidopsis Vascular Tissue Ga lweiler, L.; Guan, C.; Mu ller, A. Science, Vol. 282, Issue 5397 https://doi.org/10.1126/science.282.5397.2226	journal	December 1998
PIN1-Independent Leaf Initiation in Arabidopsis Guenot, Bernadette; Bayer, Emmanuelle; Kierzkowski, Daniel Plant Physiology, Vol. 159, Issue 4 https://doi.org/10.1104/pp.112.200402	journal	June 2012
Control of leaf vascular patterning by polar auxin transport Scarpella, E. Genes & Development, Vol. 20, Issue 8 https://doi.org/10.1101/gad.1402406	journal	April 2006
Flux-Based Transport Enhancement as a Plausible Unifying Mechanism for Auxin Transport in Meristem Development Stoma, Szymon; Lucas, Mikael; Chopard, Jérôme PLoS Computational Biology, Vol. 4, Issue 10 https://doi.org/10.1371/journal.pcbi.1000207	journal	October 2008
D6 PROTEIN KINASE Activates Auxin Transport-Dependent Growth and PIN-FORMED Phosphorylation at the Plasma Membrane Barbosa, Inês C. R.; Zourelidou, Melina; Willige, Björn C. Developmental Cell, Vol. 29, Issue 6 https://doi.org/10.1016/j.devcel.2014.05.006	journal	June 2014
Research data supporting 'Connective auxin transport in the shoot facilitates communication between shoot apices'. Bennett, Tom; Van Rongen, Martin; Ljung, Karin Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.69011	dataset	January 2016

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